Plant Communications ll Review article Variability and limits of nitrogen and phosphorus resorption during foliar senescence Marc Estiarte1,2, Matteo Campioli3, Maria Mayol2 and Josep Penuelas1,2,* 1 CSIC, Global Ecology Unit CREAF-CSIC-UAB, 08193 Bellaterra, Catalonia, Spain 2 CREAF, 08193 Cerdanyola del Vallès, Catalonia, Spain 3 Research Group of Plant and Vegetation Ecology, Department of Biology, University of Antwerp, 2610 Wilrijk, Belgium *Correspondence: Josep Penuelas (josep.penuelas@uab.cat) https://doi.org/10.1016/j.xplc.2022.100503 ABSTRACT Foliar nutrient resorption (NuR) plays a key role in ecosystem functioning and plant nutrient economy. Most of this recycling occurs during the senescence of leaves and is actively addressed by cells. Here, we discuss the importance of cell biochemistry, physiology, and subcellular anatomy to condition the outcome of NuR at the cellular level and to explain the existence of limits to NuR. Nutrients are transferred from the leaf in simple metabolites that can be loaded into the phloem. Proteolysis is the main mechanism for mobi- lization of N, whereas P mobilization requires the involvement of different catabolic pathways, making the dynamics of P in leaves more variable than those of N before, during, and after foliar senescence. The biochemistry and fate of organelles during senescence impose constraints that limit NuR. The efficiency of NuR decreases, especially in evergreen species, as soil fertility increases, which is attributed to the rela- tive costs of nutrient acquisition from soil decreasing with increasing soil nutrient availability, while the en- ergetic costs of NuR from senescing leaves remain constant. NuR is genetically determined, with substan- tial interspecific variability, and is environmentally regulated in space and time, with nutrient availability being a key driver of intraspecific variability in NuR. Key words: foliar nutrient resorption, senescence, nitrogen, phosphorus, efficiency, nutrient availability Estiarte M., Campioli M., Mayol M., and Penuelas J. (2023). Variability and limits of nitrogen and phosphorus resorption during foliar senescence. Plant Comm. 4, 100503. RESORPTION OF FOLIAR NUTRIENTS significant negative effects on growth and reproduction that result from prevention of resorption offer strong support for the DURING SENESCENCE hypothesis that resorption contributes significantly to plant Nutrient resorption (NuR), or retranslocation, is a mechanism for fitness (May and Killingbeck, 1992). conserving nutrients by retrieving them from plant organs, espe- cially leaves, and plays a key role in ecosystem functioning. Most Most of this recycling occurs during the senescence of leaves. of the N and P used for global net primary productivity (89% N Senescing leaves become a source of nutrients to support cur- and 98% P) is recycled within ecosystems (Cleveland et al., rent new growth (e.g., senescence in evergreens or sequential 2013). NuR partitions the recycling of nutrients between an senescence in herbs), to support future growth (e.g., synchro- internal plant pathway and an external ecosystem pathway. nous developmental senescence in deciduous plants), or to fill Broadly, 35% of N and 41% of P are recycled within plants, seeds to transfer nutrients to the next generation (e.g., entire and 65% of N and 59% of P are recycled externally by the plant senescence in annuals). A fraction of nutrients can be re- mineralization of dead plant organic matter in the soil before re- sorbed from mature green leaves before they senesce, especially entering plants by root uptake (Cleveland et al., 2013). Foliar in the presence of active sinks (e.g., seasonal growth in ever- NuR plays an additional role because it determines the greens [e.g., Fife et al., 2008] or seed filling). Foliar nutrients are nutritional quality of leaf litter entering the soil, influencing the also resorbed during foliar senescence induced by abiotic mineralization rates and thus the release of nutrients in organic stress, e.g., drought, when plants reduce canopy size or matter to plants and soil microbes (Ha €ttenschwiler et al., 2011). eliminate non-acclimated or damaged tissues. Nutrients in green Its importance for the N cycle is such that N resorption (NR) (Table 1) accounts for nearly 25% of the variability in the rate of Published by the Plant Communications Shanghai Editorial Office in N mineralization, because N-rich leaf litter releases N, whereas association with Cell Press, an imprint of Elsevier Inc., on behalf of CSPB and N-poor leaf litter immobilizes N (Deng et al., 2018). The CEMPS, CAS. Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). 1 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Plant Communications Nitrogen and phosphorus resorption in foliar senescence Abbreviation Definition Extra information or definition NuR nutrient resorption Nu.green nutrients in green leaves, maximum Nu.sen + Nu.res values Nu.sen nutrients that remain in the senesced leaves Nu.res nutrients that are resorbed [Nu]sen concentration of nutrients in senesced leaves [Nu]green concentration of nutrients in green leaves NuUE nutrient-use efficiency NuRE nutrient resorption efficiency Nu.res/Nu.green is the fraction of nutrients present at the nutrient peak in mature leaves that are withdrawn before foliar shedding or death Table 1. Abbreviations used in this study for variables involved in foliar nutrient resorption during foliar senescence. Nu can be substituted with N or P for all cases. leaves (Nu.green) are either resorbed (Nu.res) or remain in the incomplete resorption is associated with weak selective forces, senesced leaves (Nu.sen), so Nu.green = Nu.res + Nu.sen. such as nutrient-rich soil orders, or with factors that impede this Reduced C is also retrieved during senescence, and the impor- physiological process (e.g., drought). Inter-annual variability in tance of salvaging C skeletons for maintenance of plant C and en- resorption is common, particularly for phosphorus. This plasticity ergy reserves should not be overlooked, although we are has implications for ecosystem nutrient cycling and plant produc- focusing here on nutrients, especially N and P. tivity, and accounting for this plasticity in dynamic models of nutrient cycling will improve predictions of nutrient limitations Plant ecophysiological studies frequently describe nutrient and productivity under future climate conditions (Drenovsky resorption as an issue of efficiency, likely as a legacy from the et al., 2019). concept of nutrient-use efficiency. Nutrient resorption efficiency (NuRE) is the fraction of nutrients present at peak nutrient levels Here, we examine different mechanisms involved in NuR in mature leaves that are withdrawn before foliar shedding or (Figure 1). We start at the biochemical and subcellular levels to death (i.e., NuRE = Nu.res/Nu.green). NuRE is conveniently address the mobility of nutrients and how these biochemical used to address relative comparisons of the ability of species and subcellular levels affect the limits to resorption. We to conserve acquired nutrients. NuRE, however, poses problems examine the existence of limits to the resorption of N and P of interpretation because both terms of the ratio may change. with a large database of N and P in green and senesced leaves. We then discuss two processes identified as important for NuR: NuRE has been considered inappropriate for searches for evolu- phloem loading and foliar abscission. We next describe the tionary patterns because selection to minimize nutrient losses genetic regulation of deployment of NuR mechanisms to further acts on the nutrients remaining in senesced leaves (Nu.sen) address how the