REVIEW published: 09 February 2022 doi: 10.3389/fpls.2021.805635 Photoperiod Control of Plant Growth: Flowering Time Genes Beyond Flowering Michela Osnato 1,2* , Ignacio Cota 1 , Poonam Nebhnani 1 , Unai Cereijo 1 and Soraya Pelaz 1,3* 1 Centre for Research in Agricultural Genomics, CSIC-IRTA-UAB-UB, Barcelona, Spain, 2 Institute of Environmental Science and Technology of the Universitat Autònoma de Barcelona, Barcelona, Spain, 3 Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain Fluctuations in environmental conditions greatly influence life on earth. Plants, as sessile organisms, have developed molecular mechanisms to adapt their development to changes in daylength, or photoperiod. One of the first plant features that comes to mind as affected by the duration of the day is flowering time; we all bring up a clear Edited by: image of spring blossom. However, for many plants flowering happens at other times Manuel Pineiro, of the year, and many other developmental aspects are also affected by changes in Instituto Nacional de Investigación y daylength, which range from hypocotyl elongation in Arabidopsis thaliana to tuberization Tecnología Agraria y Alimentaria (INIA), Spain in potato or autumn growth cessation in trees. Strikingly, many of the processes affected Reviewed by: by photoperiod employ similar gene networks to respond to changes in the length of Vittoria Brambilla, light/dark cycles. In this review, we have focused on developmental processes affected University of Milan, Italy Berenice Garcia-Ponce, by photoperiod that share similar genes and gene regulatory networks. National Autonomous University Keywords: photoperiod, growth, flowering, stomata, adaptation, growth cessation, tuberization, runner of Mexico, Mexico *Correspondence: Michela Osnato michela.osnato@uab.cat INTRODUCTION Soraya Pelaz soraya.pelaz@cragenomica.es The Earth’s rotation on its axis and revolution around the sun create cycles of day and night with a 24-h period as well as changes in temperature and humidity with a 365-day period. These periodic Specialty section: alterations in environmental conditions (light duration and intensity, ambient temperature) are This article was submitted to modest in tropical and subtropical regions, where changes in precipitation determine the two main Plant Development and EvoDevo, seasons (e.g., dry and wet), but are considerable in temperate regions, where changes in the length a section of the journal of the day and ambient temperature determine the four seasons – Long Days (LDs) in spring and Frontiers in Plant Science hot summer, and Short Days (SDs) in autumn and cold winter. Received: 30 October 2021 Compared to temperature, daylight is a more predictable external cue that enables organisms Accepted: 23 December 2021 to anticipate seasonal changes and modulate their biological function consequently. The length Published: 09 February 2022 of the light period over 24 h, also named photoperiod, regulates many aspects of plant growth. Citation: For example, trees stop growing when days shorten in autumn foreseeing the arrival of cold Osnato M, Cota I, Nebhnani P, winter. There are more examples of developmental traits regulated by changes in photoperiod, Cereijo U and Pelaz S (2022) some discussed in this review. Their importance in plant development and plant adaptation Photoperiod Control of Plant Growth: Flowering Time Genes Beyond to specific habitats promoted scientific research about the molecular mechanisms underlying Flowering. photoperiodic response. Front. Plant Sci. 12:805635. Light/dark cycles and hot/cold cycles entrain the circadian clock, defined as the internal timer doi: 10.3389/fpls.2021.805635 synchronized with solar time that oscillates with a stable phase of approximately 24 h. Frontiers in Plant Science | www.frontiersin.org 1 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Light is perceived by photoreceptors that sense different In plants, photoperiod integrates the circadian clock output wavelengths of the natural sunlight spectrum (reviewed in Lin, information and the light perception to regulate plant adaptation 2000), which then transmit this information to the central to different light regimes. Accordingly, plants modulate their oscillator of the circadian clock – made of interconnected growth in response to seasonal changes and synchronize key molecular gears that generates a 24 h rhythm. Components of developmental transitions with favorable conditions to sustain the circadian clock are encoded by regulatory genes that are their ecological fitness (i.e., survival of adult organisms able activated at specific time points, such as morning-phased genes to produce progeny before their death). Different photoperiods at the beginning of the light period or evening-phased genes at regulate different developmental transitions; for example, in the beginning of the dark period. These regulatory proteins form poplar trees LDs trigger vegetative growth in spring while SDs multimeric complexes, which act in multiple feedback loops that promote growth cessation in autumn. On the other hand, the in turn affect the expression of downstream targets at different same developmental process could be regulated by different moments, from sunrise to sunset and during the night. photoperiods in different plants; a good example is the transition Genetic determinants underlying light perception and the from the vegetative to reproductive phase (also called the mechanism of the clock have been extensively characterized in the floral transition), because some plants growing in temperate model species Arabidopsis thaliana, and then identified in other regions flower when days are long whereas other plants growing plants such as rice and potato. in tropical regions prefer SD or even neutral days (12 h In Arabidopsis, five phytochrome family members (phyA to light/12 h dark) to develop reproductive structures. Hence, phyE) represent the major photoreceptors that sense red and photoperiod controls several developmental stages throughout far-red light (Clack et al., 1994). Phytochromes are localized the plant life cycle. in the cytosol in their inactive form but are translocated to In this review, we focus on processes that share genes and the nucleus in their active forms, where they associate with gene regulatory networks (GRNs) rather than those that are different regulatory proteins, including the PHYTOCHROME regulated by completely different mechanisms or without detailed INTERACTING FACTORS (PIFs, Matsushita et al., 2003). molecular/genetic studies. Genes encoding the MYB-like transcription factors CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) are expressed at dawn PHOTOPERIODIC CONTROL OF (Schaffer et al., 1998; Wang and Tobin, 1998). CCA1 HYPOCOTYL ELONGATION IN and LHY proteins interact to form the morning complex, Arabidopsis which regulates the expression of genes encoding PSEUDO- RESPONSE REGULATOR (PRR) proteins (Alabadí et al., Upon seed germination, the elongation of the hypocotyl (i.e., 2001; Farré et al., 2005; Lu et al., 2009; Kamioka et al., 2016). the stem of a germinating seedling in dicotyledonous plants) In particular, CCA1-LHY repress the key element of the is one of the earliest processes affected by photoperiod. central oscillator PRR1/TIMING OF CAB EXPRESSION 1 Molecular mechanisms underlying this developmental (TOC1) at the beginning of the light period (Alabadí et al., step have been extensively studied in Arabidopsis, which 2001; Nakamichi et al., 2010; Gendron et al., 2012). Other displays short hypocotyls when grown under LDs but long PRR genes peak sequentially throughout the day: PRR9 at hypocotyls under SDs. dawn, PRR7/PRR5/PRR3 in the afternoon and TOC1 at dusk The regulation of hypocotyl growth relies on the activity (Nakamichi et al., 2005a,b). During the night, TOC1 represses of PIF4 and PIF5, two basic helix-loop-helix (bHLH) the expression of CCA1 and LHY (Alabadí et al., 2001). transcription factors which protein abundance is controlled The morning complex also represses the expression of by the photoreceptor phyB that mediates PIFs degradation genes encoding components of the evening complex such as during the day through the 26S proteasome (Huq and Quail, GIGANTEA (GI, Fowler et al., 1999; Berns et al., 2014), EARLY 2002). Several studies indicate that the hypocotyl elongates in the FLOWERING 3 (ELF3, Hicks et al., 1996; Covington et al., dark period, consistent with higher accumulation and activity of 2001) and ELF4 (Doyle et al., 2002). The evening complex PIFs before dawn (Nozue et al., 2007). suppresses PRR9, restricting its expression to the early morning Under SD, PIFs promote hypocotyl growth at the end of (Chow et al., 2012). the long night, when they form dimers and bind to regulatory In summary, light perception triggers a cascade of molecular elements of target genes involved in cell expansion and auxin events that activate circadian clock associated genes at different signaling (Khanna et al., 2004; Kunihiro et al., 2011; Hornitschek times of the day (Pokhilko et al., 2012). Also, seasonal fluctuations et al., 2012; Zhang et al., 2013). PIFs also activate CYCLING in external conditions represent the input information that DOF FACTOR 1 (CDF1) and CDF5, two transcription factors adjusts the circadian clock year-round. Thus, this mechanism belonging to the DNA-binding with One Finger (DOF) family, measures the length of the daylight (and ambient temperature) that in turn promote the expression of YUCCA8 (YUC8), an to trigger seasonal responses. Ultimately, the clockwork regulates important auxin biosynthetic gene (Martín et al., 2018). the diurnal oscillations of the transcription of many output genes Components of the circadian clock also regulate the that control several developmental and physiological processes daily oscillation in PIFs expression and PIF protein stability. underlying the adaptation of an organism – animals and plants – The Evening Complex in association with PRRs represses to a changing environment (reviewed by Nohales and Kay, 2016). PIF4/PIF5 transcription until early night (Matsushika et al., 2000; Frontiers in Plant Science | www.frontiersin.org 2 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Nakamichi et al., 2005a,b; Nusinow et al., 2011). Unlike long (e.g., 16 h light/8 h dark). The length of the day is sensed PIFs, PRRs repress the expression of CDFs during the day, in the leaf, but the floral induction takes place in the shoot apex thus preventing hypocotyl elongation in the light period (reviewed by Zeevaart, 2009). The transition to flowering involves (Martín et al., 2018). the existence of a florigen – a mobile signal that travels from the Hypocotyl elongation is also controlled by the phytohormone leaf to the Shoot Apical Meristem (SAM) through the phloem Gibberellic Acid (GA) through the degradation of DELLA (Zeevaart, 1976; Kinoshita and Richter, 2020). proteins, negative regulators of growth able to interact with Among hundreds of flowering time genes described to date PIFs. During the light period, DELLA protein levels are high (Kinoshita and Richter, 2020), CONSTANS (CO) is one of and sequester PIFs: the formation of inactive complexes hinders the most studied regulators acting in photoperiodic flowering. PIF binding to target genes. During the dark period, GA The expression of the CO gene oscillates with the circadian accumulation triggers DELLA degradation, allowing the release rhythm and is activated in the leaf upon LD perception (Putterill of PIFs. Thus, PIFs accumulate in the nucleus at night and et al., 1995; Suárez-López et al., 2001). CO is only capable to activate downstream genes involved in hypocotyl growth before promote flowering under LD, when the peak of CO mRNA dawn (Davière et al., 2008; De Lucas et al., 2008; Feng et al., 2008). expression occurring at the end of the daytime coincides with the stabilization of CO protein mediated by light (Suárez-López et al., 2001; Valverde et al., 2004). PHOTOPERIODIC CONTROL OF Several circadian clock-associated proteins, previously described as regulators of hypocotyl growth, were also found to SEASONAL FLOWERING IN ANNUAL control CO at transcriptional or post-translational level. PLANTS Under LDs, members of the CDF family act as floral repressors by inhibiting CO expression in the first part of the light period Besides germination and seedling establishment, the transition (Fornara et al., 2009). In particular, CDF1 negatively regulates from the vegetative to the reproductive phase represents a CO in the morning by interacting with the TOPLESS (TPL) critical step for the reproductive success of flowering plants. co-repressor (Causier et al., 2012; Goralogia et al., 2017). The Floral induction must occur at the most favorable season combination of multiple mutations in CDFs genes leads to to guarantee the highest production of seeds and survival photoperiod insensitiveness and early flowering caused by CO of the offspring. This phase change is economically relevant upregulation (Fornara et al., 2009). in seed crops as it determines grain yield, an important Conversely, PRR5/PRR7/PRR9 act as floral activators by agronomic trait. Accordingly, both precocious and delayed repressing CDF1 in the afternoon (Nakamichi et al., 2007). flowering should be avoided as they might cause yield losses. Functional PRRs promote flowering under inductive conditions Early flowering plants fail to store enough energy for seed by indirectly activating CO expression but they also contribute development due to insufficient growth of photosynthetic organs; to the accumulation of CO protein in the light period (Hayama conversely, late flowering plants are vigorous, but fertility can et al., 2017). By contrast, defective PRRs reduce photoperiodic be affected if seed maturation takes place in adverse weather sensitivity: loss of PRR function causes CO downregulation, conditions. Therefore, plants should synchronize leaf and flower which leads to late flowering under LD but not under SD (Sato development with environmental conditions to optimize the et al., 2002; Yamamoto et al., 2003; Nakamichi et al., 2005a,b, timing of the formation of reproductive organs. 