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1.  Photosynthetic Responses of the Tropical Spiny Shrub Lycium nodosum (Solanaceae) to Drought, Soil Salinity and Saline Spray 
Annals of Botany  2003;92(6):757-765.
Water relations and photosynthetic characteristics of plants of Lycium nodosum grown under increasing water deficit (WD), saline spray (SS) or saline irrigation (SI) were studied. Plants of this perennial, deciduous shrub growing in the coastal thorn scrubs of Venezuela show succulent leaves which persist for approx. 1 month after the beginning of the dry season; leaf succulence is higher in populations closer to the sea. These observations suggested that L. nodosum is tolerant both to WD and salinity. In the glasshouse, WD caused a marked decrease in the xylem water potential (ψ), leaf osmotic potential (ψs) and relative water content (RWC) after 21 d; additionally, photosynthetic rate (A), carboxylation efficiency (CE) and stomatal conductance (gs) decreased by more than 90 %. In contrast, in plants treated for 21 d with a foliar spray with 35 ‰ NaCl or irrigation with a 10 % NaCl solution, ψ and RWC remained nearly constant, while ψs decreased by 30 %, and A, CE and gs decreased by more than 80 %. An osmotic adjustment of 0·60 (SS) and 0·94 MPa (SI) was measured. Relative stomatal and mesophyll limitations to A increased with both WD and SS, but were not determined for SI‐treated plants. No evidence of chronic photoinhibition due to any treatment was observed, since maximum quantum yield of PSII, Fv/Fm, did not change with either drought in the field or water or salinity stress in the glasshouse. Nevertheless, WD and SI treatments caused a decrease in the photochemical (qP) and an increase in the non‐photochemical (qN) quenching coefficients relative to controls; qN was unaffected by the SS treatment. The occurrence of co‐limitation of A by stomatal and non‐stomatal factors in plants of L. nodosum may be associated with the extended leaf duration under water or saline stress. Additionally, osmotic adjustment may partly explain the relative maintenance of A and gs in the SS and SI treatments and the tolerance to salinity of plants of this species in coastal habitats.
doi:10.1093/aob/mcg199
PMCID: PMC4243616  PMID: 14534200
Drought; Lycium nodosum; fluorescence; mesophyll limitation; saline stress; stomatal limitation; water deficit
2.  Coordinated Changes in Antioxidative Enzymes Protect the Photosynthetic Machinery from Salinity Induced Oxidative Damage and Confer Salt Tolerance in an Extreme Halophyte Salvadora persica L. 
Salinity-induced modulations in growth, photosynthetic pigments, relative water content (RWC), lipid peroxidation, photosynthesis, photosystem II efficiency, and changes in activity of various antioxidative enzymes were studied in the halophyte Salvadora persica treated with various levels of salinity (0, 250, 500, 750, and 1000 mM NaCl) to obtain an insight into the salt tolerance ability of this halophyte. Both fresh and dry biomass as well as leaf area (LA) declined at all levels of salinity whereas salinity caused an increase in leaf succulence. A gradual increase was observed in the Na+ content of leaf with increasing salt concentration up to 750 mM NaCl, but at higher salt concentration (1000 mM NaCl), the Na+ content surprisingly dropped down to the level of 250 mM NaCl. The chlorophyll and carotenoid contents of the leaf remained unaffected by salinity. The photosynthetic rate (PN), stomatal conductance (gs), the transpiration rate (E), quantum yield of PSII (ΦPSII), photochemical quenching (qP), and electron transport rate remained unchanged at low salinity (250 to 500 mM NaCl) whereas, significant reduction in these parameters were observed at high salinity (750 to 1000 mM NaCl). The RWC% and water use efficiency (WUE) of leaf remained unaffected by salinity. The salinity had no effect on maximum quantum efficiency of PS II (Fv/Fm) which indicates that PS II is not perturbed by salinity-induced oxidative damage. Analysis of the isoforms of antioxidative enzymes revealed that the leaves of S. persica have two isoforms each of Mn-SOD and Fe-SOD and one isoform of Cu-Zn SOD, three isoforms of POX, two isoforms of APX and one isoform of CAT. There was differential responses in activity and expression of different isoforms of various antioxidative enzymes. The malondialdehyde (MDA) content (a product of lipid peroxidation) of leaf remained unchanged in S. persica treated with various levels of salinity. Our results suggest that the absence of pigment degradation, the reduction of water loss, and the maintenance of WUE and protection of PSII from salinity-induced oxidative damage by the coordinated changes in antioxidative enzymes are important factors responsible for salt tolerance of S. persica.
doi:10.3389/fpls.2016.00050
PMCID: PMC4748684  PMID: 26904037
ascorbate peroxidase; catalase; halophyte; lipid peroxidation; photosynthesis; Salvadora persica; superoxide dismutase
3.  Metabolomic Response of Calotropis procera Growing in the Desert to Changes in Water Availability 
PLoS ONE  2014;9(2):e87895.
Water availability is a major limitation for agricultural productivity. Plants growing in severe arid climates such as deserts provide tools for studying plant growth and performance under extreme drought conditions. The perennial species Calotropis procera used in this study is a shrub growing in many arid areas which has an exceptional ability to adapt and be productive in severe arid conditions.
We describe the results of studying the metabolomic response of wild C procera plants growing in the desert to a one time water supply. Leaves of C. procera plants were taken at three time points before and 1 hour, 6 hours and 12 hours after watering and subjected to a metabolomics and lipidomics analysis. Analysis of the data reveals that within one hour after watering C. procera has already responded on the metabolic level to the sudden water availability as evidenced by major changes such as increased levels of most amino acids, a decrease in sucrose, raffinose and maltitol, a decrease in storage lipids (triacylglycerols) and an increase in membrane lipids including photosynthetic membranes. These changes still prevail at the 6 hour time point after watering however 12 hours after watering the metabolomics data are essentially indistinguishable from the prewatering state thus demonstrating not only a rapid response to water availability but also a rapid response to loss of water.