environment regulates their deployment, rather than on proportional NuR per se (Killingbeck, 1996; Wright emphasizing nutrient availability as a driver of the variability in and Westoby, 2003). Killingbeck (1996, 2004) has remarked on NuR within species. Finally, we introduce the role of sink the importance in evolutionary studies of the proficiency of nutrient demand in NuR. resorption, defined as the terminal nutrient concentration in senesced leaves ([Nu]sen). Nu.sen may thus be more appropriate for studying the dependence of resorption on senescence. Here, DIFFERENT MOBILITY OF VARIOUS we revisit the ideas of Killingbeck (1996, 2004) and other BIOCHEMICAL AND SUBCELLULAR authors on NuR in light of advances in our understanding of the physiology, biochemistry, and regulation of foliar senescence FRACTIONS OF N AND P and the regulation of resorption. Ecological studies previously Nutrients can be separated into non-mobilizable and potentially analyzed nutrient pools and plant demands rather than the mobilizable fractions, a difference that depends on their subcel- mechanisms that regulate NuR. These studies, therefore, usually lular location and biochemistry. To achieve complete resorption, did not differentiate between the influence of species genetic abscission or laminar death must occur after all mobilizable nutri- differences in the regulation of NuR and phenotypic differences ents have been exported and only the non-mobilizable nutrients due to the environmental regulation of resorption (see Figure 1). remain in the senesced leaf. The non-mobilizable compounds Overall, environmental and biological factors that represent a determine the limits of potential resorption. NuR will not be strong selective force for nutrient conservation, such as nutrient- complete if the realized resorption is less than the potential poor soil orders, semi-arid soil moisture regimes, or lack of plant resorption, i.e., mobilizable nutrients remain in the senesced mutualists, are associated with complete resorption, whereas leaf (Figure 1). 2 Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). Nitrogen and phosphorus resorption in foliar senescence Plant Communications Figure 1. Schematic of foliar nutrient resorption during senescence. The mobilization of nutrients requires the degradation of macro- Similarly, foliar P can be partitioned into structural or lipidic P molecules and their conversion into simple metabolites contain- (phospholipids), metabolic or easily soluble P (Pi, ATP, and sugar ing nutrients (Figure 2 and Table 2). Nutrients are transferred phosphates), and P in nucleic acids and residual components from the leaf in these simple metabolites, loaded into the (phosphoproteins and some unidentified residues) (Hidaka and phloem, and transported to sink tissues. Kitayama, 2011; Tsujii et al., 2017). The mechanisms for mobilization depend on the type of nutrient- N is thus overwhelmingly found in proteins that can be partitioned containing macromolecule. Seventy-five to 85% of foliar N is con- by their location, solubility, and accessibility. This partitioning al- tained in proteins (Chapin, 1989; Takashima et al., 2004; lows us to hypothesize about NR. For example, more N allocated Yasumura et al., 2006), 9%–15% in nucleic acids (Chapin and to cell walls in evergreen than deciduous species (Takashima Kedrowski, 1983; Evans and Seemann, 1989), and minor et al., 2004) could account for the lower NRE in evergreens. amounts (1%–2%) in chlorophylls (Makino and Osmond, 1991), The higher variability in phosphorus resorption (PR) than NR is in free amino acids, and as inorganic N (Fischer, 2007). due to P fractions being more biochemically diverse than N Proteolysis is consequently the main mechanism for mobilizing N. fractions and having a more diverse mobilization. [P]green in natural ecosystems typically ranges from 0.1 to 3.0 mg Nutrients, however, are also harbored in cell organelles other than g 1 (e.g., Vallicrosa et al., 2022). Foliar P is found in inorganic (Pi) the cell wall, and they differ in their fate during senescence. A bet- or organic (Po) forms. Pi is found in variable amounts that average ter understanding of the mobility of nutrients can be achieved by 58% of the total P pool (Veneklaas et al., 2012). The remaining Po taking into account subcellular localization and the functions of fraction is distributed as 48% in nucleic acids, 31% in lipids and the organelles and macromolecules containing the nutrients 21% in esters (Sanchez, 2007). P mobilization therefore requires (Figure 2). A more informative characterization of foliar N a variety of catabolic pathways. considers structural, photosynthetic, respiratory, and so-called storage fractions (Xu et al., 2012; Liu et al., 2018). Alternatively, Two fractions of foliar N were historically considered (Charles- proteins can be identified by their solubility: insoluble proteins Edwards et al., 1987), one metabolic or labile, assumed to be in the cell wall, detergent-soluble proteins in membranes (mostly completely available for resorption, and the other structural, thylakoid-bound), and water-soluble proteins (mostly in the chlo- assumed to be non-degradable (e.g., Niinemets and Tamm, roplast stroma). 2005). The structural fraction refers to cell-wall proteins, which contain 1.5%–13% of the foliar N (Onoda et al., 2017; Liu Understanding that NuR is actively addressed by cells is impor- et al., 2018) or even as high as 30% (Harrison et al., 2009). tant for comprehending the mobility of nutrients during resorp- The lignocellulosic cell wall is mostly not degraded during tion. The requirement of cell machinery for this active task renders senescence, which renders the structural proteins that are impossible the resorption of nutrients embedded in the cellular crosslinked and tightly bound to the cell wall mostly inaccessible machinery conducting the mobilization or nutrients in the cellular to proteases. About 75%–90% of structural proteins remain components essential for maintenance of cell viability. Several undegraded at cell death (Yasumura et al., 2006; Yasumura and decades ago, Charles-Edwards et al. (1987) envisaged that Ishida, 2011). Structural proteins have been considered to nutrients ‘‘involved in maintaining the membrane function and account for most of the N in litter (McGroody et al., 2004) and to integrity [.], and the transport processes by which materials set the lower limit for [N]sen (Yasumura et al., 2006). are exported’’ likely remained in senesced/abscised leaves. Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). 