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1.  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.
PMCID: PMC3919747  PMID: 24520340
2.  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.
PMCID: PMC2876921  PMID: 20532092
Calotropis procera leaves; fluorescence analysis; macroscopy; microscopy; pharmacognostic standardization; phytochemical screening
3.  Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass 
Journal of Experimental Botany  2008;59(12):3317-3325.
Responses of plant leaf stomatal conductance and photosynthesis to water deficit have been extensively reported; however, little is known concerning the relationships of stomatal density with regard to water status and gas exchange. The responses of stomatal density to leaf water status were determined, and correlation with specific leaf area (SLA) in a photosynthetic study of a perennial grass, Leymus chinensis, subjected to different soil moisture contents. Moderate water deficits had positive effects on stomatal number, but more severe deficits led to a reduction, described in a quadratic parabolic curve. The stomatal size obviously decreased with water deficit, and stomatal density was positively correlated with stomatal conductance (gs), net CO2 assimilation rate (An), and water use efficiency (WUE). A significantly negative correlation of SLA with stomatal density was also observed, suggesting that the balance between leaf area and its matter may be associated with the guard cell number. The present results indicate that high flexibilities in stomatal density and guard cell size will change in response to water status, and this process may be closely associated with photosynthesis and water use efficiency.
PMCID: PMC2529243  PMID: 18648104
Gas exchange; guard cell size; photosynthesis; stomatal density; water stress; water use efficiency (WUE)
4.  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.
PMCID: PMC3709063  PMID: 23825144
Seed trichome; Plasma membrane intrinsic protein (PIP); Fiber quality; Cell elongation; Tobacco; Agrobacterium
5.  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.
PMCID: PMC3883291  PMID: 24187420
Arabidopsis; calcium-sensing receptor; drought tolerance; stomatal movements; water use efficiency.
6.  To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms 
A comparative study has been made of the photosynthetic physiological ecology and carbon isotope discrimination characteristics for modern-day bryophytes and closely related algal groups. Firstly, the extent of bryophyte distribution and diversification as compared with more advanced land plant groups is considered. Secondly, measurements of instantaneous carbon isotope discrimination (Δ), photosynthetic CO2 assimilation and electron transport rates were compared during the drying cycles. The extent of surface diffusion limitation (when wetted), internal conductance and water use efficiency (WUE) at optimal tissue water content (TWC) were derived for liverworts and a hornwort from contrasting habitats and with differing degrees of thallus ventilation (as intra-thalline cavities and internal airspaces). We also explore how the operation of a biophysical carbon-concentrating mechanism (CCM) tempers isotope discrimination characteristics in two other hornworts, as well as the green algae Coleochaete orbicularis and Chlamydomonas reinhardtii. The magnitude of Δ was compared for each life form over a drying curve and used to derive the surface liquid-phase conductance (when wetted) and internal conductance (at optimal TWC). The magnitude of external and internal conductances, and WUE, was higher for ventilated, compared with non-ventilated, liverworts and hornworts, but the values were similar within each group, suggesting that both factors have been optimized for each life form. For the hornworts, leakiness of the CCM was highest for Megaceros vincentianus and C. orbicularis (approx. 30%) and, at 5%, lowest in C. reinhardtii grown under ambient CO2 concentrations. Finally, evidence for the operation of a CCM in algae and hornworts is considered in terms of the probable role of the chloroplast pyrenoid, as the origins, structure and function of this enigmatic organelle are explored during the evolution of land plants.
PMCID: PMC2606768  PMID: 18487135
bryophytes; carbon-concentrating mechanisms; carbon isotopes; mesophyll conductance; pyrenoid
7.  Differential Growth Responses to Water Balance of Coexisting Deciduous Tree Species Are Linked to Wood Density in a Bolivian Tropical Dry Forest 
PLoS ONE  2013;8(10):e73855.
A seasonal period of water deficit characterizes tropical dry forests (TDFs). There, sympatric tree species exhibit a diversity of growth rates, functional traits, and responses to drought, suggesting that each species may possess different strategies to grow under different conditions of water availability. The evaluation of the long-term growth responses to changes in the soil water balance should provide an understanding of how and when coexisting tree species respond to water deficit in TDFs. Furthermore, such differential growth responses may be linked to functional traits related to water storage and conductance. We used dendrochronology and climate data to retrospectively assess how the radial growth of seven coexisting deciduous tree species responded to the seasonal soil water balance in a Bolivian TDF. Linear mixed-effects models were used to quantify the relationships between basal area increment and seasonal water balance. We related these relationships with wood density and sapwood production to assess if they affect the growth responses to climate. The growth of all species responded positively to water balance during the wet season, but such responses differed among species as a function of their wood density. For instance, species with a strong growth response to water availability averaged a low wood density which may facilitate the storage of water in the stem. By contrast, species with very dense wood were those whose growth was less sensitive to water availability. Coexisting tree species thus show differential growth responses to changes in soil water balance during the wet season. Our findings also provide a link between wood density, a trait related to the ability of trees to store water in the stem, and wood formation in response to water availability.