Taken together these data suggest that the ability of C. procera to survive under the very harsh drought conditions prevailing in the desert might be associated with its rapid adjustments to water availability and losses.
doi:10.1371/journal.pone.0087895
PMCID: PMC3919747  PMID: 24520340
4.  Pharmacognostic standardization of leaves of Calotropis procera (Ait.) R. Br. (Asclepiadaceae) 
Calotropis procera, belonging to the Asclepidaceae family, is present more or less throughout India and in other warm, dry places such as, Warizistan, Afghanistan, Egypt, and tropical Africa. Its common names are Akra, Akanal, and Madar. The leaves of Calotropis procera are said to be valuable as an antidote for snake bite, sinus fistula, rheumatism, mumps, burn injuries, and body pain. The leaves of Calotropis procera are also used to treat jaundice. A study on Calotropis procera leaf samples extracted the air-dried leaf powder with different solvents such as petroleum-ether (60-80°C), benzene, chloroform, ethanol, and sterile water. Preliminary phytochemical analysis was done long with measurement of the leaf constants, fluorescence characteristics, and extractive values. Quantitative estimation of total ash value, acid insoluble ash, and water- soluble ash may serve as useful indices for identification of the powdered drug. Histochemical studies which reveal rows of cylindrical palisade cells and, vascular bundles may also serve as useful indices for identification of the tissues. These studies suggested that the observed pharmacognostic and physiochemical parameters are of great value in quality control and formulation development of Calotropis procera.
doi:10.4103/0974-7788.59938
PMCID: PMC2876921  PMID: 20532092
Calotropis procera leaves; fluorescence analysis; macroscopy; microscopy; pharmacognostic standardization; phytochemical screening
5.  Resource-use efficiency explains grassy weed invasion in a low-resource savanna in north Australia 
Comparative studies of plant resource use and ecophysiological traits of invasive and native resident plant species can elucidate mechanisms of invasion success and ecosystem impacts. In the seasonal tropics of north Australia, the alien C4 perennial grass Andropogon gayanus (gamba grass) has transformed diverse, mixed tree-grass savanna ecosystems into dense monocultures. To better understand the mechanisms of invasion, we compared resource acquisition and usage efficiency using leaf-scale ecophysiological and stand-scale growth traits of A. gayanus with a co-habiting native C4 perennial grass Alloteropsis semialata. Under wet season conditions, A. gayanus had higher rates of stomatal conductance, assimilation, and water use, plus a longer daily assimilation period than the native species A. semialata. Growing season length was also ~2 months longer for the invader. Wet season measures of leaf scale water use efficiency (WUE) and light use efficiency (LUE) did not differ between the two species, although photosynthetic nitrogen use efficiency (PNUE) was significantly higher in A. gayanus. By May (dry season) the drought avoiding native species A. semialata had senesced. In contrast, rates of A. gayanus gas exchange was maintained into the dry season, albeit at lower rates that the wet season, but at higher WUE and PNUE, evidence of significant physiological plasticity. High PNUE and leaf 15N isotope values suggested that A. gayanus was also capable of preferential uptake of soil ammonium, with utilization occurring into the dry season. High PNUE and fire tolerance in an N-limited and highly flammable ecosystem confers a significant competitive advantage over native grass species and a broader niche width. As a result A. gayanus is rapidly spreading across north Australia with significant consequences for biodiversity and carbon and retention.
doi:10.3389/fpls.2015.00560
PMCID: PMC4523779  PMID: 26300890
alien invasive species; ecophysiology; water use; carbon uptake; weed invasion; trait-based comparisons; stable isotopes; carbon
6.  Eco-physiological adaptation of dominant tree species at two contrasting karst habitats in southwestern China 
F1000Research  2013;2:122.
The purpose of this study was to investigate the eco-physiological adaptation of indigenous woody species to their habitats in karst areas of southwestern China. Two contrasting forest habitats were studied: a degraded habitat in Daxiagu and a well-developed habitat in Tianlongshan, and the eco-physiological characteristics of the trees were measured for three growth seasons. Photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (Tr) of the tree species in Daxiagu were 2-3 times higher than those in Tianlongshan under ambient conditions. However, this habitat effect was not significant when measurements were taken under controlled conditions. Under controlled conditions, Pn, gs, and Tr of the deciduous species were markedly higher than those for the evergreen species. Habitat had no significant effect on water use efficiency (WUE) or photochemical characteristics of PSII. The stomatal sensitivity of woody species in the degraded habitat was much higher than that in the well-developed habitat. Similarly, the leaf total nitrogen (N) and phosphorus (P) contents expressed on the basis of either dry mass or leaf area were also much higher in Daxiagu than they were in Tianlongshan. The mass-based leaf total N content of deciduous species was much higher than that of evergreen species, while leaf area-based total N and P contents of evergreens were significantly higher than those of deciduous species. The photosynthetic nitrogen- and phosphorus-use efficiencies (PNUE and PPUE) of deciduous species were much higher than those of evergreens. Further, the PPUE of the woody species in Tianlongshan was much higher than that  of the woody species in Daxiagu.
The results from three growth seasons imply that the tree species were able to adapt well to their growth habitats. Furthermore, it seems that so-called “temporary drought stress” may not occur, or may not be severe for most woody plants in karst areas of southwestern China.
doi:10.12688/f1000research.2-122.v1
PMCID: PMC3892915  PMID: 24555059
7.  Eco-physiological adaptation of dominant tree species at two contrasting karst habitats in southwestern China 
F1000Research  2013;2:122.
The purpose of this study was to investigate the eco-physiological adaptation of indigenous woody species to their habitats in karst areas of southwestern China. Two contrasting forest habitats were studied: a degraded habitat in Daxiagu and a well-developed habitat in Tianlongshan, and the eco-physiological characteristics of the trees were measured for three growth seasons. Photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (Tr) of the tree species in Daxiagu were 2-3 times higher than those in Tianlongshan under ambient conditions. However, this habitat effect was not significant when measurements were taken under controlled conditions. Under controlled conditions, Pn, gs, and Tr of the deciduous species were markedly higher than those for the evergreen species. Habitat had no significant effect on water use efficiency (WUE) or photochemical characteristics of PSII. The stomatal sensitivity of woody species in the degraded habitat was much higher than that in the well-developed habitat. Similarly, the leaf total nitrogen (N) and phosphorus (P) contents expressed on the basis of either dry mass or leaf area were also much higher in Daxiagu than they were in Tianlongshan. The mass-based leaf total N content of deciduous species was much higher than that of evergreen species, while leaf area-based total N and P contents of evergreens were significantly higher than those of deciduous species. The photosynthetic nitrogen- and phosphorus-use efficiencies (PNUE and PPUE) of deciduous species were much higher than those of evergreens. Further, the PPUE of the woody species in Tianlongshan was much higher than that  of the woody species in Daxiagu.