3 Plant Communications Nitrogen and phosphorus resorption in foliar senescence although we lack information on the fate of the hydrolytic enzymes. Vacuoles receive components of the chloroplast for degradation. Senescing cells can obtain energy from the catabolic activity of the mitochondria (see Chrobok et al., 2016), rendering chloroplasts non-essential for short-term cellular survival. Chlo- roplasts contain large amounts of water-soluble proteins for carboxylation in the stroma, such as Rubisco, and thylakoid- bound proteins for electron transfer and light capture. The high N concentration of chloroplasts, about 50%–60% of foliar N (Mostowska, 2005) or even up to 80% (Makino and Osmond, 1991), especially in mesophyll cells (Peoples and Dalling, 1988), renders their dismantling key for NuR. Chloroplasts degrade and break down before other organelles through processes that take place within and outside them. Chloro- Figure 2. Changes in compounds and organelles during the plasts decrease in size during foliar senescence by transfer of their progression of leaf senescence. Rubisco-containing bodies toward the vacuole. Chloroplasts also From Keskitalo et al. (2005), Tamary et al. (2019), Bhalerao et al. (2003), often decrease in number by vacuolar autophagy of entire chloro- Rolny et al. (2011), and Chrobok et al. (2016). plasts (Ishida and Makino, 2018; Izumi and Nakamura, 2018; Buet et al., 2019). The chloroplasts remaining at the final stages The plasmalemma is maintained to preserve cell integrity until final of senescence have been transformed into gerontoplasts after cell collapse. Previously, it was considered to increase in leakiness losing their ultrastructure and thylakoid membrane system from early stages of senescence onwards (Thompson et al., 1998), (Krupinska, 2007; Fulgosi et al., 2012), and chloroplasts can but detailed studies showed that the integrity of the plasmalemma sometimes disappear completely (Sorin et al., 2015). The degree extends to later stages (Rolny et al., 2011). Although the lipidic of degradation and disappearance determines the proportion of P fraction has been considered "structural" (e.g., Hidaka and chloroplastic nutrients that remain at the end of senescence. Kitayama, 2011), deterioration of the plasmalemma is a consequence of the partial degradation of phospholipids, the Mitochondria, despite their high concentrations of nutrients, must main components of the cell membrane (Borochov et al., 1982). remain functional to provide cells with energy and C skeletons until Phospholipid hydrolysis and replacement by galactolipids and the end of senescence. Mitochondria are constituted of a protein- sulfolipids during leaf senescence is an important strategy by rich matrix with circulating P-esters and a very protein-rich inner which plants can improve phosphorus use efficiency without membrane made of phospholipids (Horvath and Daum, 2013). compromising membrane integrity or function, especially in the The number of mitochondria can decrease during senescence, case of phosphorus deficiency. The plasmalemma also contains with declines ranging from 30% to 75% of pre-senescence con- transport proteins that are required to export the mobilized centrations (Keech et al., 2007; Ruberti et al., 2014; Chrobok nutrients to the apoplast and for their import into companion et al., 2016). Cells contain whole mitochondria (Keskitalo et al., cells through apoplastic phloem loading (Tegeder, 2014). To 2005) that contain transcripts for the catabolism of amino acids accomplish this key role, several membrane transporters are and fatty acids and that maintain respiratory metabolism until the induced during senescence, some exclusively at this stage (Have advanced stages of senescence (Chrobok et al., 2016). Large et al., 2017), suggesting that they remain among the undegraded amounts of mitochondrial nutrients can consequently remain in phospholipids until the end of senescence and are unlikely to be senesced leaves. resorbed. Nucleic acids are the most important pool of Po. The nucleus, The vacuole is a key organelle for storing nutrients and energy containing DNA and nuclear proteins, is required to govern during final major recycling at foliar senescence (Yang et al., senescence by the provision of transcripts and is maintained until 2017). During the cell’s lifespan, the vacuole acts as a final degradation at cellular death. By contrast, chloroplastic DNA compartment for storing metabolites and nutrients (Tan et al., is degraded during chloroplast dismantling (Fulgosi et al., 2012). 2019). The vacuole stores P that exceeds the requirements of Eighty percent of the P in nucleic acids is contained in RNA, cellular metabolism as Pi (Pratt et al., 2009), which under a non- mostly as ribosomal RNA (Veneklaas et al., 2012). Pi can be limiting P supply may represent a large proportion of cellular resorbed earlier without altering cellular function, but P in P (Veneklaas et al., 2012). The vacuole has a central role in ribosomes may be required for the synthesis of proteins for the degradation of proteins and RNA because it receives reprogramming senescence. Ribophagy, the autophagy of macromolecules from the cytoplasm and organelles and ribosomes, leads to the degradation of vacuolar rRNA and its because it contains most of the cellular hydrolytic enzymes associated proteins (Floyd et al., 2015). RNAses are common (Mu€ntz, 2007; Yang et al., 2017). The vacuole remains intact for during senescence, and total RNA levels decrease rapidly a long time during foliar senescence, although by the end of the (Chapin and Kedrowski, 1983; Bhalerao et al., 2003), with clear process, it may end up in such a degraded state that it cannot initial decreases in chloroplastic rRNAs and cytoplasmic rRNAs be distinguished from the cytoplasm (Keskitalo et al., 2005). followed by decreases in cytoplasmic mRNAs and tRNAs (Lim Most nutrients have already left the vacuole at this stage, and Nam, 2007). 4 Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). Nitrogen and phosphorus resorption in foliar senescence Plant Communications Function during senescence Content Period of activity during senescence Vacuole recycling (degradation of proteins and hydrolytic enzymes until the end of senescence RNA) and storage of nutrients Chloroplast source of nutrient-containing Rubisco-containing bodies and disappearance during senescence macromolecules thylakoid-bound proteins for electron transfer and light capture (degraded during senescence) Mitochondrion provide energy transcripts for the catabolism of amino until the end of senescence acids and fatty acids (not degraded during senescence) Nucleus governs senescence DNA and nuclear proteins (transcripts) until the end of senescence Table 2. Functions and activities of key organelles involved in foliar senescence. Nutrient pools recalcitrant to export depend on the organelle and (0.8/0.5 mg g 1) P (deciduous/evergreen) corresponded to its function. For example, nutrients embedded in the enzymatic incomplete resorption. Killingbeck did not advocate for a machinery responsible for mobilization are difficult to export common value of potential [Nu]sen for all species but for a range (Killingbeck, 2004). The many proteases upregulated during of values. Ha €ttenschwiler et al. (2008) later hypothesized that senescence are candidates for retention (Avice and Etienne, interspecific differences in [Nu]green should converge in [Nu]sen, 2014), but we are not aware of details on the final fates of the but the existence of a common minimum [P]sen was not many hydrolytic enzymes. Enzymes that are upregulated late supported in a neotropical rainforest where [P]sen was much more and that remain until the late stages of senescence, such as the variable than [P]green, likely because the dataset included many cysteine protease SAG12 present in vacuoles associated with values of incomplete resorption. senescence (Avice and Etienne, 2014), are more likely to remain in senesced leaves. Other candidates with activity in the late Incomplete resorption is not rare (Drenovsky et al., 2019) and stages of senescence are the cytosolic glutamine synthetase hinders the elucidation of the limits of NuR. Quantile regression GS1 and asparagine synthetase, which recycle ammonia from of [Nu]sen on [N]green has been used to delimit the limits of NuR, protein degradation to produce glutamine and asparagine, an approach that allows the limits to vary with [Nu]green. Ratnam respectively (Avila-Ospina et al., 2015). et al. (2008) used the 0.10 quantile regression on a database of savanna grasses and broadleaved species, but the slope obtained did not differ from zero, and the intercept values Limits to NuR yielded [N]sen and [P]sen similar but slightly lower than those Scaling down to the subcellular level exposes the constraints