2007). Multiple genetic determinants control the switch from In a similar way, the clock associated proteins GI and Flavin- vegetative to reproductive growth by integrating external cues binding Kelch repeat F box 1 (FKF1) positively regulate flowering and internal signals. Before floral transition, the plant undergoes mostly by preventing the action of repressors on CO. Actually, GI the juvenile-to-adult transition when it reaches the competence and FKF1 form a complex that mediates the ubiquitin-dependent to flower in response to inductive environmental conditions. degradation of CDF1 in the late afternoon, resulting in the Although photoperiod is one of the major environmental stimuli, transcriptional activation of CO at dusk (Imaizumi et al., 2005; others such as ambient/seasonal temperatures together with Sawa et al., 2007). endogenous conditions (e.g., plant age, accumulation of sugars, In the opposite way, ELF3 and ELF4 negatively regulate and hormones) contribute to finely tune the floral induction. flowering by forming different protein complexes that in turn Control of flowering time has been massively studied in affect the expression of genes of the core and output of Arabidopsis thaliana. Nevertheless, research conducted in many the circadian clock (nicely reviewed in Zhao et al., 2021). other species - including monocotyledonous plants - has shown Interestingly, the evening complex of the circadian clock that GRNs controlling the floral transition are mostly conserved, represses GI expression, ELF3 promotes GI degradation, and albeit with some variations that account for the peculiarities of ELF4 removes GI from the CO promoter (Yu et al., 2008; Kim the different plant species examined. et al., 2013; Ezer et al., 2017; Park et al., 2019). Photoreceptors also contribute to the regulation of flowering Photoperiodic Flowering Under Long time (Bagnall et al., 1995). PHYA stabilizes CO whereas PHYB Days in the Model Species Arabidopsis plays the opposite role (Valverde et al., 2004). PHYB also impairs Arabidopsis is a facultative LD plant, meaning that although it PIF function (Al-Sady et al., 2006; Goyal et al., 2016) that, in can bloom in SDs it flowers much more rapidly when days are addition to their role in hypocotyl elongation, have been shown Frontiers in Plant Science | www.frontiersin.org 3 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering to integrate light and temperature perceptions. PIF4, PIF5, and Negative Regulators of the Floral PIF7 promote flowering at warm ambient temperatures or in Transition in Arabidopsis response to the shade avoidance syndrome (Kumar et al., 2012; Floral repressors prevent precocious flowering and guarantee a Fernández et al., 2016; Galvāo et al., 2019; Silva et al., 2020). vegetative phase long enough to accumulate necessary energy Interestingly, PIFs are regulated by ELF3; PHYB stabilizes ELF3, reserves for flower and seed production (Boss et al., 2004). Besides and ELF3 interacts with PIF4 and PIF7 to impair the binding the CO repressors CDFs and ELFs, additional factors have been to their targets (Xing et al., 2001; Nieto et al., 2015; Jiang et al., described that directly regulate the florigens (reviewed in Yant 2019). et al., 2009; Kinoshita et al., 2020). Among others, two members CONSTANS is a B-box (BBX) Zinc Finger transcription factor of the Related to ABI3 and VP1 (RAV) family of transcription whose activity is also regulated by protein-protein interactions factors – named TEMPRANILLO1 (TEM1) and TEM2 – repress with other circadian regulated BBX proteins. For example, BBX19 flowering under different conditions (Castillejo and Pelaz, 2008; interacts with CO and depletes the active CO pool (Wang et al., Osnato et al., 2012; Marín-González et al., 2015; Aguilar-Jaramillo 2014), and BBX microProteins miP1a and miP1b likely act as et al., 2019), but in the photoperiod pathway TEM proteins bridge between CO and TPL in a repressor complex which results counteract CO activity in a quantitative balance to tightly control in the incapability of florigen activation (Graeff et al., 2016). FT expression (Castillejo and Pelaz, 2008). Also, TEMs seem to interact with TPL and TPL-related (TPR) proteins, and this The Florigen in Arabidopsis interaction may confer their repressive activity (Causier et al., CONSTANS activates the expression of the floral promoter 2012). However, further experiments are needed to assess this FLOWERING LOCUS T (FT) in leaf vascular tissue in LDs association requirement for TEM function. (Suárez-López et al., 2001; Takada and Goto, 2003; Valverde In wild-type plants, TEM expression levels are high at early et al., 2004). The fact that the constitutive expression of CO stages of vegetative growth but progressively decay to a minimum and FT confers very early flowering phenotype while their loss at the time of floral transition, thus allowing the activation of FT of function causes extremely late flowering (but only in LDs) by CO (Castillejo and Pelaz, 2008). Thus, TEM expression pattern suggested that these two genes might control the first moments suggests that the balance between TEM and CO activities might of the floral induction in response to photoperiod (Kardailsky be modulating FT transcription and consequently adjusting the et al., 1999; Kobayashi et al., 1999). Nevertheless, the activation timing of the floral transition under LD. Besides, as both CO of CO and FT happens in the leaf but not in the SAM in wild- and TEM are regulated by the circadian clock, they could be type plants. The circle was rounded when the FT protein was acting on FT at the same level but antagonistically. Supporting identified as the long-distance signaling molecule able to induce this hypothesis, an impaired balance between the activator flower development in the shoot apex (Corbesier et al., 2007; and the repressor results in an according variation of the FT Jaeger and Wigge, 2007; Mathieu et al., 2007). transcripts levels and alterations of flowering time. In transgenic The FT gene encodes a small globular protein belonging to plants growing in LD, accumulation of the floral activator CO the Phosphatidyl Ethanolamine Binding Protein (PEBP) family (in overexpression/gain of function lines) has the same effect (Kardailsky et al., 1999; Kobayashi et al., 1999). As FT is not on flowering as the removal of the floral repressors TEM (in itself able to bind DNA, it interacts with FD, a bZIP transcription loss of function mutants), obtaining a precocious flowering factor present at the SAM (Abe et al., 2005; Wigge et al., 2005), phenotype. In the same way, plants with reduced levels of both and this association is mediated by 14-3-3 proteins (Abe et al., CO and TEM flower at the same time as wild type plants 2019; Collani et al., 2019). The formed regulatory complex - also (Castillejo and Pelaz, 2008). known as Florigen Activation Complex (FAC) – first activates CONSTANS physically associates with NUCLEAR FACTOR Y SUPPRESSOR OF OVEREXPRESSION OF CO 1 (SOC1) and (NF-Y) proteins, which bind CCAAT sequences present in the FT APETALA1 (AP1), two genes of the MADS-box family involved promoter. This binding results in a chromatin loop that brings in floral meristem identity, by directly binding their promoters enhancers present in distal elements close to two CO Responsive (Simon et al., 1996; Samach et al., 2000; Moon et al., 2005; Yoo Elements (CORE1 and 2) found near the transcription start site et al., 2005). Similar to FT, the closely related gene TWIN SISTER of FT (Adrian et al., 2010; Tiwari et al., 2010). NF-Y proteins OF FT (TSF) is activated by CO and the encoded protein acts as help recruitment of CO to regulatory sequences in proximal a long-range signal traveling to the SAM where it also interacts elements that are essential to activate the transcription of FT with FD (Samach et al., 2000; Yamaguchi et al., 2005; Jang et al., (Cao et al., 2014). Strikingly, TEM proteins recognize a RAV 2009). binding site located in the 50 UTR of FT, very close to the Bioactive GAs act as another signal that affects flowering under CORE elements bound by CO (Castillejo and Pelaz, 2008; Cao LDs, but it is under non-inductive SDs that they play a more et al., 2014). This may account for the proposed TEM/CO evident role in floral induction (Mutasa-Göttgens and Hedden, competition for the FT binding sites. Alternatively, TEM binding 2009) when CO is almost completely inactive. DELLAs inhibit may affect the FT chromatin loop and therefore interfere with its the action of floral activators through protein interactions, thus transcriptional activation. affecting transcriptional activation of the floral integrators (FT, Circadian clock output pathway that promotes photoperiod- TSF, and SOC1) and consequently flowering time under both LDs dependent flowering comprises the antagonistic CO and TEM and SDs (Wang et al., 2016; Xu et al., 2016). activities (Castillejo and Pelaz, 2008). Hence, FT levels are the Frontiers in Plant Science | www.frontiersin.org 4 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering result of a quantitative balance between the respective promoter (Wu et al., 2009) and the floral induction in leaves (Aukerman and repressive activities in the leaf. Nevertheless, TEM genes are and Sakai, 2003; Jung et al., 2007; Mathieu et al., 2009). also expressed in the SAM and their specific downregulation in The synthesis of mature miR172 relies on five MIR172 genes the shoot apex results in early flowering phenotype, suggesting (A to E), recently shown to play common and divergent roles that FT is also repressed in this domain (Osnato et al., 2012). under different conditions (Lian et al., 2021; Ó’Maoiléidigh et al., Intriguingly, the FT repressive function of CO-miP1a7b-TPL 2021). Specifically, MIR172A/B/D also act in the SAM to control mentioned above (Graeff et al., 2016) seems to be limited to the the floral transition under SDs (Ó’Maoiléidigh et al., 2021) and SAM (Rodrigues et al., 2021). Therefore, FT could be actively MIR172A/D under LDs (Lian et al., 2021). repressed at the SAM to avoid floral transition before LDs have miR172 abundance is negatively regulated by the floral been sensed in leaves. repressors SVP and TEM. SVP represses miR172 via direct The diurnally regulated MADS-domain protein SHORT binding to pri-miR172a (Cho et al., 2012) whereas TEM1 binds a VEGETATIVE PHASE (SVP) is another important floral regulatory region of the MIR172C gene. In addition to MIR172C, repressor (Hartmann et al., 2000; Fujiwara et al., 2008; Jang MIR172A and MIR172B are also downregulated in tem double et al., 2009). At low temperatures, SVP represses FT indirectly mutants (Aguilar-Jaramillo et al., 2019). through activation of TEM2 (Marín-González et al., 2015) Conversely, miR172 expression is promoted by GI (Jung et al., as well as directly through interaction with two related 2007), showing that GI regulates flowering time also by affecting MADS-domain proteins – FLOWERING LOCUS C (FLC) and miR172 expression. FLOWERING LOCUS M (FLM). Because floral induction is key for plants species survival, the FLOWERING LOCUS T repression is mediated by SVP-FLC regulatory sequences of genes encoding key floral activators (CO, during the vernalization process (Li et al., 2008; Mateos et al., FT/TSF) have been subjected to natural variation in order to 2015) and by SVP- FLM in response to changes in ambient adapt to the environment (Liu et al., 2014; Rosas et al., 2014; Bao temperature (Lee et al., 2013; Posé et al., 2013). Interestingly, et al., 2019). the FLM is subjected to alternative RNA splicing that generates two splice forms depending on the external conditions: plants growing in cooler environments accumulate FLMβ, a protein Flowering Time Genes and Stomata variant that contains the DNA binding domain; plants growing Functioning in Arabidopsis in warmer environments accumulate FLMδ, a protein variant Stomata are specialized cell structures that control gas exchange that lacks the DNA binding domain. As a result, the SVP- FLMβ (carbon dioxide in, oxygen out) needed for photosynthesis complex delays the floral transition at low ambient temperature (Shimazaki et al., 2007). Stomata are present in several plant by directly repressing FT; by contrast, the SVP- FLMδ complex organs (e.g., leaves, stems, reproductive structures) and are fails to bind FT regulatory regions, thus accelerating flowering at composed of two guard cells, whose changes in shape determine elevated ambient temperature (Lee et al., 2013; Posé et al., 2013). the size of the pore and consequently the rate of gas exchange. Instead, loss of function mutations in SVP result in early Light and circadian clock control stomata movements. On flowering and reduced sensitivity to photoperiod or ambient the one hand, stomata open in the morning in response to blue temperature (Jeong et al., 2007). light and close at the end of the day (Kinoshita, 1999; Kinoshita The function of the floral repressors TEM and SVP could et al., 2001). On the other hand, stomata functioning is under the be prevented by the interaction with the floral activator GI, influence of outputs of the circadian clock, which regulate the found to bind sequences of the FT promoter in proximity of activity of a proton pump (H+ -ATPase) that generates osmotic SVP and TEM binding sites (Sawa and Kay, 2011). Besides pressure in the guard cells: stomata open when guard cells swell CO activation, GI might promote flowering also by impeding due to water intake and close when guard cells shrink due to accessibility of floral repressors to FT regulatory regions water loss. Mutations in genes associated with the circadian clock and/or by perturbing their repressive activity through physical (such as CCA1) affect stomata opening/closing cycle, making loss association (Sawa and Kay, 2011). of function mutants unable to anticipate the day/night changes SHORT VEGETATIVE PHASE and TEMs also control (Hassidim et al., 2017). flowering time by negatively regulating GA biosynthetic genes: Plants grown under LDs present a higher stomatal SVP represses GA20OXIDASE2 (GA20OX2) (Andrés et al., 2014) conductance than those grown under SDs, and this difference while TEM1 directly represses GA3OXIDASE1 (GA3OX1) and remains for a week after changing the conditions from LD to SD GA3OX2 (Osnato et al., 2012). (Aoki et al., 2019). Recently, some factors of the photoperiod Other key regulators of the photoperiod pathway are pathway involved in the control of the floral transition were APETALA2 (AP2) and AP2-related proteins – SCHLAFMUTZE also shown to regulate stomata functioning, including the (SMZ), SCHNARCHZAPFEN (SNZ) and TARGET OF EARLY florigen. For example, FT has a non-cell autonomous function in ACTIVATION TAGGED 1 (TOE1), TOE2, and TOE3 – that flowering time when expressed in leaf vasculature (see previous negatively regulate the floral transition by interacting with TPL section on the mobile florigen) but also a novel cell-autonomous (Aukerman and Sakai, 2003; Schmid et al., 2003; Jung et al., role in stomatal opening when expressed in leaf guard cells, 2007; Mathieu et al., 2009; Yant et al., 2010). The expression of where it promotes H+ -ATPase activity (Kinoshita et al., 2011). these AP2-like genes is regulated by microRNA172 (miR172), Moreover, there is a direct correlation between FT levels and which independently controls the juvenile to adult transition the light-induced stomatal opening, being wider when plants Frontiers in Plant Science | www.frontiersin.org 5 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering grow under LDs than under SDs (Kinoshita et al., 2011). TWIN characterized in Arabidopsis. These regulatory proteins can be SISTER OF FT (TSF), the close homolog of FT, not only promotes divided into three main families: COL (CO-like), also having flowering redundantly with FT, but also stomata opening, as one or two Zinc Finger BBX at the N-terminus; PRR, also mutations in TSF impair stomatal responses (Ando et al., 2013). having a pseudo receiver domain at the N-terminus; CMF (CCT Together with the florigens, the floral activators GI and CO Motif Family), only having a CCT domain at the C-terminus are also involved in stomata functioning: while mutations in GI- (reviewed in Li and Xu, 2017). While members of the COL and CO-FT/TSF suppress stomatal opening induced by light, their PRR families have been identified in both monocot and dicot overexpression rescues the closed stomata phenotype of mutants species, comparative and phylogenetic analyses of CCT proteins defective in the blue light receptors phototropins (Kinoshita in grasses suggested that the monocot-specific CMF group likely et al., 2011; Ando et al., 2013). Likewise, photoperiod is able to derived from common ancestors of the COL group after the change the epigenetic regulation of SOC1 (Aoki et al., 2019) and monocot-dicot divergence (Cockram et al., 2012). the overexpression of the floral integrator SOC1 in guard cells Here, we review strategies underlying flowering time in promote stomata opening (Kimura et al., 2015). important cereal crops, with a particular focus on the regulatory Conversely, ELF3 – a circadian clock associated protein that role of species-specific CCT-domain containing proteins acting represses floral activators – negatively regulate stomata opening: upstream of the conserved florigen. the elf3 mutants exhibit a permanently open stomata phenotype under continuous light. Thus, the circadian rhythm on the stomatal opening regulation may depend at least partially on Photoperiodic Flowering in Cereals of ELF3 regulation of FT (Kinoshita et al., 2011). Tropical Origin From a physiological point of view, the control of stomatal The two most cultivated cereal crops worldwide, maize (Zea movements mediated by key regulators of the photoperiodic mays) and Asian rice (Oryza sativa), derive from wild species pathway may be beneficial for plants undergoing the floral grown more than 9000 years ago in tropical and subtropical transition in suboptimal conditions. When grown under regions. Precisely, maize was domesticated from Zea mays water limitation, adult plants might activate the so-called ssp. parviglumis (also known as Teosinte) in central Mexico drought escape, which consists of early flowering and (Matsuoka et al., 2002; Yang et al., 2019) whereas Asian rice was accelerated metabolism: open stomata result in increased domesticated from Oryza rufipogon in the Yangtze River basin in gas exchange and photosynthetic activity (Shavrukov et al., China (Purugganan, 2014). 