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Some Physiological Processes Related to Water Use Efficiency of Higher Plants
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Agricultural Sciences in China 2006. 5(6): 403-41 1
June 2006
Some Physiological Processes Related to Water Use Efficiency of Higher Plants GUO Shi-wei, ZHOU Yi, SONG Na and SHEN Qi-rong College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China
Abstract Water use efficiency (WUE) of higher plants is of vital importance in the dry-land agricultural ecosystem in terms of the development of water-saving agriculture. Of all the approaches used to improve WUE, the intrinsic water use efficiency (WUE,, the ratio of CO, assimilation rate to transpiration rate) can be a right index, as the variation of WUE, is correlated with the physiological and biochemical processes of higher plants. The measurements of leaf gas exchange and carbon isotope discrimination (D I F ) are the two ways to detect the variation in WUE,. This article reviewed some physiological processes related to WUE,, including the relationship between CO, assimilation and stomatal conductance and WUE, and water absorption. The relationship between WUE and aquaporin and the yield are discussed as well.
Key words: water use efficiency, gas exchange, carbon isotope discrimination, water channel
INTRODUCTION Water is the single most limiting resource for world agriculture and food production, highly exceeding other key limitations. Large amount of water is used in field production of food crops, leading to a deficit of fresh water resources in many arid or semi-arid areas in the world. The optimization of plant irrigation protocols is essential for saving water and preserving water quality. The goal of optimization is to increase plant dry matter production, yield quantity, and yield quality for a given water volume, which is so-called water use efficiency ( W E ) . WUE by higher plants is of vital importance in the dry-land agricultural ecosystem in terms of the development of water-saving agriculture (Udayakumar et al. 1998). Therefore, in the modern agricultural ecosystem, the established optimal water management is highly regulated to achieve two objectives: ( 1 ) to maximize the water uptake by plants from the soil to compete with water loss (i.e., leakage and evaporation),
and the capacity for water delivery to the foliage, which is related to the water holding capacity of soil, the capacity of root water uptake, and the hydraulic conductivity of the xylem of the root and stem (Davis and Quick 1998); and (2) to optimize the water use efficiency (WUE), which is associated with the economic yield produced and the total water consumed (Kafkafi 1997). To improve W E in field scale, field water managers and plant breeders have achieved much progress, but only several approaches succeeded in raising physiological water use efficiency (Udayakumar et al. 1998), as the complicated factors required. Of all the approaches to improve WUE, the intrinsic water use efficiency (WUE,, the ratio of CO, assimilation rate to transpiration rate) (Stanhill 1986) can be a useful parameter, as the variation of W E T is correlated with the physiological and biochemical processes of higher plants. However, because of the complicated interaction between the parameters of gas exchange and contrary effects of stomatal conductance, transpiration rate and CO, assimilation rate, it is difficult to estimate and study
Received 20 July. 2005 Accepted 19 March, 2006 GUO Shi-wei. Ph D, Associate Professor, Tel: +86-25-84396393. E-mail: sguoBnjau,edu.cn
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water use efficiency in this physiological aspect. Thus, the relationship between the amounts of assimilated CO, and transpired water by improving plant physiological performance is still a matter of trial and error. Of most interest in this article are: (1) the biochemical and physiological processes related to intrinsic water use efficiency, and (2) the relationship between water use efficiency and aquaporin and yield.
DEFINITIONS OF WATER USE EFFICIENCY WUE of higher plants is defined as biomass andor economic yield produced per unit of water consumed. Generally, according to different research objectives and the pathways of water consumption and loss, W E may be defined at three different levels (Stanhill 1986): 1 ) Leaf level. WUE, the so-called intrinsic water use efficiency, is defined as the simultaneous ratio of net carbon assimilation to water transpiration of the stomata from a leaf (WUE,=A/E). This is the WUE, of the photosynthetic process. 2) Whole plant level. WUE is defined as the ratio of the biomass produced to total water used. WUE at this level is always lower than Leaf Level WUE, because of the water loss associated with non-photosynthetic processes and respiratory carbon loss during conversion of initial photosynthate to standing biomass. 3 ) Stand or crop level. WUE is defined as the ratio of the biomass produced to total water inputs to the whole ecosystem (yieldtotal water input). At this level, WUE is further decreased by the fraction of total water inputs from rain or irrigation that is never taken up by the plants. Crop level WUE is of importance for economical considerations, and integrates processes at all levels. Much progress has already been made in improving crop level WUE by irrigation practices that are more efficient in timing, allocation, and delivery of water to minimize secondary runoff, seepage, and unproductive evaporation from the soil surface (Stanhill 1986; Tuong and Bhuiyan 1999). Breeding for plant characteristics that maximize water extraction capabilities, such as deep roots, high hydraulic capacities for water transport, and high stomatal conductance can sometimes increase crop level WUE simply by increasing total productive water use and consequently by decreasing the evaporation