PMCID: PMC3792103  PMID: 24116001
8.  Water stress drastically reduces root growth and inulin yield in Cichorium intybus (var. sativum) independently of photosynthesis 
Journal of Experimental Botany  2012;63(12):4359-4373.
Root chicory (Cichorium intybus var. sativum) is a cash crop cultivated for inulin production in Western Europe. This plant can be exposed to severe water stress during the last 3 months of its 6-month growing period. The aim of this study was to quantify the effect of a progressive decline in water availability on plant growth, photosynthesis, and sugar metabolism and to determine its impact on inulin production. Water stress drastically decreased fresh and dry root weight, leaf number, total leaf area, and stomatal conductance. Stressed plants, however, increased their water-use efficiency and leaf soluble sugar concentration, decreased the shoot-to-root ratio and lowered their osmotic potential. Despite a decrease in photosynthetic pigments, the photosynthesis light phase remained unaffected under water stress. Water stress increased sucrose phosphate synthase activity in the leaves but not in the roots. Water stress inhibited sucrose:sucrose 1-fructosyltransferase and fructan:fructan 1 fructosyltransferase after 19 weeks of culture and slightly increased fructan 1-exohydrolase activity. The root inulin concentration, expressed on a dry-weight basis, and the mean degree of polymerization of the inulin chain remained unaffected by water stress. Root chicory displayed resistance to water stress, but that resistance was obtained at the expense of growth, which in turn led to a significant decrease in inulin production.
PMCID: PMC3421980  PMID: 22577185
Cichorium intybus; drought; growth; inulin; photosynthesis; root chicory; sugar metabolism; water deficit; water stress
9.  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.
PMCID: PMC2700874  PMID: 19418072
Liana distribution; Nitrogen-use efficiency; Tropical forest physiology; Water-use efficiency
10.  Seedling Stage Strategies as a Means of Habitat Specialization in Herbaceous Plants 
PLoS ONE  2011;6(7):e23006.
The regeneration niche has been little investigated in studies of community assembly and plant distribution. We examined adaptive associations between seedling traits and habitat specialization. Two habitat contrasts were investigated across several evolutionary lineages of angiosperms: species specialized to forest vs. open habitats and to dry vs. wet habitats. We also tested whether effects of shade and drought vary independently or, alternatively, if shade may amplify effects on drought-stressed plants. Seedling response in terms of growth rate, height, slenderness, specific leaf area (SLA) and degree of elongation (longest internode; petiole or leaf-sheath depending on species' morphology) to light and watering treatments was assessed. We used a factorial design involving three light regimes and two watering frequencies. The open-shaded habitat contrast and the dry-wet habitat contrast were investigated using six and five pairs of congeneric species, respectively. The congeneric species pair design controlled for confounding effects of evolutionary history prior to divergence in habitat specialization. Seedling growth rate generally decreased with shade and reduced watering frequency. Plant height was generally largest at intermediate light. Specialization to shaded habitats was associated with a more conservative growth strategy, i.e. showing a more modest growth response to increasing light. Species from all habitats showed the highest relative elongation at intermediate light, except for the moist-habitat species, for which elongation increased with shade. Contrary to our expectations, species from dry habitats grew bigger than species from moist habitats in all treatments. SLA responded to the light treatment, but not to watering regime. The contrasting light and moisture conditions across habitats appear to not have selected for differences in SLA. We conclude that seedling phase strategies of resource allocation in temperate herbs contribute to their habitat specialization. Habitat-specific seedling strategies and trade-offs in response to resource availability and environmental conditions may be important to adaptive specialization.
PMCID: PMC3146528  PMID: 21829576
11.  Leaf Photosynthetic Rate of Tropical Ferns Is Evolutionarily Linked to Water Transport Capacity 
PLoS ONE  2014;9(1):e84682.