on from Killingbeck (1996) (5 and 8 mg g 1 N for grasses and NuR imposed by cell physiology. Cellular components other than broadleaved trees, respectively, and 0.3 mg g 1 P for both the cell wall also remain in leaves after senescence has ended, functional groups). along with the nutrients they contain (see Figure 2). In addition to the nutrients embedded in the cell wall, those required to Here, we present the limits to NuR using a database of N and P in maintain metabolic activity (mitochondria) and cellular integrity green and senescent leaves including circa 1800 and 1500 points (plasmalemma), those required to regulate the cell (nucleus), for N and P, respectively (see Figure 3 for a description of the those in the enzymatic machinery for mobilizing nutrients or in database). We estimated the limits to NuR using the 0.05 transporters for phloem loading, and those in undegraded parts quantile regression on this database. The regression indicates of the vacuoles and chloroplasts will also remain. These that the limits to NuR increase as [Nu]green increases in a similar nutrients, which are not recycled in most plants, determine the way for both N (slope = 0.181 ± 0.012, p = 0.0000) and P physiological limits to NuR (e.g., Killingbeck, 2004; Tully et al., (slope = 0.203 ± 0.0168, p = 0.0000). The increase in the limits 2013). Figure 1 represents the strictly non-mobilizable nutrients with [Nu]green indicates either that the absolute amount of that delimit NuR as a small part of the total nutrients available nutrients in non-resorbable fractions (i.e., the strictly non- for resorption. mobilizable nutrients in Figure 1) is larger when [Nu]green is more concentrated or that species adapted to nutrient impoverished When the amount of N in senesced whole leaves is greater than the environments (and with lower [Nu]green) have mechanisms that amount in structural proteins in the cell walls of green leaves, this enable them to scour leaf nutrients more deeply (i.e., in Figure 1 means that N other than that in the cell walls remains in senesced the species-specific limit approaches the structural and func- leaves. Alternatively, remnants of chloroplastic N in senesced tional limits of NuR). The limits of resorption are clear for N even leaves are unequivocal when NRE is lower than the percentage of at the lowest [N]green because the intercept of the regression is N allocated to the photosynthetic apparatus, which may account clearly positive (intercept = 1.593 ± 0.162, p = 0.0000). This is for 30% in evergreens and 40% in deciduous plants (Takashima not the case for P, whose limits of resorption blur at very low et al., 2004). Killingbeck (1996) proposed that, after "complete" [P]green values, leading to a negative intercept of the quantile resorption, [Nu]sen attains concentrations <0.7% (7 mg g 1) for regression (intercept = 0.023 ± 0.006, p = 0.0000). N and <0.05% (0.5 mg g 1) for P in deciduous plants and <0.04% (0.4 mg g 1) in evergreens. He therefore suggested Differential effects of environmental conditions on the timing and that concentrations >1.0% (10 mg g 1) N and 0.08%/0.05% strength of N-mobilization versus P-mobilization processes may Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). 5 Plant Communications Nitrogen and phosphorus resorption in foliar senescence Figure 3. [Nu]sen versus [Nu]green for foliar N and foliar P. Top black dotted lines represent the points where [Nu]sen is 100% of [Nu]green (i.e., NuRE = 0%), the middle line where it is 50% (i.e., NuRE = 50%), and the lower line where it is 25% (i.e., NuRE = 75%). Vergutz et al. (2012) suggested using a mass loss correction factor (MLCF) of 0.784, 0.780, and 0.745 to account for leaf mass loss during leaf senescence due to resorption processes in deciduous broadleaf, evergreen broadleaf, and coniferous species, respectively. The MLCF decreases the value of [Nu]sen and increases estimates of NuRE. We chose not to introduce such correction for individual entries in the database because we found it likely that individual values for mass loss vary depending on the actual performance of the senescence process. However, for orientation purposes, green and orange lines in the plots represent NuRE values of 0%, 50%, and 25% after correction for leaf mass loss using an MLCF of 0.763 obtained by averaging the values for broadleaves and conifers suggested by Vergutz et al. (2012). The blue line represents the 0.05 conditional quantile regression line to the data and delineates the lower 5th percentile of the points. We used this line to define the limits of NuR. The data presented correspond to our merging of four databases (Vergutz et al., 2012; Hayes et al., 2014; Sohrt et al., 2018; Jiang et al., 2019). Data from Freschet et al. (2010) were excluded from the database of Vergutz et al. because the values were anomalously low for the two elements and the two leaf stages. The final database included 1773 entries for [N]green and [N]sen and 1417 entries for [P]green and [P]sen. alter the coordination of relationships between these two implication of the hypothesis is that NuRE decreases as soil elements. For example, N fertilization weakens the relationship fertility increases, as does its competitive advantage, because between [N]green and [P]green but does not weaken the relationship the relative costs of acquiring nutrients from soil decrease as con- between [N]sen and [P]sen (You et al., 2018), suggesting that centrations of soil nutrients increase, but the energetic costs of [Nu]sen can be anchored to a lower limit of non-mobilizable nutri- NuR from senescing leaves remain constant. ents but that [Nu]green mostly depends on nutrient uptake and has less-strict limits that can even increase dramatically after luxury The diversity of nutrient-containing compounds and organelles, uptake. larger for P than for N, may add heterogeneity to the costs of resorption. For example, proteins were the source of 87% of [P]green is more variable than [N]green (e.g., Rejmánková,2005; the N removed during senescence, whereas 45% and 32% of re- Ha€ttenschwiler et al., 2008; Vallicrosa et al., 2022). [P]sen is also sorbed P came from nucleic acids and phospholipids, respec- more variable than [N]sen (e.g., Aerts et al., 2012), perhaps tively, in several Alaskan trees (Chapin and Kedrowski, 1983). reflecting differences in the mobilization potentials of N- and Overall support for the hypothesis of costs is provided by P-containing molecules (i.e., Han et al., 2013). Higher variabilities stronger mobilization of nutrients from recalcitrant compounds of [P]green and [P]sen lead to higher variability of PRE (phosphorus in nutrient-poor soils (Hidaka and Kitayama, 2011; Tsujii resorption efficiency) compared with NRE (Ha €ttenschwiler et al., et al., 2017). 