2017) to provide more nutrients and energy for the anticipated In both regions, wild ancestors behaved as SD plants, meaning reproductive development. that flowering is promoted in response to a photoperiod of 12 h light/12 h dark or below this critical daylength. Through centuries of cultivation, maize and rice spread to higher latitudes thanks to CONSERVATION AND DIVERSIFICATION the artificial selection of mutant plants that acquired the ability to OF FLOWERING TIME GENES IN flower when daytime is above 12 h of light. It follows that natural CEREAL CROPS variation in photoperiodic response has allowed the expansion of cereals of tropical origin to temperate regions characterized by a In the last decades, independent groups demonstrated that single LD growing season. Which is the molecular basis of this members of the PEBP family showing high similarities with the adaptation? Arabidopsis FT trigger flowering in different plant species (some Unlike the Arabidopsis CO, the rice homolog of CO – called reviews: Andrés and Coupland, 2012; Wickland and Hanzawa, Heading date 1 (Hd1) – promotes flowering under inductive 2015; Khosa et al., 2021), reinforcing the idea of the existence SDs but delays it under LDs (Yano et al., 2000; Izawa et al., of a universal florigen. For instance, the FT orthologs in the 2002; Kojima et al., 2002). In non-inductive conditions, Hd1 most cultivated cereal crops studied so far have been mapped to protein interacts with Grain number plant height and heading the Heading date 3a (Hd3a) locus in rice (Tamaki et al., 2007), date 7 (Ghd7), a floral repressor belonging to the CMF family DAYS TO ANTHESIS 8 (DTA8) locus corresponding to ZEA that is active when the daylength exceeds 13.5 h light (Xue CENTRORADIALIS 8 (ZCN8) in maize (Danilevskaya et al., et al., 2008; Itoh et al., 2010; Nemoto et al., 2016). Ghd7 delays 2011; Lazakis et al., 2011; Meng et al., 2011; Guo et al., 2018), the reproductive phase under LDs by repressing Early heading VERNALIZATION 3 (VRN3) loci corresponding to HvFT1 and date 1 (Ehd1), which encodes a B-type response regulator that TaFT in barley and wheat (Yan et al., 2006; Faure et al., 2007; activates the florigen in the leaf (Doi et al., 2004; Itoh et al., Kikuchi et al., 2009). 2010). Ghd7 also regulates overall plant growth and grain yield: Despite the conserved function of FT-like proteins, cereals a prolonged vegetative phase under LD correlates with increased have evolved species-specific molecular mechanisms that plant biomass and seed production (Xue et al., 2008). Likewise, regulate plant response to photoperiod and modulate time the PRR-like protein Days to heading 7 (DTH7/OsPRR37) also to flowering (also termed heading date in rice, barley and delays the floral transition under LD by repressing the floral wheat). To date, major factors found to control circadian activator Ehd1, leading to increased plant height and grain rhythms and photoperiodic flowering in cereals contain the CCT production (Gao et al., 2014). domain – a conserved sequence of 41–43 amino acids named Like the Arabidopsis CO, Hd1 physically associates with after CONSTANS, CO-like, and TOC1 proteins previously rice NF-Y proteins: the formation of heterotrimeric complexes Frontiers in Plant Science | www.frontiersin.org 6 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering containing NF-YB and NF-YC subunits is instrumental for circadian clock associated protein similar to Arabidopsis PRR7 binding to specific regulatory sequences of the downstream target that positively regulates the florigen HvFT1 under LDs (Turner gene Hd3a (Goretti et al., 2017; Shen et al., 2020). Intriguingly, et al., 2005). Upon floral induction, Ppd-H1 also accelerates OsPRR37 also seems to interact with heterodimers formed by early and late phases of reproductive growth by activating floral NF-YB and NF-YC (Goretti et al., 2017). Thus, NF-Y proteins homeotic genes (Digel et al., 2015). play key roles for the correct functioning of the rice CCT-type Genetic variation at Ppd-H1 associate with phenotypic regulators, which control important traits related to agronomic variation in the timing of reproductive development. Precisely, performance by negatively regulating heading date under LD. many recessive alleles contain Single Nucleotide Polymorphisms It’s important to highlight that genetic variation at loci (SNPs) responsible for amino acid changes in conserved domains encoding major floral repressors underlies phenotypic variation that impair Ppd-H1 protein function, including the SNP79 in photoperiod responsiveness of varieties adapted to temperate (G- > T, described by Turner et al., 2005). Varieties carrying regions. In fact, rice accessions cultivated in Europe harbor loss functional Ppd-H1 alleles (G at position 79) differentially express of function mutations in Hd1/ Gh7/OsPRR37 that fail to repress HvFT1 in response to daylength, leading to accelerated flowering the floral transition under LDs (Gómez-Ariza et al., 2015; Goretti under LD but delayed flowering under SD (Turner et al., et al., 2017). 2005). Conversely, varieties carrying defective ppd-H1 alleles Recent findings further support the conserved function of (G- > T SNP79) flower late even when grown under LD, CCT-type floral repressors in maize. Indeed, ZmCTT9 and because of reduced expression of CO-like genes and HvFT1 ZmCCT10 – the maize orthologs of Ghd7 – map to DAYS (Turner et al., 2005). TO ANTHESIS 9 (DTA9) and DTA10 loci, two of the most In European barley accessions, the frequency of two alleles important QTLs controlling flowering time in this cereal crop at SNP48 (C- > T, described by Jones et al., 2008) correlates (Guo et al., 2018). Over time, the accumulation of polymorphisms with clinal variation in flowering phenotype. Specifically, the in key DTA loci, caused by intense transposon activity, has functional Ppd-H1 allele (C at position 48) predominates in determined alterations of photoperiod sensitivity in selected Southern Europe, characterized by a short growing season; in maize cultivars. Specifically, maize accessions cultivated in these regions, cultivars accelerate flower development in spring Northern and Southern America carry defective alleles of and seeds reach maturity before terminal drought in summer. ZmCTT9 and ZmCCT10, which correlate with activation of the By contrast, the non-functional ppd-H1 allele (C- > T SNP48) florigen ZCN8 and consequently accelerated flowering under LD predominates at Northern latitudes, characterized by a long (Yang et al., 2013; Huang et al., 2017; Guo et al., 2018). growing season; in these regions, accessions with prolonged To sum up, the selection of genetic variants with reduced vegetative phase also show increased biomass accumulation and activity of LD floral repressors has allowed the expansion of rice higher grain yield at harvesting. Thus, polymorphisms at Ppd- and maize cultivation outside tropical and subtropical regions, to H1 underly adaptation to different environmental conditions and a wider range of growing areas at higher latitudes and daylength largely explain latitude-dependent geographical distribution of above 12 h of light (Figure 1). barley varieties, at least in Europe. In the hexaploidy genome of wheat, three orthologs of the barley Ppd-H1 (Ppd-A1, Ppd-B1, and Ppd-D1) were identified Photoperiodic Flowering in Temperate and Ppd-D1 shown to have the greatest contribution to the Cereals regulation of flowering (Guo et al., 2010; Würschum et al., 2018). Barley (Hordeum vulgare) and wheat (Triticum aestivum), the A semi-dominant mutation caused by a 2 kb deletion in the founders of agriculture in the old world, derive from wild promoter region of Ppd-D1 converts a LD plant into a day neutral ancestors grown 10,000 years ago in the middle east (discussed plant by altering the diurnal expression pattern of Ppd-D1. Under by Haas et al., 2019). Over the centuries, the cultivation of these SD, the peak of Ppd-D1 transcription shifts from the light to dark grain crops had expanded from the Fertile Crescent (Latitude N phase, causing induction of the florigen TaFT1 and promotion of 38) to temperate regions in Europe and Asia with similar latitude, flowering regardless of daylength (Beales et al., 2007). Additional mainly across the East-West axis, in which cold winter is followed polymorphisms in the regulatory sequences of Ppd-D1 were by warm LDs and hot summer is followed by cool SDs. identified in a panel of 500 common wheat varieties cultivated Temperate cereals behave as quantitative LD plants, meaning worldwide (Guo et al., 2010). To a large extent, accessions with that flowering is delayed when days are short but promoted higher Ppd-D1 expression (under LD) flower earlier than those when days become longer. Specifically, floral induction occurs with lower Ppd-D1 expression. Similar to barley, photoperiod in spring when plants reach a threshold determined by a certain sensitive accessions delay flowering under SD while photoperiod number of LDs. However, seasonal changes in the photoperiod insensitive varieties initiate the reproductive phase regardless of do not directly affect the timing of the floral transition, which daylength (Guo et al., 2010). is under the influence of vernalization, but rather the initiation To recap, PRR proteins promote flowering under LD in of reproductive structures at the shoot apex in barley and wheat temperate cereals. Mutations in the coding sequence of Ppd-H1 (reviewed by Hyles et al., 2020). largely explain alterations in the timing of flower development Modern winter varieties of barley are sown in autumn and in barley, whereas mutations at regulatory regions of Ppd-D1 usually accelerate flowering in spring (Turner et al., 2005). This gene contribute to variation in the photoperiodic responsiveness response is mediated by Photoperiod-H1 (Ppd-H1), a barley in wheat. Together with vernalization requirements, changes in Frontiers in Plant Science | www.frontiersin.org 7 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering FIGURE 1 | Adaptation of cereal growth to different latitudes. Maps showing the expansion of maize (left) and rice (right) cultivation outside their region of origin. The selection of mutation in genes encoding CCT-type floral repressors that alter photoperiodic response allowed activation of the florigen under non inductive LDs. the activity of Ppd proteins have determined the adaptation of belonging to the Populus genus, which have also served as models temperate cereals to different geographic regions, thus allowing to investigate the function of putative orthologs of Arabidopsis their cultivation in a wide range of agroecosystems. flowering time regulators. In Populus trichocarpa (California poplar), two FT-like genes have been identified: PtFT1 and PtFT2 (Böhlenius et al., 2006; PHOTOPERIODIC CONTROL OF Hsu et al., 2006). Their transcripts accumulate in different SEASONAL GROWTH IN PERENNIAL domains and seasons: the former in stem and apical buds in late PLANTS winter, the latter in leaves in late spring-early summer (Böhlenius et al., 2006; Hsu et al., 2006, 2011). In contrast to annual herbaceous plants that complete their life Although constitutive expression of each of the two FT cycle and die within a single year, perennial plants can live for paralogs caused early flowering in transgenic poplars (Böhlenius several growing seasons - continuously in warm climates and et al., 2006; Hsu et al., 2006), inducible expression of FT1 discontinuously in temperate climates. and FT2 (driven by Heat shock promoter) resulted in different Photoperiodic cues and changes in ambient temperature phenotypes, pointing to a possible sub-functionalization of FT- greatly influence the seasonal behavior of tree populations like genes (Hsu et al., 2011). Indeed, transient induction of growing in temperate regions (Wareing, 1956). Indeed, woody FT1 (but not FT2) under SD at low temperature promotes the perennials display active growth in response to lengthening days formation of reproductive structures within 1 month from the in spring but growth cessation in response to shortening days at heat treatment (Hsu et al., 2011). By contrast, transient induction the end of the summer. Below a critical photoperiod in autumn, of FT2 (but not FT1) promotes vegetative growth under LD and the apical buds formed enter a dormant state (completed in 2– inhibits growth cessation under SD. These findings indicate that 3 months) to withstand very low temperatures and reduced light FT1 activation in winter is required for the onset of reproductive in winter (Garner and Allard, 1923). Generally, trees pause their structures whereas FT2 activation in spring promotes vegetative vegetative growth in the cold season but resume it the next spring growth (Hsu et al., 2011). (Garner and Allard, 1923). Moreover, FT2 suppression in autumn mediates growth In woody perennials, the production of flower buds can take cessation in response to environmental limitations (Hsu et al., several years as plants have to undergo the transition from the 2011). Actually, the critical daylength required to induce growth juvenile to the adult phase to acquire the competence to form cessation is longer in trees growing at northern latitudes reproductive structures. Following first-time flowering, trees compared to those at southern latitudes, implying that alterations flower every year throughout their life span. Thus, the perennial in photoperiodic response might have determined adaptation of growth habit consists of annual cycles of growth and dormancy as tree populations to different environments (Frewen et al., 2000; well as annual cycles of vegetative and reproductive development, Böhlenius et al., 2006). depending on the season. Supporting the sub-functionalization of the two FT paralogs Surprisingly, annuals and perennials share similar molecular in poplar, large scale expression analysis of transgenic mechanisms underlying photoperiod response, despite the plants mis expressing FT-like genes revealed differences substantial differences in their life history traits. So far, most in the molecular networks controlled by FT1 and FT2: of the studies aimed at unraveling the photoperiodic control while genes involved in reproductive development act of seasonal growth in trees have been conducted in species downstream of FT1 at winter onset, genes involved in Frontiers in Plant Science | www.frontiersin.org 8 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering vegetative growth and stress response act downstream of Gene expression analyses in wild-type spruce showed that FT2 (Hsu et al., 2011). PaFTL1 mRNA accumulates after the winter in male reproductive To summarize, the differential expression of FT paralogs in structures whereas PaFTL2 mRNA accumulates in shoots in contrasting seasons (FT1 in late winter, FT2 in mid spring) response to decreasing daylength, coinciding with growth reinforces a diverged regulatory function in annual cycles of cessation and bud set (Gyllenstrand et al., 2007; Karlgren vegetative and reproductive growth (Hsu et al., 2011). In et al., 2011; Klintenäs et al., 2012). Interestingly, overexpression woody perennials, FT-like proteins appear to integrate key of PaFTL1 do not cause morphogenetic effects in transgenic environmental signals (photoperiod and ambient temperature) to spruce, whereas constitutive expression of PaFTL2 in tissue promote seasonal growth under warm LD in spring but increase cultures caused growth arrest and death within 6 months survival (via dormancy) under cold SD in winter. (Klintenäs et al., 2012). Factors showing similarity to components of the Additional genetic and physiologic studies revealed that Arabidopsis photoperiodic pathway seem to have a conserved (latitudinal) clinal variation in the photoperiodic control of function in trees. growth cessation associates with genetic variation in PaFTL2 Downstream of FT-like proteins, poplar FD Like 1 (FDL1) promoter and one variant of the PaGI protein in Norway spruce and Like AP1 (LAP1) genes also show continuous upregulation as well as Siberian spruce (Chen et al., 2012, 2014). during bud development (Ruttink et al., 2007). Under LD, FT2, To conclude, FT/TFL1-like proteins might have retained and FDL1 promote vegetative growth in spring by activating a general function as growth regulators in gymnosperm and LAP1. As days become shorter, the downregulation of these genes acquired a specific function as flowering time regulators in allows growth cessation (Böhlenius et al., 2006; Hsu et al., 2006; angiosperms. The knowledge about these mechanisms will be Ruttink et al., 2007). very useful in the years to come. With shifting seasons and Upstream of FT-like