Ferns usually have relatively lower photosynthetic potential than angiosperms. However, it is unclear whether low photosynthetic potential of ferns is linked to leaf water supply. We hypothesized that there is an evolutionary association of leaf water transport capacity with photosynthesis and stomatal density in ferns. In the present study, a series of functional traits relating to leaf anatomy, hydraulics and physiology were assessed in 19 terrestrial and 11 epiphytic ferns in a common garden, and analyzed by a comparative phylogenetics method. Compared with epiphytic ferns, terrestrial ferns had higher vein density (Dvein), stomatal density (SD), stomatal conductance (gs), and photosynthetic capacity (Amax), but lower values for lower epidermal thickness (LET) and leaf thickness (LT). Across species, all traits varied significantly, but only stomatal length (SL) showed strong phylogenetic conservatism. Amax was positively correlated with Dvein and gs with and without phylogenetic corrections. SD correlated positively with Amax, Dvein and gs, with the correlation between SD and Dvein being significant after phylogenetic correction. Leaf water content showed significant correlations with LET, LT, and mesophyll thickness. Our results provide evidence that Amax of the studied ferns is linked to leaf water transport capacity, and there was an evolutionary association between water supply and demand in ferns. These findings add new insights into the evolutionary correlations among traits involving carbon and water economy in ferns.
PMCID: PMC3886989  PMID: 24416265
12.  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
13.  Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture 
Annals of Botany  2012;109(6):1091-1100.
Background and Aims
Plasticity in structural and functional traits related to water balance may determine plant performance and survival in ecosystems characterized by water limitation or high levels of rainfall variability, particularly in perennial herbaceous species with long generation cycles. This paper addresses whether and the extent to which several such seasonal to long-term traits respond to changes in moisture availability.
Using a novel approach that integrates ecology, physiology and anatomy, a comparison was made of lifetime functional traits in the root xylem of a long-lived perennial herb (Potentilla diversifolia, Rosaceae) growing in dry habitats with those of nearby individuals growing where soil moisture had been supplemented for 14 years. Traditional parameters such as specific leaf area (SLA) and above-ground growth were also assessed.
Key Results
Individuals from the site receiving supplemental moisture consistently showed significant responses in all considered traits related to water balance: SLA was greater by 24 %; roots developed 19 % less starch storing tissue, an indicator for drought-stress tolerance; and vessel size distributions shifted towards wider elements that collectively conducted water 54 % more efficiently – but only during the years for which moisture was supplemented. In contrast, above-ground growth parameters showed insignificant or inconsistent responses.
The phenotypic changes documented represent consistent, dynamic responses to increased moisture availability that should increase plant competitive ability. The functional plasticity of xylem anatomy quantified in this study constitutes a mechanistic basis for anticipating the differential success of plant species in response to climate variability and change, particularly where water limitation occurs.
PMCID: PMC3336947  PMID: 22396436
Alpine tundra; climate change; drought stress; functional anatomy; herb-chronology; hydraulic conductivity; intervascular xylem; phenotypic plasticity; Potentilla diversifolia; specific leaf area; starch; vessel size
14.  Responses of photosynthetic capacity to soil moisture gradient in perennial rhizome grass and perennial bunchgrass 
BMC Plant Biology  2011;11:21.
Changing water condition represents a dramatic impact on global terrestrial ecosystem productivity, mainly by limiting plant functions, including growth and photosynthesis, particularly in arid and semiarid areas. However, responses of the potential photosynthetic capacity to soil water status in a wide range of soil moisture levels, and determination of their thresholds are poorly understood. This study examined the response patterns of plant photosynthetic capacity and their thresholds to a soil moisture gradient in a perennial rhizome grass, Leymus chinensis, and a perennial bunchgrass, Stipa grandis, both dominant in the Eurasian Steppe.
Severe water deficit produced negative effects on light-saturated net CO2 assimilation rate (Asat), stomatal conductance (gs), mesophyll conductance (gm), maximum carboxylation velocity (Vc,max), and maximal efficiency of PSII photochemistry (Fv/Fm). Photosynthetic activity was enhanced under moderate soil moisture with reductions under both severe water deficit and excessive water conditions, which may represent the response patterns of plant growth and photosynthetic capacity to the soil water gradient. Our results also showed that S. grandis had lower productivity and photosynthetic potentials under moderate water status, although it demonstrated generally similar relationship patterns between photosynthetic potentials and water status relative to L. chinensis.
