REVIEW published: 20 May 2022 doi: 10.3389/fpls.2022.833030 An Overview of the Isoprenoid Emissions From Tropical Plant Species Zhaobin Mu 1,2,3, 4, Joan Llusià 3,4*, Jianqiang Zeng 1, 2, 5, Yanli Zhang 1, 2,6, Dolores Asensio 3,4, Kaijun Yang 3, 4, Zhigang Yi 7, Xinming Wang 1,2, 5,6* and Josep Peñuelas 3,4 1 State Key Laboratory of Organic Geochemistry and Guangdong Key Laboratory of Environmental Protection and Resources Utilization, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, China, 2 CAS Center for Excellence in Deep Earth Science, Guangzhou, China, 3 CSIC, Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Spain, 4 CREAF, Barcelona, Spain, 5 College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, China, 6 Center for Excellence in Regional Atmospheric Environment, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China, 7 Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China Edited by: Violeta Velikova, Terrestrial vegetation is the largest contributor of isoprenoids (a group of biogenic volatile Institute of Plant Physiology and organic compounds (BVOCs)) to the atmosphere. BVOC emission data comes mostly Genetics (BAS), Bulgaria from temperate regions, and less is known about BVOC emissions from tropical vegetation, Reviewed by: Maja Simpraga, even though it is estimated to be responsible for >70% of BVOC emissions. This review Ghent University, Belgium summarizes the available data and our current understanding of isoprenoid emissions Kathryn Emmerson, Commonwealth Scientific and from tropical plant species and the spatial and temporal variation in emissions, which are Industrial Research Organisation strongly species-specific and regionally variable. Emission models lacking foliar level data (CSIRO), Australia for tropical species need to revise their parameters to account for seasonal and diurnal Rüdiger Grote, Karlsruhe Institute of Technology variation due to differences in dependencies on temperature and light of emissions from (KIT), Germany plants in other ecosystems. More experimental information and determining how emission *Correspondence: capacity varies during foliar development are warranted to account for seasonal variations Joan Llusià j.llusia@creaf.uab.cat more explicitly. Xinming Wang Keywords: BVOCs, isoprenoids, tropical species, emission inventory, emission variations, emission models wangxm@gig.ac.cn Specialty section: This article was submitted to INTRODUCTION Functional Plant Ecology, a section of the journal A diverse array of volatile and semi-volatile chemicals is emitted by terrestrial vegetation (Goldstein Frontiers in Plant Science and Galbally, 2007; Guenther et al., 2012), which is by far the largest contributor to the global Received: 15 December 2021 annual flux of reactive volatile organic compounds to the atmosphere (Lamarque et al., 2010; Accepted: 26 April 2022 Guenther et al., 2012). Emissions of BVOCs from vegetation account for 90% of total global Published: 20 May 2022 non-methane VOCs (NMVOCs; Guenther et al., 1995; Singh et al., 2011). Isoprenoids have the Citation: highest rates of emission and the greatest atmospheric impact (Guenther et al., 1995; Kuhn Mu Z, Llusià J, Zeng J, Zhang Y, et al., 2004b) among BVOCs. Their emissions are highly dependent on land cover, including Asensio D, Yang K, Yi Z, Wang X and the composition and dominance of plant species and the environmental conditions that influence Peñuelas J (2022) An Overview of the Isoprenoid Emissions From Tropical species physiology (Guenther et al., 1995; Taylor et al., 2018, 2019). BVOC emissions from Plant Species. terrestrial vegetation have been studied for several decades because they play important roles Front. Plant Sci. 13:833030. in atmospheric chemistry and plant physiology (Went, 1960; Rasmussen, 1972). On the one doi: 10.3389/fpls.2022.833030 hand, they strongly affect atmospheric composition by contributing to the photochemical production Frontiers in Plant Science | www.frontiersin.org 1 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species of ozone and the formation of secondary particles (Fehsenfeld subtropical and tropical regions, where more than 100 species et al., 1992; Wang et al., 2007; Singh et al., 2014), thereby were studied taking both emitted isoprene and terpenes into influencing regional air quality and climate (Peñuelas and Llusià, consideration (Figure 1; Appendix S1). Isoprene was the main 2003; Derwent et al., 2007; Peñuelas and Staudt, 2010; Guenther compound, which was emitted by 76.1% (83 of 109) of the et al., 2012). On the other hand, there are BVOCs that can species studied in Brazil, 73.5% (100 of 136) in India, 58.3% mediate plant–plant, plant–insect, and plant–microbe interactions (63 of 108) in China, and 53.8% (70 of 130) in the Republic (Peñuelas and Llusià, 2001; Kishimoto et al., 2006; Gershenzon of South Africa. Isoprene may thus be emitted by more than and Dudareva, 2007; Peñuelas and Staudt, 2010; Jardine et al., half of all tropical terrestrial species, while the neotropics 2015; Maag et al., 2015) and protect photosynthetic membranes represented by Amazonian regions may have larger proportions against abiotic stresses (Peñuelas and Llusià, 2002; Vickers et al., of emitters compared to other tropics. There is a large proportion 2009; Jardine et al., 2017; Yàñez-Serrano et al., 2018). of emitters among tropical species, as emitting species outperform Although the tropics are estimated to emit >70% of the non-emitting species by assimilating more carbon at high global total BVOC emissions (Karl et al., 2007; Jones et al., temperatures (Taylor et al., 2019). Meanwhile, this coincided 2011), the number of investigations there has been heavily with the previous inference that isoprene is likely to be a key limited by complexity in eco-regional variety and species diversity, compound of vegetation in response to environmental stresses as well as logistical and methodological difficulties (Geron et al., and climate change, especially in tropical forests emitting more 2002; Kuhn et al., 2002, 2004a,b; Harley et al., 2004; Bracho- isoprene than other ecosystems (Guenther et al., 2006; Taylor Nunez et al., 2013). These disadvantages also hinder our et al., 2018). However, the distributions of isoprene-emitting understanding of the chemistry of the lower troposphere over species on the landscape vary quantitatively with climatic factors. the tropics (Harley et al., 2004; Kuhn et al., 2004a; Paton-Walsh For example, Taylor et al. (2018) provided explicit estimates et al., 2022). Furthermore, it should be added that the magnitude of the proportion of emitting trees, which increases with mean and chemical speciation of BVOC emissions of vegetation are annual temperature and decreases with length of dry season. highly species-specific (Wang et al., 2007) and vary with Notably, the percentages of emitters are much higher than environmental conditions and the developmental stages of plants those in previous reports, indicating that more than one-third (Lerdau and Throop, 2000; Kuhn et al., 2004a; Wilske et al., of species emit isoprene in tropical forests (Harley et al., 2004; 2007). Studies of species-level BVOC emissions that provide Taylor et al., 2018). Furthermore, Jardine et al. (2020) found the emission factor measured at the leaf level under standard 61.9% of all 113 investigated dominant species in the Amazon conditions (leaf temperature of 30°C and photosynthetically basin emitted isoprene, which is also lower than the 76.1% active radiation (PAR) of 1,000 μmol m−2 s−1; Guenther et al., reported in this study. This may be due to our compilation 1993; Monson et al., 2012) are essential for developing regional focused on quantitative measurements of emissions rather than models that can be used to predict emissions across large spatial “survey-type” emission inventories; qualitative or semi- and temporal scales (Lerdau and Throop, 2000). quantitative emission potential studies were excluded from our The primary aim of this paper is to compile a BVOC compilation. In addition, this study included larger quantities emission factor inventory of tropical species and to explore of plant species from tropical and subtropical landscapes, not their basic emission characteristics. We collected and analyzed only trees growing in forests. However, these inferences still available data for isoprenoid emissions from tropical plants warrant validation through further similar screening studies for all tropical and some subtropical regions (30°N to 30°S; throughout the world (Llusià et al., 2014). Appendix S1). We discuss our current understanding of the We used the foliar level data in μg g−1 dw h−1 to determine family- effects on BVOC emissions of the diurnal and seasonal variations level capacity of isoprene emissions (Appendix S1). There were due to environmental and physiological factors. Finally, we review three typical patterns for family-level isoprene emissions in tropical studies of emission models and techniques for measurement plants. The most important families for isoprene emissions include used for tropical species. The scope of this review is to summarize Anacardiaceae, Arecaceae, Burseraceae, Clusiaceae, Euphorbiaceae, the dynamics determining the variation in BVOC emission Fabaceae, Flacourtiaceae, Lauraceae, Lecythidaceae, Moraceae, capacity across space and time in tropical landscapes. Compared Myristicaceae, Myrtaceae, Poaceae, Rhamnaceae, Sapotaceae, and to the recent comprehensive review of BVOCs from the Amazonia Verbenaceae. Species in the families Annonaceae, Araliaceae, (Yáñez-serrano et al., 2020), our review is differentiated by Asteraceae, Bignoniaceae, Boraginaceae, Celastraceae, Lamiaceae, having an emission factor inventory across larger tropical Lythraceae, Melastomataceae, Meliaceae, Rosaceae, Rubiaceae, landscapes and a more specific focus toward updating the Rutaceae, Simaroubaceae, Theaceae, Ulmaceae, and Violaceae were tropical emission algorithms. not emitters or very low emitters (Figure 2A; Appendix S1). Families, such as Apocynaceae, Combretaceae, Ebenaceae, Fagaceae, Hypericaceae, Malvaceae, Pinaceae, and Sapindaceae, were also PROFILE OF ISOPRENOID EMISSIONS low emitters but contained one or two species that were high emitters. FROM TROPICAL SPECIES Studies of terpenes were much less common than those of isoprene and dominated by monoterpenes or monoterpenes BVOC emissions released by tropical plant species have been combined with sesquiterpenes. Meanwhile, tropical plants emit studied most in Brazil (South America), India and China (Asia), much less terpenes than isoprene in terms of the amount and and the Republic of South Africa (Africa; Figure 1) among capacity of emitters (Figure 2). The most important tropical plant Frontiers in Plant Science | www.frontiersin.org 2 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species FIGURE 1 | Distribution of the tropical plant species with isoprenoid emissions reviewed in this study (Appendix S1). Red represents areas where isoprene is the only isoprenoid reported, blue represents areas where terpenes are the only isoprenoids reported, green represents areas where isoprene, terpenes, or both isoprene and terpenes are the isoprenoids reported. The size of the circle is proportional to the number of tropical species studied. families for terpene emission included Araliaceae, Euphorbiaceae, invasion of alien plants may lead to regional changes in biogenic Fabaceae, Lauraceae, Myrtaceae, Rubiaceae, Rutaceae, Theaceae, terpene emissions (Harley et al., 1994; Litvak et al., 1996; and Verbenaceae (Figure 2B; Appendix S1). Llusià et al., 2010). These studies have been concentrated mostly in India, China, Isoprenoid emissions vary greatly among plant species Malaysia, and the United States (Figure 1; Appendix S1). The (Appendix S1). Emissions of isoprenoids of different species Asia-Pacific islands had a similarly high percentage, with 97.2% vary by several orders of magnitude (Harley et al., 1999; (70 of 72) of the species studied in Hawaii and 95.3% (41 of Kesselmeier and Staudt, 1999), especially for isoprene 43) in Borneo emitting monoterpenes, but the continents had (Appendix S1; Figure 2A). This capacity to form and emit much lower percentages, with 75.7% (81 of 107) and 47.4% volatiles by a large fraction of tree species and a few herbaceous (46 of 97) of the species studied in India and China, respectively. species (Appendix S1) is associated with the activity of the In addition, Llusià et al. (2010) recorded sesquiterpenes from synthase enzyme specific for each isoprenoid (Silver and Fall, 68.1% (49 of 72) of the species studied in Hawaii to 81.4% 1991; Harley et al., 2003). These rates of production catalyzed (35 of 43) and in Borneo (Llusià et al., 2014). At the same by enzymes vary widely across and within species and are time, these authors found that there are variations in terpene influenced by a wide range of factors, such as light intensity emission capacity between exotic and native species. The rates and temperature experienced by the leaves during measurement of total terpene emission were 1.5-fold higher in exotic than and in the days prior to measurement, foliar age, and canopy native species (p < 0.05) and only coincided with a significant position (Harley et al., 1999, 2003; Sharkey et al., 1999; Geron difference in α-pinene (p < 0.05), which was more than twice et al., 2000; Pétron et al., 2001), and even the levels of air as high in exotic species in Hawaii (Llusià et al., 2010), while pollutants, such as ozone (Bison et al., 2018; Yáñez-serrano the rates of isoprene emission from 42 tropical tree species et al., 2020). Therefore, these data obtained by quantitative did not differ significantly between exotic and native species measurements were used to identify the emitting taxa but were in Okinawa (Tambunan et al., 2006). These findings suggest not robust enough to assign species-specific emission capacities, that invasive species may benefit from a higher terpene emission especially for those species that were characterized as emitters rate, eventually by being better protected against multiple stresses or non-emitters based on a single measurement or a few and that the higher terpene emission may partly account for measurements (Harley et al., 2014). In addition, the sample their acclimation in the new environment, which may also plants were selected as representative of the species, but this imply that invasive species may respond more competitively variability within species in emission can sometimes to new combined stresses driven by global change in tropical be sufficiently large to prevent identifying potential significant regions (Llusià et al., 2010; Loreto and Fineschi, 2015). Meanwhile, differences in emissions between species. Thus, unidentified islands may be much more subject to species invasion than variations in emissions between species in these studies also inland continents (Bellard et al., 2017; Dawson et al., 2017), occurred, which can be due in part to factors, such as the which is supported by significantly higher percentages of terpene growth environment and/or the stage of development or even emitters on Asia-Pacific islands. These results indicate that the measurement technique. Frontiers in Plant Science | www.frontiersin.org 3 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species A B FIGURE 2 | Factors of isoprene (A) and terpene (B) emissions with more than three species for tropical plant families (Appendix S1). The box is drawn from the first quartile (Q1) with a whisker to the minimum to the third quartile (Q3) with a whisker to the maximum. The median is represented by the line in the box, and outliers are identified by dots. The width of box is proportional to the number of tropical species studied. The evolutionary divergence of genes that code for enzymes were found only randomly and rarely among terpene compounds of isoprenoid synthesis has been reported in narrow phylogenetic and were not found for total quantities of monoterpenes groups (Bohlmann et al., 1998; Llusià et al., 2010, 2014), but (k = 0.139 and p = 0.876) and total quantities of sesquiterpenes a general phylogenetic determinant for plant emission is not (k = 0.511 and p = 0.152) in Hawaii or total quantities of terpenes clear (Welter et al., 2012; Loreto and Fineschi, 2015). To the (k = 0.016 and p = 0.995) in Borneo. Moreover, we did not find best of our knowledge, significant phylogenetic signals have this relationship for isoprene (k = 0.409 and p = 0.182) among been found for some individual terpene compounds, such as 42 plant species in Okinawa. On the other hand, the relationship α-pinene (k = 0.651 and p = 0.009) in Hawaii (Llusià et al., 2010) between plant species and isoprene emissions was observed and ocimene and γ-terpinene (k = 1.15 and p = 0.03, and k = 1.31 in two of the most commonly studied plant families containing and p = 0.03, respectively) in Borneo (Llusià et al., 2014), >40 species. Moraceae (41 species, k = 0.146 and p = 0.578) and indicating strong resemblance in specific terpene emissions Fabaceae (108 species, k = 0.110 and p = 0.109; Appendices S1 among the most closely related species (Llusià et al., 2010) and S2), and the phylogenetic signals were insignificant for on Asia-Pacific islands and the potential of capacity to emit the two dominant families (Webb and Donoghue, 2005). A volatile compounds using as a basis for studying taxonomic previous study reported that isoprene emissions are likely relationships in plants (Loreto et al., 1998; Llusià et al., 2010). ancestral within the family Fabaceae (Monson et al., 2013), These relationships, however, were not ubiquitous. For example, while Fabaceae harboring many strong emitters still had very in the above studies, we pointed out that phylogenetic signals low isoprene emissions in this study (Figure 2B; Appendix S1). Frontiers in Plant Science | www.frontiersin.org 4 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species The lower emission potentials were thus generally not due to isoprene precursor substrate dimethylallyl diphosphate (DMAPP; a lack of genera with characteristically high emissions but Geron et al., 2000; Brüggemann and Schnitzler, 2002). These indicated a lower emission potential within specific phylogenetic variations can be influenced by a number of physiological and lines (Llusià et al., 2010; Monson et al., 2013), which may environmental drivers, including the seasonal dependence of obscure the recognition of phylogenetic signals at the family foliar maturation, changes in the growth environment of leaves, level. Although the phylogenetic distribution of isoprene availability of water and nutrients, and even the growth conditions emissions broadly across the phylogeny of plants, isoprene preceding measurement (Harley et al., 1999, 2003; Sharkey synthase is so readily lost and gained that its signal can et al., 1999; Geron et al., 2000; Pétron et al., 2001; Kuhn be difficult to distinguish from noise in the phylogeny at both et al., 2004b; Alves et al., 2014, 2018). The rates of isoprene large and fine phylogenetic scales (Monson et al., 2013; Loreto emission from mature leaves of tropical plants were commonly and Fineschi, 2015). However, the lack of phylogenetic higher and sometimes more than two-fold higher in the dry relationships of isoprenoids in this study could be masked by season than in the wet season (Guenther et al., 1999b; Klinger the multiple factors that control their synthesis and emission et al., 2002; Kuhn et al., 2004a; Geron et al., 2006; Wilske (Peñuelas and Llusià, 2001). et al., 2007). Isoprene emissions increased during the dry season due to higher cumulative exposure to solar radiation (Sharkey et al., 1999; Geron et al., 2000, 2006; Pétron et al., 2001) and SEASONAL AND DIURNAL VARIATIONS lower water availability under similar temperature conditions. This increase in the dry season is quite frequent in much of OF ISOPRENOID EMISSIONS FROM the Amazon, especially when radiation and soil water retention TROPICAL SPECIES are high and deep roots allow sustained transpiration (Maeda et al., 2017), which is part of the mechanism for dry season Emissions can differ greatly between trees of the same species greening (Huete et al., 2006) and is also linked to the emission and even between leaves from the same tree due to differences seasonality demonstrated by Alves et al. (2018). Isoprene in the growth environment and/or developmental stage (Lerdau emissions from Celtis philippensis leaves in Xishuangbanna in and Throop, 2000; Kuhn et al., 2004a; Wilske et al., 2007; China, however, were higher from new leaves in the wet season Laffineur et al., 2011; Šimpraga et al., 2011, 2019; Alves et al., (September) than from old leaves of the previous dry season 2018). These differences can be due to diurnal and seasonal (April; Wilske et al., 2007). These results were in accordance phenological cycles, including large uncertainties derived from with the finding that the production of isoprene decreases individual plant health, status of herbivory, local soil moisture dramatically with foliar senescence (Harley et al., 1994; Tambunan content and nutrient availability, local shading and microclimate, et al., 2006), so higher rates of isoprene emission for tropical foliar age, and past meteorological conditions (Kesselmeier and plants can be expected with the flush of new leaves compared Staudt, 1999; Geron et al., 2001; Niinemets et al., 2010; Llusià to old leaves (Kuhn et al., 2004a,b). Isoprene emissions in et al., 2010, 2014; Alves et al., 2018). Puerto Rico did not differ significantly between seasons among Pisonia albida, Bursera simaruba, Capparis indica, Capparis Seasonal Variations cyanophollora, and Clusia rosea (Lerdau and Keller, 1997). Environmental conditions, such as temperature and light intensity, In contrast to the increase in isoprene emissions, monoterpene generally vary