proteins, two paralogs of GI have been climate conditions, new breeding programs need to be launched identified in the hybrid P. tremula × P. tremuloides and shown to develop species adapted to changing conditions and to keep up to play a critical role in the regulation of seasonal growth (Ding with the increasing demand on forest resources. et al., 2018). Silencing lines downregulating both PttGI and PttGIL initiate growth cessation and formation of apical buds even under LDs, and these processes occurred within 1 week PHOTOPERIODIC CONTROL OF in plants shifted from LD to SD, indicating a hypersensitive GROWTH ABOVE AND BELOW GROUND response to photoperiod (Ding et al., 2018). Conversely, plants overexpressing PttGI and PttGIL initiate growth cessation at least In addition to flowering in annual plants and growth habit 1 month after the shortening of daylength, indicating a decreased in perennial plants, photoperiod also controls vegetative sensitivity to photoperiod (Ding et al., 2018). In these transgenic propagation in relevant food plants such as potato (Solanum plants, alterations of the critical daylength that induces growth tuberosum), the most important non-cereal crop for direct cessation and bud set correlate with mis regulation of PttFT2, human consumption, and strawberry (Fragaria x ananassa), which is downregulated in GI silencing lines and upregulated in one of the most widely consumed berry crops in the world. GI overexpression lines (Ding et al., 2018). In commercial plant varieties, asexual reproduction through Additional molecular and biochemical analyses revealed that vegetative structures represents an essential propagation strategy PttGIs positively regulate PttFT2 by directly binding its promoter, that allows producing identical daughter plants that keep the likely by forming complexes with FKF1-like and CDF-like desirable characteristics of the mother plant. proteins (Ding et al., 2018). Thus, GI-like proteins in Populus trees act as strong transcriptional activators of FT, largely Flowering Versus Tuberization in Potato independently of CO-like proteins. Potato (Solanum tuberosum) is the fourth most cultivated The effect of photoperiod on seasonal growth has also been food plant globally after maize, rice and wheat (FAO 20191 ). studied in other perennials. In the non-woody perennial leafy Its domestication from wild Solanum species started 8,000– spurge (Euphorbia esula L.), crown buds (i.e., adventitious buds 10,000 years ago in the Andean highlands, an arid region 3,000– located on the underground stem) show downregulation of a FT- 4,500 m above sea level characterized by cold temperatures, saline like gene and induction of DORMANCY ASSOCIATED MADS- soils, and high solar radiation (Zimmerer, 1998; Spooner et al., BOX (DAM) genes (Horvath et al., 2008), which share similarities 2005; Sukhotu and Hosaka, 2006). with the Arabidopsis SVP. DAMs play key regulatory roles in the Diploid landraces (2n = 24) underwent autopolyploidization maintenance of dormancy in Euphorbia and might be acting as and gave origin to the cultivated tetraploids (2n = 48) belonging repressor of the FT-like gene (Horvath et al., 2008). to the Solanum tuberosum group Andigena (Hardigan et al., 2017; Photoperiod controls seasonal growth in angiosperms as well Gutaker et al., 2019). Later, the cultivation of potato expanded as in gymnosperms (Heide, 1974). Several studies done in the to highland equatorial regions and to southern latitudes. In conifer Picea abies (Norway spruce) uncovered the presence of Argentina and Chile, Solanum tuberosum group Chilotanum two genes encoding PEBP proteins that share similarities with diversified from its upland progenitors to adapt to LD conditions the Arabidopsis florigen FT and the anti-florigen TERMINAL (Ghislain et al., 2009). Together with wild species, these landraces FLOWER 1 (TFL1, Shannon and Meeks-Wagner, 1991), and so renamed PaFTLs (Karlgren et al., 2011). 1 http://www.fao.org/faostat Frontiers in Plant Science | www.frontiersin.org 9 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering have substantially contributed to the development of modern Indeed, StSP6A silencing lines display decreased tuberization varieties (known as Neo-tuberosum, 2n = 48) that are grown but increased flower bud development when grown under SDs globally in a wide environmental range (Hardigan et al., 2017). (Plantenga et al., 2019). The high heterozygosity of the potato genome, which resulted As photoperiod controls tuber initiation, several groups have from wild species introgression and polyploidy, has hampered explored the possible role of homologs of Arabidopsis flowering classical genetic studies, and favored vegetative propagation time regulators in this process. through tubers, storage organs growing in the soil that also Among the three CO-like genes (StCOL1/StCOL2/StCOL3, bear vegetative buds for the following season. Potato plants located in tandem array on chromosome 2) identified in can use asexual reproduction via tuberization as well as sexual the potato genome (Abelenda et al., 2016; Ramírez Gonzales reproduction through flowering. Nevertheless, tuber initiation et al., 2021), StCOL1 displays the highest transcription in and flower development seem to be antagonistic processes leaves and preferential accumulation under LDs when the (Plantenga et al., 2019). peak of expression coincides with light (Navarro et al., 2011; In potato, photoperiod controls the formation of vegetative Abelenda et al., 2016; Ramírez Gonzales et al., 2021). StCOL1 structures that differentiate from underground stems called downregulation in transgenic RNAi lines accelerated tuberization stolons (Batutis and Ewing, 1982), which form new shoots (González-Schain et al., 2012) and the constitutive expression above ground under LDs but form tubers below ground of Arabidopsis CO in Andigena potato resulted in delayed under SDs. Once formed, dormancy of the apical meristem is tuberization under SD (Martínez-García et al., 2002). Taken induced before winter. together, these findings indicate that CO functions as suppressor The considerable genetic variation in potato accessions, a of stolon-to-tuber transition in potato, likely by repressing the result of centuries of domestication and diversification (Hardigan tuberigen under non-inductive daylengths. et al., 2017; Li Y. et al., 2018), has led to a large phenotypic Detailed expression analysis of FT-like genes (Abelenda variation in responsiveness to photoperiod. Indeed, tuberization et al., 2014) in StCOL1 silencing lines revealed upregulation is promoted by SDs in all species but this process can also of the tuber-inducing StSP6A but down-regulation of StSP5G, occur under LDs in modern varieties (Rodríguez-Falcón et al., which is normally highly expressed in leaves under LDs but 2006). For example, in the obligate SD varieties of the Andigena decays under SDs (Navarro et al., 2011). Additional molecular group, tuberization is induced under 12 h light/12 h dark but studies demonstrated that StCOL1 directly activates StSP5G is completely abolished above this critical daylength (reviewed under LDs by binding to a conserved TGTGGT DNA motif by Jackson, 1999). By contrast, selected varieties growing in (similar to the CORE bound by AtCO) in its regulatory temperate regions trigger the transition from stolon to tuber regions. Upon activation, StSP5G represses tuberization under under LDs. Thus, alteration of photoperiodic response represents non-inductive conditions by negatively regulating StSP6A a key adaptive trait also in potato (Morris et al., 2014). transcription. Thus, the two FT paralogues StSP6A and StSP5G The link between potato tuberization and daylength was act antagonistically during tuber formation in potato. As described almost a century ago (Garner and Allard, 1923) but the supporting evidence, RNAi lines downregulating StSP5G showed main tuber-inducing molecule was characterized only 10 years StSP6A upregulation in leaves and accelerated tuberization under ago (Navarro et al., 2011). The so-called tuberigen is encoded by LD (Abelenda et al., 2016). SELF PRUNING 6A (StSP6A), named after the tomato florigen Another crucial factor involved in the regulation of SELF-PRUNING (homolog of FT). tuberization is StCDF1 (Kloosterman et al., 2013), the homolog Although three additional FT-like genes (StSP5G, StSP5G- of the CO repressors AtCDFs (Fornara et al., 2009). Allelic like, and StSP3A) were identified in the potato genome (Xu variation at StCDF1 underlies a major QTL controlling yield et al., 2011), only StSP6A showed expression in leaves that and other traits related to maturity – such as the duration correlated with tuber formation at the stolon tip in SDs (Navarro of the plant life cycle, the onset of senescence, and timing of et al., 2011). Since StSP6A is also transcribed in stolons, a relay tuber induction under LDs (Kloosterman et al., 2013). Very late mechanism could regulate StSP6A expression and sustain the maturing genotypes harbor functional StCDF1 alleles encoding production of the tuberigen in stolons (Navarro et al., 2011). full length proteins, whereas very early maturing genotypes Several lines of evidence suggest that StSP6A functions as harbor defective StCDF1 alleles (caused by the insertion of the main tuberization signal that travels from the leaves to the transposable elements in the 30 end of the gene) that encode target meristem (i.e., the tip of the stolon below ground) whereas deleted versions lacking part of the C-terminus (Kloosterman the related StSP3D as regulator of flowering (Navarro et al., et al., 2013). In Arabidopsis, the C-term domain is essential 2011). Supporting their distinct roles, transgenic potato plants for interaction with the GI-FKF1 complex that mediates CDFs overexpressing StSP6A form tubers even under non-inductive degradation (Imaizumi et al., 2005; Sawa et al., 2007). Protein- LDs while StSP3D silencing lines flower late but do not display protein interaction studies confirmed that the full length StCDF1 alterations in tuber formation (Navarro et al., 2011). (encoded by late alleles) physically associates with StGI1 and It was originally hypothesized that tuberization could impair StFKF1, while truncated StCDF1 (encoded by early alleles) fails flowering by serving as sink for photosynthates. However, to associate with its regulators and evades StFKF1-mediated a recent study reported that it is the activity of StSP6A ubiquitination. Thus, the circadian clock proteins StGI and that promotes tuber formation below ground but inhibits StFKF1 control the accumulation of StCDF1 by binding its flower development above ground (Plantenga et al., 2019). C-terminus: while full length StCDF1 displays a peak of protein Frontiers in Plant Science | www.frontiersin.org 10 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering (Xu et al., 1998; Jackson et al., 2000; Kloosterman et al., 2007; Bou-Torrent et al., 2011). Phytochromes are also involved in the photoperiodic control of tuberization. Among the five phytochrome genes identified in the potato genome, StPHYB and StPHYF play the most prominent role in the inhibition of tuberization in response to LDs (Jackson and Prat, 1996; Jackson et al., 1998; Zhou et al., 2019). In fact, silencing of StPHYB or StPHYF caused tuberization in LD in a graft-transmissible manner (Jackson and Prat, 1996; Jackson et al., 1998; Zhou et al., 2019). StPHYB and StPHYF might interact to form heterodimer and stabilize the StCOL1 protein (Abelenda et al., 2016; Zhou et al., 2019). The homeodomain protein StBEL5 is another crucial transcription factor involved in the regulation of tuber formation: StBEL5 overexpression promotes tuberization FIGURE 2 | Regulatory mechanism underlying tuber formation in potato. under LDs (Banerjee et al., 2007), whereas StBEL5 silencing Right, components of the genetic pathway controlling tuberization. The reduces tuberization (Sharma et al., 2016). Although StBEL5 tuberigen StSP6 is indirectly activated by StCDF1 and repressed by StCOL1 expression itself does not seem to be affected by photoperiod through StSP5G. (Chatterjee et al., 2007), SDs result in increased StBEL5 transcript levels and facilitated movement of its mRNA from leaves to stolons (Lin et al., 2013), where it is translated and functional abundance at midday, truncated proteins accumulate constantly (Banerjee et al., 2007, 2009). during the day (Kloosterman et al., 2013). Last, microRNAs miR156 and miR172 are also involved in Recent studies demonstrated that StCDF1 represses CO-like tuberization. Overexpression of miR156 reduces normal below- genes by directly binding DOF consensus sequence in their ground tuberization but leads to aerial tuber formation in promoter regions (Ramírez Gonzales et al., 2021). Therefore, potato (Bhogale et al., 2014) and even in non-tuberizing tomato StCDF1 promotes tuber formation by indirectly suppressing (Eviatar-Ribak et al., 2013). the tuber repressor StSP5G (via StCOL1/2) and activating the Overexpression of miR172 in Andigena potato promotes tuber inducer StSP6A (Figure 2). Indeed, transgenic plants tuberization in LDs, likely through downregulation of an AP2- overexpressing StCDF1 show strong upregulation of SP6A and like gene and upregulation of StBEL5 (Martín et al., 2009). downregulation of StSP5G and StCOL1 (Kloosterman et al., Both these tuberization phenotypes caused by overexpression 2013). Interestingly, overexpression of shorter StCDF1 variants of microRNAs are graft-transmissible (Martín et al., 2009; in Andigena potato does not affect flowering but accelerates Bhogale et al., 2014), showing that they could also be part of tuberization under LD and senescence, leading to a shorter life mobile tuberization signal together with StSP6A. cycle (Kloosterman et al., 2013). A Genome-Wide Association Study (GWAS) carried out on a pool of 83 potato cultivars reinforced the correlation between Flowering Versus Runner Formation in polymorphisms at StCDF1 locus and maturity phenotype Strawberry (Kloosterman et al., 2013). Likewise, the analysis of several In strawberry, axillary meristems have three possible destinies: StCDF1 haplotypes confirmed that most modern LD-adapted they can remain dormant or develop into either a crown varieties carry defective StCDF1 alleles encoding shortened forms branch (a new leaf rosette which may eventually produce that escape degradation by the proteasome mediated by circadian an inflorescence) or a runner, horizontal elongated stem that clock proteins (Hardigan et al., 2017). This diurnal deregulation grows above the ground (Darrow, 1966). This means that for results in increased stability of StCDF1 protein, which leads to a particular axillary meristem, flowering and runnering are constitutive repression of StSP5A and accumulation of StSP6A mutually exclusive (Hytönen et al., 2009; Mouhu et al., 2013). under LDs. Thus, naturally occurring structural variants of In general, conditions that promote flowering decrease the StCDF1 account for the adaptation of potato varieties to higher number of runners, and many strawberry cultivars develop latitudes characterized by LD summer and SD winter. runners under LDs when flowering is not induced (Hartmann, Besides components of the photoperiodic pathway, 1947; Konsin et al., 2001; Hytönen et al., 2004). gibberellins also have a role in the formation of tubers. Strawberry varieties can be classified in two groups depending Treatments with exogenous GA promote stolon elongation but on their photoperiodic behavior: most are seasonal SD-flowering inhibit tuberization (Kumar and Wareing, 1974; Xu et al., 1998). plants that readily produce runners in LDs, while others Conversely, application of a GA biosynthesis inhibitor allows are ever-flowering plants that develop reproductive structures tuberization in non-inducing LDs (Jackson and Prat, 1996). preferentially under LDs but produce very few runners or are More recently, several GA metabolism genes have been shown completely runnerless (Darrow and Waldo, 1934; Nishiyama and to be involved in different stages of the tuberization process Kanahama, 2002; Mouhu et al., 2009). Frontiers in Plant Science | www.frontiersin.org 11 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Given the agronomic relevance of runner formation for Strawberry species belong to the Fragaria genus and vary in asexual reproduction of commercial strawberries (Hytönen their ploidy, ranging from diploid to decaploid (Hummer and