The experiments tested and confirmed the hypothesis that responsive threshold points appear when plants are exposed to a broad water status range, with different responses between the two key species. It is suggested that vegetation structure and function may be shifted when a turning point of soil moisture occurs, which translates to terms of future climatic change prediction in semiarid grasslands.
PMCID: PMC3037845  PMID: 21266062
15.  Inhibition of Calotropis procera Latex-Induced Inflammatory Hyperalgesia by Oxytocin and Melatonin 
Mediators of Inflammation  2005;2005(6):360-365.
The latex of the wild growing plant Calotropis procera produces inflammation of the skin and mucous membranes upon accidental exposure. On local administration it elicits an intense inflammatory response due to the release of histamine and prostaglandins that is associated with hyperalgesia. In the present study we have evaluated the anti-inflammatory and antinociceptive activity of oxytocin and melatonin against rat paw edema induced by dried latex (DL) of C procera and compared it with that against carrageenan-induced paw edema. Aqueous extract of DL of C procera or carrageenan (1%) was injected into the subplantar surface of the rat paw and the paw volume was measured at 0, 1, 2, 3, 4, 6, 10, and 24 hours. The associated hyperalgesic response and functional impairment were also evaluated concomitantly by dorsal flexion pain test, motility test, and stair climbing ability test. The inhibitory effect of oxytocin and melatonin on edema formation and hyperalgesic response was compared with dexamethasone. DL-induced edema formation was maximum at 2 hours and was associated with decreased pain threshold and functional impairment. Treatment with melatonin significantly attenuated the edematous response while both oxytocin and melatonin increased the pain threshold and improved functional parameters. Both oxytocin and melatonin significantly inhibited the hyperalgesia associated with DL-induced paw edema. Oxytocin was found to be as effective as melatonin in ameliorating the hyperalgesic response. However, it was found to be less effective than melatonin in attenuating edema formation.
PMCID: PMC1533899  PMID: 16489256
16.  Interactive effects of elevated CO2, warming, and drought on photosynthesis of Deschampsia flexuosa in a temperate heath ecosystem 
Journal of Experimental Botany  2011;62(12):4253-4266.
Global change factors affect plant carbon uptake in concert. In order to investigate the response directions and potential interactive effects, and to understand the underlying mechanisms, multifactor experiments are needed. The focus of this study was on the photosynthetic response to elevated CO2 [CO2; free air CO2 enrichment (FACE)], drought (D; water-excluding curtains), and night-time warming (T; infrared-reflective curtains) in a temperate heath. A/Ci curves were measured, allowing analysis of light-saturated net photosynthesis (Pn), light- and CO2-saturated net photosynthesis (Pmax), stomatal conductance (gs), the maximal rate of Rubisco carboxylation (Vcmax), and the maximal rate of ribulose bisphosphate (RuBP) regeneration (Jmax) along with leaf δ13C, and carbon and nitrogen concentration on a monthly basis in the grass Deschampsia flexuosa. Seasonal drought reduced Pn via gs, but severe (experimental) drought decreased Pn via a reduction in photosynthetic capacity (Pmax, Jmax, and Vcmax). The effects were completely reversed by rewetting and stimulated Pn via photosynthetic capacity stimulation. Warming increased early and late season Pn via higher Pmax and Jmax. Elevated CO2 did not decrease gs, but stimulated Pn via increased Ci. The T×CO2 synergistically increased plant carbon uptake via photosynthetic capacity up-regulation in early season and by better access to water after rewetting. The effects of the combination of drought and elevated CO2 depended on soil water availability, with additive effects when the soil water content was low and D×CO2 synergistic stimulation of Pn after rewetting. The photosynthetic responses appeared to be highly influenced by growth pattern. The grass has opportunistic water consumption, and a biphasic growth pattern allowing for leaf dieback at low soil water availability followed by rapid re-growth of active leaves when rewetted and possibly a large resource allocation capability mediated by the rhizome. This growth characteristic allowed for the photosynthetic capacity up-regulations that mediated the T×CO2 and D×CO2 synergistic effects on photosynthesis. These are clearly advantageous characteristics when exposed to climate changes. In conclusion, after 1 year of experimentation, the limitations by low soil water availability and stimulation in early and late season by warming clearly structure and interact with the photosynthetic response to elevated CO2 in this grassland species.
PMCID: PMC3153679  PMID: 21586430
CLIMAITE; climate change; FACE; grassland; leaf δ13C; multifactor experiment; stomatal conductance; water use efficiency
17.  Rubisco activity in Mediterranean species is regulated by the chloroplastic CO2 concentration under water stress 
Journal of Experimental Botany  2011;62(2):653-665.