seasonally less in tropical than temperate emissions were lower in the dry season than in the wet season ecosystems. Primary physiology indicated by the net for Apeiba tibourbou at an Amazonian site (10°08′43″S, photosynthetic rate varied little in the Congo (Serça et al., 62°54′27″W; Kuhn et al., 2004a) and for Hevea brasiliensis at 2001) and Amazon regions (Andreae et al., 2002; Kuhn et al., a Xishuangbanna site (21°55′25″N, 101°16′05″E; Wang et al., 2004a) and was not greatly affected by seasonal changes in 2007). The differences in emissions between the dry and wet rainfall or the amount of soil moisture (Roberts et al., 1990; seasons, however, were not as large at the Amazonian site Kuhn et al., 2004a; Rottenberger et al., 2004). More recent than at the Xishuangbanna site, where the difference in water studies demonstrated significant photosynthetic seasonality, with availability was more extreme. Although light-dependent foliar photosynthesis increasing during the dry season in Amazon terpenes exited the plant predominantly through the stomata evergreen forests, and demonstrated leaf age-dependent (Loreto et al., 1996b; Wang et al., 2007), their decrease in physiology as the mechanism (Wu et al., 2016; Albert et al., emission could not be explained by the lower stomatal 2018). In addition, lower rates of stomatal conductance and conductance in the dry season. This tended to be offset by transpiration in the dry season are caused by a lower foliar high biosynthesis/concentrations of intercellular terpenes, water potential, leading to lower evaporative cooling and hence increasing the gradient of leaf-to-air terpene vapor pressure higher foliar temperatures (Guenther et al., 1999b). (Fall and Monson, 1992; Kuhn et al., 2004a). Low emission The seasonal variations in isoprene emissions may be species- rates were accompanied by low rates of transpiration and specific and have been correlated with the inherent capacity photosynthesis, indicating that the canopy in the dry season of leaves to synthesize isoprene (Monson et al., 1994; Schnitzler may have been senescent (Wang et al., 2007). The low emissions et al., 1997; Kuhn et al., 2004a), depending on the activity of in the dry season may be from small residual stored pools extractable isoprene synthase (Kuzma and Fall, 1993; Lehning and may be masked by instantaneous emissions in the wet et al., 1999; Kuhn et al., 2004a) and/or the availability of the season, whereas the large emissions in the wet season may Frontiers in Plant Science | www.frontiersin.org 5 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species be mostly due to sources of rapid synthesis (not stored; Wang et al., 2007) at the beginning of the wet season. The increase et al., 2007). However, Jardine et al. (2017) showed highly and decrease in cis-ocimene emissions during the day suggests seasonally dynamic monoterpene emissions from an Amazon that the diurnal pattern of these emissions may be under site, with total quantities of monoterpenes significantly increasing circadian control. This circadian control might act via the during the dry season under an El Niño drought, during which substrate supply or the production or activity of synthases period leaves reduced transpiration and rose in temperature. (Wilkinson et al., 2006; Loivamaki et al., 2007), indicating The composition of emissions from A. tibourbou in the that tropical monoterpene emissions are expected to have Amazonian forest differed little between the dry and wet seasons environmental and physiological controls similar to those of (Kuhn et al., 2004a), but emissions from H. brasiliensis in isoprene (Kuhn et al., 2002; Jardine et al., 2017). Xishuangbanna (Wang et al., 2007) consisted of few compounds due to much lower emissions in the dry season. Monoterpene emissions for tropical species are generally dominated by only MODIFICATION OF THE G93 MODEL a few compounds, with sabinene, α-pinene, β-pinene, and TO PREDICT ISOPRENOID EMISSIONS limonene together accounting for approximately 90% of the total amounts in both seasons (Kuhn et al., 2002, 2004a; Wang FROM TROPICAL SPECIES et al., 2007; Wilske et al., 2007). β-ocimene was found at Emission inventories and model calculations have been developed concentrations similar to α-pinene in an Amazon canopy study to define the strength of regional and global BVOC emissions, (Jardine et al., 2015) and therefore may be another dominant but they rely mostly on studies of VOC emissions from temperate compound emitted by tropical species. The species had different areas of North America and Europe, and more efforts in patterns of emitted monoterpene groups, but some patterns parameterizations are warranted for tropical regions (Guenther were consistent across different tropical species: emissions of et al., 1996b, 1999b, 2012; Holm et al., 2014; Mutanda et al., α-pinene and/or limonene were present or even higher with 2016; Higa et al., 2018). the flush of new leaves and decreased as the leaves aged, but myrcene and/or camphene tended to be present in the emissions of old leaves (Wilske et al., 2007). Higher α-pinene and limonene Description of the G93 Model for Isoprene emissions in a species were also concurrent with higher foliar Emission temperatures in one season compared to the other season The G93 model, with its further developments, is the most (Wilske et al., 2007). widely used model for emissions of isoprene and other BVOCs from plants (Guenther et al., 1993, 2006, 2020). It simulates Diurnal Variations instantaneous emission rates as a product of the response The diurnal pattern of isoprenoid emissions was very similar functions for light and temperature after adjustment by a among tropical species (Kuhn et al., 2002, 2004a; Padhy and species-specific emission factor. Foliar temperature and light Varshney, 2005b), despite differences in emission composition intensity are the primary drivers of vegetation emissions. Its and magnitude. The emissions of all isoprenoids were negligible further developments, such as G99 (Guenther et al., 1999b) at night, increased in the morning as the air temperature and and MEGAN (Guenther et al., 2006), were expressed as functions light intensity increased, and rates were more or less maintained of more drivers, for example, the influence of leaf age and when emissions were highest and decreased in the afternoon the past conditions of light intensity and temperature (Kuhn et al., 2002, 2004a; Padhy and Varshney, 2005b; Jardine experienced by the leaves were considered. They were used et al., 2017). Isoprene emissions were confined to the daytime to model the landscape/ecosystem foliar emissions into the only (Rinne et al., 2002; Kuhn et al., 2004a; Padhy and Varshney, above-canopy atmosphere. 2005b) and were not affected by the decrease in stomatal Different compounds do not necessarily follow the G93 conductance at midday, as reported for Sorocea guilleminiana algorithm, especially where the compounds are controlled by in a diel course of measurements by Kuhn et al. (2004a). No environmental parameters other than light and temperature emissions of monoterpenes were detected at night in species and other circadian controls, but G93 is still the most important that did not store terpenes, even at high temperatures (Kuhn model for describing biogenic isoprenoid emissions due to its et al., 2004a). The emission of α-pinene, however, was variable extensive and indiscriminate use in predicting isoprene emissions in some species and was not correlated with either day or from plants in both temperate and tropical regions (Benjamin night (Padhy and Varshney, 2005a). et al., 1996; He et al., 2000; Owen et al., 2001; Harley et al., Total monoterpene emissions have a distinct diel cycle, with 2004; Kuhn et al., 2004a,b; Padhy and Varshney, 2005a). The most emitted monoterpenes following this pattern of emissions performance of G93 is satisfactory for predicting the rate of and accounting for a similar proportion of the composition isoprene emission from temperate species but possibly not for throughout the day (Kuhn et al., 2002, 2004a) within individual estimating the rate from tropical species, with studies already species; however, variability in emissions existed in compounds, negating the possibility that the observations may have been such as sabinene and limonene, among species (Wang et al., due to differences in method or environmental conditions, 2007). Interestingly, the emission of cis-ocimene from suggesting that emission responses may differ between tropical H. brasiliensis had a distinct diurnal trend, with a significantly and temperate plants (Kuhn et al., 2004a,b; Guenther et al., higher contribution to the total emissions at midday (Wang 2006; Bracho-Nunez et al., 2013). Frontiers in Plant Science | www.frontiersin.org 6 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species The G93 model estimates isoprene emissions (I) as a function Lerdau, 1999; Lerdau and Throop, 1999), Puerto Rico (Lerdau of two environmental drivers, temperature and light intensity: and Keller, 1997) and Brazil (Alves et al., 2014). Harley et al. (2004), however, reported isoprene light saturation at a PPFD I = Is.CT .CL (1) of 1,500 μmol m−2 s−1 for Mangifera indica, and Kuhn et al. (2004a) reported isoprene light saturation at PPFDs <1,000 μmol m−2 s−1 for Hymenaea courbaril. The emission rate where I is the predicted emission rate at temperature T for F. virgata in Okinawa normalized to temperature increased (K) and photosynthetically active radiation (PAR) of L linearly with light intensity up to 1,700 μmol m−2 s−1 in a (μmol m−2 s−1) and Is is the basal emission rate (emission phytotron (Tambunan et al., 2006), did not saturate up to factor). CT and CL are coefficients for temperature and light 1,800 μmol m−2 s−1 in the field (Tambunan et al., 2006) and intensity, respectively, and are defined by: stabilized at light intensities >1,200 μmol m−2 s−1 in plastic pots (Oku et al., 2008) under natural conditions. Light saturation −1   CT = exp CT 1 (T −Ts )( RTS T )− 1   1+ exp CT 2 (T − Tm)( RTsT )− 1    (2) for isoprene emissions may therefore vary among tropical         species and even for the same species under different growth conditions. Isoprene emissions for at least some tropical taxa did not saturate at light intensities under natural conditions. (3) Foliar temperature was well correlated with light intensity, but =CL (α CL1L)(1 + α 2 L2 )−0.5 the differences in CL between plant species were smaller at higher temperatures; the poorer performance of G93 for high where CT1 = 95,000 J mol−1, CT2 = 230,000 J mol−1, Tm = 314 K, emission rates at high temperatures for tropical trees was α = 0.0027, CL1 = 1.066, R = 8.314 J K−1 mol−1 and Ts is the foliar therefore mostly due to the low efficiencies of CT in G93 (Oku temperature under standard conditions (303 K, Guenther et al., 2008, 2014; Mutanda et al., 2016). These observations et al., 1993). strongly indicate that the general