et al., 2009), molecular studies have been employed to Hancock, 2009; Edger et al., 2019). Since the octoploid genome understand the regulatory mechanisms controlling this process. of the widely cultivated garden strawberry (Fragaria x ananassa) New knowledge could be used in breeding programs for makes genetic analysis impractical, research has been performed crop improvements. mostly in diploid woodland strawberry (Fragaria vesca). FIGURE 3 | Frankenstein plant. Representation of an imaginary plant showing specific developmental processes controlled by similar components of the photoperiodic pathway in different plant species. Under LDs (right) leaf and flower development, runner formation (specific for strawberry). Under SD (left) bud set/dormancy and growth cessation (perennial trees), tuber formation (specific for potato). TABLE 1 | Role of FT-like genes in photoperiod-controlled processes discussed in the review. Organism Gene name Role of FT-like genes in photoperiod-controlled processes Arabidopsis thaliana FT, TSF Positive regulation of flowering under LD and control of stomata opening Oryza sativa Hd3a,RFT1 Positive regulation of flowering under SD Positive regulation of flowering under LD Zea mays ZCN8 Positive regulation of flowering (days to anthesis) Hordeum vulgare HvFT1 Positive regulation of flowering (heading date) Triticum aestivum TaFT1 Positive regulation of flowering (heading date) Populus trichocarpa PtFT1PtFT2 Promotion of growth cessation and bud formation. Promotion of bud burst Picea abies PaFT4 Promotion of growth cessation and bud set Solanum tuberosum StSP6A Positive regulation of tuberization Fragaria vesca FvFT1 Positive regulation of runner formation Frontiers in Plant Science | www.frontiersin.org 12 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Gibberellins are essential for the differentiation of vegetative Serrano-Mislata et al., 2017), especially at the transition from the structures from axillary meristems: runner formation is vegetative to the reproductive phase. promoted by treatments with exogenous GA even in runnerless The antagonism between FT and TFL1 at the shoot apex might varieties (Thompson and Guttridge, 1959; Tenreira et al., represent a brake to slow down the floral transition and avoid 2017), but prevented by chemical inhibition of GA biosynthesis accelerated flower development when conditions are not optimal (Guttridge and Thompson, 1964; Ramina et al., 1985; Hytönen for reproductive success. et al., 2009). Interestingly, runnerless accessions harbor a According to a recent review by Périlleux et al. (2019), deletion in the GA biosynthetic gene FvGA20ox4, which is the influence of TFL1 goes beyond the control of flowering mostly expressed in axillary meristems and developing runners time: TFL1 also regulates multiple developmental processes (Tenreira et al., 2017). Furthermore, a genetic screen conducted throughout the plant life cycle such as the juvenile to adult phase with a runnerless woodland strawberry accession led to the change, shoot growth and inflorescence architecture. Likewise, identification of a mutation in a gene called Suppressor of the action of FT-like proteins greatly impacts several life history Runnerless (SRL) (Caruana et al., 2018), which was renamed traits in different plants, from Arabidopsis to annual cereals FvRGA1 because of its high similarity with DELLA gene, that and perennial trees, suggesting that PEBPs may play a general caused constitutive runner formation (Kang et al., 2013). A later function as plant growth regulators. study showed that FvRGA1 silencing induces the formation of In the plant species examined here, the GRNs converging runners in non-runnering varieties (Li W. et al., 2018). on FT-like factors regulate specific stages of plant development Runner formation in strawberry also shares crucial in response to daylength. Intriguingly, genetic variation components with the photoperiodic pathway that control in components of the photoperiod pathway underlies the flowering in Arabidopsis. phenotypic variation that has allowed plant adaptation to new Under LDs, FvCO is required for the expression of FvFT1 environments that differ from those of the site of origin. (Rantanen et al., 2014; Kurokura et al., 2017), although the Many polymorphisms described thus far impair the function interplay between FvCO and FvFT1 is not exactly the same as in of regulators acting upstream of FT-like genes, such as loss of Arabidopsis, since FvCO mRNA is expressed at different times function mutations in floral repressors. This likely represents during the day. Upon activation, FvFT1 induces FvSOC1, which a “survival strategy” to preserve the functionality of PEBPs as promotes the expression of GA biosynthetic genes including fundamental growth regulators and only fine-tune their activity FvGA20ox4 (Andrés et al., 2021). Consequently, accumulation in response to changes in external conditions. of GA causes the degradation of the FvRGA1/SRL, leading to In cereals, the domestication syndrome encompasses a set runner formation. Interestingly, treatments with GA biosynthesis of changes in natural populations affecting the architecture inhibitors block runner formation even in plants overexpressing of vegetative and reproductive organs (e.g., prostrate to erect FvSOC1 (Mouhu et al., 2013). growth, seed shattering). Instead, the diversification phase relied Under SDs, FvFT1 is repressed, FvSOC1 is not active and GAs on the selection of novel varieties that better adapted to new do not accumulate; this means that FvRGA1/SRL is not degraded agroecosystems. Noteworthy, genetic diversity in loci encoding and able to repress runnering. circadian clock proteins largely accounts for phenotypic diversity Flowering is also inhibited by FvSOC1 through FvTFL1, in plant response to photoperiod, which has contributed to adjust which displays similarities with the Arabidopsis antiflorigen. the reproductive phase to different environmental conditions and As supporting evidence, perpetual flowering accessions carry ultimately has favored the cultivation of cereals outside their area mutations in the FvTFL1 gene (Koskela et al., 2012; Mouhu et al., of domestication. In fact, the huge genetic variability underlying 2013) that impair its function as floral repressor. photoperiod sensitivity has facilitated the reproductive success of cultivated cereals in tropical, subtropical and temperate regions. As the regulation of the floral transition in cereals has influenced CONCLUDING REMARKS both grain yield and adaptive growth, it can be considered one of the most important agronomic traits to obtain improved varieties In this review, we have highlighted the function of those adapted to stressful conditions arising from changing climates. components of the photoperiod pathway that happen to In the same manner, selection of allelic variants in the genes regulate different developmental processes in different plant responsible for photoperiodic control of potato tuberization species (Figure 3 and Supplementary Table 1). The genetic has allowed its widespread cultivation at different latitudes and pathways that control plant development in response to climates, releasing productivity from the constraints of its genetic photoperiodic cues presented here converge on the regulation adaptation to its natural environment. Strawberry is yet another of members of the PEBP family highly similar to the florigen example of a crop in which classical breeding has been based FT (Table 1). on the alteration of similar GRNs controlling photoperiodic Decades of research in the model species Arabidopsis responses, prior to any knowledge of the molecular interactions thaliana led to the identification and functional characterization between its components. of hundreds of regulatory genes acting upstream of the In perennials, changes in photoperiod regulate the critical florigen FT (schematically reported in FLOR-ID, Bouché et al., growth status for tree survival: active growth in warm LDs and 2016). Nevertheless, little is known about the regulation growth cessation in cold SDs. The onset of both, to grow and stop of the antiflorigen TFL1 (Fernández-Nohales et al., 2014; growing, is controlled by FT-like genes. Frontiers in Plant Science | www.frontiersin.org 13 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering In other non-woody perennials, FT orthologs also regulate FUNDING growth and dormancy; as their role in the control of vegetative development may precede their involvement in floral induction, We thank our funders: Grant PGC2018-095804-B-I00 funded flowering could also be perceived as a growing period. by MCIN/AEI/ 10.13039/501100011033 and by “ERDF A way of making Europe,” by the “European Union,” and CERCA Programme/Generalitat de Catalunya 2017 SGR FUTURE PERSPECTIVES 718 to SP. Grant FJCI-2017-32273 funded by MCIN/AEI/ 10.13039/501100011033 to IC. Grant BES-2017-080626 funded In the face of climate change, it’s extremely important to increase by MCIN/AEI/ 10.13039/501100011033 and by “ESF Investing in our knowledge on the interaction between the photoperiod your future” to UC, and Grant LCF/BQ/DI18/11660020, which pathway and other environmental conditions such as ambient received funding from the EU-H2020 through MSCA Grant temperature or water availability. 713673 from the INPhINIT programme of La Caixa Foundation It is well established that plants alter their developmental to PN. UC and PN performed this work within the frame of processes to adapt to fluctuating temperatures. For example, a Program of the Universitat Autònoma de Barcelona. We hypocotyl elongation and flowering time in Arabidopsis are acknowledge financial support from the Spanish Ministry of controlled by the photoperiod but are also greatly influenced Science and Innovation-State Research Agency (AEI), through by ambient temperatures. Indeed, warmer temperatures promote the “Severo Ochoa Programme for Centres of Excellence in R&D” hypocotyl growth and accelerate flowering. Also, low watering SEV-2015-0533 and CEX2019-000902-S. conditions promote precocious flowering, mainly through anticipated activation of the florigen FT (Riboni et al., 2013). Interestingly, overexpression of the main tuberigen StSP6A in transgenic potato has been used to increase tuber production ACKNOWLEDGMENTS under drought and heat stress conditions that are known to negatively impact tuber yield and quality (Lehretz et al., 2021). We would like to acknowledge all plant scientists whose work Altogether, these studies further highlight the connection has inspired this review, and we would like to apologize to those between photoperiod responses and other environmental authors who were not mentioned due to limited space. factors as well as the potential of components of the photoperiod pathway as targets for genetic improvement in important plant species. SUPPLEMENTARY MATERIAL The Supplementary Material for this article can be found AUTHOR CONTRIBUTIONS online at: https://www.frontiersin.org/articles/10.3389/fpls.2021. 805635/full#supplementary-material All authors contributed to the article and approved the submitted manuscript. PN and UC prepared the table. MO, IC, and UC Supplementary Table 1 | List of genes involved in the regulation of different ideated figures. MO and SP designed the structure of the review. developmental processes in response to photoperiod. REFERENCES the Arabidopsis circadian clock. Science 293, 880–883. doi: 10.1126/science. 1061320 Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., et al. Al-Sady, B., Ni, W., Kircher, S., Schäfer, E., and Quail, P. H. (2006). Photoactivated (2005). FD, a bZIP protein mediating signals from the floral pathway integrator phytochrome induces rapid PIF3 phosphorylation prior to proteasome- ft at the shoot apex. Science 309, 1052–1056. mediated degradation. Mol. Cell 23, 439–446. doi: 10.1016/j.molcel.2006.06. Abe, M., Kosaka, S., Shibuta, M., Nagata, K., Uemura, T., Nakano, A., et al. 011 (2019). Transient activity of the florigen complex during the floral transition Ando, E., Ohnishi, M., Wang, Y., Matsushita, T., Watanabe, A., Hayashi, Y., et al. in Arabidopsis thaliana. Development 146:dev171504. doi: 10.1242/dev. (2013). TWIN SISTER OF FT, GIGANTEA, and CONSTANS have a positive 171504 but indirect effect on blue light-induced stomatal opening in Arabidopsis. Plant Abelenda, J. A., Cruz-Oró, E., Franco-Zorrilla, J. M., and Prat, S. (2016). Potato Physiol. 162, 1529–1538. StCONSTANS-like1 suppresses storage organ formation by directly activating Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to the FT-like StSP5G repressor. Curr. Biol. 26, 872–881. seasonal cues. Nat. Rev. Genet. 13, 627–639. doi: 10.1038/nrg3291 Abelenda, J. A., Navarro, C., and Prat, S. (2014). Flowering and tuberization: a tale Andrés, F., Porri, A., Torti, S., Mateos, J., Romera-Branchat, M., García-Martínez, J. of two nightshades. Trends Plant Sci. 19, 115–122. L., et al. (2014). SHORT VEGETATIVE PHASE reduces gibberellin biosynthesis Adrian, J., Farrona, S., Reimer, J. J., Albani, M. C., Coupland, G., and Turck, at the Arabidopsis shoot apex to regulate the floral transition. Proc. Natl. Acad. F. (2010). Cis-regulatory elements and chromatin state coordinately control Sci. U.S.A. 111, E2760–E2769. temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis. Andrés, J., Caruana, J., Liang, J., Samad, S., Monfort, A., Liu, Z., et al. Plant Cell 22, 1425–1440. doi: 10.1105/tpc.110.074682 (2021). Woodland strawberry axillary bud fate is dictated by a crosstalk of Aguilar-Jaramillo, A. E., Marín-González, E., Matías-Hernández, L., Osnato, M., environmental and endogenous factors. Plant Physiol. 187, 1221–1234. doi: Pelaz, S., and Suárez-López, P. (2019). TEMPRANILLO is a direct repressor of 10.1093/plphys/kiab421 the microRNA miR172. Plant J. 100, 522–535. doi: 10.1111/tpj.14455 Aoki, S., Toh, S., Nakamichi, N., Hayashi, Y., Wang, Y., Suzuki, T., et al. (2019). Alabadí, D., Oyama, T., Yanovsky, M. J., Harmon, F. G., Más, P., and Kay, Regulation of stomatal opening and histone modification by photoperiod in S. A. (2001). Reciprocal regulation between TOC1 and LHY/CCA1 within Arabidopsis thaliana. Sci. Rep. 9:10054. Frontiers in Plant Science | www.frontiersin.org 14 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Aukerman, M. J., and Sakai, H. (2003). Regulation of flowering time and floral transcription via direct binding to the pri-miR172a promoter in Arabidopsis. organ identity by a MicroRNA and lts APETALA2-Like target genes. Plant Cell FEBS Lett. 586, 2332–2337. doi: 10.1016/j.febslet.2012.05.035 15, 2730–2741. doi: 10.1105/tpc.016238 Chow, B. Y., Helfer, A., Nusinow, D. A., and Kay, S. A. (2012). ELF3 recruitment to Bagnall, D. J., King, R. W., Whitelam, G. C., Boylan, M. T., Wagner, D., and Quail, the PRR9 promoter requires other evening complex members in the Arabidopsis P. H. (1995). Flowering responses to altered expression of phytochrome in circadian clock. Plant Signal Behav. 7, 170–173. doi: 10.4161/psb.18766 mutants and transgenic lines of Arabidopsis thaliana (L.) Heynh. Plant Physiol. Clack, T., Mathews, S., and Sharrock, R. A. (1994). The phytochrome apoprotein 108, 1495–1503. doi: 10.1104/pp.108.4.1495 family in Arabidopsis is encoded by five genes: the sequences and expression of Banerjee, A. K., Chatterjee, M., Yu, Y., Suh, S.-G., Miller, W. A., and Hannapel, PHYD and PHYE. Plant Mol. Biol. 25, 413–427. doi: 10.1007/BF00043870 D. J. (2007). Dynamics of a mobile RNA of potato involved in a long-distance Cockram, J., Thiel, T., Steuernagel, B., Stein, N., Taudien, S., Bailey, P. C., et al. signaling pathway. Plant Cell 18, 3443–3457. (2012). Genome dynamics explain the evolution of flowering time CCT domain Banerjee, A. K., Lin, T., and Hannapel, D. J. (2009). Untranslated regions of a gene families in the poaceae. PLoS One 7:e45307. doi: 10.1371/journal.pone. mobile transcript mediate RNA metabolism. Plant Physiol. 151, 1831–1843. 0045307 Bao, S., Hua, C., Huang, G., Cheng, P., Gong, X., Shen, L., et al. (2019). Molecular Collani, S., Neumann, M., Yant, L., and Schmid, M. (2019). FT modulates genome- basis of natural variation in photoperiodic flowering responses. Dev. Cell 50, wide DNA-binding of the bZIP transcription factor FD. Plant Physiol. 180, 90–101.e3. doi: 10.1016/j.devcel.2019.05.018. 