Water stress decreases the availability of the gaseous substrate for ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) by decreasing leaf conductance to CO2. In spite of limiting photosynthetic carbon assimilation, especially in those environments where drought is the predominant factor affecting plant growth and yield, the effects of water deprivation on the mechanisms that control Rubisco activity are unclear. In the present study, 11 Mediterranean species, representing different growth forms, were subject to increasing levels of drought stress, the most severe one followed by rewatering. The results confirmed species-specific patterns in the decrease in the initial activity and activation state of Rubisco as drought stress and leaf dehydration intensified. Nevertheless, all species followed roughly the same trend when Rubisco activity was related to stomatal conductance (gs) and chloroplastic CO2 concentration (Cc), suggesting that deactivation of Rubisco sites could be induced by low Cc, as a result of water stress. The threshold level of Cc that triggered Rubisco deactivation was dependent on leaf characteristics and was related to the maximum attained for each species under non-stressing conditions. Those species adapted to low Cc were more capable of maintaining active Rubisco as drought stress intensified.
PMCID: PMC3003812  PMID: 21115663
Drought; mesophyll conductance; photosynthesis; stomatal conductance
18.  Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant 
Journal of Experimental Botany  2009;61(3):765-775.
The interaction of photosynthesis and respiration has been studied in vivo under conditions of limited water supply and after consecutive rewatering. The role of the alternative (valt) and cytochrome (vcyt) pathways on drought stress-induced suppression of photosynthesis and during photosynthetic recovery was examined in the Nicotiana sylvestris wild type (WT) and the complex I-deficient CMSII mutant. Although photosynthetic traits, including net photosynthesis (AN), stomatal (gs) and mesophyll conductances (gm), as well as respiration (vcyt and valt) differed between well-watered CMSII and WT, similar reductions of AN, gs, and gm were observed during severe drought stress. However, total respiration (Vt) remained slightly higher in CMSII due to the still increased vcyt (to match ATP demand). valt and maximum carboxylation rates remained almost unaltered in both genotypes, while in CMSII, changes in photosynthetic light harvesting (i.e. Chl a/b ratio) were detected. In both genotypes, photosynthesis and respiration were restored after 2 d of rewatering, predominantly limited by a delayed stomatal response. Despite complex I dysfunction and hence altered redox balance, the CMSII mutant seems to be able to adjust its photosynthetic machinery during and after drought stress to reduce photo-oxidation and to maintain the cell redox state and the ATP level.
PMCID: PMC2814110  PMID: 19933320
Alternative oxidase (AOX); complex I dysfunction; drought stress; mesophyll conductance; photosynthesis; recovery
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.
PMCID: PMC3808328  PMID: 24006421
Arabidopsis; drought tolerance; NF-YB; poplar; transcription factor; water-use efficiency.
20.  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.
PMCID: PMC3892915  PMID: 24555059
21.  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.
PMCID: PMC3892915  PMID: 24555059
22.  Stem hydraulic traits and leaf water-stress tolerance are co-ordinated with the leaf phenology of angiosperm trees in an Asian tropical dry karst forest 
Annals of Botany  2012;110(1):189-199.
Background and Aims
The co-occurring of evergreen and deciduous angiosperm trees in Asian tropical dry forests on karst substrates suggests the existence of different water-use strategies among species. In this study it is hypothesized that the co-occurring evergreen and deciduous trees differ in stem hydraulic traits and leaf water relationships, and there will be correlated evolution in drought tolerance between leaves and stems.
A comparison was made of stem hydraulic conductivity, vulnerability curves, wood anatomy, leaf life span, leaf pressure–volume characteristics and photosynthetic capacity of six evergreen and six deciduous tree species co-occurring in a tropical dry karst forest in south-west China. The correlated evolution of leaf and stem traits was examined using both traditional and phylogenetic independent contrasts correlations.
Key Results
It was found that the deciduous trees had higher stem hydraulic efficiency, greater hydraulically weighted vessel diameter (Dh) and higher mass-based photosynthetic rate (Am); while the evergreen species had greater xylem-cavitation resistance, lower leaf turgor-loss point water potential (π0) and higher bulk modulus of elasticity. There were evolutionary correlations between leaf life span and stem hydraulic efficiency, Am, and dry season π0. Xylem-cavitation resistance was evolutionarily correlated with stem hydraulic efficiency, Dh, as well as dry season π0. Both wood density and leaf density were closely correlated with leaf water-stress tolerance and Am.