parameterization of G93 is not suitable for tropical trees, corroborating findings from Modification of the G93 Model to Predict Africa where specific modifications of parameters and seasonality Isoprene Emissions From Tropical Species were suggested (Guenther et al., 1999b). Isoprene emissions for tropical species increased exponentially Harley et al. (2004) used the temperature- and light-dependent with temperatures up to 40°C (Keller and Lerdau, 1999; Lerdau algorithm of G99 to estimate foliar emissions of M. indica. and Throop, 1999; Harley et al., 2004) and stabilized at higher The light response of isoprene emission (EL) is thus calculated temperatures than for temperate species, sometimes even >45°C in dependence on PPFD (μmol m−2 s−1) according to: (Alves et al., 2014). This difference could be due to differences (4) in the growth conditions (Monson et al., 1992), so the optimal EL = Es (α CL PPFD ) / [(1 + α 2 PPFD 2 )0.5 ] temperature for isoprene emission by tropical species may vary considerably. CT for G93 postulates that the maximal temperature- dependent isoprene emission is almost 2-fold higher than the where Es is the emission rate under standard conditions (emission basal emission rate (Is). This magnitude is between 2 and 4 factor), and α and CL are empirical coefficients. for most temperate plants (Monson et al., 1992; Sharkey and The temperature response of isoprene emissions (ET) is Monson, 2014) but is >5 for most tropical tree species and > 10 accordingly represented in dependence on leaf temperature (TL, K) as: for the regional highest emitters (Ficus virgata and Calophyllum inophyllum; Oku et al., 2008, 2014; Higa et al., 2018). The ET = Eopt CT 2 exp ( CT 1 x ) / {CT 2 − CT 1[1 − exp (CT 2 x)]} (5) pattern of the response of isoprene emissions to temperature for tropical species thus notably differed from the pattern where x = [(1/Topt) − (1/TL)]/R, R is the gas constant predicted by the G93 model. In addition, the actual relative (0.008314 kJ K−1 mol−1), Topt is the temperature optimum (K), emission rate under standard conditions was notably lower than Eopt is the emission rate (μg C g−1 h−1) at Topt, and CT1 and that postulated by the G93 model, which tended to overestimate CT2 are empirical coefficients representing the energies of Is when the average Is was estimated by G93 under variable activation and deactivation, respectively (kJ mol−1). α and CL conditions of temperature and light intensities for tropical species in Eq. (4), and CT1 and CT2 in Eq. (5) are determined by the (Oku et al., 2008). Therefore, G93 may provide higher normalized non-linear best fit using a non-linear least squares regression emission rates under standard conditions but lower rates for routine (KaleidaGraph, Synergy Software; Harley et al., 2004). predicted emissions under high temperatures and light intensities, Another approach to define optimized parameterization of which also tended to overestimate the emission rate in the the G93 algorithm without changing anything of the model morning and evening and to underestimate the rate at midday as such has been introduced as the iterative “Ping-Pong” method (Oku et al., 2008; Higa et al., 2018). (Mutanda et al., 2016). This process was successfully used to Some tropical species were not light saturated for isoprene simultaneously define parameters CT1 and CT2 in Eq. (2), and emission up to a photosynthetic photon flux density (PPFD) α in Eq. (3) (Mutanda et al., 2016; Higa et al., 2018). For of 2,000 μmol m−2 s−1 in the Republic of Panama (Keller and illustration, original and changed parameters are presented in Frontiers in Plant Science | www.frontiersin.org 7 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species Table 1 for the species applied in these two studies. This table M = Ms. exp ( β (T − Ts ) ) (8) shows that temperature-related parameters for all tropical species were found to be approximately 1.5 (CT2)- and 2 (CT1)-fold those of the original approach. Also, the procedure resulted where M is the rate of monoterpene emission at temperature T in a generally higher sensitivity to light (up to 4.5-fold higher α). (K), Ms is the rate of monoterpene emission at a standard Besides the modifications in parameterization of G93, temperature Ts (K). β (K−1) is an empirical coefficient that establishes supplementary formulas were also proposed to predict isoprene the dependence on temperature of the emission rate in the equation. emissions from some tropical species. Keller and Lerdau (1999) This β (K−1) varies between monoterpenes with different vapor proposed a simple formula (Eq. (6)) as an alternative to the pressures and solubilities, and plants with different storage and light response formula (Eq. (3)) of G93 to account for the emission pathways (Guenther et al., 1993). Guenther et al. (1993) lack of light saturation in tropical species. Oku et al. (2008) indicated that the estimates of β varied from 0.057 to 0.144 K−1, modified the formula for calculating the factor CL (Eq. (7)) with about half the estimates falling within the range of to incorporate a decrease in the observed rate of isoprene 0.09 ± 0.015 K−1 among all 28 estimates collected. Eq. (8) was emission from F. virgata at high light intensity. typically used to simulate the dependence on temperature of the rate of monoterpene emission (Lamb et al., 1987; Pierce and b Waldruff, 1991; Roselle et al., 1991). It usually works for terpene- CL = ( aL ) (6) storing species for which changes in relative humidity and light intensity have a negligible impact on short-term variations in where a = 0.001 μmol m−2 s−1, the non-linear best fit subject to monoterpene emissions (Juuti et al., 1990; Guenther et al., 1991). the constraint that CL equal unity at PAR of 1,000 μmol m−2 s−1, It is, however, known that some species emit monoterpenes was achieved with b = 0.3460 for 12 tropical species investigated directly from production without hosting any specific terpene (Keller and Lerdau, 1999). storages (Staudt and Seufert, 1995; Staudt and Bertin, 1998; Owen et al., 2002; Dindorf et al., 2006). At an Amazonian CL =(α CL1L) (1 + α 2 L2 )−0.5 (1 + e(β +γ L ) ) −1 (7) site, monoterpene emission from A. tibourbou showed the same dependence on light as isoprene emission, with no monoterpenes released under dark conditions and with an increase and where β and γ are new empirical coefficients determined by saturation at low and higher light intensities, respectively (Kuhn the non-linear best fit (Oku et al., 2008). et al., 2002, 2004a). Similarly, the emissions of sabinene, α-pinene, and β-pinene from H. brasiliensis at a Xishuangbanna site, in Description and Modification of the G93 response to temperature were very similar to those of isoprene Model for Monoterpenes emissions (Guenther et al., 1993), although the maximum In contrast to isoprene, however, monoterpene-producing plants temperature was lower than normal for isoprene emissions mostly accumulate pools of monoterpenes and store them in from leaves (Geron et al., 2006). This indicates that monoterpene specialized structures, such as resin ducts, glandular trichomes, emissions may be under similar physiological controls as light- or similar structures (Monson et al., 1995; Kesselmeier and dependent isoprene emissions for some tropical species. In Staudt, 1999; Kuhn et al., 2002, 2004a). Monoterpene emissions addition, Jardine et al. (2015) found the light dependence of are often regarded as originating from storage only. In this monoterpene emissions from seven tree species across the case, the process can be described as temperature-dependent Amazon Basin by conducting light curves under constant with a simple exponential equation, as also suggests the temperature and CO2. For example, measurements on the leaves G93 model: of a common pioneer species Cecropia sciadophylla showed TABLE 1 | G93 parameters for various tropical species as obtained from optimization in Mutanda et al. (2016) and Higa et al. (2018). Species Optimized G93 G93 Reference CT1 CT2 α M score M score Casuarin equisetifolia 187,125 ± 14,570 151,300 ± 46,881 0.0052 ± 0.0008 0.011 ± 0.003 0.089 ± 0.018 Mutanda et al. (2016)** Ficus septica 158,500 ± 15,471 287,250 ± 94,715 0.0034 ± 0.0006 0.105 ± 0.029 0.205 ± 0.033 Mutanda et al. (2016) Bauhiniav ariegata 173,500 ± 13,714 310,500 ± 25,423 0.0019 ± 0.0003 0.023 ± 0.007 0.070 ± 0.013 Higa et al., 2018 Calophyllum inophyllum 222,000 ± 20,251 386,833 ± 54,449 0.0117 ± 0.0085 0.069 ± 0.020 0.284 ± 0.042 Higa et al., 2018 Garcinia subelliptica 208,750 ± 13,278 342,500 ± 66,666 0.0097 ± 0.0048 0.026 ± 0.007 0.136 ± 0.027 Higa et al., 2018 Mangifera indica (red) 168,333 ± 7,339 303,833 ± 62,414 0.0116 ± 0.0033 0.007 ± 0.002 0.045 ± 0.011 Higa et al., 2018 Mangifera indica (yellow) 181,167 ± 3,919 303,667 ± 34,108 0.0063 ± 0.0025 0.015 ± 0.004 0.066 ± 0.012 Higa et al., 2018 Syzygium cumini 193,833 ± 9,821 365,500 ± 21,465 0.0030 ± 0.0002 0.025 ± 0.006 0.091 ± 0.018 Higa et al., 2018 Syzygium samarangense 193,333 ± 2,186 385,333 ± 15,423 0.0049 ± 0.0014 0.009 ± 0.002 0.077 ± 0.015 Higa et al., 2018 Normalized mean square error (M score) is given for the optimized and standard parameterization in G93 (CT1 = 95,000, CT2 = 230,000, α = 0.0027). Performance values are means from n = 3–4. Frontiers in Plant Science | www.frontiersin.org 8 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species light-dependent emissions of six monoterpenes, with the elucidate how the models can be modified to identify the dominance of trans-β-ocimene and cis-β-ocimene in the light- effects of foliar phenology on isoprenoid emissions. dependent emissions. Monoterpenes are formed from photosynthetic intermediates and may share the same synthetic pathway with isoprene within plant plastids (Loreto et al., 1996a; Kuhn et al., 2002), so TECHNIQUES FOR SAMPLING AND monoterpene synthesis may also be assumed to depend on light MEASURING ISOPRENOID EMISSIONS intensity, supported also by widely reported canopy scale light- FROM TROPICAL SPECIES dependent emissions of monoterpenes from Amazonian rainforest (Rinne et al., 2002; Karl et al., 2007; Yàñez-Serrano et al., 2015, Enclosed measurement systems, initially developed by 2018; Jardine et al., 2017). For species that lack specific storage Zimmerman (1979), are the most commonly used sampling pools, the isoprene algorithm of G93 consequently fits the observed method for studying BVOCs from tropical plants (Guenther data of their monoterpene emissions well because monoterpene et al., 1996a; Greenberg et al., 2003; Harley et al., 2003, emissions were modeled analogously to isoprene emissions (Kuhn 2004; Padhy and Varshney, 2005a; Tambunan et al., 2006; et al., 2002; Wang et al., 2007). We suggest that a strong dependence Singh et al., 2008, 2011; Niinemets et al., 2011; Malik et al., of monoterpene emissions on light intensity may be widespread 2018, 2019; Zeng et al., 2022). Enclosure, however, may among tropical tree species, which has a strong impact