The results from three growth seasons imply that the tree species were able to adapt well to their growth habitats. Furthermore, it seems that so-called “temporary drought stress” may not occur, or may not be severe for most woody plants in karst areas of southwestern China.
doi:10.12688/f1000research.2-122.v2
PMCID: PMC3892915  PMID: 24555059
karst habitat; photosynthesis; chlorophyll fluorescence; stomatal sensitivity; water potential
8.  Differential drought tolerance in tree populations from contrasting elevations 
AoB Plants  2014;6:plu069.
To investigate the differential drought tolerance between populations of Pinus tabuliformis from high-elevation (HP) and low-elevation (LP), seedlings of these two populations were subjected to a gradual depletion of soil water availability with a series of traits related to growth and water use efficiency being measured. From our results, we found that all the measured variables from the HP were affected less by drought compared to those of the LP, and most aspects of the HP were canalized against drought stress. We thus drew a conclusion that the two populations responded differentially to drought stress with the HP showing higher drought tolerance than the LP.
To predict the ecological consequences of climate change for a widely distributed tree species, it is essential to develop a deep understanding of the ecophysiological responses of populations from contrasting climates to varied soil water availabilities. In the present study, we focused on Pinus tabuliformis, one of the most economically and ecologically important tree species in China. In a greenhouse experiment, we exposed trees from high-elevation (HP) and low-elevation (LP) populations to low (80 % of field capacity, FC), mild (60 % FC), moderate (40 % FC) and severe (20 % FC) water stresses. Leaf gas exchange, biomass production and allocation, as well as water-use efficiency, were measured during the experiment. Increasing soil water stress clearly decreased the relative growth rate (RGR), total dry mass (TDM), light-saturated photosynthetic rate (Asat), stomatal conductance (gs), total water use (TWU) and whole-plant water-use efficiency (WUEWP). In contrast, intrinsic water-use efficiency (WUEi) and carbon isotope composition (δ13C) both increased significantly with increasing soil water stress for both populations. Only in the LP did the root/shoot ratio (R/S ratio) significantly increase when the water stress increased. A strong positive correlation between Asat and gs coupled with a reduced intercellular CO2 concentration (Ci) probably suggested that stomatal limitations were the main cause of the decreased Asat. However, all the measured variables from the HP were affected less by drought compared with those of the LP, and most aspects of the HP were canalized against drought stress, which was reflected by the relatively higher RGR, TDM and WUEWP. Overall, the results suggest that the two populations responded differentially to drought stress with the HP showing higher drought tolerance than the LP, which was reflected by its faster seedling growth rate and more efficient water use under drought conditions.
doi:10.1093/aobpla/plu069
PMCID: PMC4268489  PMID: 25387750
Carbon isotope composition; drought tolerance; growth; leaf gas exchange; Pinus tabuliformis; water-use efficiency.
9.  The Mediterranean evergreen Quercus ilex and the semi-deciduous Cistus albidus differ in their leaf gas exchange regulation and acclimation to repeated drought and re-watering cycles 
Journal of Experimental Botany  2011;62(14):5207-5216.
Plants may exhibit some degree of acclimation after experiencing drought, but physiological adjustments to consecutive cycles of drought and re-watering (recovery) have scarcely been studied. The Mediterranean evergreen holm oak (Q. ilex) and the semi-deciduous rockrose (C. albidus) showed some degree of acclimation after the first of three drought cycles (S1, S2, and S3). For instance, during S2 and S3 both species retained higher relative leaf water contents than during S1, despite reaching similar leaf water potentials. However, both species showed remarkable differences in their photosynthetic acclimation to repeated drought cycles. Both species decreased photosynthesis to a similar extent during the three cycles (20–40% of control values). However, after S1 and S2, photosynthesis recovered only to 80% of control values in holm oak, due to persistently low stomatal (gs) and mesophyll (gm) conductances to CO2. Moreover, leaf intrinsic water use efficiency (WUE) was kept almost constant in this species during the entire experiment. By contrast, photosynthesis of rockrose recovered almost completely after each drought cycle (90–100% of control values), while the WUE was largely and permanently increased (by 50–150%, depending on the day) after S1. This was due to a regulation which consisted in keeping gs low (recovering to 50–60% of control values after re-watering) while maintaining a high gm (even exceeding control values during re-watering). While the mechanisms to achieve such particular regulation of water and CO2 diffusion in leaves are unknown, it clearly represents a unique acclimation feature of this species after a drought cycle, which allows it a much better performance during successive drought events. Thus, differences in the photosynthetic acclimation to repeated drought cycles can have important consequences on the relative fitness of different Mediterranean species or growth forms within the frame of climate change scenarios.
doi:10.1093/jxb/err233
PMCID: PMC3193022  PMID: 21813795
Acclimation; drought–recovery cycles; mesophyll and stomatal conductance; osmotic adjustment; photosynthetic limitation analysis; water use efficiency
10.  Effects of Fully Open-Air [CO2] Elevation on Leaf Photosynthesis and Ultrastructure of Isatis indigotica Fort 
PLoS ONE  2013;8(9):e74600.
Traditional Chinese medicine relies heavily on herbs, yet there is no information on how these herb plants would respond to climate change. In order to gain insight into such response, we studied the effect of elevated [CO2] on Isatis indigotica Fort, one of the most popular Chinese herb plants. The changes in leaf photosynthesis, chlorophyll fluorescence, leaf ultrastructure and biomass yield in response to elevated [CO2] (550±19 µmol mol–1) were determined at the Free-Air Carbon dioxide Enrichment (FACE) experimental facility in North China. Photosynthetic ability of I. indigotica was improved under elevated [CO2]. Elevated [CO2] increased net photosynthetic rate (PN), water use efficiency (WUE) and maximum rate of electron transport (Jmax) of upper most fully-expended leaves, but not stomatal conductance (gs), transpiration ratio (Tr) and maximum velocity of carboxylation (Vc,max). Elevated [CO2] significantly increased leaf intrinsic efficiency of PSII (Fv’/Fm’) and quantum yield of PSII(ΦPSII), but decreased leaf non-photochemical quenching (NPQ), and did not affect leaf proportion of open PSII reaction centers (qP) and maximum quantum efficiency of PSII (Fv/Fm). The structural chloroplast membrane, grana layer and stroma thylakoid membranes were intact under elevated [CO2], though more starch grains were accumulated within the chloroplasts than that of under ambient [CO2]. While the yield of I. indigotica was higher due to the improved photosynthesis under elevated [CO2], the content of adenosine, one of the functional ingredients in indigowoad root was not affected.
doi:10.1371/journal.pone.0074600
PMCID: PMC3776829  PMID: 24058596
11.  Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato 
Journal of Experimental Botany  2014;66(3):863-878.