2008; Han et al., 2013), with PRE reported to vary two-fold with moderate variation in [P]green (Kobe et al., 2005). This variability The variety of P fractions and differences in their degradation may explain discrepancies in studies of the relationships of pathways have been suggested to underlie the variability among [P]green with PR. Tsujii et al. (2017) predicted a strong correlation species in PR associated with gradients of soil P availability. between [P]green and [P]sen because they hypothesized that a Hidaka and Kitayama (2011) reported that metabolic P and P in constant PRE would be expected if the relative amount of mobile nucleic acids decreased across species as the availability of P P was a function of total foliar P. Another study, however, decreased, whereas PR increased. The amount of P resorbed reported that the variability in PR among species was by species in P-poor soils exceeded the metabolic-P fraction, independent of [P]green (Ha €ttenschwiler et al., 2008). indicating that a high PR requires resorption from immobile frac- tions (Hidaka and Kitayama, 2011). Another study found that PR was proportionally higher from the lipid and nucleic acid P COST OF RESORPTION fractions than from the easily soluble and residual P fractions The link between plant economy and nutrient partitioning among and that lower [P]sen and higher PRE were associated with compounds has been used as a benchmark to account for the greater degradation of the residual fraction in species growing variability in NuR among species based on the costs of resorp- where P is scarce (Tsujii et al., 2017). tion. The process of nutrient resorption requires energy con- sumption, for example, the process of loading nutrients from Easily soluble simple compounds are already mobile, and their the source organ to the phloem through the symplastic transport resorption therefore has a minor additional cost; according to pathway and then unloading from the phloem to the sink organ. the hypothesis, they should be completely resorbed. For Wright and Westoby (2003) hypothesized that the trade-off be- example, the resorption of Pi, the main form of P in the phloem tween nutrients resorbed and those taken up by roots depended (Młodzinska and Zboin ska, 2016), only requires the action on the relative cost of obtaining nutrients from each source. One of membrane transporters (Versaw and Garcia, 2017). The 6 Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). Nitrogen and phosphorus resorption in foliar senescence Plant Communications presence of Pi and free amino acids in senesced leaves suggests not in the intensely studied Arabidopsis and cereals. Abscission that they are resorbed less than predicted (see phloem loading for truncates phloem transport and hence NuR. Leaves detach at an extended discussion), which is in apparent contradiction with the abscission zone, a few layers of cells at the base of the the cost hypothesis. However, these compounds are also petiole that differentiate long before the onset of senescence obtained from the degradation of macromolecules and are (Primka and Smith, 2019). Detachment occurs after dissolution found in leaves while transiting toward export; they can be by enzymatic hydrolysis of the pectin in the middle lamella that trapped in leaf litter if abscission occurs before complete binds cells. This dissolution is ultimately triggered (Patharkar resorption, but this does not contradict the cost hypothesis. and Walker, 2018) and progresses with the progression of laminar senescence. We believe that a more detailed assessment of the economy of resorption is needed to update the ideas proposed by Wright Leaf lifespan is genetically determined by a hormonally governed and Westoby (2003). We have to incorporate not only the process, although the process may be regulated by external fac- nutrients, but also the energy and C concentrations of the tors and stresses. Both foliar abscission and laminar senescence resorbed compounds that would be wasted when leaves fall if are stimulated by ethylene and inhibited by auxin, facilitating their the compounds were not resorbed. We also have to take into coordination. Leaves that are shed when completely yellow account that energy for resorption can be supplied by contain living laminar cells and are often assumed to have catabolizing compounds whose energy would be lost if they completed senescence and hence NuR, although the last step remained non-catabolized in fully senesced leaves. in foliar cell senescence is programmed cell death. Abscission and laminar senescence, however, can be uncoordinated, e.g., in marcescent trees that maintain attached leaves after death of TWO ADDITIONAL KEY STEPS FOR the laminar cells. The opposite may occur in non-marcescent NUTRIENT RESORPTION: PHLOEM trees when events in the abscission zone progress faster than the senescence of the lamina and leaves containing chlorophyll LOADING AND FOLIAR ABSCISSION are shed, for example, because of drought (Renterı́a et al., The final outcome of NuR could potentially be affected by phloem 2005; Renterı́a and Jaramillo, 2011). loading and foliar abscission. Phloem loading of mobile metabo- lites is the final step of resorption after nutrients are mobilized. Abscission before the completion of senescence could underlie the Mobilized nutrients should ideally be completely exported, higher [Nu]sen in leaves that fall earlier in winter in deciduous plants but simple metabolites, such as Pi and amino acids, may be (Niinemets and Tamm, 2005; See et al., 2015). For example, NuR in an important fraction of [Nu]sen (Chapin and Kedrowski, 1983; a winter deciduous clone (Populus tremuloides) was lower in leaves Da Ros and Mansfield, 2020), raising the possibility that NuR that abscised earlier within individual ramets and was also lower in may be limited by low phloem loading (Chapin and Moilanen, older ramets senescing earlier than in younger ramets senescing 1991). This possibility led Yasumura et al. (2006) to propose later (Killingbeck et al., 1990). NuR in the same clone was also that [N]sen >25% accounted for by proteins was due to lower for 3 consecutive years when abscission occurred 1 week accumulation of free amino acids. Similarly, low PR and earlier, likely owing to drought during the preceding summer accumulation of Pi in senesced leaves under abundant P was (Killingbeck et al., 1990). The importance of abscission, however, suggested to indicate a limitation in the rate of Pi export by cannot be ascertained from this type of field data, because the transporters at the vacuole (Da Ros and Mansfield, 2020). timing of the onset of senescence and its rate of progression must be known in order to determine whether premature The suggested role of phloem loading as a bottleneck for NuR has abscission or the effect of stress on nutrient mobilization is the not been demonstrated. Low NR in the crop Brassica napus was cause of low NuR. The longer the period between the onset of attributed to limited N phloem loading, but this was not supported senescence and abscission, the more likely it is that resorption by evidence from the dynamics of amino acids in the leaves or the will be complete. Truncating NuR before the completion of phloem or by the expression of amino acid permeases (Tilsner senescence notably reduces the resorption of all nutrients, et al., 2005). Low NR in one cultivar was instead attributed to producing a signal resembling the coordination of resorption delayed proteolysis and hence delayed N mobilization and among nutrients. export (Girondé et al., 2015a, 2015b). However, studies must be extended phylogenetically beyond the brassicas to resolve VARIABILITY IN NuR: NuR IS the importance of loading for NuR. Studies of deciduous species with synchronous senescence throughout the canopy, GENETICALLY DETERMINED (NOW THIS, in which large amounts of mobile metabolites are in the phloem NOW THAT) AND ENVIRONMENTALLY when resorption is intense, would emphasize the importance of REGULATED (MORE THIS, LESS THAT) loading. Studies during synchronous senescence could resolve whether high concentrations of mobile metabolites in laminar Genetic regulation cells are required until late senescence to maintain gradients Beyond the contribution of abscission, the regulation of senes- with the phloem. If so, this would increase the probability of cence is the main source of variation in NuR. Foliar senescence nutrient permanence in the litter if abscission is not finely lasts from days to a few weeks and progresses by an ordered suc- coordinated with senescence. cession of molecular, biochemical, physiological, and cellular events that unfold over time in a highly regulated manner Foliar abscission is another important step for NuR. Leaves (Jansson and Thomas, 2008). The regulation of events associated abscise at the end of senescence in many plant species, although with NuR during foliar senescence involves controls at the Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). 