on the underestimate emissions due to foliar shading (Guenther et al., magnitude and distribution of both past analysis and future 1996a) and contribute erratic emissions to α-pinene (Padhy prediction for these compounds (Rinne et al., 2002; Kuhn et al., and Varshney, 2005b). LI-6400 (LI-COR, Inc., Lincoln, NE, 2004a; Jardine et al., 2015). United States; Keller and Lerdau, 1999; Lerdau and Throop, 1999; Geron et al., 2002, 2006; Alves et al., 2014; Jardine et al., 2016) and ADC (LCpro, ADC BioScientific Ltd., Potential Modification of the G93 Model to Hoddesdon, United Kingdom; Geron et al., 2006; Llusià et al., Predict Seasonal Variations in Isoprenoid 2010, 2014) gas-exchange systems have also been widely used Emissions for sampling VOC emissions. In addition, Taylor et al. (2021) The G93 model may not fully account for seasonal variations introduced a new field instrument called “PORCO” based because these long-term differences in rates of isoprenoid emission on photoionization of organic compounds for measuring cannot be reconciled solely with instantaneous meteorological emissions in the tropics. data of light intensity and temperature (Yokouchi and Ambe, BVOCs can also be characterized and quantified using different 1984; Alves et al., 2018). The influence of seasonality is important methods. Sensible choice and collocation in analytical adaptations in Amazonia (Kuhn et al., 2002) and Xishuangbanna (Wang can facilitate their quantification (Merfort, 2002; Helmig et al., et al., 2007). Other important tropical regions (e.g., Borneo), 2004; Tholl et al., 2006; Bracho-Nunez et al., 2013) and enable however, have little or no climatic seasonality, so emission a broad range of BVOCs to be determined (Guenther et al., algorithms need to be more region-specific (Higa et al., 2018). 1999a; Bracho-Nunez et al., 2013). A portable photoionization Isoprene emission from tropical plants is also associated with detector (PID) was used in flow-through mode to qualitatively physiological and developmental changes during the growing identify VOC emitters (Klinger, 1998) and semi-quantitatively season, the capacity of isoprene emission to vary with foliar age assign in situ emission potentials as high, moderate, or low (Geron and the highest capacity of isoprene emission from young mature et al., 1994; Klinger et al., 2002). VOC emissions have also been leaves (recently fully expanded; Kuhn et al., 2004b; Alves et al., quantified using a Photovac Voyager portable gas chromatograph 2014), indicating a variable inherent capacity of plants to synthesize (Lerdau and Throop, 1999; Geron et al., 2002; Harley et al., 2003). isoprene during foliar development. Foliar physiological activity Proton transfer reaction-mass spectrometry (PTR-MS) for detecting associated with isoprene emissions depends on the ontogenetic all VOCs with proton affinities higher than water has facilitated stage of the leaves, increasing rapidly in developing leaves and the study of short-chain oxygenated VOCs (Bracho-Nunez et al., decreasing in senescing leaves due to programmed cell death 2013). Other studies, however, have confirmed the difficulty of (Niinemets et al., 2004; Alves et al., 2014). using PTR-MS for measuring monoterpene and sesquiterpene In addition to the changes in isoprene emission capacity, emissions, reporting high fragmentation patterns (Tani et al., 2003; Alves et al. (2014) also found that light saturation for isoprene Demarcke et al., 2009; Bracho-Nunez et al., 2011, 2013). Gas emission could also vary with foliar age, demonstrating that chromatography with a flame ionization detector (GC-FID) has biological changes due to aging could also influence the pattern been widely used for measuring isoprene emissions (Varshney of the response of isoprene emission to light. These results, and Singh, 2003; Padhy and Varshney, 2005b; Singh and Varshney, however, disagreed with those by Kuhn et al. (2004a), who 2006; Singh et al., 2007; Bracho-Nunez et al., 2013; Malik et al., stated that the inherent capacity of a plant to synthesize isoprene 2018) and is more sensitive than PTR-MS for measuring varied without modifying the function of the light response sesquiterpene emissions (Bracho-Nunez et al., 2013). GC-FID, during foliar development. Alves et al. (2018) demonstrated however, misses some VOCs, such as α-terpinene, due to its low that characterizing the isoprene emission capacity throughout performance in separation/identification (Wilske et al., 2007). the seasons based on the leaf area index and phenology improved Methods using a gas chromatograph coupled to a mass spectrometer the model observation agreement. More studies are needed to (GC–MS) are more specific than PTR-MS methods (Guenther Frontiers in Plant Science | www.frontiersin.org 9 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species et al., 1996a; Bracho-Nunez et al., 2011) and are suitable for the and edited the manuscript. All authors contributed to the article determination of heavier VOCs, including sesquiterpenes (Otter and approved the submitted version. et al., 2002; Bracho-Nunez et al., 2013). FUNDING CONCLUSION This study was supported by the Natural Science Foundation This review contributes to the global database of BVOC emissions of China (project nos. 42022023 and 41961144029), the from tropical plants (Appendix S1). Such emissions may represent Chinese Academy of Sciences (QYZDJ-SSW-DQC032), the local features due to the high biodiversity of most tropical ecosystems. Hong Kong Research Grants Council (T24-504/17-N), the Future field observations of tropical species may ultimately allow Department of Science and Technology of Guangdong Province the estimation of average ecosystem emissions that could then (2020B1212060053, 2017BT01Z134, and 2019B121205006), be scaled to estimate regional emissions. More long-term the Spanish Government project PID2019-110521GB-I00, measurements are needed to better characterize seasonal and the Catalan Government project SGR2017-1005, and the interannual variability for estimating the present and future impacts Fundación Ramón Areces grant ELEMENTAL-CLIMATE. ZM of BVOC fluxes, and more attention should be given to also acknowledges the financial support from the China sesquiterpenes, whose emissions are rarely studied but are highly Scholarship Council and the Guangdong Provincial variable and uncertain, perhaps due to methodological limitations Postdoctoral Talent-Introduction Program. and the inherent association of sesquiterpenes with stress and phenology (Bracho-Nunez et al., 2011, 2012). A better understanding of the behavior of BVOC emissions from the screening of additional ACKNOWLEDGMENTS plant species will increase our confidence in predictive models, so more experimental information is needed on how the capacities We thank Hongyan Zhang and Xiaoxiao Feng from China of species-specific isoprene emissions vary during foliar Agricultural University for help with data collection. We are developmental stages to improve models that predict emissions grateful to the helpful comments provided by reviewers. from tropical species (Alves et al., 2014). Many uncertainties in emission models based on poor simulations of foliar-scale emissions, among other factors, however, remain (Mutanda et al., 2016). SUPPLEMENTARY MATERIAL Future investigations of more possible sources are warranted, including examining the role of biodiversity and plant competition, The Supplementary Material for this article can be found online comparing different sampling and analytical techniques (Bracho- at: https://www.frontiersin.org/articles/10.3389/fpls.2022.833030/ Nunez et al., 2013), or creating techniques that encompass most full#supplementary-material of the BVOC emissions. Appendix S1 | Isoprenoid emissions for the tropical plants in this study. Rates of isoprene and terpene emissions with more than three species for tropical plant families. Isoprene emissions from plant species of the family Moraceae and AUTHOR CONTRIBUTIONS Fabaceae in phylogenetic trees. JP, JL, and XW conceived the idea and revised the manuscript. Appendix S2 | Phylogenetic tree of species of the family Moraceae ZM drafted the manuscript. JZ, YZ, DA, KY, and ZY reviewed and Fabaceae. Bellard, C., Rysman, J., Leroy, B., Claud, C., and Mace, G. M. (2017). A global REFERENCES picture of biological invasion threat on islands. Nat. Ecol. Evol. 1, 1862–1869. doi: 10.1038/s41559-017-0365-6 Albert, L. P., Wu, J., Prohaska, N., de Camargo, P. B., Huxman, T. E., Tribuzy, E. S., Benjamin, M. T., Sudol, M., Bloch, L., and Winer, A. M. (1996). Low-emitting et al. (2018). Age-dependent leaf physiology and consequences for crown- urban forests: a taxonomic methodology for assigning isoprene and scale carbon uptake during the dry season in an Amazon evergreen forest. monoterpene emission rates. Atmos. Environ. 30, 1437–1452. doi: New Phytol. 219, 870–884. doi: 10.1111/nph.15056 10.1016/1352-2310(95)00439-4 Alves, E. G., Harley, P., de C Gonçalves, J. F., da Silva Moura, C. E., and Bison, J. V., Cardoso-Gustavson, P., de Moraes, R. M., da Silva Pedrosa, G., Jardine, K. (2014). Effects of light and temperature on isoprene Cruz, L. S., Freschi, L., et al. (2018). Volatile organic compounds and nitric emission at different leaf developmental stages of eschweilera coriacea in oxide as responses of a Brazilian tropical species to ozone: the emission Central Amazon. Acta Amaz 44, 9–18. doi: 10.1590/S0044-596720 profile of young and mature leaves. Environ. Sci. Pollut. Res. 25, 3840–3848. 14000100002 doi: 10.1007/s11356-017-0744-1 Alves, E. G., Tóta, J., Turnipseed, A., Guenther, A. B., Vega Bustillos, J. O. Bohlmann, J., Meyer-Gauen, G., and Croteau, R. (1998). Plant terpenoid synthases: W., Santana, R. A., et al. (2018). Leaf phenology as one important driver molecular biology and phylogenetic analysis. Proc. Natl. Acad. Sci. U. S. A. of seasonal changes in isoprene emissions in Central Amazonia. Biogeosciences 95, 4126–4133. doi: 10.1073/pnas.95.8.4126 15, 4019–4032. doi: 10.5194/bg-15-4019-2018 Bracho-Nunez, A., Knothe, N., Costa, W. R., Liberato, M. A. R., Kleiss, B., Andreae, M. O., Artaxo, P., Brandão, C., Carswell, F. E., Ciccioli, P., Da Rottenberger, S., et al. (2012). Root anoxia effects on physiology and Costa, A. L., et al. (2002). Biogeochemical cycling of carbon, water, energy, emissions of volatile organic compounds (VOC) under short- and long- trace gases, and aerosols in Amazonia: the LBA-EUSTACH experiments. J. term inundation of trees from Amazon floodplains. Springerplus 1, 1–9. Geophys. Res. Atmos 107:524. doi: 10.1029/2001JD000524 doi: 10.1186/2193-1801-1-9 Frontiers in Plant Science | www.frontiersin.org 10 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species Bracho-Nunez, A., Knothe, N. M., Welter, S., Staudt, M., Costa, W. R., African EXPRESSO study domain. J. Geophys. Res. Atmos. 