Journal of Photochemistry and Photobiology B: Biology
Regulation of photosynthesis, fluorescence, stomatal conductance and water-use efficiency of cowpea (Vigna unguiculata [L.] Walp.) under drought
Graphical abstract
Highlights
► Dynamics of photosynthesis and water-use efficiency parameters in 15 cowpea genotypes in response to drought is examined. ► Photosynthesis and chlorophyll fluorescence declined linearly with decreasing soil water content. ► Intrinsic water-use efficiency increased under drought stress. ► Stomatal regulation is a major limitation to photosynthesis under drought conditions in cowpea cultivars.
Introduction
Drought is a major abiotic stress limiting plant productivity worldwide, especially in the arid and semi-arid agro-ecosystems [1]. The predicted changes in climate may lead to precipitation extremes and drought intensities on regional scale. However, decrease in precipitation will be widespread in subtropical region associated with higher temperature and increased evapotranspiration [2]. In general, drought stress induces an array of morphological, physiological, biochemical, and molecular responses, in which photosynthesis being one of the primary physiological target [3]. Understanding the detrimental effects of drought on plant processes and mechanisms of drought tolerance in crop species, particularly those adapted to dry conditions will help to improve their agronomic performance by incorporating the superior traits into new species or cultivars [4].
Stomatal regulated reduction in transpiration is a common response of plants to drought stress which also provides an opportunity to increase plant water-use efficiency [5]. Under moderate drought stress conditions, reduced stomatal conductance (gs) is the primary cause of photosynthetic inhibition from reduced supply of CO2 to the intercellular space [6]. In general, atmospheric CO2 diffuses through stomata to the intercellular space (i.e. stomatal limitation) then across the mesophyll (mesophyll limitations) at the carboxylation site. Therefore, mesophyll conductance (gm) and biochemical limitation (bL) (often termed as non-stomatal limitations) to photosynthesis mainly under severe water stress has also gained importance in the recent years and their relative importance to photosynthesis limitation has been subjected to long-standing debate [7], [8], [9], [10], [11].
The finite role of gm has been accepted and the concentration of CO2 in to the inter-cellular spaces (Ci) has been estimated to differ from CO2 concentration in the chloroplast (Cc) which varies within species due to their sensitivity to a range of internal and external factors including, leaf development stage, leaf structure and anatomy, radiation, CO2, temperature, water, and nutrient condition [7 and references therein, [8], [12]. Severe water stress can also lead to metabolic impairments including limitations to phosphorylation [13], RuBp (ribulose 1,5-bisphosphate) regeneration [14], and Rubisco activity [15] thus indicating, biochemical limitations to photosynthesis. Although, the role of non-stomatal limitations to photosynthesis is apparent, controversies still exit due to the assumptions and errors in the estimation of gm and bL under drought [16], [17]. Photosystem II (PSII) is highly sensitive to light and down regulation of photosynthesis under drought stress causes an energy imbalance in the PSII reaction center leading to photoinhibition [18]. Mechanisms have evolved in the plant to protect from photoinhibition, such as non-photochemical quenching, electron (e−) transport to molecules other than CO2, most importantly to oxygen, which leads to photorespiration and/or Mehler reaction [11], [19], non-radiative energy dissipation mechanisms [20], [21], and chlorophyll concentration changes [18]. However, these processes ultimately lead to the lower quantum yield of PSII [19].
Cowpea is an important legume crop mostly grown in the arid and sub-arid zones of the world where the production mostly depends upon rain as a sole source of water supply [22], [23]. Among all legumes, cowpea has the maximum diversity for plant type, growth habit, maturity, seed type and adapted to a wide range of environments which may serve as a model legume crop [22], [24]. Cowpea exhibits broad adaptation mechanisms to drought, such as drought escape, drought avoidance by decreasing leaf area, dehydration avoidance, and vegetative stage drought tolerance by delayed leaf senescence [24], [25], [26], [27]. Cowpea plants have shown dehydration avoidance by maintaining high leaf water status without osmotic adjustment which has indicated a common response pattern of photosynthetic processes in relation to soil water content (SWC) or drought induced changes in gs independent to leaf osmotic potential [25], [26], [27].