7 Plant Communications Nitrogen and phosphorus resorption in foliar senescence genetic, developmental, and environmental levels (Brant and Chen, of genetics for NuR (Chapin and Moilanen, 1991; Minoletti and 2015). The genetics of regulation sets the species-specific limits for Boerner, 1994; Killingbeck, 2004), even considering that genetic NuR (Figure 1). In practice, the external environment and internal factors are stronger determinants of NR patterns than are plant conditions regulate the deployment of genetically environmental factors (Stewart et al., 2008). Fittingly, NuR and determined steps for NuR during senescence. Environmental [Nu]green, especially for N but also for P, have been reported to be regulation likely prevents NuR from reaching species-specific rooted within phylogenetic lines (e.g., Tsujii et al., 2017). limits, and a fraction of mobilizable nutrients are not mobilized and remain in senesced leaves (Figure 1). Genetic differences produced during crop breeding provide use- ful systems for studying the regulatory mechanisms that control Leaves follow an ontogenetic and age-dependent developmental NuR. Oilseed rape (B. napus), which has been intensively studied pathway toward senescence that is assumed to transit through because of its low NRE during the vegetative phase (Avice and three phases (Jibran et al., 2013; Schippers, 2015). Leaves first Etienne, 2014), has provided enlightening information. For pass through the young growth phase, when they do not respond example, genotypes with a higher NRE under N limitation break to senescence-inducing factors, and then through the mature down more soluble protein and have higher activities of serine phase, when they become sensitive to internal and external and cysteine proteases (Girondé et al., 2015a, 2015b), perhaps senescence-inducing factors, i.e., they are able to senesce. Senes- due to the higher hormonal ratio ([salicylic acid] + [abscisic cence is the last phase. The ability to senesce is acquired through acid])/([cytokinins]) during foliar senescence (Poret et al., 2017). changes associated with age and increases with age. The different rates of amino acid export that underlie genotypic variability in the NR response to N availability may also depend Foliar senescence reprograms the transcriptome (Breeze et al., on differences in the regulation of amino acid transporters 2011; Stigter and Plaxton, 2015) and affects the expression of (Girondé et al., 2015a, 2015b). thousands of genes to shift cellular metabolism from anabolic to catabolic (Guo, 2013). This shift is achieved by downregulating In observational studies, genetic differences may underlie differ- many genes, such as those involved in photosynthesis, and ences in NuR among populations (Staaf and Stjernquist, 1986) upregulating the so-called senescence-associated genes (Lim and even individuals (Nordell and Karlsson, 1995). Certainty is et al., 2007; Breeze et al., 2011; Kim et al., 2018). The achieved with controlled and common garden experiments that upregulated genes follow a coordinated schedule to turn on allow us to discern the genetic basis of differences in NuR the physiological and cellular mechanisms and establish the performance, e.g., among poplar clones (Harvey and van den metabolic machinery for the mobilization of nutrients. Driessche, 1999), among populations of Pinus sylvestris (Oleksyn et al., 2003) or Metrosideros polymorpha (Treseder and Vitousek, The developmental pathway to senescence is controlled by the 2001), or among Helianthus species (Rea et al., 2018). interplay between plant hormones and incorporates signals from reactive oxygen species and sugars (Lim et al., 2007). Differences in NuR in the field among sympatric species in the Phytohormones regulate the activation or repression of genes same environment, e.g., as reported in a neotropical rainforest encoding transcription factors, which initiate the signaling (Ha€ttenschwiler et al., 2008), clearly indicate differences in either cascades that affect gene expression (Woo et al., 2013). The the environmental or genetic regulation of NuR. An obvious onset of senescence is regulated by transcription factors from example is a subtropical deciduous tree species that extends its different families (NAC, MYB, AP2, and WRKY) (Luoni et al., foliar lifespan into winter, with leaves in a senescence-like state 2019). The NAC family, which includes the well-known transcrip- with reduced chlorophyll and accumulation of anthocyanins. This tion factors ORE1 and AtNAP and some microRNAs for post- tree species has higher NRE and PRE than coexisting deciduous transcriptional regulation, plays a central role in foliar senescence trees that have no anthocyanin and do not extend foliar lifespan (Kim et al., 2018). (Zhang et al., 2013). NuR differs in many coexisting species, e.g., in forests (Ha €ttenschwiler et al., 2008) and shrublands (Drenovsky et al., 2010). For instance, Figure 4 shows that, Intergenotypic/interspecific variability along an altitudinal gradient, a deciduous shrub and a grass The overall variability in NuR across plants is also partly due to have very different patterns of NR as a function of [N]green, genetically determined species-specific differences in the regula- with the grass being able to scour both N and P more deeply tion of senescence and the mechanisms that control NuR during NuR. (Figure 1). Foliar senescence is highly conserved. The details of deployment of the program are genetically differentiated Species and genotypes generally differ in how tightly they (Chrobok et al., 2016). Different aspects of this differentiation deploy and activate the machinery for NuR and in the sensitivity have been detected, e.g., in the timing of foliar senescence, as of deployment to external factors. Genetic differences in NuR described in cotton lines, likely caused by differences in the under natural conditions are assumed to be determined by evolu- expression of genes associated with hormones and transcription tionary history (Killingbeck and Whitford, 2001). Constitutively factors (Kong et al., 2013), in pigment dynamics by senescence, high NuR leads to high NuUE, which is advantageous and thus as described in trees differing in shade tolerance (Garcia-Plazaola an adaptation to nutrient-poor habitats (Vitousek, 1982). The et al., 2003), or in the mechanisms of dismantling chloroplasts, as strong selection of traits to minimize nutrient loss in nutrient- described for barley cultivars (Krupinska et al., 2012). poor habitats (Killingbeck, 1996; Aerts, 1999) would accordingly lead to genotypic differentiation and species-specific programs Genetic differences in foliar senescence also affect nutrient mobili- of foliar senescence and nutrient transport mechanisms (Kim zation and export. Many studies have emphasized the importance et al., 2016). 