104, 30625–30639. Liberato, M. A., et al. (2013). Leaf level emissions of volatile organic doi: 10.1029/1999JD900391 compounds (VOC) from some Amazonian and Mediterranean plants. Guenther, A., Baugh, W., Davis, K., Hampton, G., Harley, P., Klinger, L., et al. Biogeosciences 10, 5855–5873. doi: 10.5194/bg-10-5855-2013 (1996a). Isoprene fluxes measured by enclosure, relaxed eddy accumulation, Bracho-Nunez, A., Welter, S., Staudt, M., and Kesselmeier, J. (2011). Plant surface layer gradient, mixed layer gradient, and mixed layer mass balance specific volatile organic compound emission rates from young and mature techniques. J. Geophys. Res. Atmos. 101, 18555–18567. doi: 10.1029/96JD00697 leaves of Mediterranean vegetation. J. Geophys. Res. Atmos. 116:D16304. Guenther, A., Hewitt, C. N., Erickson, D., Fall, R., Geron, C., Graedel, T., doi: 10.1029/2010JD015521 et al. (1995). A global model of natural volatile organic compound emissions. Brüggemann, N., and Schnitzler, J. P. (2002). Diurnal variation of dimethylallyl J. Geophys. Res. Atmos. 100, 8873–8892. doi: 10.1029/94JD02950 diphosphate concentrations in oak (Quercus robur) leaves. Physiol. Plantarum Guenther, A. B., Jiang, X., Heald, C. L., Sakulyanontvittaya, T., Duhl, T., 115, 190–196. doi: 10.1034/j.1399-3054.2002.1150203.x Emmons, L. K., et al. (2012). The model of emissions of gases and aerosols Dawson, W., Moser, D., Van Kleunen, M., Kreft, H., Pergl, J., Pyšek, P., et al. from nature version 2.1 (MEGAN2.1): an extended and updated framework (2017). Global hotspots and correlates of alien species richness across for modeling biogenic emissions. Geosci. Model Dev. 5, 1471–1492. doi: taxonomic groups. Nat. Ecol. Evol. 1, 1–7. doi: 10.1038/s41559- 10.5194/gmd-5-1471-2012 017-0186 Guenther, A., Jiang, X., Shah, T., Huang, L., Kemball-Cook, S., and Yarwood, G. Demarcke, M., Amelynck, C., Schoon, N., Dhooghe, F., Van Langenhove, H., (2020). “Model of emissions of gases and aerosol from nature version 3 and Dewulf, J. (2009). Laboratory studies in support of the detection of (MEGAN3) for estimating biogenic emissions,” in Air Pollution Modeling sesquiterpenes by proton-transfer-reaction mass spectrometry. Int. J. Mass and Its Application XXVI. eds. C. Mensink, W. Gong and A. Hakami (Cham: Spectrom. 279, 156–162. doi: 10.1016/j.ijms.2008.10.023 Springer International Publishing). Derwent, R. G., Simmonds, P. G., Manning, A. J., and Spain, T. G. (2007). Guenther, A., Karl, T., Harley, P., Wiedinmyer, C., Palmer, P. I., and Geron, C. Trends over a 20-year period from 1987 to 2007 in surface ozone at the (2006). Estimates of global terrestrial isoprene emissions using MEGAN atmospheric research station, Mace Head Ireland. Atmos. Environ. 41, (model of emissions of gases and aerosols from nature). Atmos. Chem. 9091–9098. doi: 10.1016/j.atmosenv.2007.08.008 Phys. 6, 3181–3210. doi: 10.5194/acp-6-3181-2006 Dindorf, T., Kuhn, U., Ganzeveld, L., Schebeske, G., Ciccioli, P., Holzke, C., Guenther, A., Monson, R., and Fall, R. (1991). Isoprene and monoterpene et al. (2006). Significant light and temperature dependent monoterpene emission rate variability: observations with eucalyptus and emission rate emissions from European beech (Fagus sylvatica L.) and their potential algorithm development. J. Geophys. Res. Atmos. 96, 10799–10808. doi: impact on the European volatile organic compound budget. J. Geophys. Res. 10.1029/91JD00960 Atmos. 111, 1–15. doi: 10.1029/2005JD006751 Guenther, A., Otter, L., Zimmerman, P., Greenberg, J., Scholes, R., and Scholes, M. Fall, R., and Monson, R. K. (1992). Isoprene emission rate and intercellular (1996b). Biogenic hydrocarbon emissions from southern African savannas. isoprene concentration as influenced by stomatal distribution and conductance. J. Geophys. Res. Atmos. 101, 25859–25865. doi: 10.1029/96JD02597 Plant Physiol. 100, 987–992. doi: 10.1104/pp.100.2.987 Guenther, A. B., Zimmerman, P. R., Harley, P. C., Monson, R. K., and Fall, R. Fehsenfeld, F., Calvert, J., Fall, R., Goldan, P., Guenther, A. B., Hewitt, C. N., (1993). Isoprene and monoterpene emission rate variability: model evaluations et al. (1992). Emissions of volatile organic compounds from vegetation and and sensitivity analyses. J. Geophys. Res. Atmos. 98, 12609–12617. doi: the implications for atmospheric chemistry. Global Biogeochem. Cy. 6, 389–430. 10.1029/93JD00527 doi: 10.1029/92GB02125 Harley, P., Eller, A., Guenther, A., and Monson, R. K. (2014). Observations Geron, C., Guenther, A., Greenberg, J., Loescher, H. W., Clark, D., and Baker, B. and models of emissions of volatile terpenoid compounds from needles of (2002). Biogenic volatile organic compound emissions from a lowland tropical ponderosa pine trees growing in situ: control by light, temperature and wet forest in Costa Rica. Atmos. Environ. 36, 3793–3802. doi: 10.1016/ stomatal conductance. Oecologia 176, 35–55. doi: 10.1007/s00442-014-3008-5 S1352-2310(02)00301-1 Harley, P. C., Litvak, M. E., Sharkey, T. D., and Monson, R. K. (1994). Isoprene Geron, C., Guenther, A., and Harley, P. (2001). Isoprene emission capacity for emission from velvet bean leaves (Interations among nitrogen availability, U.S. tree species. Atmos. Environ. 35, 3341–3352. doi: 10.1016/ growth photon flux density, and leaf development). Plant Physiol. 105, S1352-2310(00)00407-6 279–285. doi: 10.1104/pp.105.1.279 Geron, C. D., Guenther, A. B., and Pierce, T. E. (1994). An improved model Harley, P. C., Monson, R. K., and Lerdau, M. T. (1999). Ecological and evolutionary for estimating emissions of volatile organic compounds from forests in the aspects of isoprene emission from plants. Oecologia 118, 109–123. doi: eastern United States. J. Geophys. Res. Atmos. 99, 12773–12791. doi: 10.1007/s004420050709 10.1029/94JD00246 Harley, P., Otter, L., Guenther, A., and Greenberg, J. (2003). Micrometeorological Geron, C., Guenther, A., Sharkey, T., and Arnts, R. R. (2000). Temporal variability and leaf-level measurements of isoprene emissions from a Southern African in basal isoprene emission factor. Tree Physiol. 20, 799–805. doi: 10.1093/ Savanna. J. Geophys. Res. Atmos. 108:2592. doi: 10.1029/2002JD002592 treephys/20.12.799 Harley, P., Vasconcellos, P., Vierling, L., de S Pinheiro, C. C., Greenberg, J., Geron, C., Owen, S., Guenther, A., Greenberg, J., Rasmussen, R., Bai, J. H., Guenther, A., et al. (2004). Variation in potential for isoprene emissions et al. (2006). Volatile organic compounds from vegetation in southern Yunnan among Neotropical forest sites. Glob. Chang. Biol. 10, 630–650. doi: 10.1111/j. Province, China: emission rates and some potential regional implications. 1529-8817.2003.00760.x Atmos. Environ. 40, 1759–1773. doi: 10.1016/j.atmosenv.2005.11.022 He, C. R., Murray, F., and Lyons, T. (2000). Monoterpene and isoprene emissions Gershenzon, J., and Dudareva, N. (2007). The function of terpene natural from 15 Eucalyptus species in Australia. Atmos. Environ. 34, 645–655. doi: products in the natural world. Nat. Chem. Biol. 3, 408–414. doi: 10.1038/ 10.1016/S1352-2310(99)00219-8 nchembio.2007.5 Helmig, D., Bocquet, F., Pollmann, J., and Revermann, T. (2004). Analytical Goldstein, A. H., and Galbally, I. E. (2007). Known and unexplored organic techniques for sesquiterpene emission rate studies in vegetation enclosure constituents in the earth’s atmosphere. Environ. Sci. Technol. 41, 1514–1521. experiments. Atmos. Environ. 38, 557–572. doi: 10.1016/j.atmosenv.2003.10.012 doi: 10.1021/es072476p Higa, T., Parveen, S., Mutanda, I., Iqbal, M. A., Inafuku, M., Hashimoto, F., Greenberg, J. P., Guenther, A., Harley, P., Otter, L., Veenendaal, E. M., Hewitt, C. N., et al. (2018). Evaluation of isoprene emission rates of tropical trees by an et al. (2003). Eddy flux and leaf-level measurements of biogenic VOC iterative optimization procedure for G-93 parameters. Atmos. Environ. 192, emissions from mopane woodland of Botswana. J. Geophys. Res. Atmos. 209–217. doi: 10.1016/j.atmosenv.2018.08.059 108, 1–9. doi: 10.1029/2002JD002317 Holm, J. A., Jardine, K., Guenther, A. B., Chambers, J. Q., and Tribuzy, E. Guenther, A., Archer, S., Greenberg, J., Harley, P., Helmig, D., Vierling, L., (2014). Evaluation of MEGAN-CLM parameter sensitivity to predictions of et al. (1999a). Biogenic hydrocarbon emissions and landcover climate in a isoprene emissions from an Amazonian rainforest. Atmos. Chem. Phys. subtropical savanna change. Phys. Chem. Earth 24, 659–667. doi: 10.1016/ Discuss. 14, 23995–24041. doi: 10.5194/acpd-14-23995-2014 S1464-1909(99)00062-3 Huete, A. R., Didan, K., Shimabukuro, Y. E., Ratana, P., Saleska, S. R., Hutyra, L. R., Guenther, A., Baugh, B., Brasseur, G., Greenberg, J., Harley, P., Klinger, L., et al. (2006). Amazon rainforests green-up with sunlight in dry season. et al. (1999b). Isoprene emission estimates and uncertainties for the Central Geophys. Res. Lett. 33, 2–5. doi: 10.1029/2005GL025583 Frontiers in Plant Science | www.frontiersin.org 11 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species Jardine, A. B., Jardine, K. J., Fuentes, J. D., Martin, S. T., Martins, G., Durgante, F., Lehning, A., Zimmer, I., Steinbrecher, R., Bruggemann, N., and Schnitzler, J. P. et al. (2015). Highly reactive light-dependent monoterpenes in the Amazon. (1999). Isoprene synthase activity and its relation to isoprene emission in Geophys. Res. Lett. 42, 1576–1583. doi: 10.1002/2014GL062573 Quercus robur L. leaves. Plant Cell Environ. 22, 495–504. doi: 10.1046/j.1365- Jardine, K. J., Jardine, A. B., Holm, J. A., Lombardozzi, D. L., Negron-Juarez, R. I., 3040.1999.00425.x Martin, S. T., et al. (2017). Monoterpene “thermometer” of tropical forest- Lerdau, M., and Keller, M. (1997). Controls on isoprene emission from trees atmosphere response to climate warming. Plant Cell Environ. 40, 441–452. in a subtropical dry forest. Plant Cell Environ. 20, 569–578. doi: 10.1111/j. doi: 10.1111/pce.12879 1365-3040.1997.00075.x Jardine, K. J., Jardine, A. B., Souza, V. F., Carneiro, V., Ceron, J. V., Gimenez, B. O., Lerdau, M. T., and Throop, H. L. (1999). Isoprene emissions and photosynthesis et al. (2016). Methanol and isoprene emissions from the fast growing tropical in a tropical forest canopy: implications for model development. Ecol. Appl. pioneer species Vismia guianensis (Aubl.) Pers. (Hypericaceae) in the Central 9, 1109–1117. doi: 10.1890/1051-0761(1999)009[1109:IEAPIA]2.0.CO;2 Amazon forest. Atmos. Chem. Phys. 16, 6441–6452. doi: 10.5194/ Lerdau, M., and Throop, H. L. (2000). Sources of variability in isoprene acp-16-6441-2016 emission and photosynthesis in two species of tropical wet forest trees. Jardine, K. J., Zorzanelli, R. F., Gimenez, B. O., de Oliveira Piva, L. R., Teixeira, A., Biotropica 32, 670–676. doi: 10.1646/0006-3606(2000)032[0670:SOVIIE] Fontes, C. G., et al. (2020). Leaf isoprene and monoterpene emission 2.0.CO;2 distribution across hyperdominant tree genera in the Amazon basin. Litvak, M. E., Loreto, F., Harley, P. C., Sharkey, T. D., and Monson, R. K. Phytochemistry 175:112366. doi: 10.1016/j.phytochem.2020.112366 (1996). The response of isoprene emission rate and photosynthetic rate to Jones, C. E., Hopkins, J. R., and Lewis, A. C. (2011). In situ measurements photon flux and nitrogen supply in aspen and white oak trees. Plant Cell of isoprene and monoterpenes within a south-east Asian tropical rainforest. Environ. 