Highlight
Overexpression of a cell wall invertase gene promotes dehydration avoidance and WUE, and delays senescence in tomato through limiting stomatal conductance and inducing sink metabolism and photosynthesis in source leaves.
Drought stress conditions modify source–sink relations, thereby influencing plant growth, adaptive responses, and consequently crop yield. Invertases are key metabolic enzymes regulating sink activity through the hydrolytic cleavage of sucrose into hexose monomers, thus playing a crucial role in plant growth and development. However, the physiological role of invertases during adaptation to abiotic stress conditions is not yet fully understood. Here it is shown that plant adaptation to drought stress can be markedly improved in tomato (Solanum lycopersicum L.) by overexpression of the cell wall invertase (cwInv) gene CIN1 from Chenopodium rubrum. CIN1 overexpression limited stomatal conductance under normal watering regimes, leading to reduced water consumption during the drought period, while photosynthetic activity was maintained. This caused a strong increase in water use efficiency (up to 50%), markedly improving water stress adaptation through an efficient physiological strategy of dehydration avoidance. Drought stress strongly reduced cwInv activity and induced its proteinaceous inhibitor in the leaves of the wild-type plants. However, the CIN1-overexpressing plants registered 3- to 6-fold higher cwInv activity in all analysed conditions. Surprisingly, the enhanced invertase activity did not result in increased hexose concentrations due to the activation of the metabolic carbohydrate fluxes, as reflected by the maintenance of the activity of key enzymes of primary metabolism and increased levels of sugar-phosphate intermediates under water deprivation. The induced sink metabolism in the leaves explained the maintenance of photosynthetic activity, delayed senescence, and increased source activity under drought stress. Moreover, CIN1 plants also presented a better control of production of reactive oxygen species and sustained membrane protection. Those metabolic changes conferred by CIN1 overexpression were accompanied by increases in the concentrations of the senescence-delaying hormone trans-zeatin and decreases in the senescence-inducing ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in the leaves. Thus, cwInv critically functions at the integration point of metabolic, hormonal, and stress signals, providing a novel strategy to overcome drought-induced limitations to crop yield, without negatively affecting plant fitness under optimal growth conditions.
doi:10.1093/jxb/eru448
PMCID: PMC4321548  PMID: 25392479
Cell wall invertase; cytokinins; drought stress; ethylene; source–sink relationships; tomato.
12.  Differentiation of water-related traits in terrestrial and epiphytic Cymbidium species 
Epiphytes that grow in the canopies of tropical and subtropical forests experience different water regimes when compared with terrestrial plants. However, the differences in adaptive strategies between epiphytic and terrestrial plants with respect to plant water relations remain poorly understood. To understand how water-related traits contrast between epiphytic and terrestrial growth forms within the Cymbidium (Orchidaceae), we assessed leaf anatomy, hydraulics, and physiology of seven terrestrial and 13 epiphytic species using a common garden experiment. Compared with terrestrial species, epiphytic species had higher values for leaf mass per unit area (LMA), leaf thickness (LT), epidermal thickness, saturated water content (SWC) and the time required to dry saturated leaves to 70% relative water content (T70). However, vein density (Dvein), stomatal density (SD), and photosynthetic capacity (Amax) did not differ significantly between the two forms. T70 was positively correlated with LT, LMA, and SWC, and negatively correlated with stomatal index (SI). Amax showed positive correlations with SD and SI, but not with Dvein. Vein density was marginally correlated with SD, and significantly correlated with SI. Overall, epiphytic orchids exhibited substantial ecophysiological differentiations from terrestrial species, with the former type showing trait values indicative of greater drought tolerance and increased water storage capacity. The ability to retain water in the leaves plays a key role in maintaining a water balance in those epiphytes. Therefore, the process of transpiration depends less upon the current substrate water supply and enables epiphytic Cymbidium species to adapt more easily to canopy habitats.
doi:10.3389/fpls.2015.00260
PMCID: PMC4406080  PMID: 25954289
Cymbidium; drought tolerance; epiphytes; photosynthesis; succulence; water loss; water storage; water supply
13.  Effects of Arbuscular-Mycorrhizal Glomus Species on Drought Tolerance: Physiological and Nutritional Plant Responses 
The tolerance of lettuce plants (Lactuca sativa L. cv. Romana) to drought stress differed with the arbuscular-mycorrhizal fungal isolate with which the plants were associated. Seven fungal species belonging to the genus Glomus were studied for their ability to enhance the drought tolerance of lettuce plants. These fungi had different traits that affected the drought resistance of host plants. The ranking of arbuscular-mycorrhizal fungal effects on drought tolerance, based on the relative decreases in shoot dry weight, was as follows: Glomus deserticola > Glomus fasciculatum > Glomus mosseae > Glomus etunicatum > Glomus intraradices > Glomus caledonium > Glomus occultum. In this comparative study specific mycorrhizal fungi had consistent effects on plant growth, mineral uptake, the CO(inf2) exchange rate, water use efficiency, transpiration, stomatal conductance, photosynthetic phosphorus use efficiency, and proline accumulation under either well-watered or drought-stressed conditions. The ability of the isolates to maintain plant growth effectively under water stress conditions was related to higher transpiration rates, levels of leaf conductance, and proline, N, and P contents. Differences in proline accumulation in leaves among the fungal symbioses suggested that the fungi were able to induce different degrees of osmotic adjustment. The detrimental effects of drought were not related to decreases in photosynthesis or water use efficiency. Neither of these parameters was related to P nutrition. The differences in P and K acquisition, transpiration, and stomatal conductance were related to the mycorrhizal efficiencies of the different fungi. Our observations revealed the propensities of different Glomus species to assert their protective effects during plant water stress. The greater effectiveness of G. deserticola in improving water deficit tolerance was associated with the lowest level of growth reduction (9%) under stress conditions. The growth of plants colonized by G. occultum was reduced by 70% after a progressive drought stress period. In general, the different protective effects of the mycorrhizal isolates were not associated with colonizing ability. Nevertheless, G. deserticola was the most efficient fungus and exhibited the highest levels of mycorrhizal colonization, as well as the greatest stimulation of physiological parameters.