8 Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). Nitrogen and phosphorus resorption in foliar senescence Plant Communications Figure 4. Values from two contrasting spe- cies (a deciduous evergreen and a grass) sampled along a 1000-m altitudinal gradient on two different bedrock types. Note wider [N]green in the grass than in the decid- uous evergreen but wider [N]sen in the deciduous evergreen than in the grass. The top dotted line indicates where [Nu]sen is 100% of [Nu]green (i.e., NuRE = 0%), the middle line where it is 50% (i.e., NuRE = 50%), and the lower line where it is 25% (i.e., NuRE = 75%). Data are from Gerdol et al. (2019). Regulation of senescence by environmental conditions How changes in the timing and progression of senescence including nutrient availability induced by stress affect NuR is not yet known. The interaction be- Phytohormones are key regulators of senescence. Cytokinins, tween age and stress regulates deployment of mobilization auxins, and gibberellins are hormones that repress senescence, mechanisms as stress-induced foliar senescence progresses and jasmonic acid, abscisic acid, salicylic acid (SA), and ethylene and may affect NuR; this likely underlies part of the intraspecific are hormones that promote senescence. Hormones (auxin and variability in NuR. How stress-induced changes in leaves before brassinosteroids, but also ethylene) in young leaves may indi- senescence alter NuR is even less well understood. rectly affect the timing of senescence by changing the timing of modifications associated with age. Hormones such as SA regu- Environmental regulation is responsible for part of the phenotypic late the progression of senescence after it is initiated (Jibran variability in NuR (Figure 1) reported in observational studies et al., 2013; Schippers, 2015). (Drenovsky et al., 2019). Variability in NuR in naturally grown individuals and populations across years has been observed in Plants suffer stress from many physical factors, including heat, records of environmental variability (e.g., Acer saccharum cold, drought, salinity, strong light, and nutrient limitation, and [Pregitzer et al., 2010], Fagus sylvatica [Khanna et al., 2009], from biotic factors such as pathogenic infection. Plants synthesize deciduous and evergreen shrubs [Drenovsky et al., 2013], phytohormones to adjust their physiology to resist these stresses Quercus robur [Covelo et al., 2008], and Populus tremuloides (Luoni et al., 2019). Phytohormones also integrate stress signals [Killingbeck et al., 1990]). into the developmental program, which may accelerate senescence or, if the leaves are old enough, lead to stress- Light has been described as a factor affecting NuR (i.e., Garcia- induced senescence. If the leaves are immature, or if the stress Plazaola et al., 2003; Brunel-Muguet et al., 2013), although this is too weak to trigger the onset of senescence in mature leaves, is not always the case (Yasumura et al., 2006). Both drought only physiological changes associated with the stress are induced, and temperature have direct effects on NuR that are also not senescence changes, although such changes may activate associated with effects on the phenology of foliar senescence, mechanisms for nutrient mobilization. The signals from radical ox- as has been reviewed for deciduous trees (Estiarte and ygen species generated under stress may also alter changes asso- Peñuelas, 2015). The overall effect of water stress is a ciated with age (Khanna-Chopra, 2012) or regulate the timing of reduction in NuR, whereas the effects of warming on NuR in senescence in mature leaves (Pintó-Marijuan and Munné-Bosch, winter deciduous species have not been elucidated. The effects 2014). Radical oxygen species generated early in senescence of temperature are intertwined with those of water stress in can regulate the progression of senescence after it is initiated climates with dry seasons, and higher resorption during wet (Khanna-Chopra, 2012). years has been reported in dry deciduous species (Renterı́a et al., 2005; Renterı́a and Jaramillo, 2011). An example of Cells can reprogram themselves to cope with stress, making some differences in [Nu]sen among years that differ in the amount and proteins unnecessary after the reprograming. The cellular machin- distribution of precipitation can be seen in Figure 5. ery to remove these proteins and to eliminate molecules damaged by stress mostly overlaps with the machinery required to degrade The connection between senescence and nutrient stress is molecules to mobilize nutrients for NuR (e.g., Simova-Stoilova obvious: foliar senescence is the terminal mechanism for nutrient et al., 2010). Similarly, the upregulation of genes encoding recycling across organs, and plants recycle nutrients when they proteases and mobilization mechanisms is a response common are nutrient limited. Not surprisingly, the expression of genes for re- to several stresses and to foliar senescence (e.g., Simova- cycling before senescence mostly overlaps with their expression Stoilova et al., 2010), and many transcription factors that regulate during early senescence. For example, genes for degrading pro- age-induced senescence are therefore also involved in plant stress teins (Comadira et al., 2015) and genes for autophagy (Safavi-Rizi tolerance (i.e., Sade et al., 2018). For example, 28 of the 43 genes et al., 2018) under N limitation are expressed before senescence encoding transcription factors induced during senescence in is triggered. The overall overlap has been documented in Arabidopsis are also induced by stress (Chen et al., 2002). Arabidopsis, where 38% of the genes upregulated under P deficit Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). 9 Plant Communications Nitrogen and phosphorus resorption in foliar senescence Figure 5. Mean values of 3–8 individuals from 17 mostly dry deciduous species from a tropical dry deciduous forest in 2 consec- utive years that differed in precipitation. The top dotted line indicates where [Nu]sen is 100% of [Nu]green (i.e., NuRE = 0%), the middle line where it is 50% (i.e., NuRE = 50%), and the lower line where it is 25% (i.e., NuRE = 75%). Data are from Renterı́a and Jaramillo (2011). Note how, for many species, [N]green values that were similar between both years ended up with very different [N]sen values between years, likely because of differences in the amount and seasonality of precipitation. The pattern for [P]sen had some similarities, although not for all species. are also upregulated during senescence, and the overlap also 2003), despite widespread claims of higher resorption under encompasses 40% of the downregulated genes (Stigter and nutrient limitation. Plaxton, 2015). A metanalysis of a large number of fertilization experiments (Yuan The regulatory relevance is clear after the advance in the timing of and Chen, 2015) revealed increasing [N]sen and [P]sen and senescence under nutrient stress (Cote et al., 1989). The decreasing NRE and PRE in response to fertilization with the relevance is even clearer when senescence is reversed by respective nutrients and decreasing NRE and PRE in response to relieving nutrient limitation, e.g., in barley leaves, in which N combined N and P fertilization. The increases in [Nu]sen occurred supply reversed the regulation of many of the nearly 2000 after a 27% increase in [N]green and a 73% increase in [P]green genes associated with the induction of premature senescence with N and P fertilization, respectively (Yuan and Chen, 2015), by N limitation (Schildhauer et al., 2008; Fataftah et al., 2018). consistent with the positive relationship between [Nu]green and [Nu]sen reported at the intraspecific level for both N and P (Kobe The overlap is obvious at the post-transcriptional level because et al., 2005; Mao et al., 2015). many mechanisms for scavenging nutrients that act before the onset of senescence also act during the early stages of senes- A lack of clear patterns in some experiments are likely to have cence. For example, one of many Arabidopsis purple acid been caused by the effects of nutrients on growth and sink phosphatases that predominate in the vacuole and cell wall nutrient