19, 549–559. doi: 10.1111/j.1365-3040.1996.tb00388.x Atmos. Chem. Phys. 11, 6971–6984. doi: 10.5194/acp-11-6971-2011 Llusià, J., Peñuelas, J., Sardans, J., Owen, S. M., and Niinemets, Ü. (2010). Juuti, S., Arey, J., and Atkinson, R. (1990). Monoterpene emission rate Measurement of volatile terpene emissions in 70 dominant vascular plant measurements from a Monterey Pine. J. Geophys. Res. Atmos. 95, 7515–7519. species in Hawaii: aliens emit more than natives. Glob. Ecol. Biogeogr. 19, doi: 10.1029/JD095iD06p07515 863–874. doi: 10.1111/j.1466-8238.2010.00557.x Karl, T., Guenther, A., Yokelson, R. J., Greenberg, J., Potosnak, M., Blake, D. R., Llusià, J., Sardans, J., Niinemets, Ü., Owen, S. M., and Peñuelas, J. (2014). A et al. (2007). The tropical forest and fire emissions experiment: emission, screening study of leaf terpene emissions of 43 rainforest species in Danum chemistry, and transport of biogenic volatile organic compounds in the Valley conservation area (Borneo) and their relationships with chemical lower atmosphere over Amazonia. J. Geophys. Res. Atmos. 112, 1–17. doi: and morphological leaf traits. Plant Biosyst. 148, 307–317. doi: 10.1029/2007JD008539 10.1080/11263504.2013.770803 Keller, M., and Lerdau, M. (1999). Isoprene emission from tropical forest canopy Loivamaki, M., Louis, S., Cinege, G., Zimmer, I., Fischbach, R. J., and Schnitzler, J. P. leaves. Glob. Biogeochem. Cy. 13, 19–29. doi: 10.1029/1998GB900007 (2007). Circadian rhythms of isoprene biosynthesis in Grey poplar leaves. Kesselmeier, J., and Staudt, M. (1999). Biogenic volatile organic compounds Plant Physiol. 143, 540–551. doi: 10.1104/pp.106.092759 (VOC): an overview on emission, physiology and ecology. J. Atmos. Chem. Loreto, F., Ciccioli, P., Brancaleoni, E., Valentini, R., De Lillis, M., Csiky, O., 33, 23–88. doi: 10.1023/A:1006127516791 et al. (1998). A hypothesis on the evolution of isoprenoid emission by oaks Kishimoto, K., Matsui, K., Ozawa, R., and Takabayashi, J. (2006). Analysis of based on the correlation between emission type and Quercus taxonomy. defensive responses activated by volatile allo-ocimene treatment in Arabidopsis Oecologia 115, 302–305. doi: 10.1007/s004420050520 thaliana. Phytochemistry 67, 1520–1529. doi: 10.1016/j.phytochem.2006.05.027 Loreto, F., Ciccioli, P., Cecinato, A., Brancaleoni, E., Frattoni, M., Fabozzi, C., Klinger, L. F. (1998). Patterns in volatile organic compound emissions along et al. (1996a). Evidence of the photosynthetic origin of monoterpenes emitted a savanna-rainforest gradient in Central Africa. J. Geophys. Res. Atmos. 103, by Quercus ilex L. leaves by C-13 labeling. Plant Physiol. 110, 1317–1322. 1443–1454. doi: 10.1029/97JD02928 doi: 10.1104/pp.110.4.1317 Klinger, L. F., Li, Q. J., Guenther, A. B., Greenberg, J. P., Baker, B., and Bai, J. H. Loreto, F., Ciccioli, P., Cecinato, A., Brancaleoni, E., Frattoni, M., and Tricoli, D. (2002). Assessment of volatile organic compound emissions from ecosystems (1996b). Influence of environmental factors and air composition on the of China. J. Geophys. Res. Atmos. 107:76. doi: 10.1029/2001JD001076 emission of α-pinene from Quercus ilex leaves. Plant Physiol. 110, 267–275. Kuhn, U., Rottenberger, S., Biesenthal, T., Wolf, A., Schebeske, G., Ciccioli, P., doi: 10.1104/pp.110.1.267 et al. (2004a). Seasonal differences in isoprene and light-dependent monoterpene Loreto, F., and Fineschi, S. (2015). Reconciling functions and evolution of emission by Amazonian tree species. Glob. Chang. Biol. 10, 663–682. doi: isoprene emission in higher plants. New Phytol. 206, 578–582. doi: 10.1111/ 10.1111/j.1529-8817.2003.00771.x nph.13242 Kuhn, U., Rottenberger, S., Biesenthal, T., Wolf, A., Schebeske, G., Ciccioli, P., Maag, D., Erb, M., Köllner, T. G., and Gershenzon, J. (2015). Defensive weapons et al. (2002). Isoprene and monoterpene emissions of Amazonian tree species and defense signals in plants: Some metabolites serve both roles. BioEssays during the wet season: direct and indirect investigations on controlling 37, 167–174. doi: 10.1002/bies.201400124 environmental functions. J. Geophys. Res. Atmos. 107, 1–13. doi: Maeda, E. E., Ma, X., Wagner, F. H., Kim, H., Oki, T., Eamus, D., et al. (2017). 10.1029/2001JD000978 Evapotranspiration seasonality across the Amazon Basin. Earth Syst. Dynam. Kuhn, U., Rottenberger, S., Biesenthal, T., Wolf, A., Schebeske, G., Ciccioli, P., 8, 439–454. doi: 10.5194/esd-8-439-2017 et al. (2004b). Strong correlation between isoprene emission and gross Malik, T. G., Gajbhiye, T., and Pandey, S. K. (2018). Seasonality in emission photosynthetic capacity during leaf phenology of the tropical tree species patterns of isoprene from two dominant tree species of Central India: Hymenaea courbaril with fundamental changes in volatile organic compounds implications on terrestrial carbon emission and climate change. Proc. Int. emission composition during early leaf development. Plant Cell Environ. Acad. Ecol. Environ. Sci. 8, 204–212. 27, 1469–1485. doi: 10.1111/j.1365-3040.2004.01252.x Malik, T. G., Gajbhiye, T., and Pandey, S. K. (2019). Some insights into Kuzma, J., and Fall, R. (1993). Leaf isoprene emission rate is dependent on composition and monoterpene emission rates from selected dominant tropical leaf development and the level of isoprene synthase. Plant Physiol. 101, tree species of Central India: plant-specific seasonal variations. Ecol. Res. 435–440. doi: 10.1104/pp.101.2.435 34, 821–834. doi: 10.1111/1440-1703.12058 Laffineur, Q., Aubinet, M., Schoon, N., Amelynck, C., Müller, J. F., Dewulf, J., Merfort, I. (2002). Review of the analytical techniques for sesquiterpenes and et al. (2011). Isoprene and monoterpene emissions from a mixed temperate sesquiterpene lactones. J. Chromatogr. A 967, 115–130. doi: 10.1016/ forest. Atmos. Environ. 45, 3157–3168. doi: 10.1016/j.atmosenv.2011.02.054 S0021-9673(01)01560-6 Lamarque, J. F., Bond, T. C., Eyring, V., Granier, C., Heil, A., Klimont, Z., Monson, R. K., Grote, R., Niinemets, Ü., and Schnitzler, J. P. (2012). Modeling et al. (2010). Historical (1850–2000) gridded anthropogenic and biomass the isoprene emission rate from leaves. New Phytol. 195, 541–559. doi: burning emissions of reactive gases and aerosols: methodology and application. 10.1111/j.1469-8137.2012.04204.x Atmos. Chem. Phys. 10, 7017–7039. doi: 10.5194/acp-10-7017-2010 Monson, R. K., Harley, P. C., Litvak, M. E., Wildermuth, M., Guenther, A. B., Lamb, B., Guenther, A., Gay, D., and Westberg, H. (1987). A national inventory Zimmerman, P. R., et al. (1994). Environmental and developmental controls of biogenic hydrocarbon emissions. Atmos. Environ. 21, 1695–1705. doi: over the seasonal pattern of isoprene emission from aspen leaves. Oecologia 10.1016/0004-6981(87)90108-9 99, 260–270. doi: 10.1007/BF00627738 Frontiers in Plant Science | www.frontiersin.org 12 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species Monson, R. K., Jaeger, C. H., Adams, W. W., Driggers, E. M., Silver, G. M., Rasmussen, R. A. (1972). What do the hydrocarbons from trees contribute to and Fall, R. (1992). Relationships among isoprene emission rate, photosynthesis, air pollution? J. Air Pollut. Control Assoc. 22, 537–543. doi: and isoprene synthase activity as influenced by temperature. Plant Physiol. 10.1080/00022470.1972.10469676 98, 1175–1180. doi: 10.1104/pp.98.3.1175 Rinne, H. J. I., Guenther, A. B., Greenberg, J. P., and Harley, P. C. (2002). Monson, R. K., Jones, R. T., Rosenstiel, T. N., and Schnitzler, J. -P. (2013). Isoprene and monoterpene fluxes measured above Amazonian rainforest Why only some plants emit isoprene. Plant Cell Environ. 36, 503–516. doi: and their dependence on light and temperature. Atmos. Environ. 36, 2421–2426. 10.1111/pce.12015 doi: 10.1016/S1352-2310(01)00523-4 Monson, R. K., Lerdau, M. T., Sharkey, T. D., Schimel, D. S., and Fall, R. (1995). Roberts, J., Cabral, O. M. R., and de Aguiar, L. F. (1990). Stomatal and boundary- Biological aspects of constructing volatile organic compound emission inventories. layer conductance in an Amazonian terra firme rain forest. J. Appl. Ecol. Atmos. Environ. 29, 2989–3002. doi: 10.1016/1352-2310(94)00360-W 27, 336–353. doi: 10.2307/2403590 Mutanda, I., Inafuku, M., Iwasaki, H., Saitoh, S., Fukuta, M., Watanabe, K., Roselle, S. J., Pierce, T. E., and Schere, K. L. (1991). The sensitivity of regional et al. (2016). Parameterization of G-93 isoprene emission formula for tropical ozone modeling to biogenic hydrocarbons. J. Geophys. Res. Atmos. 96, trees Casuarina equisetifolia and Ficus septica. Atmos. Environ. 141, 287–296. 7371–7394. doi: 10.1029/91JD00005 doi: 10.1016/j.atmosenv.2016.06.052 Rottenberger, S., Kuhn, U., Wolf, A., Schebeske, G., Oliva, S. T., Tavares, T. M., Niinemets, Ü., Arneth, A., Kuhn, U., Monson, R. K., Peñuelas, J., and Staudt, M. et al. (2004). Exchange of short-chain aldehydes between Amazonian vegetation (2010). The emission factor of volatile isoprenoids: stress, acclimation, and and the atmosphere. Ecol. Appl. 14, 247–262. doi: 10.1890/01-6027 developmental responses. Biogeosciences 7, 2203–2223. doi: 10.5194/ Schnitzler, J. P., Lehning, A., and Steinbrecher, R. (1997). Seasonal pattern of bg-7-2203-2010 isoprene synthase activity in Quercus robur leaves and its significance for Niinemets, Ü., Kuhn, U., Harley, P. C., Staudt, M., Arneth, A., Cescatti, A., et al. modeling isoprene emission rates. Botanica Acta 110, 240–243. doi: 10.1111/ (2011). Estimations of isoprenoid emission capacity from enclosure studies: j.1438-8677.1997.tb00635.x measurements, data processing, quality and standardized measurement protocols. Serça, D., Guenther, A., Klinger, L., Vierling, L., Harley, P., Druilhet, A., et al. Biogeosciences 8, 2209–2246. doi: 10.5194/bg-8-2209-2011 (2001). EXPRESSO flux measurements at upland and lowland Congo tropical Niinemets, Ü., Kull, O., and Tenhunen, J. D. (2004). Within canopy variation forest site. Tellus Ser. B Chem. Phys. Meteorol. 53, 220–234. doi: 10.3402/ in the rate of development of photosynthetic capacity is proportional to tellusb.v53i3.16593 integrated quantum flux density in temperate deciduous trees. Plant Cell Sharkey, T. D., and Monson, R. K. (2014). The future of isoprene emission Environ. 27, 293–313. doi: 10.1111/j.1365-3040.2003.01143.x from leaves, canopies and landscapes. Plant Cell Environ. 37, 1727–1740. Oku, H., Fukuta, M., Iwasaki, H., Tambunan, P., and Baba, S. (2008). Modification doi: 10.1111/pce.12289 of the isoprene emission model G93 for tropical tree Ficus virgata. Atmos. Sharkey, T. D., Singsaas, E. L., Lerdau, M. T., and Geron, C. D. (1999). Weather Environ. 