Crop adaptation to rain-fed conditions can be achieved by improved water-use efficiency (WUE) or by increasing water supply to the plant through improved root system [24]. Intrinsic water-use efficiency estimated as a ratio of A/gs has been recognized as a measure of carbon gain per unit of water loss and found to be inversely proportional to the ratio of intercellular and ambient CO2 concentrations (Ci/Ca) [28], [29]. Large variability in WUE has been reported among several species as well as cultivars within a species including cowpea [28], [30], [31]. Because higher rates of leaf photosynthesis are often associated with faster crop growth rates, a combination of higher photosynthesis and improved WUE may play a vital role for yield enhancement of crops under drought stress conditions [5], [31].
Although, studies have shown that cowpea photosynthetic performance can recover considerably once the drought stress is relieved, transient photoinhibition or residual impairment of photosystems at very low gs have also been observed [21], [27]. The protective mechanisms for maintaining the photosynthetic apparatus under drought stress condition in cowpea are not well understood [32]. In drought stress, gs has been shown to relate well and exhibit a specific pattern over almost all the important photosynthetic parameters similarly [11], [16], [33] which may not essentially reflect the cause and effect relationship. However, it will be helpful to evaluate the relative importance of different processes limiting photosynthesis at a wide range of gs caused by drought stress and may shed light on the current debate regarding to stomatal vs. non-stomatal limitations. The extent of stomatal limitation to various photosynthetic parameters can be assessed by simultaneous measurement of leaf gas exchange, fluorescence, and WUE parameters under drought stress conditions [5], [16]. The genotypic diversity in cowpea for the physiological responses to drought will help to comprehend how one or a combination of physiological processes interacts with each other to manage drought stress. The objectives of the study were to determine the relative regulation of various photosynthetic parameters to drought induced stomatal conductance and to evaluate the relative responses of different photosynthetic processes among cowpea genotypes under drought stress and determine whether the genotypes representing diverse sites of origin would group based on their relative physiological tolerance to drought.
Section snippets
Plant material and experimental conditions
An outdoor container experiment was conducted in 2006 at the R.R. Foil Plant Science Research Center, Mississippi State University, Mississippi State (33°28′N, 88°47′W) MS, USA. Fifteen cowpea genotypes representing diverse sites of origin (Table 1) were seeded in 12-L pots, filled with fine sand on 2 August 2006. The pots were 0.65 m in height and 0.15 m in diameter with a small hole at the bottom to drain excess water. The study was comprised of 600 pots with 40 pots per genotype in two
Gas exchange, photosynthetic and water-use efficiency parameters under drought
The combined analysis of all cowpea genotypes showed no relationship between LRWC and SWC (Fig. 1A). However, photosynthesis (A) showed a linear relationship with SWC (Fig. 1B). The gs exhibited an exponential relationship with SWC and decreased to zero under severe drought conditions (Fig. 1C). Similar to the A, the transpiration rate (E) also exhibited a linear relationship with SWC (Fig. 1D).
Photosynthesis rate declined linearly as drought stress-induced Ci decreased to a minimum value of 95
Role of stomatal conductance under drought stressed conditions
Since, gs is responsive to almost all external and internal factors related to drought, it represents a highly integrative basis for overall effect of drought on photosynthetic parameters [16]. Once this relationship is determined, the proportional changes in each process can then be estimated at any point of gs, representing various degree of water stress. The important event observed in the first gs region (gs > 1.8) clearly indicates that cowpea transpired excessively without any gain in
Conclusions
The current study showed the drought avoidance behavior of cowpea by maintaining higher leaf water status. However, soil water status affected the gs and photosynthetic parameters measured in leaves, exhibiting a pattern of gradual response of photosynthetic parameters to the distinguished four regions of stomatal conductance. Stomatal conductance is the major limitation to A under drought conditions in cowpea; however, a pronounced non-stomatal limitation can occur under severe drought
Abbreviations
A photosynthesis Cc CO2 concentration in the chloroplast Ci intercellular CO2 concentration Ca ambient CO2 concentration Fv′/Fm′ quantum efficiency by oxidized (open) PSII reaction center gs stomatal conductance gm mesophyll conductance SWC soil water content WUE water-use efficiency
Acknowledgements
This research was funded in part by the Department of Energy, and USDA-UVB Monitoring Program at Colorado State University, CO. We also thank Drs. Harry Hodges, John Read and Mengmeng Gu for their comments and suggestions, Mr. David Brand for technical support, and Dr. Jeff Ehlers, Department of Botany and Plant Sciences, University of California-Riverside, CA, USA for providing seed. This article is a contribution from the Department of Plant and Soil Sciences, Mississippi State University,
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