367–380. doi: 10.1104/pp.18.01505 Batutis, E. J., and Ewing, E. E. (1982). Far-Red reversal of red light effect during Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., et al. (2007). FT long-night induction of potato (Solanum tuberosum L.) Tuberization. Plant protein movement contributes to long-distance signaling in floral induction of Physiol. 69, 672–674. Arabidopsis. Science 316, 1030–1033. Beales, J., Turner, A., Griffiths, S., Snape, J. W., and Laurie, D. A. (2007). A pseudo- Covington, M. F., Panda, S., Xing Liang, Liu, Strayer, C. A., Wagner, D. R., et al. response regulator is misexpressed in the photoperiod insensitive Ppd-D1a (2001). ELF3 modulates resetting of the circadian clock in Arabidopsis. Plant mutant of wheat (Triticum aestivum L.). Theor. Appl. Genet. 115, 721–733. Cell 13, 1305–1315. doi: 10.1105/tpc.13.6.1305 doi: 10.1007/s00122-007-0603-4 Danilevskaya, O. N., Meng, X., McGonigle, B., and Muszynski, M. G. (2011). Berns, M. C., Nordström, K., Cremer, F., Tóth, R., Hartke, M., Simon, S., Beyond flowering time: pleiotropic function of the maize flowering hormone et al. (2014). Evening expression of Arabidopsis GIGANTEA is controlled by Florigen. Plant Signal. Behav. 6, 1267–1270. doi: 10.4161/psb.6.9.16423 combinatorial interactions among evolutionarily conserved regulatory motifs. Darrow, G. M. (1966). The Strawberry: History, Breeding, and Physiology. Plant Cell 26, 3999–4018. doi: 10.1105/tpc.114.129437 New York, NY: Holt, Rinehart and Winston. Bhogale, S., Mahajan, A. S., Natarajan, B., Rajabhoj, M., Thulasiram, H. V., Darrow, G. M., and Waldo, G. F. (1934). Responses of Strawberry Varieties and and Banerjee, A. K. (2014). MicroRNA156: a potential graft-transmissible Species to Duration of the Daily Light Period. Washington, DC: U.S. Dept. of MicroRNA that modulates plant architecture and tuberization in Solanum Agriculture. tuberosum ssp. andigena. Plant Physiol. 164, 1011–1027. Davière, J. M., de Lucas, M., and Prat, S. (2008). Transcriptional factor interaction: Böhlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A. M., Jansson, S., a central step in DELLA function. Curr. Opin. Genet. Dev. 18, 295–303. doi: Strauss, S. H., et al. (2006). CO/FT regulatory module controls timing of 10.1016/j.gde.2008.05.004 flowering and seasonal growth cessation in trees. Science 312, 1040–1043. doi: De Lucas, M., Davière, J. M., Rodríguez-Falcón, M., Pontin, M., Iglesias-Pedraz, 10.1126/science.1126038 J. M., Lorrain, S., et al. (2008). A molecular framework for light and Boss, P. K., Bastow, R. M., Mylne, J. S., and Dean, C. (2004). Multiple pathways in gibberellin control of cell elongation. Nature 451, 480–484. doi: 10.1038/nature the decision to flower: enabling, promoting, and resetting. Plant Cell 16(Suppl.), 06520 S18–S31. doi: 10.1105/tpc.015958 Digel, B., Pankin, A., and von Korff, M. (2015). Global transcriptome profiling Bouché, F., Lobet, G., Tocquin, P., and Périlleux, C. (2016). FLOR-ID: an of developing leaf and shoot apices reveals distinct genetic and environmental interactive database of flowering-time gene networks in Arabidopsis thaliana. control of floral transition and inflorescence development in barley. Plant Cell Nucleic Acids Res. 44, D1167–D1171. doi: 10.1093/nar/gkv1054 27, 2318–2334. doi: 10.1105/tpc.15.00203 Bou-Torrent, J., Martínez-García, J. F., García-Martínez, J. L., and Prat, S. (2011). Ding, J., Böhlenius, H., Rühl, M. G., Chen, P., Sane, S., Zambrano, J. A., et al. Gibberellin A1 metabolism contributes to the control of photoperiod-mediated (2018). GIGANTEA-like genes control seasonal growth cessation in Populus. tuberization in potato. PLoS One 6:e24458. doi: 10.1371/journal.pone.0024458 New Phytol. 218, 1491–1503. doi: 10.1111/nph.15087 Cao, S., Kumimoto, R. W., Gnesutta, N., Calogero, A. M., Mantovani, R., and Doi, K., Izawa, T., Fuse, T., Yamanouchi, U., Kubo, T., Shimatani, Z., et al. (2004). Holt, B. F. (2014). A distal CCAAT/NUCLEAR FACTOR Y complex promotes Ehd1, a B-type response regulator in rice, confers short-day promotion of chromatin looping at the FLOWERING LOCUS T promoter and regulates the flowering and controls FT-like gene expression independently of Hd1. Genes timing of flowering in Arabidopsis. Plant Cell 26, 1009–1017. doi: 10.1105/tpc. Dev. 18, 926–936. 113.120352 Doyle, M. R., Davis, S. J., Bastow, R. M., McWatters, H. G., Kozma-Bognár, L., Caruana, J. C., Sittmann, J. W., Wang, W., and Liu, Z. (2018). Suppressor of Nagy, F., et al. (2002). The ELF4 gene controls circadian rhythms and flowering runnerless encodes a DELLA protein that controls runner formation for asexual time in Arabidopsis thaliana. Nature 419, 74–77. doi: 10.1038/nature00954 reproduction in strawberry. Mol. Plant 11, 230–233. Edger, P. P., Poorten, T. J., VanBuren, R., Hardigan, M. A., Colle, M., McKain, Castillejo, C., and Pelaz, S. (2008). The balance between CONSTANS and M. R., et al. (2019). Origin and evolution of the octoploid strawberry genome. TEMPRANILLO activities determines FT expression to trigger flowering. Curr. Nat. Genet. 51, 541–547. Biol. 18, 1338–1343. Eviatar-Ribak, T., Shalit-Kaneh, A., Chappell-Maor, L., Amsellem, Z., Eshed, Causier, B., Ashworth, M., Guo, W., and Davies, B. (2012). The TOPLESS Y., and Lifschitz, E. (2013). A cytokinin-activating enzyme promotes tuber interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 158, formation in tomato. Curr. Biol. 23, 1057–1064. 423–438. Ezer, D., Jung, J. H., Lan, H., Biswas, S., Gregoire, L., Box, M. S., et al. (2017). Chatterjee, M., Banerjee, A. K., and Hannapel, D. J. (2007). A BELL1 -like gene of The evening complex coordinates environmental and endogenous signals in potato is light activated and wound inducible. Plant Physiol. 145, 1435–1443. Arabidopsis. Nat. Plants 3:17087. doi: 10.1038/nplants.2017.87 Chen, J., Källman, T., Ma, X., Gyllenstrand, N., Zaina, G., Morgante, M., et al. Farré, E. M., Harmer, S. L., Harmon, F. G., Yanovsky, M. J., and Kay, S. A. (2005). (2012). Disentangling the roles of history and local selection in shaping clinal Overlapping and distinct roles of PRR7 and PRR9 in the Arabidopsis circadian variation of allele frequencies and gene expression in Norway spruce (Picea clock. Curr. Biol. 15, 47–54. doi: 10.1016/j.cub.2004.12.067 abies). Genetics 191, 865–881. doi: 10.1534/genetics.112.140749 Faure, S., Higgins, J., Turner, A., and Laurie, D. A. (2007). The FLOWERING Chen, J., Tsuda, Y., Stocks, M., Källman, T., Xu, N., Kärkkäinen, K., et al. (2014). LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176, 599–609. Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 doi: 10.1534/genetics.106.069500 and gigantea? Genetics 197, 1025–1038. doi: 10.1534/genetics.114.163063 Feng, S., Martínez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., et al. (2008). Cho, H. J., Kim, J. J., Lee, J. H., Kim, W., Jung, J. H., Park, C. M., et al. (2012). Coordinated regulation of Arabidopsis thaliana development by light and SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 gibberellins. Nature 451, 475–479. doi: 10.1038/nature06448 Frontiers in Plant Science | www.frontiersin.org 15 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Fernández, V., Takahashi, Y., Le Gourrierec, J., and Coupland, G. (2016). Guo, Z., Song, Y., Zhou, R., Ren, Z., and Jia, J. (2010). Discovery, evaluation and Photoperiodic and thermosensory pathways interact through CONSTANS to distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol. 185, 841–851. promote flowering at high temperature under short days. Plant J. 86, 426–440. doi: 10.1111/j.1469-8137.2009.03099.x doi: 10.1111/tpj.13183 Gutaker, R. M., Weiß, C. L., Ellis, D., Anglin, N. L., Knapp, S., Luis Fernández- Fernández-Nohales, P., Domenech, M. J., Martínez, De Alba, A. E., Micol, Alonso, J., et al. (2019). The origins and adaptation of European potatoes J. L., Ponce, M. R., et al. (2014). AGO1 controls Arabidopsis inflorescence reconstructed from historical genomes. Nat. Ecol. Evol. 3, 1093–1101. architecture possibly by regulating TFL1 expression. Ann. Bot. 114, 1471–1481. Guttridge, C. G., and Thompson, P. A. (1964). The effect of gibberellins on growth doi: 10.1093/aob/mcu132 and flowering of Fragaria and Duchesnea. J. Exp. Bot. 15, 631–646. Fornara, F., Panigrahi, K. C. S., Gissot, L., Sauerbrunn, N., Rühl, M., Jarillo, Gyllenstrand, N., Clapham, D., Källman, T., and Lagercrantz, U. (2007). A Norway J. A., et al. (2009). Arabidopsis DOF transcription factors act redundantly to spruce FLOWERING LOCUS T homolog is implicated in control of growth reduce CONSTANS expression and are essential for a photoperiodic flowering rhythm in conifers. Plant Physiol. 144, 248–257. doi: 10.1104/pp.107.095802 response. Dev. Cell 17, 75–86. doi: 10.1016/j.devcel.2009.06.015 Haas, M., Schreiber, M., and Mascher, M. (2019). Domestication and crop Fowler, S., Lee, K., Onouchi, H., Samach, A., Richardson, K., Morris, B., evolution of wheat and barley: genes, genomics, and future directions. J. Integr. et al. (1999). GIGANTEA: a circadian clock-controlled gene that regulates Plant Biol. 61, 204–225. doi: 10.1111/jipb.12737 photoperiodic flowering in Arabidopsis and encodes a protein with several Hardigan, M. A., Laimbeer, F. P. E., Newton, L., Crisovan, E., Hamilton, J. P., possible membrane-spanning domains. EMBO J. 18, 4679–4688. doi: 10.1093/ Vaillancourt, B., et al. (2017). Genome diversity of tuber-bearing Solanum emboj/18.17.4679 uncovers complex evolutionary history and targets of domestication in the Frewen, B. E., Chen, T. H. H., Howe, G. T., Davis, J., Antje Rohde, Boerjan, W., cultivated potato. Proc. Natl. Acad. Sci. U S A. 114, E9999–E10008. et al. (2000). Quantitative trait loci and candidate gene mapping of bud set Hartmann, H. T. (1947). Some effects of temiperature and photoperiod on. Plant and bud flush in populus. Genetics 154, 837–845. doi: 10.1093/genetics/154. Physiol. 22, 407–420. 2.837 Hartmann, U., Höhmann, S., Nettesheim, K., Wisman, E., Saedler, H., and Huijser, Fujiwara, S., Oda, A., Yoshida, R., Niinuma, K., Miyata, K., Tomozoe, Y., P. (2000). Molecular cloning of SVP: a negative regulator of the floral transition et al. (2008). Circadian clock proteins LHY and CCA1 regulate SVP protein in Arabidopsis. Plant J. 21, 351–360. doi: 10.1046/j.1365-313X.2000.00682.x accumulation to control flowering in Arabidopsis. Plant Cell 20, 2960–2971. Hassidim, M., Dakhiya, Y., Turjeman, A., Hussien, D., Shor, E., Anidjar, A., doi: 10.1105/tpc.108.061531 et al. (2017). CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and the circadian Galvāo, V. C., Fiorucci, A. S., Trevisan, M., Franco-Zorilla, J. M., Goyal, A., control of stomatal aperture. Plant Physiol. 175, 1864–1877. Schmid-Siegert, E., et al. (2019). PIF transcription factors link a neighbor threat Hayama, R., Sarid-Krebs, L., Richter, R., Fernández, V., Jang, S., and Coupland, cue to accelerated reproduction in Arabidopsis. Nat. Commun. 10:4005. doi: G. (2017). PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein 10.1038/s41467-019-11882-7 to promote flowering in response to day length. EMBO J. 36, 904–918. doi: Gao, H., Jin, M., Zheng, X. M., Chen, J., Yuan, D., Xin, Y., et al. (2014). Days 10.15252/embj.201693907 to heading 7, a major quantitative locus determining photoperiod sensitivity Heide, O. M. (1974). Growth and dormancy in norway spruce ecotypes (Picea and regional adaptation in rice. Proc. Natl. Acad. Sci. U S A. 111, 16337–16342. abies) I. interaction of photoperiod and temperature. Physiol. Plant 30, 1–12. doi: 10.1073/pnas.1418204111 doi: 10.1111/j.1399-3054.1974.tb04983.x Garner, W. W., and Allard, H. A. (1923). Further studies on photoperiodism, the Hicks, K. A., Millar, A. J., Carré, I. A., Somers, D. E., Straume, M., Meeks-Wagner, response of plants to relative length of day and night. J. Agric. Res. 23, 871–920. D. R., et al. (1996). Conditional circadian dysfunction of the Arabidopsis early- Gendron, J. M., Pruneda-Paz, J. L., Doherty, C. J., Gross, A. M., Kang, S. E., flowering 3 mutant. Science 274, 790–792. doi: 10.1126/science.274.5288.790 and Kay, S. A. (2012). Arabidopsis circadian clock protein, TOC1,is a DNA- Hornitschek, P., Kohnen, M. V., Lorrain, S., Rougemont, J., Ljung, K., López- binding transcription factor. Proc. Natl. Acad. Sci. U S A. 109, 3167–3172. Vidriero, I., et al. (2012). Phytochrome interacting factors 4 and 5 control doi: 10.1073/pnas.1200355109 seedling growth in changing light conditions by directly controlling auxin Ghislain, M., Núñez, J., Herrera, M. D. R., and Spooner, D. M. (2009). The signaling. Plant J. 71, 699–711. doi: 10.1111/j.1365-313X.2012.05033.x single Andigenum origin of Neo-Tuberosum potato materials is not supported Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmapuram, J., and Anderson, by microsatellite and plastid marker analyses. Theor. Appl. Genet. 118, J. V. (2008). Transcriptome analysis identifies novel responses and potential 963–969. regulatory genes involved in seasonal dormancy transitions of leafy spurge Gómez-Ariza, J., Galbiati, F., Goretti, D., Brambilla, V., Shrestha, R., Pappolla, A., (Euphorbia esula L.). BMC Genomics 9:536. doi: 10.1186/1471-2164-9-536 et al. (2015). Loss of floral repressor function adapts rice to higher latitudes in Hsu, C. Y., Adams, J. P., Kim, H., No, K., Ma, C., Strauss, S. H., et al. (2011). Europe. J. Exp. Bot. 66, 2027–2039. doi: 10.1093/jxb/erv004 FLOWERING LOCUS T duplication coordinates reproductive and vegetative González-Schain, N. D., Díaz-Mendoza, M., Zurczak, M., and Suárez-López, P. growth in perennial poplar. Proc. Natl. Acad. Sci. U S A. 108, 10756–10761. (2012). Potato CONSTANS is involved in photoperiodic tuberization in a doi: 10.1073/pnas.1104713108 graft-transmissible manner. Plant J. 70, 678–690. Hsu, C. Y., Liu, Y., Luthe, D. S., and Yuceer, C. (2006). Poplar FT2 shortens Goralogia, G. S., Liu, T. K., Zhao, L., Panipinto, P. M., Groover, Bains, Y. S., the juvenile phase and promotes seasonal flowering. Plant Cell 18, 1846–1861. et al. (2017). CYCLING DOF FACTOR 1 represses transcription through the doi: 10.1105/tpc.106.041038 TOPLESS co-repressor to control photoperiodic flowering in Arabidopsis. Plant Huang, C., Sun, H., Xu, D., Chen, Q., Liang, Y., Wang, X., et al. (2017). ZmCCT9 J. 92, 244–262. doi: 10.1111/tpj.13649 enhances maize adaptation to higher latitudes. Proc. Natl. Acad. Sci. U S A. 115, Goretti, D., Martignago, D., Landini, M., Brambilla, V., Gómez-Ariza, J., Gnesutta, E334–E341. doi: 10.1073/pnas.1718058115 N., et al. (2017). Transcriptional and post-transcriptional mechanisms limit Hummer, K. E., and Hancock, J. (2009). “Strawberry genomics: botanical history, heading date 1 (Hd1) function to adapt rice to high latitudes. PLoS Genet. cultivation, traditional breeding, and new technologies,” in Genetics and 13:e1006530. doi: 10.1371/journal.pgen.1006530 Genomics of Rosaceae, eds K. Folta and S. Gardiner (New York, NY: Springer). Goyal, A., Karayekov, E., Galvão, V. C., Ren, H., Casal, J. J., and Fankhauser, Huq, E., and Quail, P. H. (2002). PIF4, a phytochrome-interacting bHLH factor, C. (2016). Shade promotes phototropism through phytochrome B-Controlled functions as a negative regulator of phytochrome B signaling in Arabidopsis. Auxin production. Curr. Biol. 26, 3280–3287. doi: 10.1016/j.cub.2016.10.001 EMBO J. 21, 2441–2450. doi: 10.1093/emboj/21.10.2441 Graeff, M., Straub, D., Eguen, T., Dolde, U., Rodrigues, V., Brandt, R., et al. Hyles, J., Bloomfield, M. T., Hunt, J. R., Trethowan, R. M., and Trevaskis, B. (2016). MicroProtein-Mediated recruitment of CONSTANS into a TOPLESS (2020). Phenology and related traits for wheat adaptation. Heredity (Edinb) 125, trimeric complex represses flowering in Arabidopsis. PLoS Genet. 12:e1005959. 417–430. doi: 10.1038/s41437-020-0320-1 doi: 10.1371/journal.pgen.1005959 Hytönen, T., Elomaa, P., Moritz, T., and Junttila, O. (2009). Gibberellin mediates Guo, L., Wang, X., Zhao, M., Huang, C., Li, C., Li, D., et al. (2018). Stepwise cis- daylength-controlled differentiation of vegetative meristems in strawberry Regulatory changes in ZCN8 contribute to maize flowering-time adaptation. (Fragaria × ananassa Duch). BMC Plant Biol. 9:18. doi: 10.1186/1471-2229-9- Curr. Biol. 28, 3005–3015.e4. doi: 10.1016/j.cub.2018.07.029. 18 Frontiers in Plant Science | www.frontiersin.org 16 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Hytönen, T., Palonen, P., Mouhu, K., and Junttila, O. (2004). Crown branching and Kim, Y., Lim, J., Yeom, M., Kim, H., Kim, J., Wang, L., et al. (2013). ELF4 regulates cropping potential in strawberry (Fragaria X ananassa Duch.) can be enhanced GIGANTEA chromatin access through subnuclear sequestration. Cell Rep. 3, by daylength treatments. J. Hortic. Sci. Biotechnol. 