The results reveal the clear distinctions in stem hydraulic traits and leaf water-stress tolerance between the co-occurring evergreen and deciduous angiosperm trees in an Asian dry karst forest. A novel pattern was demonstrated linking leaf longevity with stem hydraulic efficiency and leaf water-stress tolerance. The results show the correlated evolution in drought tolerance between stems and leaves.
PMCID: PMC3380589  PMID: 22585930
Tropical dry forest; karst; leaf habit; hydraulic conductivity; cavitation resistance; leaf water-stress tolerance; wood density; leaf density; phylogenetic independent contrasts
23.  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).
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.
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.
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
24.  Rising atmospheric carbon dioxide concentration and the future of C4 crops for food and fuel 
Crops with the C4 photosynthetic pathway are vital to global food supply, particularly in the tropical regions where human well-being and agricultural productivity are most closely linked. While rising atmospheric [CO2] is the driving force behind the greater temperatures and water stress, which threaten to reduce future crop yields, it also has the potential to directly benefit crop physiology. The nature of C4 plant responses to elevated [CO2] has been controversial. Recent evidence from free-air CO2 enrichment (FACE) experiments suggests that elevated [CO2] does not directly stimulate C4 photosynthesis. Nonetheless, drought stress can be ameliorated at elevated [CO2] as a result of lower stomatal conductance and greater intercellular [CO2]. Therefore, unlike C3 crops for which there is a direct enhancement of photosynthesis by elevated [CO2], C4 crops will only benefit from elevated [CO2] in times and places of drought stress. Current projections of future crop yields have assumed that rising [CO2] will directly enhance photosynthesis in all situations and, therefore, are likely to be overly optimistic. Additional experiments are needed to evaluate the extent to which amelioration of drought stress by elevated [CO2] will improve C4 crop yields for food and fuel over the range of C4 crop growing conditions and genotypes.
PMCID: PMC2690454  PMID: 19324804
climate change; photosynthesis; CO2 fertilization; maize; sorghum; food security
25.  Seasonal variation of carbon fluxes in a sparse savanna in semi arid Sudan 
Large spatial, seasonal and annual variability of major drivers of the carbon cycle (precipitation, temperature, fire regime and nutrient availability) are common in the Sahel region. This causes large variability in net ecosystem exchange and in vegetation productivity, the subsistence basis for a major part of the rural population in Sahel. This study compares the 2005 dry and wet season fluxes of CO2 for a grass land/sparse savanna site in semi arid Sudan and relates these fluxes to water availability and incoming photosynthetic photon flux density (PPFD). Data from this site could complement the current sparse observation network in Africa, a continent where climatic change could significantly impact the future and which constitute a weak link in our understanding of the global carbon cycle.
The dry season (represented by Julian day 35–46, February 2005) was characterized by low soil moisture availability, low evapotranspiration and a high vapor pressure deficit. The mean daily NEE (net ecosystem exchange, Eq. 1) was -14.7 mmol d-1 for the 12 day period (negative numbers denote sinks, i.e. flux from the atmosphere to the biosphere). The water use efficiency (WUE) was 1.6 mmol CO2 mol H2O-1 and the light use efficiency (LUE) was 0.95 mmol CO2 mol PPFD-1. Photosynthesis is a weak, but linear function of PPFD. The wet season (represented by Julian day 266–273, September 2005) was, compared to the dry season, characterized by slightly higher soil moisture availability, higher evapotranspiration and a slightly lower vapor pressure deficit. The mean daily NEE was -152 mmol d-1 for the 8 day period. The WUE was lower, 0.97 mmol CO2 mol H2O-1 and the LUE was higher, 7.2 μmol CO2 mmol PPFD-1 during the wet season compared to the dry season. During the wet season photosynthesis increases with PPFD to about 1600 μmol m-2s-1 and then levels off.
Based on data collected during two short periods, the studied ecosystem was a sink of carbon both during the dry and wet season 2005. The small sink during the dry season is surprising and similar dry season sinks have not to our knowledge been reported from other similar savanna ecosystems and could have potential management implications for agroforestry. A strong response of NEE versus small changes in plant available soil water content was found. Collection and analysis of flux data for several consecutive years including variations in precipitation, available soil moisture and labile soil carbon are needed for understanding the year to year variation of the carbon budget of this grass land/sparse savanna site in semi arid Sudan.
PMCID: PMC2632635  PMID: 19046418

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