PMCID: PMC1388347  PMID: 16534929
14.  Operation of the Xanthophyll Cycle and Degradation of D1 Protein in the Inducible CAM plant, Talinum triangulare, under Water Deficit 
Annals of Botany  2003;92(3):393-399.
Changes in photochemical activity induced by water deficit were investigated in Talinum triangulare, an inducible CAM plant. The aim was to analyse the interactions between C3 photosynthesis, induction and activity of CAM, photosynthetic energy regulation and the mechanisms responsible for photoprotection and photoinhibition under water stress. Gas exchange, chlorophyll a fluorescence, titratable acidity, carotenoid composition and relative contents of the PSII reaction centre protein (D1) were measured. A decrease in xylem tension (ψ) from –0·14 to –0·2 MPa substantially decreased daytime net CO2 assimilation and daily carbon gain, and induced CAM, as shown by CO2 assimilation during the night and changes in titratable acidity; a further decrease in ψ decreased nocturnal acid accumulation by 60 %. Non-photochemical quenching of chlorophyll a fluorescence (NPQ) increased with water deficit, but decreased with a more severe drought (ψ below –0·2 MPa), when CAM activity was low. NPQ was lower at 0900 h (during maximum decarboxylation rates) than at 1400 h, when malate pools were depleted. Down-regulation of PSII activity related to the rise in NPQ was indicated by a smaller quantum yield of PSII photochemistry (ΦPSII) in droughted compared with watered plants. However, ΦPSII was larger at 0900 h than at 1400 h. The de-epoxidation state of the xanthophyll cycle increased with drought and was linearly related to NPQ. Intrinsic quantum yield of PSII (FV/FM) measured at dusk was also lower in severely stressed plants than in controls. Under maximum photosynthetic photon flux and high decarboxylation rates of organic acids, the D1 content in leaves of droughted plants showing maximal CAM activity was identical to the controls; increased drought decreased D1 content by more than 30 %. Predawn samples had D1 contents similar to leaves sampled at peak irradiance, with no signs of recovery after 12 h of darkness. It is concluded that under mild water stress, early induction of CAM, together with an increased energy dissipation by the xanthophyll cycle, prevents net degradation of D1 protein; when water deficit is more severe, CAM and xanthophyll cycle capacities for energy dissipation decline, and net degradation of D1 proceeds.
doi:10.1093/aob/mcg153
PMCID: PMC4257515  PMID: 12881404
CAM; D1 protein; photoinhibition; Talinum triangulare; water deficit; xanthophylls.
15.  Resource use and efficiency, and stomatal responses to environmental drivers of oak and pine species in an Atlantic Coastal Plain forest 
Pine-oak ecosystems are globally distributed even though differences in anatomy and leaf habit between many co-occurring oaks and pines suggest different strategies for resource use, efficiency and stomatal behavior. The New Jersey Pinelands contain sandy soils with low water- and nutrient-holding capacity providing an opportunity to examine trade-offs in resource uptake and efficiency. Therefore, we compared resource use in terms of transpiration rates and leaf nitrogen content and resource-use efficiency including water-use efficiency (WUE) via gas exchange and leaf carbon isotopes and photosynthetic nitrogen-use efficiency (PNUE) between oaks (Quercus alba, Q. prinus, Q. velutina) and pines (Pinus rigida, P. echinata). We also determined environmental drivers [vapor pressure deficit (VPD), soil moisture, solar radiation] of canopy stomatal conductance (GS) estimated via sap flow and stomatal sensitivity to light and soil moisture. Net assimilation rates were similar between genera, but oak leaves used about 10% more water and pine foliage contained about 20% more N per unit leaf area. Therefore, oaks exhibited greater PNUE while pines had higher WUE based on gas exchange, although WUE from carbon isotopes was not significantly different. For the environmental drivers of GS, oaks had about 10% lower stomatal sensitivity to VPD normalized by reference stomatal conductance compared with pines. Pines exhibited a significant positive relationship between shallow soil moisture and GS, but only GS in Q. velutina was positively related to soil moisture. In contrast, stomatal sensitivity to VPD was significantly related to solar radiation in all oak species but only pines at one site. Therefore, oaks rely more heavily on groundwater resources but have lower WUE, while pines have larger leaf areas and nitrogen acquisition but lower PNUE demonstrating a trade-off between using water and nitrogen efficiently in a resource-limited ecosystem.
doi:10.3389/fpls.2015.00297
PMCID: PMC4423344  PMID: 25999966
photosynthesis; canopy conductance; sap flow; nitrogen-use efficiency; water-use efficiency
16.  Identification and characterization of plasma membrane aquaporins isolated from fiber cells of Calotropis procera  
Calotropis procera, commonly known as “milkweed”, possesses long seed trichomes for seed dispersal and has the ability to survive under harsh conditions such as drought and salinity. Aquaporins are water channel proteins expressed in all land plants, divided into five subfamilies plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), NOD26-like proteins (NIPs), small basic intrinsic proteins (SIPs), and the unfamiliar X intrinsic proteins (XIPs). PIPs constitute the largest group of water channel proteins that are involved in different developmental and regulatory mechanisms including water permeability, cell elongation, and stomata opening. Aquaporins are also involved in abiotic stress tolerance and cell expansion mechanisms, but their role in seed trichomes (fiber cells) has never been investigated. A large number of clones isolated from C. procera fiber cDNA library showed sequence homology to PIPs. Both expressed sequence tags (ESTs) and real-time polymerase chain reaction (PCR) studies revealed that the transcript abundance of this gene family in fiber cells of C. procera is greater than that of cotton. Full-length cDNAs of CpPIP1 and CpPIP2 were isolated from C. procera fiber cDNA library and used for constructing plant expression vectors under constitutive (2×35S) and trichome-specific (GhLTP3) promoters. Transgenic tobacco plants were developed via Agrobacterium-mediated transformation. The phenotypic characteristics of the plants were observed after confirming the integration of transgene in plants. It was observed that CpPIP2 expression cassette under 2×35S and GhLTP3 promoter enhanced the numbers of stem and leave trichomes. However, 2×35S::CpPIP2 has a more amplified effect on trichome density and length than GhLTP3::CpPIP2 and other PIP constructs. These findings imply the role of C. procera PIP aquaporins in fiber cell elongation. The PIPs-derived cell expansion mechanism may be exploited through transgenic approaches for improvement of fiber staple length in cotton and boosting of defense against sucking insects by enhancing plant pubescence.
doi:10.1631/jzus.B1200233
PMCID: PMC3709063  PMID: 23825144
Seed trichome; Plasma membrane intrinsic protein (PIP); Fiber quality; Cell elongation; Tobacco; Agrobacterium
17.  Regulation of the calcium-sensing receptor in both stomatal movement and photosynthetic electron transport is crucial for water use efficiency and drought tolerance in Arabidopsis  
Journal of Experimental Botany  2013;65(1):223-234.