42, 8747–8754. doi: 10.1016/j.atmosenv.2008.08.036 effects on isoprene emission capacity and applications in emissions algorithms. Oku, H., Inafuku, M., Takamine, T., Nagamine, M., Saitoh, S., and Fukuta, M. Ecol. Appl. 9, 1132–1137. doi: 10.1890/1051-0761(1999)009[1132:WEOIEC] (2014). Temperature threshold of isoprene emission from tropical trees, 2.0.CO;2 Ficus virgata and Ficus septica. Chemosphere 95, 268–273. doi: 10.1016/j. Silver, G. M., and Fall, R. (1991). Enzymatic synthesis of isoprene from chemosphere.2013.09.003 dimethylallyl diphosphate in aspen leaf extracts. Plant Physiol. 97, 1588–1591. Otter, L. B., Guenther, A., and Greenberg, J. (2002). Seasonal and spatial doi: 10.1104/pp.97.4.1588 variations in biogenic hydrocarbon emissions from southern African savannas Šimpraga, M., Ghimire, R. P., Van Der Straeten, D., Blande, J. D., Kasurinen, A., and woodlands. Atmos. Environ. 36, 4265–4275. doi: 10.1016/ Sorvari, J., et al. (2019). Unravelling the functions of biogenic volatiles in S1352-2310(02)00333-3 boreal and temperate forest ecosystems. Eur. J. For. Res. 138, 763–787. doi: Owen, S. M., Boissard, C., and Hewitt, C. N. (2001). Volatile organic compounds 10.1007/s10342-019-01213-2 (VOCs) emitted from 40 Mediterranean plant species: VOC speciation and Šimpraga, M., Verbeeck, H., Demarcke, M., Joó, É., Amelynck, C., Schoon, N., extrapolation to habitat scale. Atmos. Environ. 35, 5393–5409. doi: 10.1016/ et al. (2011). Comparing monoterpenoid emissions and net photosynthesis S1352-2310(01)00302-8 of beech (Fagus sylvatica L.) in controlled and natural conditions. Atmos. Owen, S. M., Harley, P., Guenther, A., and Hewitt, C. N. (2002). Light dependency Environ. 45, 2922–2928. doi: 10.1016/j.atmosenv.2011.01.047 of VOC emissions from selected Mediterranean plant species. Atmos. Environ. Singh, A. P., Singh, R., Mina, U., Singh, M. P., and Varshney, C. K. (2011). 36, 3147–3159. doi: 10.1016/S1352-2310(02)00235-2 Emissions of monoterpene from tropical Indian plant species and assessment Padhy, P. K., and Varshney, C. K. (2005a). Emission of volatile organic compounds of VOC emission from the forest of Haryana state. Atmos. Pollut. Res. 2, (VOC) from tropical plant species in India. Chemosphere 59, 1643–1653. 72–79. doi: 10.5094/APR.2011.009 doi: 10.1016/j.chemosphere.2005.01.046 Singh, R., Singh, M. P., and Singh, A. P. (2014). Ozone forming potential of Padhy, P. K., and Varshney, C. K. (2005b). Isoprene emission from tropical tropical plant species of the Vidarbha region of Maharashtra state of India. tree species. Environ. Pollut. 135, 101–109. doi: 10.1016/j.envpol.2004.10.003 Urban For. Urban Green. 13, 814–820. doi: 10.1016/j.ufug.2014.05.007 Paton-Walsh, C., Emmerson, K. M., Garland, R. M., Keywood, M., Hoelzemann, J. J., Singh, R., Singh, A. P., Singh, M. P., Kumar, A., and Varshney, C. K. (2008). Huneeus, N., et al. (2022). Key challenges for tropospheric chemistry in Emission of isoprene from common Indian plant species and its implications the southern hemisphere. Elementa-Sci. Anthrop. 10, 1–35. doi: 10.1525/ for regional air quality. Environ. Monit. Assess. 144, 43–51. doi: 10.1007/ elementa.2021.00050 s10661-007-9940-7 Peñuelas, J., and Llusià, J. (2001). The complexity of factors driving volatile Singh, A. P., and Varshney, C. K. (2006). Isoprene emission from the forest organic compound emissions by plants. Biol. Plantarum 44, 481–487. doi: of Haryana state. Environ. Monit. Assess. 122, 145–151. doi: 10.1007/ 10.1023/A:1013797129428 s10661-005-9170-9 Peñuelas, J., and Llusià, J. (2002). Linking photorespiration, monoterpenes and Singh, A. P., Varshney, C. K., and Singh, U. K. (2007). Seasonal variations in thermotolerance in Quercus. New Phytol. 155, 227–237. doi: isoprene emission from tropical deciduous tree species. Environ. Monit. 10.1046/j.1469-8137.2002.00457.x Assess. 131, 231–235. doi: 10.1007/s10661-006-9471-7 Peñuelas, J., and Llusià, J. (2003). BVOCs: plant defense against climate warming? Staudt, M., and Bertin, N. (1998). Light and temperature dependence of the Trends Plant Sci. 8, 105–109. doi: 10.1016/S1360-1385(03)00008-6 emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex Peñuelas, J., and Staudt, M. (2010). BVOCs and global change. Trends Plant L.) leaves. Plant Cell Environ. 21, 385–395. doi: 10.1046/j.1365- Sci. 15, 133–144. doi: 10.1016/j.tplants.2009.12.005 3040.1998.00288.x Pétron, G., Harley, P., Greenberg, J., and Guenther, A. (2001). Seasonal temperature Staudt, M., and Seufert, G. (1995). Light-dependent emission of monoterpenes variations influence isoprene emission. Geophys. Res. Lett. 28, 1707–1710. by holm oak (Quercus ilex). Naturwissenschaften 82, 89–92. doi: 10.1007/ doi: 10.1029/2000GL011583 BF01140148 Pierce, T. E., and Waldruff, P. S. (1991). PC-BEIS: a personal computer version Tambunan, P., Baba, S., Kuniyoshi, A., Iwasaki, H., Nakamura, T., Yamasaki, H., of the biogenic emissions inventory system. J. Air Waste Manage. Assoc. et al. (2006). Isoprene emission from tropical trees in Okinawa Island, 41, 937–941. doi: 10.1080/10473289.1991.10466890 Japan. Chemosphere 65, 2138–2144. doi: 10.1016/j.chemosphere.2006.06.013 Frontiers in Plant Science | www.frontiersin.org 13 May 2022 | Volume 13 | Article 833030 Mu et al. Isoprenoid Emissions From Tropical Species Tani, A., Hayward, S., and Hewitt, C. N. (2003). Measurement of monoterpenes Wu, J., Albert, L. P., Lopes, A. P., Restrepo-Coupe, N., Hayek, M., Wiedemann, K. T., and related compounds by proton transfer reaction-mass spectrometry (PTR- et al. (2016). Leaf development and demography explain photosynthetic seasonality MS). Int. J. Mass Spectrom. 223-224, 561–578. doi: 10.1016/ in Amazon evergreen forests. Science 351, 972–976. doi: 10.1126/science.aad5068 S1387-3806(02)00880-1 Yáñez-Serrano, A. M., Bourtsoukidis, E., Alves, E. G., Bauwens, M., Stavrakou, T., Taylor, T. C., McMahon, S. M., Smith, M. N., Boyle, B., Violle, C., van Haren, J., Llusià, J., et al. (2020). Amazonian biogenic volatile organic compounds et al. (2018). Isoprene emission structures tropical tree biogeography and under global change. Glob. Chang. Biol. 26, 4722–4751. doi: 10.1111/gcb.15185 community assembly responses to climate. New Phytol. 220, 435–446. doi: Yàñez-Serrano, A. M., Nölscher, A. C., Bourtsoukidis, E., Alves, E. G., Ganzeveld, L., 10.1111/nph.15304 Bonn, B., et al. (2018). Monoterpene chemical speciation in a tropical Taylor, T. C., Smith, M. N., Slot, M., and Feeley, K. J. (2019). The capacity rainforest: variation with season, height, and time of day at the Amazon to emit isoprene differentiates the photosynthetic temperature responses of Tall Tower Observatory (ATTO). Atmos. Chem. Phys. 18, 3403–3418. doi: tropical plant species. Plant Cell Environ. 42, 2448–2457. doi: 10.1111/ 10.5194/acp-18-3403-2018 pce.13564 Yáñez-Serrano, A. M., Nölscher, A. C., Williams, J., Wolff, S., Alves, E., Taylor, T. C., Wisniewski, W. T., Alves, E. G., Oliveira Junior, R. C., and Martins, G. A., et al. (2015). Diel and seasonal changes of biogenic volatile Saleska, S. R. (2021). A new field instrument for leaf volatiles reveals an organic compounds within and above an Amazonian rainforest. Atmos. unexpected vertical profile of isoprenoid emission capacities in a tropical Chem. Phys. 15, 3359–3378. doi: 10.5194/acp-15-3359-2015 forest. Front. For. Glob. Chang. 4:668228. doi: 10.3389/ffgc.2021.668228 Yokouchi, Y., and Ambe, Y. (1984). Factors affecting the emission of monoterpenes Tholl, D., Boland, W., Hansel, A., Loreto, F., Röse, U. S. R., and Schnitzler, J. P. from red pine (Pinus densifiora). Plant Physiol. 75, 1009–1012. doi: 10.1104/ (2006). Practical approaches to plant volatile analysis. Plant J. 45, 540–560. pp.75.4.1009 doi: 10.1111/j.1365-313X.2005.02612.x Zeng, J., Zhang, Y., Zhang, H., Song, W., Wu, Z., and Wang, X. (2022). Design Varshney, C. K., and Singh, A. P. (2003). Isoprene emission from Indian trees. and characterization of a semi-open dynamic chamber for measuring biogenic J. Geophys. Res. Atmos. 108:3866. doi: 10.1029/2003JD003866 volatile organic compound (BVOC) emissions from plants. Atmos. Meas. Vickers, C. E., Gershenzon, J., Lerdau, M. T., and Loreto, F. (2009). A unified Tech. 15, 79–93. doi: 10.5194/amt-15-79-2022 mechanism of action for volatile isoprenoids in plant abiotic stress. Nat. Zimmerman, P. R. (1979). Determination of emission rates of hydrocarbons Chem. Biol. 5, 283–291. doi: 10.1038/nchembio.158 from indigenous species of vegetation in the Tampa/St. Petersburg, Florida Wang, Y. F., Owen, S. M., Li, Q. J., and Peñuelas, J. (2007). Monoterpene area, Tampa Bay area photochemical oxidant study, final report, appendix emissions from rubber trees (Hevea brasiliensis) in a changing landscape C, EPA Rep. 904/9-77-028, U.S. Environ. Prot. Agency, Atlanta, GA. and climate: chemical speciation and environmental control. Glob. Chang. Biol. 13, 2270–2282. doi: 10.1111/j.1365-2486.2007.01441.x Conflict of Interest: The authors declare that the research was conducted in Webb, C. O., and Donoghue, M. J. (2005). Phylomatic: tree assembly for applied the absence of any commercial or financial relationships that could be construed phylogenetics. Mol. Ecol. Notes 5, 181–183. doi: 10.1111/j.1471-8286. as a potential conflict of interest. 2004.00829.x Welter, S., Bracho-Nuñez, A., Mir, C., Zimmer, I., Kesselmeier, J., Lumaret, R., Publisher’s Note: All claims expressed in this article are solely those of the et al. (2012). The diversification of terpene emissions in Mediterranean authors and do not necessarily represent those of their affiliated organizations, oaks: lessons from a study of Quercus suber, Quercus canariensis and its or those of the publisher, the editors and the reviewers. Any product that may hybrid Quercus afares. Tree Physiol. 32, 1082–1091. doi: 10.1093/treephys/ be evaluated in this article, or claim that may be made by its manufacturer, is tps069 not guaranteed or endorsed by the publisher. Went, F. W. (1960). Blue hazes in the atmosphere. Nature 187, 641–643. doi: 10.1038/187641a0 Copyright © 2022 Mu, Llusià, Zeng, Zhang, Asensio, Yang, Yi, Wang and Peñuelas. Wilkinson, M. J., Owen, S. M., Possell, M., Hartwell, J., Gould, P., Hall, A., This is an open-access article distributed under the terms of the Creative Commons et al. (2006). Circadian control of isoprene emissions from oil palm (Elaeis Attribution License (CC BY). The use, distribution or reproduction in other forums guineensis). Plant J. 47, 960–968. doi: 10.1111/j.1365-313X.2006.02847.x is permitted, provided the original author(s) and the copyright owner(s) are credited Wilske, B., Cao, K. F., Schebeske, G., Chen, J. W., Wang, A., and Kesselmeier, J. and that the original publication in this journal is cited, in accordance with accepted (2007). Isoprenoid emissions of trees in a tropical rainforest in Xishuangbanna, academic practice. No use, distribution or reproduction is permitted which does not SW China. Atmos. Environ. 41, 3748–3757. doi: 10.1016/j.atmosenv.2007.01.008 comply with these terms. Frontiers in Plant Science | www.frontiersin.org 14 May 2022 | Volume 13 | Article 833030