demands (see next) but also by the distortion in NuR for P recycling under P deficit also predominates during caused by abiotic and biotic stresses under field conditions. senescence, when its role is so important that PR is greatly impaired in deficient mutants (Robinson et al., 2012). Overlap between the responses to nutrient limitation and senescence THE OTHER SIDE: SINK NUTRIENT suggests that a senescence program deployed on top of the signal for starvation of a nutrient is reinforced in mechanisms DEMAND that mobilize that nutrient. Evidence supporting such a Nutrients used to supply primary growth and reproductive sinks reinforcement includes, for instance, that nitrate nutrition are provided mainly by internal reserves. Nutrients stored in regulates expression of genes encoding glutamate synthases twigs, stems, or roots of deciduous trees during the leafless sea- and asparagine synthetases during senescence, which are key son provide nutrients for the seasonal growth of shoots. In growth enzymes for the synthesis of phloem-transported amino forms other than deciduous trees, many of the nutrient reserves acids (Avila-Ospina et al., 2015), or that autophagy is induced are contained in leaves; they provide nutrients for sequential in old leaves approaching senescence and under N growth of leaves in herbs, seasonal growth of shoots in many ev- starvation because autophagy is needed for N remobilization ergreens, and seed filling in many species of monocarpic plants. under both limiting and ample supplies of nitrate (Guiboileau et al., 2012). Similarly, RNAses become more abundant during Nutrients retrieved from leaves to directly meet sink demand can be senescence, as they do under P deprivation (Morcuende retrieved from green leaves but also often from senescing leaves. et al., 2007). NuR of evergreens from seasonal climates was hypothesized to be driven by shoot growth (Nambiar and Fife, 1991) because NuR Reports on the dependence of nutrient efficiency on plant nutrient from both senescing and mature green leaves is nearly status suggest differential regulation of the degree of resorption concurrent with shoot growth (Miyazawa et al., 2004; Pornon and and therefore of senescence. Plant nutrient status, and hence Lamaze, 2007; Fife et al., 2008). soil nutrient availability, are assumed to exert a key control on NuR in accordance with the nutrient conservation function of Sink demand can also account for changes in NuR with plant devel- foliar senescence. Identification of the phenotypic effects of opment. Nutrient demands change with ageing because of nutrient availability on NuR, however, has produced mixed results changes in productivity, growth, and allocation (e.g., Brant and that have revealed no clear pattern (e.g., van Heerwaarden et al., Chen, 2015) and may therefore lead to changes in NuR. For 10 Plant Communications 4, 100503, March 13 2023 ª 2022 The Author(s). Nitrogen and phosphorus resorption in foliar senescence Plant Communications example, higher NR in adults than in juvenile stages of deciduous changes in litter quality, and plant competition. Study of model trees is due to the larger N sink in adults (e.g., Fagus crenata, plant species, such as beech, which has a broad distribution under Yasumura et al., 2005). Shifts in the controls of internal nutrients various climatic and soil conditions and has also been well studied in response to increasing sink size in a chronosequence of a genetically, would enable deeper investigation of the mechanisms deciduous conifer were also proposed to underlie the increase in of nutrient resorption in terms of ecology, physiology, biochemistry, NR associated with age when [N]green increased but [N]sen metabolomics, and genetics. Meanwhile, we can conclude that (1) decreased, and the availability of soil N tended to decrease as foliar nutrient resorption (NuR) plays a key role in ecosystem func- the stand aged (Sun et al., 2016). Similarly, difficulties in resolving tioning and plant nutrient economy, (2) nutrients are transferred the apparent inconsistencies in the variation in NuR under from the leaf in simple metabolites that can be loaded into the fertilization (i.e., Peng et al., 2019) may be due to interactions with phloem, (3) proteolysis is the main mechanism for N mobilization, changes in plant size and nutrient demand. whereas P mobilization requires the involvement of different cata- bolic pathways, making the dynamics of P in leaves more variable The relationship between sink nutrient demand and NuR has than those of N before, during, and after foliar senescence, (4) the been hypothesized to underlie differences in nutrient conserva- biochemistry and fate of organelles during senescence impose tion patterns, e.g., to account for the low NuR in slowly growing constraints that limit NuR, (5) the efficiency of NuR decreases, evergreen shrubs in Patagonia compared with the higher NuR especially in evergreen species, as soil fertility increases, which is of faster growing perennial grasses with a higher sink strength attributed to relative costs of soil nutrient acquisition decreasing (Carrera et al., 2000). Similar reasoning has also led to the with increasing soil nutrient availability, while the energetic costs speculation that plants under continuous tropical growth would of NuR from senescing leaves remain constant, and (6) NuR is continuously have a strong sink and consequently a high NuR genetically determined, with substantial interspecific variability, (Rejmánková, 2005). and environmentally regulated in space and time, with nutrient availability being a key driver of variability in NuR within species. Beyond vegetative growth, reproductive efforts impose an addi- tional demand with the potential to deplete nutrients from the FUNDING leaves of reproductive trees (Pakonen et al., 1988, May and This research was supported by Spanish Government grants PID2020- Killingbeck, 1992; Tully et al., 2013) and hence affect NuR. For 112738GB-I00, PID2019-110521GB-I00, and TED2021-132627B-I00, example, reproductive efforts regulated the nutrient response of Fundación Ramón Areces grant CIVP20A6621, and Catalan Government a tropical N-fixing tree that flushes leaves and flowers throughout grant SGR2017-1005. the year. Foliar [N]sen and [P]sen are lower in trees with larger short- and long-term reproductive demands than in trees with AUTHOR CONTRIBUTIONS smaller demands (Tully et al., 2013). M.E and J.P. designed the review. M.E. gathered and analyzed the data and wrote the first draft. M.E., M.C., M.M., and J.P. contributed to the an- The shift toward the reproductive stage in short-lived plants with alyses and interpretation of the results and to the revision and improve- sequential senescence is often accompanied by an increase in ment of the text. NuR (Malagoli et al., 2005). Optimal resorption in annual plants is also considered to require close synchronization between ACKNOWLEDGMENTS sink formation and senescence of the source organ (Pottier No conflict of interest declared. et al., 2014). For example, the low sink capacity before pod filling in the annual crop B. napus has been proposed to be the Received: August 19, 2022 Revised: November 17, 2022 main bottleneck for foliar NR at this stage, and NR accordingly Accepted: December 8, 2022 improved when the sink increased at the filling stage (Tilsner Published: December 13, 2022 et al., 2005). Similarly, NR decreased in oilseed rape and soybean in the absence, or after the removal, of seeds to fill REFERENCES (Malagoli et al., 2005; Htwe et al., 2011). Aerts, R. (1999). Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J.Exp.Bot. 50:29–37. 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