Plant calcium sensing receptor (CAS) optimizes photosynthesis by its effect on the formation of photosynthetic electron transport. CAS also regulates transpiration under water stress. A novel correlation between CAS and plant water use efficiency is revealed
Production per amount of water used (water use efficiency, WUE) is closely correlated with drought tolerance. Although stomatal aperture can regulate WUE, the underlying molecular mechanisms are still unclear. Previous reports revealed that stomatal closure was inhibited in the calcium-sensing receptor (CAS) antisense line of Arabidopsis (CASas). Here it is shown that decreased drought tolerance and WUE of CASas was associated with higher stomatal conductance due to improper regulation of stomatal aperture, rather than any change of stomatal density. CASas plants also had a lower CO2 assimilation rate that was attributed to a lower photosynthetic electron transport rate, leading to higher chlorophyll fluorescence. Gene co-expression combined with analyses of chlorophyll content and transcription levels of photosynthesis-related genes indicate that CAS is involved in the formation of the photosynthetic electron transport system. These data suggest that CAS regulates transpiration and optimizes photosynthesis by playing important roles in stomatal movement and formation of photosynthetic electron transport, thereby regulating WUE and drought tolerance.
doi:10.1093/jxb/ert362
PMCID: PMC3883291  PMID: 24187420
Arabidopsis; calcium-sensing receptor; drought tolerance; stomatal movements; water use efficiency.
18.  Assessment of drought tolerance of 49 switchgrass (Panicum virgatum) genotypes using physiological and morphological parameters 
Background
Switchgrass (Panicum virgatum L.) is a warm-season C4 grass that is a target lignocellulosic biofuel species. In many regions, drought stress is one of the major limiting factors for switchgrass growth. The objective of this study was to evaluate the drought tolerance of 49 switchgrass genotypes. The relative drought stress tolerance was determined based on a set of parameters including plant height, leaf length, leaf width, leaf sheath length, leaf relative water content (RWC), electrolyte leakage (EL), photosynthetic rate (Pn), stomatal conductance (gs), transpiration rate (Tr), intercellular CO2 concentration (Ci), and water use efficiency (WUE).
Results
SRAP marker analysis determined that the selected 49 switchgrass genotypes represent a diverse genetic pool of switchgrass germplasm. Principal component analysis (PCA) and drought stress indexes (DSI) of each physiological parameter showed significant differences in the drought stress tolerance among the 49 genotypes. Heatmap and PCA data revealed that physiological parameters are more sensitive than morphological parameters in distinguishing the control and drought treatments. Metabolite profiling data found that under drought stress, the five best drought-tolerant genotypes tended to have higher levels of abscisic acid (ABA), spermine, trehalose, and fructose in comparison to the five most drought-sensitive genotypes.
Conclusion
Based on PCA ranking value, the genotypes TEM-SEC, TEM-LoDorm, BN-13645-64, Alamo, BN-10860-61, BN-12323-69, TEM-SLC, T-2086, T-2100, T-2101, Caddo, and Blackwell-1 had relatively higher ranking values, indicating that they are more tolerant to drought. In contrast, the genotypes Grif Nebraska 28, Grenville-2, Central Iowa Germplasm, Cave-in-Rock, Dacotah, and Nebraska 28 were found to be relatively sensitive to drought stress. By analyzing physiological response parameters and different metabolic profiles, the methods utilized in this study identified drought-tolerant and drought-sensitive switchgrass genotypes. These results provide a foundation for future research directed at understanding the molecular mechanisms underlying switchgrass tolerance to drought.
Electronic supplementary material
The online version of this article (doi:10.1186/s13068-015-0342-8) contains supplementary material, which is available to authorized users.
doi:10.1186/s13068-015-0342-8
PMCID: PMC4578271  PMID: 26396590
Panicum virgatum; Germplasm; Drought tolerance; SRAP marker; Genetic diversity; PCA; Metabolites
19.  Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis  
Journal of Experimental Botany  2013;64(14):4589-4601.
Water deficit is a serious environmental factor limiting the growth and productivity of plants worldwide. Improvement of drought tolerance and efficient water use are significant strategies to overcome this dilemma. In this study, a drought-responsive transcription factor, NUCLEAR FACTOR Y subunit B 7 (PdNF-YB7), induced by osmotic stress (PEG6000) and abscisic acid, was isolated from fast-growing poplar clone NE-19 [Populus nigra × (Populus deltoides × Populus nigra)]. Ectopic overexpression of PdNF-YB7 (oxPdB7) in Arabidopsis enhanced drought tolerance and whole-plant and instantaneous leaf water-use efficiency (WUE, the ratio of biomass produced to water consumed). Overexpressing lines had an increase in germination rate and root length and decrease in water loss and displayed higher photosynthetic rate, instantaneous leaf WUE, and leaf water potential to exhibit enhanced drought tolerance under water scarcity. Additionally, overexpression of PdNF-YB7 in Arabidopsis improved whole-plant WUE by increasing carbon assimilation and reducing transpiration with water abundance. These drought-tolerant, higher WUE transgenic Arabidopsis had earlier seedling establishment and higher biomass than controls under normal and drought conditions. In contrast, Arabidopsis mutant nf-yb3 was more sensitive to drought stress with lower WUE. However, complementation analysis indicated that complementary lines (nf-yb3/PdB7) had almost the same drought response and WUE as wild-type Col-0. Taken together, these results suggest that PdNF-YB7 positively confers drought tolerance and improves WUE in Arabidopsis; thus it could potentially be used in breeding drought-tolerant plants with increased production even under water deficiency.
doi:10.1093/jxb/ert262
PMCID: PMC3808328  PMID: 24006421
Arabidopsis; drought tolerance; NF-YB; poplar; transcription factor; water-use efficiency.