79, 466–471. 671–677. doi: 10.1016/j.celrep.2013.02.021 Imaizumi, T., Schultz, T. F., Harmon, F. G., Ho, L. A., and Kay, S. A. (2005). Kimura, Y., Aoki, S., Ando, E., Kitatsuji, A., Watanabe, A., Ohnishi, M., et al. Plant science: FKF1 F-box protein mediates cyclic degradation of a repressor (2015). A flowering integrator, SOC1, Affects stomatal opening in Arabidopsis of CONSTANS in Arabidopsis. Science 309, 293–297. thaliana. Plant Cell Physiol. 56, 640–649. Itoh, H., Nonoue, Y., Yano, M., and Izawa, T. (2010). A pair of floral regulators sets Kinoshita, A., and Richter, R. (2020). Genetic and molecular basis of floral critical day length for Hd3a florigen expression in rice. Nat. Genet. 42, 635–638. induction in Arabidopsis thaliana. J. Exp. Botany 71, 2490–2504. doi: 10.1038/ng.606 Kinoshita, A., Vayssières, A., Richter, R., Sang, Q., Roggen, A., van Driel, A. D., et Izawa, T., Oikawa, T., Sugiyama, N., Tanisaka, T., Yano, M., and Shimamoto, K. al. (2020). Regulation of shoot meristem shape by photoperiodic signaling and (2002). Phytochrome mediates the external light signal to repress FT orthologs phytohormones during floral induction of Arabidopsis. Elife 9:e60661. in photoperiodic flowering of rice. Genes Dev. 16, 2006–2020. doi: 10.1101/gad. Kinoshita, T. (1999). Blue light activates the plasma membrane H+-ATPase by 999202 phosphorylation of the C-terminus in stomatal guard cells. EMBO J. 18, 5548– Jackson, S. D. (1999). Multiple signaling pathways control tuber induction in 5558. potato. Plant Physiol. 119, 1–8. Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M., and Shimazaki, K. Jackson, S. D., and Prat, S. (1996). Control of tuberisation in potato by gibberellins (2001). phot1 and phot2 mediate blue light regulation of stomatal opening. and phytochrome B. Physiol. Plant 98, 407–412. Nature 414, 656–660. Jackson, S. D., James, P. E., Carrera, E., Prat, S., and Thomas, B. (2000). Regulation Kinoshita, T., Ono, N., Hayashi, Y., Morimoto, S., Nakamura, S., Soda, M., et al. of transcript levels of a potato gibberellin 20-Oxidase gene by light and (2011). FLOWERING LOCUS T regulates stomatal opening. Curr. Biol. 21, phytochrome B. Plant Physiol. 124, 423–430. 1232–1238. Jackson, S. D., James, P., Prat, S., and Thomas, B. (1998). Phytochrome B affects the Klintenäs, M., Pin, P. A., Benlloch, R., Ingvarsson, P. K., and Nilsson, O. (2012). levels of a graft-transmissible Signal involved in Tuberization1. Plant Physiol. Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes 117, 29–32. provides evidence for dramatic biochemical evolution in the angiosperm FT Jaeger, K. E., and Wigge, P. A. (2007). FT protein acts as a long-range signal in lineage. New Phytol. 196, 1260–1273. doi: 10.1111/j.1469-8137.2012.04332.x Arabidopsis. Curr. Biol. 17, 1050–1054. Kloosterman, B., Abelenda, J. A., Gomez, M., del, M. C., Oortwijn, M., de Boer, Jang, S., Torti, S., and Coupland, G. (2009). Genetic and spatial interactions J. M., et al. (2013). Naturally occurring allele diversity allows potato cultivation between FT, TSF and SVP during the early stages of floral induction in in northern latitudes. Nature 495, 246–250. Arabidopsis. Plant J. 60, 614–625. doi: 10.1111/j.1365-313X.2009.03986.x Kloosterman, B., Navarro, C., Bijsterbosch, G., Lange, T., Prat, S., Visser, R. G. F., Jeong, H. L., Seong, J. Y., Soo, H. P., Hwang, I., Jong, S. L., and Ji, H. A. (2007). Role et al. (2007). StGA2ox1 is induced prior to stolon swelling and controls GA of SVP in the control of flowering time by ambient temperature in Arabidopsis. levels during potato tuber development. Plant J. 52, 362–373. Genes Dev. 21, 397–402. doi: 10.1101/gad.1518407 Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M., and Araki, T. (1999). A pair of Jiang, Y., Yang, C., Huang, S., Xie, F., Xu, Y., Liu, C., et al. (2019). The ELF3-PIF7 related genes with antagonistic roles in mediating flowering signals. Science 286, interaction mediates the circadian gating of the shade response in Arabidopsis. 1960–1962. iScience 22, 288–298. doi: 10.1016/j.isci.2019.11.029 Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T., et al. Jones, H., Leigh, F. J., Mackay, I., Bower, M. A., Smith, L. M. J., Charles, M. P., (2002). Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to et al. (2008). Population-based resequencing reveals that the flowering time flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. adaptation of cultivated barley originated east of the fertile crescent. Mol. Biol. 43, 1096–1105. Evol. 25, 2211–2219. doi: 10.1093/molbev/msn167 Konsin, M., Voipio, I., and Palonen, P. (2001). Influence of photoperiod and Jung, J. H., Seo, Y. H., Pil, J. S., Reyes, J. L., Yun, J., Chua, N. H., et al. (2007). duration of short-day treatment on vegetative growth and flowering of The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering strawberry (Fragaria X ananassa duch). J. Hortic. Sci. Biotechnol. 76, 77–82. independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736–2748. doi: Koskela, E. A., Mouhu, K., Albani, M. C., Kurokura, T., Rantanen, M., 10.1105/tpc.107.054528 Sargent, D. J., et al. (2012). Mutation in TERMINAL FLOWER1 reverses the Kamioka, M., Takao, S., Suzuki, T., Taki, K., Higashiyam, T., Kinoshita, T., photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. et al. (2016). Direct repression of evening genes by CIRCADIAN CLOCK- Plant Physiol. 159, 1043–1054. ASSOCIATED1 in the Arabidopsis circadian clock. Plant Cell 28, 696–711. Kumar, D., and Wareing, P. F. (1974). Studies on tuberization of Solanum doi: 10.1105/tpc.15.00737 andigena. ii. growth hormones and tuberization. New Phytol. 73, Kang, C., Darwish, O., Geretz, A., Shahan, R., Alkharouf, N., and Liua, Z. (2013). 833–840. Genome-scale transcriptomic insights into early-stage fruit development in Kumar, S. V., Lucyshyn, D., Jaeger, K. E., Alós, E., Alvey, E., Harberd, N. P., woodland strawberry Fragaria vesca. Plant Cell 25, 1960–1978. et al. (2012). Transcription factor PIF4 controls the thermosensory activation Kardailsky, I., Shukla, V. K., Ahn, J. H., Dagenais, N., Christensen, S. K., Nguyen, of flowering. Nature 484, 242–245. doi: 10.1038/nature10928 J. T., et al. (1999). Activation tagging of the floral inducer FT. Science 286, Kunihiro, A., Yamashino, T., Nakamichi, N., Niwa, Y., Nakanishi, H., and Mizuno, 1962–1965. T. (2011). PHYTOCHROME-INTERACTING FACTOR 4 and 5 (PIF4 and Karlgren, A., Gyllenstrand, N., Källman, T., Sundström, J. F., Moore, D., Lascoux, PIF5) activate the Homeobox ATHB2 and auxin-inducible IAA29 genes in M., et al. (2011). Evolution of the PEBP gene family in plants: functional the coincidence mechanism underlying photoperiodic control of plant growth diversification in seed plant evolution. Plant Physiol. 156, 1967–1977. doi: 10. of Arabidopsis thaliana. Plant Cell Physiol. 52, 1315–1329. doi: 10.1093/pcp/ 1104/pp.111.176206 pcr076 Khanna, R., Huq, E., Kikis, E. A., Al-Sady, B., Lanzatella, C., and Quail, P. H. (2004). Kurokura, T., Samad, S., Koskela, E., Mouhu, K., and Hytönen, T. (2017). A novel molecular recognition motif necessary for targeting photoactivated Fragaria vesca CONSTANS controls photoperiodic flowering and vegetative phytochrome signaling to specific basic helix-loop-helix transcription factors. development. J. Exp. Bot. 68, 4839–4850. Plant Cell 16, 3033–3044. doi: 10.1105/tpc.104.025643 Lazakis, C. M., Coneva, V., and Colasanti, J. (2011). ZCN8 encodes a potential Khosa, J., Bellinazzo, F., Kamenetsky Goldstein, R., Macknight, R., and Immink, orthologue of Arabidopsis FT florigen that integrates both endogenous and R. G. H. (2021). PHOSPHATIDYLETHANOLAMINE-BINDING PROTEINS: photoperiod flowering signals in maize. J. Exp. Bot. 62, 4833–4842. doi: 10.1093/ the conductors of dual reproduction in plants with vegetative storage organs. jxb/err129 J. Exp. Bot. 72, 2845–2856. doi: 10.1093/jxb/erab064 Lee, J. H., Ryu, H. S., Chung, K. S., Posé, D., Kim, S., Schmid, M., et al. (2013). Kikuchi, R., Kawahigashi, H., Ando, T., Tonooka, T., and Handa, H. (2009). Regulation of temperature-responsive flowering by MADS-box transcription Molecular and functional characterization of pebp genes in barley reveal the factor repressors. Science 342, 628–632. doi: 10.1126/science.1241097 diversification of their roles in flowering. Plant Physiol. 149, 1341–1353. doi: Lehretz, G. G., Sonnewald, S., Lugassi, N., Granot, D., and Sonnewald, U. (2021). 10.1104/pp.108.132134 Future-Proofing potato for drought and heat tolerance by overexpression Frontiers in Plant Science | www.frontiersin.org 17 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering of hexokinase and SP6A. Front. Plant Sci. 11:614534. doi: 10.3389/fpls.2020. Moon, J., Lee, H., Kim, M., and Lee, I. (2005). Analysis of flowering pathway 614534 integrators in Arabidopsis. Plant Cell Physiol. 46, 292–299. doi: 10.1093/pcp/ Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., et al. (2008). A repressor pci024 complex governs the integration of flowering signals in Arabidopsis. Dev. Cell Morris, W. L., Hancock, R. D., Ducreux, L. J. M., Morris, J. A., Usman, M., Verrall, 15, 110–120. doi: 10.1016/j.devcel.2008.05.002 S. R., et al. (2014). Day length dependent restructuring of the leaf transcriptome Li, W., Zhang, J., Sun, H., Wang, S., Chen, K., Liu, Y., et al. (2018). FveRGA1, and metabolome in potato genotypes with contrasting tuberization phenotypes. encoding a DELLA protein, negatively regulates runner production in Fragaria Plant Cell Environ. 37, 1351–1363. vesca. Planta 247, 941–951. Mouhu, K., Hytönen, T., Folta, K., Rantanen, M., Paulin, L., Auvinen, P., et al. Li, Y., and Xu, M. (2017). CCT family genes in cereal crops: a current overview. (2009). Identification of flowering genes in strawberry, a perennial SD plant. Crop J. 5, 449–458. doi: 10.1016/j.cj.2017.07.001 BMC Plant Biol. 9:122. doi: 10.1186/1471-2229-9-122 Li, Y., Colleoni, C., Zhang, J., Liang, Q., Hu, Y., Ruess, H., et al. (2018). Genomic Mouhu, K., Kurokura, T., Koskela, E. A., Albert, V. A., Elomaa, P., and Hytönen, T. analyses yield markers for identifying agronomically important genes in potato. (2013). The Fragaria vesca homolog of SUPPRESSOR OF OVEREXPRESSION Mol. Plant 11, 473–484. OF CONSTANS1 represses flowering and promotes vegetative growth. Plant Lian, H., Wang, L., Ma, N., Zhou, C. M., Han, L., Zhang, T. Q., et al. (2021). Cell 25, 3296–3310. Redundant and specific roles of individual MIR172 genes in plant development. Mutasa-Göttgens, E., and Hedden, P. (2009). Gibberellin as a factor in floral PLoS Biol. 19:e3001044. doi: 10.1371/journal.pbio.3001044 regulatory networks. J. Exp. Bot. 60, 1979–1989. doi: 10.1093/jxb/erp040 Lin, C. (2000). Photoreceptors and regulation of flowering time. Plant Physiol. 123, Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N. H., and Sakakibara, 39–50. doi: 10.1104/pp.123.1.39 H. (2010). PSEUDO-RESPONSE ReGULATORS 9, 7, and 5 are transcriptional Lin, T., Sharma, P., Gonzalez, D. H., Viola, I. L., and Hannapel, D. J. (2013). repressors in the Arabidopsis circadian clock. Plant Cell 22, 594–605. doi: 10. The impact of the long-distance transport of a BEL1 -Like messenger RNA on 1105/tpc.109.072892 development. Plant Physiol. 161, 760–772. Nakamichi, N., Kita, M., Ito, S., Sato, E., Yamashino, T., and Mizuno, T. (2005a). Liu, L., Adrian, J., Pankin, A., Hu, J., Dong, X., Von Korff, M., et al. (2014). Induced The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately and natural variation of promoter length modulates the photoperiodic response play essential roles for circadian clock function. Plant Cell Physiol. 46, 609–619. of FLOWERING LOCUS T. Nat. Commun. 5:4558. doi: 10.1038/ncomms5558 doi: 10.1093/pcp/pci061 Lu, S. X., Knowles, S. M., Andronis, C., Ong, M. S., and Tobin, E. M. Nakamichi, N., Kita, M., Ito, S., Yamashino, T., and Mizuno, T. (2005b). PSEUDO- (2009). Circadian clock associated1 and late elongated hypocotyl function RESPONSE REGULATORS, PRR9, PRR7 and PRR5, Together play essential synergistically in the circadian clock of Arabidopsis. Plant Physiol. 150, 834–843. roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 46, doi: 10.1104/pp.108.133272 686–698. doi: 10.1093/pcp/pci086 Marín-González, E., Matías-Hernández, L., Aguilar-Jaramillo, A. E., Lee, J. H., Nakamichi, N., Kita, M., Niinuma, K., Ito, S., Yamashino, T., Mizoguchi, T., et al. Ahn, J. H., Suárez-López, P., et al. (2015). SHORT VEGETATIVE PHASE up- (2007). Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 regulates TEMPRANILLO2 floral repressor at low ambient temperatures. Plant and PRR5 coordinately and positively regulate flowering time through the Physiol. 169, 1214–1224. doi: 10.1104/pp.15.00570 canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol. Martín, A., Adam, H., Diìaz-Mendoza, M., Żurczak, M., Gonzaìlez-Schain, 48, 822–832. doi: 10.1093/pcp/pcm056 N. D., and Suaìrez-Loìpez, P. (2009). Graft-transmissible induction of potato Navarro, C., Abelenda, J. A., Cruz-Oró, E., Cuéllar, C. A., Tamaki, S., Silva, J., tuberization by the microRNA miR172. Development 136, 2873–2881. et al. (2011). Control of flowering and storage organ formation in potato by Martín, G., Rovira, A., Veciana, N., Soy, J., Toledo-Ortiz, G., Gommers, C. M. M., FLOWERING LOCUS T. Nature 478, 119–122. et al. (2018). Circadian waves of transcriptional repression shape PIF-Regulated Nemoto, Y., Nonoue, Y., Yano, M., and Izawa, T. (2016). Hd1,a CONSTANS photoperiod-responsive growth in Arabidopsis. Curr. Biol. 28, 311–318.e5. doi: ortholog in rice, functions as an Ehd1 repressor through interaction with 10.1016/j.cub.2017.12.021. monocot-specific CCT-domain protein Ghd7. Plant J. 86, 221–233. Martínez-García, J. F., Virgós-Soler, A., and Prat, S. (2002). Control of Nieto, C., López-Salmerón, V., Davière, J. M., and Prat, S. (2015). ELF3-PIF4 photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time interaction regulates plant growth independently of the evening complex. Curr. gene CONSTANS. Proc. Natl. Acad. Sci. U S A. 99, 15211–15216. Biol. 25, 187–193. doi: 10.1016/j.cub.2014.10.070 Mateos, J. L., Madrigal, P., Tsuda, K., Rawat, V., Richter, R., Romera-Branchat, Nishiyama, M., and Kanahama, K. (2002). Effects of temperature and photoperiod M., et al. (2015). Combinatorial activities of SHORT VEGETATIVE PHASE on flower bud initiation of day-neutral and everbearing strawberries. Acta and FLOWERING LOCUS C define distinct modes of flowering regulation in Hortic. 567, 253–255. Arabidopsis. Genome Biol. 16:31. doi: 10.1186/s13059-015-0597-1 Nohales, M. A., and Kay, S. A. (2016). Molecular mechanisms at the core of the Mathieu, J., Warthmann, N., Küttner, F., and Schmid, M. (2007). Export of FT plant circadian oscillator. Nat. Struct. Mol. Biol. 23, 1061–1069. doi: 10.1038/ protein from phloem companion cells is sufficient for floral induction in nsmb.3327 Arabidopsis. Curr. Biol. 17, 1055–1060. Nozue, K., Covington, M. F., Duek, P. D., Lorrain, S., Fankhauser, C., Harmer, S. L., Mathieu, J., Yant, L. J., Mürdter, F., Küttner, F., and Schmid, M. (2009). Repression et al. (2007). Rhythmic growth explained by coincidence between internal and of flowering by the miR172 target SMZ. PLoS Biol. 7:e1000148. doi: 10.1371/ external cues. Nature 448, 358–361. doi: 10.1038/nature05946 journal.pbio.1000148 Nusinow, D. A., Helfer, A., Hamilton, E. E., King, J. J., Imaizumi, T., Schultz, Matsuoka, Y., Vigouroux, Y., Goodman, M. M., Sanchez, J. G., Buckler, E., and T. F., et al. (2011). The ELF4-ELF3-"LUX complex links the circadian clock to Doebley, J. (2002). A single domestication for maize shown by multilocus diurnal control of hypocotyl growth. Nature 475, 398–402. doi: 10.1038/nature1 microsatellite genotyping. Proc. Natl. Acad. Sci. U S A. 99, 6080–6084. doi: 0182 10.1073/pnas.052125199 Ó’Maoiléidigh, D. S., van Driel, A. D., Singh, A., Sang, Q., Le Bec, N., Vincent, C., Matsushika, A., Makino, S., Kojima, M., and Mizuno, T. (2000). Circadian waves et al. (2021). Systematic analyses of the MIR172 family members of Arabidopsis of expression of the APRR1/TOC1 family of pseudo-response regulators in define their distinct roles in regulation of APETALA2 during floral transition. Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol. PLoS Biol. 19:e3001043. doi: 10.1371/journal.pbio.3001043 41, 1002–1012. doi: 10.1093/pcp/pcd043 Osnato, M., Castillejo, C., Matías-Hernández, L., and Pelaz, S. (2012). Matsushita, T., Mochizuki, N., and Nagatani, A. (2003). Dimers of the N-terminal TEMPRANILLO genes link photoperiod and gibberellin pathways to control domain of phytochrome B are functional in the nucleus. Nature 424, 571–574. flowering in Arabidopsis. Nat. Commun. 3:808. doi: 10.1038/ncomms1810 doi: 10.1038/nature01837 Park, H. J., Baek, D., Cha, J. Y., Liao, X., Kang, S. H., McClung, C. R., et al. (2019). Meng, X., Muszynski, M. G., and Danilevskaya, O. N. (2011). The FT-like ZCN8 Hos15 interacts with the histone deacetylase hda9 and the evening complex gene functions as a floral activator and is involved in photoperiod sensitivity in to epigenetically regulate the floral activator gigantea. Plant Cell 31, 37–51. maize. Plant Cell 23, 942–960. doi: 10.1105/tpc.110.081406 doi: 10.1105/tpc.18.00721 Frontiers in Plant Science | www.frontiersin.org 18 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Périlleux, C., Bouché, F., Randoux, M., and Orman-Ligeza, B. (2019). Turning Serrano-Mislata, A., Goslin, K., Zheng, B., Rae, L., Wellmer, F., Graciet, E., et al. meristems into fortresses. Trends Plant Sci. 24, 431–442. doi: 10.1016/j.tplants. (2017). Regulatory interplay between LEAFY, APETALA1/CAULIFLOWER 2019.02.004 and TERMINAL FLOWER1: new insights into an old relationship. Plant Signal. Plantenga, F. D. M., Bergonzi, S., Abelenda, J. A., Bachem, C. W. B., Visser, R. G. F., Behav. 12:e1370164. doi: 10.1080/15592324.2017.1370164 Heuvelink, E., et al. (2019). The tuberization signal StSP6A represses flower bud Shannon, S., and Meeks-Wagner, D. R. (1991). A mutation in the Arabidopsis development in potato. J. Exp. Bot. 70, 937–948. TFL1 gene affects inflorescence meristem development. Plant Cell 3, 877–892. Pokhilko, A., Fernández, A. P., Edwards, K. D., Southern, M. M., Halliday, K. J., and doi: 10.1105/tpc.3.9.877 Millar, A. J. (2012). The clock gene circuit in Arabidopsis includes a repressilator Sharma, P., Lin, T., and Hannapel, D. J. (2016). Targets of the StBEL5 transcription with additional feedback loops. Mol. Syst. Biol. 8:574. doi: 10.1038/msb.2012.6 factor include the FT ortholog StSP6A. Plant Physiol. 170, 310–324. Posé, D., Verhage, L., Ott, F., Yant, L., Mathieu, J., Angenent, G. C., et al. (2013). Shavrukov, Y., Kurishbayev, A., Jatayev, S., Shvidchenko, V., Zotova, L., Koekemoer, Temperature-dependent regulation of flowering by antagonistic FLM variants. F., et al. (2017). Early flowering as a drought escape mechanism in plants: how Nature 503, 414–417. doi: 10.1038/nature12633 can it aid wheat production? Front. Plant Sci. 8:1950. doi: 10.3389/fpls.2017. Purugganan, M. D. (2014). An evolutionary genomic tale of two rice species. Nat. 01950 Genet. 46, 931–932. doi: 10.1038/ng.3071 Shen, C., Liu, H., Guan, Z., Yan, J., Zheng, T., Yan, W., et al. (2020). Putterill, J., Robson, F., Lee, K., Simon, R., and Coupland, G. (1995). The Structural insight into DNA recognition by CCT/NF-YB/YC complexes in plant CONSTANS gene of Arabidopsis promotes flowering and encodes a protein photoperiodic flowering. Plant Cell 32, 3469–3484. showing similarities to zinc finger transcription factors. Cell 80, 847–857. doi: Shimazaki, K., Doi, M., Assmann, S. M., and Kinoshita, T. (2007). Light regulation 10.1016/0092-8674(95)90288-0 of stomatal movement. Annu. Rev. Plant Biol. 58, 219–247. Ramina, A., Tonutti, P., and Tosi, T. (1985). The effect of paclobutrazol on Silva, C. S., Nayak, A., Lai, X., Hutin, S., Hugouvieux, V., Jung, J. H., et al. (2020). strawberry growth and fruiting. J. Hortic. Sci. 60, 501–506. Molecular mechanisms of evening complex activity in Arabidopsis. Proc. Natl. Ramírez Gonzales, L., Shi, L., Bergonzi, S. B., Oortwijn, M., Franco-Zorrilla, J. M., Acad. Sci. U S A. 117, 6901–6909. doi: 10.1073/pnas.1920972117 Solano-Tavira, R., et al. (2021). Potato CYCLING DOF FACTOR 1 and its Simon, R., Igeno, M. I., and Coupland, G. (1996). Activation of floral meristem lncRNA counterpart StFLORE link tuber development and drought response. identity genes in Arabidopsis. Nature 384, 59–62. doi: 10.1038/384059a0 Plant J. 105, 855–869. Spooner, D. M., McLean, K., Ramsay, G., Waugh, R., and Bryan, G. J. (2005). A Rantanen, M., Kurokura, T., Mouhu, K., Pinho, P., Tetri, E., Halonen, L., et al. single domestication for potato based on multilocus amplified fragment length (2014). Light quality regulates flowering in FvFT1/FvTFL1 dependent manner polymorphism genotyping. Proc. Natl. Acad. Sci. U S A. 102, 14694–14699. in the woodland strawberry Fragaria vesca. Front. Plant Sci. 5:271. doi: 10.3389/ Suárez-López, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., and fpls.2014.00271 Coupland, G. (2001). CONSTANS mediates between the circadian clock and Riboni, M., Galbiati, M., Tonelli, C., and Conti, L. (2013). GIGANTEA enables the control of flowering in Arabidopsis. Nature 410, 1116–1120. doi: 10.1038/ drought escape response via abscisic acid-dependent activation of the florigens 35074138 and SUPPRESSOR of OVEREXPRESSION of CONSTANS11[c][w]. Plant Sukhotu, T., and Hosaka, K. (2006). Origin and evolution of Andigena potatoes Physiol. 162, 1706–1719. doi: 10.1104/pp.113.217729 revealed by chloroplast and nuclear DNA markers. Genome 49, 636–647. Rodrigues, V. L., Dolde, U., Sun, B., Blaakmeer, A., Straub, D., Eguen, T., et al. Takada, S., and Goto, K. (2003). Terminal Flower2, an Arabidopsis homolog of (2021). A microProtein repressor complex in the shoot meristem controls heterochromatin protein1, counteracts the activation of flowering locus T by the transition to flowering. Plant Physiol. 187, 187–202. doi: 10.1093/plphys/ constans in the vascular tissues of leaves to regulate flowering time. Plant Cell kiab235 15, 2856–2865. doi: 10.1105/tpc.016345 Rodríguez-Falcón, M., Bou, J., and Prat, S. (2006). SEASONAL CONTROL Tamaki, S., Matsuo, S., Wong, H. L., Yokoi, S., and Shimamoto, K. (2007). Hd3a OF TUBERIZATION IN POTATO: conserved elements with the flowering protein is a mobile flowering signal in rice. Science 316, 1033–1036. response. Annu. Rev. Plant Biol. 57, 151–180. Tenreira, T., Pimenta Lange, M. J., Lange, T., Bres, C., Labadie, M., Monfort, A., Rosas, U., Mei, Y., Xie, Q., Banta, J. A., Zhou, R. W., Seufferheld, G., et al. (2014). et al. (2017). A specific gibberellin 20-oxidase dictates the flowering-runnering Variation in Arabidopsis flowering time associated with cis-regulatory variation decision in diploid strawberry. Plant Cell 29, 2168–2182. in CONSTANS. Nat. Commun. 5:3651. doi: 10.1038/ncomms4651 Thompson, P. A., and Guttridge, C. G. (1959). Effect of gibberellic acid on the Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J., initiation of flowers and runners in the strawberry. Nature 184, BA72–BA73. et al. (2007). A molecular timetable for apical bud formation and dormancy Tiwari, S. B., Shen, Y., Chang, H. C., Hou, Y., Harris, A., Ma, S. F., et al. (2010). induction in poplar. Plant Cell 19, 2370–2390. doi: 10.1105/tpc.107.052811 The flowering time regulator CONSTANS is recruited to the FLOWERING Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, LOCUS T promoter via a unique cis-element. New Phytol. 187, 57–66. doi: M. F., et al. (2000). Distinct roles of constans target genes in reproductive 10.1111/j.1469-8137.2010.03251.x development of Arabidopsis. Science 288, 1613–1616. doi: 10.1126/science.288. Turner, A., Beales, J., Faure, S., Dunford, R. P., and Laurie, D. A. (2005). Botany: 5471.1613 the pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in Sato, E., Nakamichi, N., Yamashino, T., and Mizuno, T. (2002). Aberrant barley. Science 310, 1031–1034. doi: 10.1126/science.1117619 expression of the Arabidopsis circadian-regulated APRR5 gene belonging to Valverde, F., Mouradov, A., Soppe, W., Ravenscroft, D., Samach, A., and Coupland, the APRR1/TOC1 quintet results in early flowering and hypersensitiveness G. (2004). Photoreceptor regulation of CONSTANS protein in photoperiodic to light in early photomorphogenesis. Plant Cell Physiol. 43, 1374–1385. doi: flowering. Science 303, 1003–1006. doi: 10.1126/science.1091761 10.1093/pcp/pcf166 Wang, C. Q., Guthrie, C., Sarmast, M. K., and Dehesh, K. (2014). BBX19 interacts Sawa, M., and Kay, S. A. (2011). GIGANTEA directly activates flowering locus with CONSTANS to repress FLOWERING LOCUS T transcription, defining T in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U S A. 108, 11698–11703. a flowering time checkpoint in Arabidopsis. Plant Cell 26, 3589–3602. doi: doi: 10.1073/pnas.1106771108 10.1105/tpc.114.130252 Sawa, M., Nusinow, D. A., Kay, S. A., and Imaizumi, T. (2007). FKF1 and Wang, H., Pan, J., Li, Y., Lou, D., Hu, Y., and Yu, D. (2016). The DELLA- GIGANTEA complex formation is required for day-length measurement in CONSTANS transcription factor cascade integrates gibberellic acid and Arabidopsis. Science 318, 261–265. photoperiod signaling to regulate flowering. Plant Physiol. 172, 479–488. doi: Schaffer, R., Ramsay, N., Samach, A., Corden, S., Putterill, J., Carré, I. A., et al. 10.1104/pp.16.00891 (1998). The late elongated hypocotyl mutation of Arabidopsis disrupts circadian Wang, Z. Y., and Tobin, E. M. (1998). Constitutive expression of the CIRCADIAN rhythms and the photoperiodic control of flowering. Cell 93, 1219–1229. doi: CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and 10.1016/S0092-8674(00)81465-8 suppresses its own expression. Cell 93, 1207–1217. doi: 10.1016/S0092-8674(00) Schmid, M., Uhlenhaut, N. H., Godard, F., Demar, M., Bressan, R., Weigel, D., et al. 81464-6 (2003). Dissection of floral induction pathways using global expression analysis. Wareing, P. F. (1956). Photoperiodism in woody plants. Annu. Rev. Plant Physiol. Development 130, 6001–6012. doi: 10.1242/dev.00842 7, 191–214. doi: 10.1146/annurev.pp.07.060156.001203 Frontiers in Plant Science | www.frontiersin.org 19 February 2022 | Volume 12 | Article 805635 Osnato et al. Flowering Time Genes Beyond Flowering Wickland, D. P., and Hanzawa, Y. (2015). The FLOWERING LOCUS closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell T/TERMINAL FLOWER 1 gene family: functional evolution and molecular 12, 2473–2484. doi: 10.1105/tpc.12.12.2473 mechanisms. Mol. Plant 8, 983–997. doi: 10.1016/j.molp.2015.01.007 Yant, L., Mathieu, J., and Schmid, M. (2009). Just say no: floral repressors help Wigge, P. A., Kim, M. C., Jaeger, K. E., Busch, W., Schmid, M., Lohmann, J. U., et al. Arabidopsis bide the time. Curr. Opin. Plant Biol. 12, 580–586. doi: 10.1016/j. (2005). Integration of spatial and temporal information during floral induction pbi.2009.07.006 in Arabidopsis. Science 309, 1056–1059. doi: 10.1126/science.1114358 Yant, L., Mathieu, J., Dinh, T. T., Ott, F., Lanz, C., Wollmann, H., et al. (2010). Wu, G., Park, M. Y., Conway, S. R., Wang, J. W., Weigel, D., and Poethig, R. S. Orchestration of the floral transition and floral development in Arabidopsis (2009). The sequential action of miR156 and miR172 regulates developmental by the bifunctional transcription factor APETALA2. Plant Cell. 22, 2156–2170. timing in Arabidopsis. Cell 138, 750–759. doi: 10.1016/j.cell.2009.06.031 doi: 10.1105/tpc.110.075606 Würschum, T., Langer, S. M., Longin, C. F. H., Tucker, M. R., and Leiser, Yoo, S. K., Chung, K. S., Kim, J., Lee, J. H., Hong, S. M., Yoo, S. J., et al. (2005). W. L. (2018). A three-component system incorporating Ppd-D1, copy number CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS variation at Ppd-B1, and numerous small-effect quantitative trait loci facilitates 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant adaptation of heading time in winter wheat cultivars of worldwide origin. Plant Physiol. 139, 770–778. doi: 10.1104/pp.105.066928 Cell Environ. 41, 1407–1416. doi: 10.1111/pce.13167 Yu, J. W., Rubio, V., Lee, N. Y., Bai, S., Lee, S. Y., Kim, S. S., et al. (2008). COP1 and Xing, L. L., Covington, M. F., Fankhauser, C., Chory, J., and Wagner, D. R. (2001). ELF3 control circadian function and photoperiodic flowering by regulating GI ELF3 encodes a circadian clock-regulated nuclear protein that functions in stability. Mol. Cell 32, 617–630. doi: 10.1016/j.molcel.2008.09.026 an Arabidopsis PHYB signal transduction pathway. Plant Cell 13, 1293–1304. Zeevaart, J. A. D. (1976). Physiology of flower formation. Annu. Rev. Plant Physiol. doi: 10.1105/tpc.13.6.1293 27, 321–348. Xu, F., Li, T., Xu, P. B., Li, L., Du, S. S., Lian, H. L., et al. (2016). DELLA proteins Zeevaart, J. A. D. (2009). My journey from horticulture to plant biology. Annu. Rev. physically interact with CONSTANS to regulate flowering under long days in Plant Biol. 60, 1–19. doi: 10.1146/annurev.arplant.043008.092010 Arabidopsis. FEBS Lett. 590, 541–549. doi: 10.1002/1873-3468.12076 Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J. M., Speed, T. P., et al. Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P., et al. (2011). Genome sequence (2013). A quartet of PIF bHLH factors provides a transcriptionally centered and analysis of the tuber crop potato. Nature 475, 189–195. signaling Hub that regulates seedling morphogenesis through differential Xu, X., van Lammeren, A. A. M., Vermeer, E., and Vreugdenhil, D. (1998). The expression-patterning of shared target genes in Arabidopsis. PLoS Genet. role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber 9:e1003244. doi: 10.1371/journal.pgen.1003244 formation in Vitro1. Plant Physiol. 117, 575–584. Zhao, H., Xu, D., Tian, T., Kong, F., Lin, K., Gan, S., et al. (2021). Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., et al. (2008). Natural Molecular and functional dissection of EARLY-FLOWERING 3 (ELF3) and variation in Ghd7 is an important regulator of heading date and yield potential ELF4 in Arabidopsis. Plant Sci. 303:110786. doi: 10.1016/j.plantsci.2020.1 in rice. Nat. Genet. 40, 761–767. doi: 10.1038/ng.143 10786 Yamaguchi, A., Kobayashi, Y., Goto, K., Abe, M., and Araki, T. (2005). TWIN Zhou, T., Song, B., Liu, T., Shen, Y., Dong, L., Jing, S., et al. (2019). Phytochrome F SISTER of FT (TSF) acts as a floral pathway integrator redundantly with FT. plays critical roles in potato photoperiodic tuberization. Plant J. 98, 42–54. Plant Cell Physiol. 46, 1175–1189. doi: 10.1093/pcp/pci151 Zimmerer, K. S. (1998). The ecogeography of andean potatoes. Bioscience 48, Yamamoto, Y., Sato, E., Shimizu, T., Nakamich, N., Sato, S., Kato, T., et al. (2003). 445–454. Comparative genetic studies on the APRR5 and APRR7 genes belonging to the APRR1/TOC1 quintet implicated in circadian rhythm, control of flowering Conflict of Interest: The authors declare that the research was conducted in the time, and early photomorphogenesis. Plant Cell Physiol. 44, 1119–1130. doi: absence of any commercial or financial relationships that could be construed as a 10.1093/pcp/pcg148 potential conflict of interest. Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., et al. (2006). The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc. Natl. Publisher’s Note: All claims expressed in this article are solely those of the authors Acad. Sci. U S A. 103, 19581–19586. doi: 10.1073/pnas.0607142103 and do not necessarily represent those of their affiliated organizations, or those of Yang, C. J., Samayoa, L. F., Bradbury, P. J., Olukolu, B. A., Xue, W., York, A. M., the publisher, the editors and the reviewers. Any product that may be evaluated in et al. (2019). The genetic architecture of teosinte catalyzed and constrained this article, or claim that may be made by its manufacturer, is not guaranteed or maize domestication. Proc. Natl. Acad. Sci. U S A. 116, 5643–5652. doi: 10.1073/ endorsed by the publisher. pnas.1820997116 Yang, Q., Li, Z., Li, W., Ku, L., Wang, C., Ye, J., et al. (2013). CACTA- Copyright © 2022 Osnato, Cota, Nebhnani, Cereijo and Pelaz. This is an open-access like transposable element in ZmCCT attenuated photoperiod sensitivity and article distributed under the terms of the Creative Commons Attribution License accelerated the postdomestication spread of maize. Proc. Natl. Acad. Sci. U S (CC BY). The use, distribution or reproduction in other forums is permitted, provided A. 110, 16969–16974. doi: 10.1073/pnas.1310949110 the original author(s) and the copyright owner(s) are credited and that the original Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., et al. publication in this journal is cited, in accordance with accepted academic practice. No (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Plant Science | www.frontiersin.org 20 February 2022 | Volume 12 | Article 805635