20.  Differences in drought sensitivities and photosynthetic limitations between co-occurring C3 and C4 (NADP-ME) Panicoid grasses 
Annals of Botany  2010;105(3):493-503.
Background and Aims
The success of C4 plants lies in their ability to attain greater efficiencies of light, water and nitrogen use under high temperature, providing an advantage in arid, hot environments. However, C4 grasses are not necessarily less sensitive to drought than C3 grasses and are proposed to respond with greater metabolic limitations, while the C3 response is predominantly stomatal. The aims of this study were to compare the drought and recovery responses of co-occurring C3 and C4 NADP-ME grasses from the subfamily Panicoideae and to determine stomatal and metabolic contributions to the observed response.
Methods
Six species of locally co-occurring grasses, C3 species Alloteropsis semialata subsp. eckloniana, Panicum aequinerve and Panicum ecklonii, and C4 (NADP-ME) species Heteropogon contortus, Themeda triandra and Tristachya leucothrix, were established in pots then subjected to a controlled drought followed by re-watering. Water potentials, leaf gas exchange and the response of photosynthetic rate to internal CO2 concentrations were determined on selected occasions during the drought and re-watering treatments and compared between species and photosynthetic types.
Key Results
Leaves of C4 species of grasses maintained their photosynthetic advantage until water deficits became severe, but lost their water-use advantage even under conditions of mild drought. Declining C4 photosynthesis with water deficit was mainly a consequence of metabolic limitations to CO2 assimilation, whereas, in the C3 species, stomatal limitations had a prevailing role in the drought-induced decrease in photosynthesis. The drought-sensitive metabolism of the C4 plants could explain the observed slower recovery of photosynthesis on re-watering, in comparison with C3 plants which recovered a greater proportion of photosynthesis through increased stomatal conductance.
Conclusions
Within the Panicoid grasses, C4 (NADP-ME) species are metabolically more sensitive to drought than C3 species and recover more slowly from drought.
doi:10.1093/aob/mcp307
PMCID: PMC2826257  PMID: 20106844
C3 and C4 Panicoid grasses; NADP-ME subtype; drought response; stomatal and metabolic limitations; drought recovery
21.  Seasonal differences in leaf-level physiology give lianas a competitive advantage over trees in a tropical seasonal forest 
Oecologia  2009;161(1):25-33.
Lianas are an important component of most tropical forests, where they vary in abundance from high in seasonal forests to low in aseasonal forests. We tested the hypothesis that the physiological ability of lianas to fix carbon (and thus grow) during seasonal drought may confer a distinct advantage in seasonal tropical forests, which may explain pan-tropical liana distributions. We compared a range of leaf-level physiological attributes of 18 co-occurring liana and 16 tree species during the wet and dry seasons in a tropical seasonal forest in Xishuangbanna, China. We found that, during the wet season, lianas had significantly higher CO2 assimilation per unit mass (Amass), nitrogen concentration (Nmass), and δ13C values, and lower leaf mass per unit area (LMA) than trees, indicating that lianas have higher assimilation rates per unit leaf mass and higher integrated water-use efficiency (WUE), but lower leaf structural investments. Seasonal variation in CO2 assimilation per unit area (Aarea), phosphorus concentration per unit mass (Pmass), and photosynthetic N-use efficiency (PNUE), however, was significantly lower in lianas than in trees. For instance, mean tree Aarea decreased by 30.1% from wet to dry season, compared with only 12.8% for lianas. In contrast, from the wet to dry season mean liana δ13C increased four times more than tree δ13C, with no reduction in PNUE, whereas trees had a significant reduction in PNUE. Lianas had higher Amass than trees throughout the year, regardless of season. Collectively, our findings indicate that lianas fix more carbon and use water and nitrogen more efficiently than trees, particularly during seasonal drought, which may confer a competitive advantage to lianas during the dry season, and thus may explain their high relative abundance in seasonal tropical forests.
doi:10.1007/s00442-009-1355-4
PMCID: PMC2700874  PMID: 19418072
Liana distribution; Nitrogen-use efficiency; Tropical forest physiology; Water-use efficiency
22.  Photosynthetic Carbon Reduction and Carbon Oxidation Cycles are the Main Electron Sinks for Photosystem II Activity During a Mild Drought 
Annals of Botany  2002;89(7):887-894.
Stomatal closure can explain the inhibition of net CO2 uptake by a leaf subjected to a mild drought: the photosynthetic apparatus appears resistant to lack of water. Changes in both the water content of leaves maintained in a constant environment and the ambient CO2 molar fraction during measurements on well‐hydrated leaves lead to similar effects on net CO2 uptake and whole chain electron transport as estimated by leaf chlorophyll fluorescence measurements. In particular, it is shown that photosystem II (PSII) functioning and its regulation are not qualitatively changed during desiccation and that the variations in PSII photochemistry can simply be understood by changes in substrate availability in this condition. Moreover, an analysis of the literature shows that when inhibition of net CO2 uptake by C3 leaves under drought (Phaseolus vulgaris L., Helianthus annus L. and Solanum tuberosum L.) was lower than 80 %, elevated CO2 completely restored the photosynthetic capacity. The CO2 molar fraction in the chloroplasts declines as stomata close in drying leaves. As a consequence, in C3 plants, ribulose‐1,5‐bisphosphate oxygenation increases and becomes the main sink for photosynthetic electrons. Depending on the prevailing photon flux density, the O2 uptake through photorespiratory activity can entirely replace carbon dioxide as an electron acceptor, or not. The rate of the Mehler reaction remains low and unchanged during desiccation. However, drought could also involve CO2‐sensitive modification of the photosynthetic metabolism depending on plant growth conditions and possibly also on plant species.
doi:10.1093/aob/mcf064
PMCID: PMC4233800  PMID: 12102514
Chloroplastic carbon dioxide molar ratio; drought stress; high CO2 effect; Lavatera trimestris L. var. splendens; Pisum sativum L.; photorespiration; photosynthesis; stomatal effect
23.  Non-Stomatal Limitation to Photosynthesis in Cinnamomum camphora Seedings Exposed to Elevated O3 
PLoS ONE  2014;9(6):e98572.
Ozone (O3) is the most phytotoxic air pollutant for global forests, with decreased photosynthesis widely regarded as one of its most common effects. However, controversy exists concerning the mechanism that underlies the depressing effects of O3 on CO2 assimilation. In the present study, seedlings of Cinnamomum camphora, a subtropical evergreen tree species that has rarely been studied, were exposed to ambient air (AA), ambient air plus 60 [ppb] O3 (AA+60), or ambient air plus 120 [ppb] O3 (AA+120) in open-top chambers (OTCs) for 2 years. Photosynthetic CO2 exchange and chlorophyll a fluorescence were investigated in the second growing season (2010). We aim to determine whether stomatal or non-stomatal limitation is responsible for the photosynthesis reduction and to explore the potential implications for forest ecosystem functions. Results indicate that elevated O3 (E-O3) reduced the net photosynthetic rates (PN) by 6.0-32.2%, with significant differences between AA+60 and AA+120 and across the four measurement campaigns (MCs). The actual photochemical efficiency of photosystem II (PSII) in saturated light (Fv′/Fm′) was also significantly decreased by E-O3, as was the effective quantum yield of PSII photochemistry (ΦPSII). Moreover, E-O3 significantly and negatively impacted the maximum rates of carboxylation (Vcmax) and electron transport (Jmax). Although neither the stomatal conductance (gs) nor the intercellular CO2 concentration (Ci) was decreased by E-O3, PN/gs was significantly reduced. Therefore, the observed reduction in PN in the present study should not be attributed to the unavailability of CO2 due to stomatal limitation, but rather to the O3-induced damage to Ribulose-1,5-bisphosphate carboxylase/oxygenase and the photochemical apparatus. This suggests that the down-regulation of stomatal conductance could fail to occur, and the biochemical processes in protoplasts would become more susceptible to injuries under long-term O3 exposure, which may have important consequences for forest carbon and water budget.
doi:10.1371/journal.pone.0098572
PMCID: PMC4043779  PMID: 24892748
24.  Multiple adaptive responses of Australian native perennial legumes with pasture potential to grow in phosphorus- and moisture-limited environments 
Annals of Botany  2010;105(5):755-767.
Background and Aims
Many Australian legumes have evolved in low-phosphorus (P) soils and low-rainfall areas. Therefore a study was made of the interaction of soil [P] and water availability on growth, photosynthesis, water-use efficiency (WUE) and P nutrition of two Australian native legumes with pasture potential, Cullen australasicum and C. pallidum, and the widely grown exotic pasture legume, lucerne (Medicago sativa).
Methods
Plants were grown in a glasshouse at 3, 10 and 30 mg P kg−1 dry soil for 5 months. At week 10, two drought treatments were imposed, total pot dried (all-dry) and only top soil dried (top-dry), while control pots were maintained at field capacity.
Key Results
Shoot dry weight produced by lucerne was never higher than that of C. australasicum. For C. pallidum only, shoot dry weight was reduced at 30 mg P kg−1 dry soil. The small root system of the Cullen species was quite plastic, allowing plants to access P and moisture efficiently. Lucerne always had a higher proportion of its large root system in the top soil layer compared with Cullen species. All species showed decreased photosynthesis, leaf water potential and stomatal conductance when exposed to drought, but the reductions were less for Cullen species, due to tighter stomatal control, and consequently they achieved a higher WUE. All species showed highest rhizosphere carboxylate concentrations in the all-dry treatment. For lucerne only, carboxylates decreased as P supply increased. Citrate was the main carboxylate in the control and top-dry treatments, and malate in the all-dry treatment.
Conclusions
Multiple adaptive responses of Cullen species and lucerne favoured exploitation of low-P soils under drought. The performance of undomesticated Cullen species, relative to that of lucerne, shows their promise as pasture species for environments such as in south-western Australia where water and P are limiting, especially in view of a predicted drying and warming climate.
doi:10.1093/aob/mcq040
PMCID: PMC2859915  PMID: 20421234
Australian native legumes; carboxylates; climate change; Cullen spp.; drought; Medicago sativa; novel crops; perennial pastures; phosphorus; photosynthesis; root distribution; water-use efficiency
25.  Physiological advantages of C4 grasses in the field: a comparative experiment demonstrating the importance of drought 
Global Change Biology  2014;20(6):1992-2003.
Global climate change is expected to shift regional rainfall patterns, influencing species distributions where they depend on water availability. Comparative studies have demonstrated that C4 grasses inhabit drier habitats than C3 relatives, but that both C3 and C4 photosynthesis are susceptible to drought. However, C4 plants may show advantages in hydraulic performance in dry environments. We investigated the effects of seasonal variation in water availability on leaf physiology, using a common garden experiment in the Eastern Cape of South Africa to compare 12 locally occurring grass species from C4 and C3 sister lineages. Photosynthesis was always higher in the C4 than C3 grasses across every month, but the difference was not statistically significant during the wettest months. Surprisingly, stomatal conductance was typically lower in the C3 than C4 grasses, with the peak monthly average for C3 species being similar to that of C4 leaves. In water-limited, rain-fed plots, the photosynthesis of C4 leaves was between 2.0 and 7.4 μmol m−2 s−1 higher, stomatal conductance almost double, and transpiration 60% higher than for C3 plants. Although C4 average instantaneous water-use efficiencies were higher (2.4–8.1 mmol mol−1) than C3 averages (0.7–6.8 mmol mol−1), differences were not as great as we expected and were statistically significant only as drought became established. Photosynthesis declined earlier during drought among C3 than C4 species, coincident with decreases in stomatal conductance and transpiration. Eventual decreases in photosynthesis among C4 plants were linked with declining midday leaf water potentials. However, during the same phase of drought, C3 species showed significant decreases in hydrodynamic gradients that suggested hydraulic failure. Thus, our results indicate that stomatal and hydraulic behaviour during drought enhances the differences in photosynthesis between C4 and C3 species. We suggest that these drought responses are important for understanding the advantages of C4 photosynthesis under field conditions.
doi:10.1111/gcb.12498
PMCID: PMC4237462  PMID: 24677339
C3 photosynthesis; C4 photosynthesis; drought; gas exchange; PACMAD; Poaceae; stomatal conductance; water potential

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