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from the surface of the soil (Shan and Xu 1991). Improvements in plant level W E also hold the promise of gains in total crop WUE. WUE of individual C, crop plants often varies two-to-three folds among genotypes grown under common conditions, and even more among wild plants (Rounick and Winterbourn 1986; Brooks el al. 1997). WUE of crops is generally low compared to many wild species (Franks and Farquhar 1999). Despite the obvious opportunities for improved production under water limiting conditions, breeding efforts for plant and leaf level WUE have achieved only limited success (Johnson and Li 1999). One reason why progress is lagging in this area is that some key traits at the leaf level usually have counteracting effects on the opposite parameters, such as the ratio of total water usage to efficient water usage (Udayakumar et al. 1998). For example, maximizing total water use generally involves high stomatal conductance, whereas low stomatal conductance favors high ratio of carbon gain to water loss. Classical selection for yield in field trials most often select to increase total water use, even at the cost of leaf level WUE. Attempts to select high WUE are also directly confounded by unintended side effects (Johnson and Li 1999; Rowe 1995). More effective breeding strategies for WUE require a better understanding of the underlying genetics controlling WUE, and their pleiotropic effects on the related traits of total water capture and/or photosynthetic capacity. In contrast to the W E at whole plant and crop levels, the W E at leaf level represents the physiological parts of the photosynthetic process, and may explain the majority of variance in the whole plant level WUE. Furthermore, to understand how photosynthesis affects WUE, many problematic pleiotropic effects related to the photosynthetic process and WUE must be explained and resolved, for example, how stomata behavior controls the ratio of fixed CO, and lost water vapor.
INSTRINSIC WATER USE EFFICIENCY Water is essential for growth in higher plants, and most of the water absorbed by plants is lost during the gas exchange processes. A normal plant growing in temperate climates requires 700- 1 300 mol H,O for the fixation of I mol CO, (Heldt 1997). However, plants differ in their capacity to regulate the amount of carbon that
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Some Physiological Processes Related to Water Use Efficiency of Higher Plants
is gained per unit of water lost. Such differences can be referred to as differences in intrinsic water use efficiency, WUE,, which is defined as the ratio of instantaneous rate of CO, assimilation and transpiration (Condon et al. 2002). According to Fick’s law, the intrinsic water use efficiency can be described by a relatively simple equation (Eq. l):
Both A (CO, assimilation rate) and E (transpiration rate) are the product of two factors: stomata conductance (g) for either CO, (gc) or water vapor (g,) and the concentration difference of either CO, (caand ci) or water vapor (wa and wi) between the air outside and inside the leaf. Because H,O and CO, share a common diffusion pathway between the leaf intercellular airspaces and the atmosphere, A/E in leaf level WUE is directly related to the relative magnitudes of the respective diffusion gradients (Farquhar et al. 1989) (Eq.2):
WUET=
ca-ci 1.6 (wi-wa)
Where the factor 1.6 refers to the relative diffusivities of CO, and water vapor in air. In C, plants, the variation in ci is often considered in physiological studies as intrinsic WUE to distinguish this plant trait from the background effects of environ-
2
1
-
IntercellularCOI concentration
mental conditions that also have a strong effect on actual WE,. Because the internal air spaces of a leaf are always close to being saturated with water vapor, wi is determined mainly by leaf temperature. To the first approximation, wi is determined primarily by environmental air temperature, however, wi may also be controlled by the plant itself during the opening and closing of the stomata. It is true that the ca (CO, concentration in atmosphere) is constant and cannot be controlled by plants, then Eq.2 indicates that WUE, is negatively correlated with ci (the intercellular CO, concentration), for a photosynthesizing leaf of nonstressed C, plants, the ratio of ci to ca is typically around 0.7 (Farquhar et al. 1989), this “operating” value of ci/cais determined by the balance between stomatal conductance and photosynthetic capacity. Although stomatal conductance (g,> does not appear explicitly in Eq.2, the ratio of the biochemical potential for carbon fixation to stomatal conductance represents the balance between the supply of CO, and its consumption and determines ci (Farquhar and Sharkey 1982). Therefore, stomatal conductance influences the supply of CO, to the intercellular spaces of leaf, whereas photosynthetic capacity determines the demand for CO,. Fig.-A, B show a typical intercellular CO, response curve (A-ci curve) that is measured under saturating light intensity. Under low CO, supply, the CO, assimilation rate is limited by the activity of Rubisco and under high CO, supply, the CO, assimilation rate is limited by the regeneration rate of RuBP,
L
1
Intercellular CO, concrnlratlon
+
Fig. A schematic illustration demonstrating the dependence of ci on the relationship between stomatal conductance and CO, assimilation rate. Both figures describe the two possible approaches to increase W W . Fig.-A (left) shows increased WUE via increased carboxylation efficiency (initial slope of the A-c, curve) and constant stomatal conductance (the solid line). Fig.-B (right) shows the increased WUE via stomatal closure with constant carboxylation efficiency (Guo 2001).
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and this is further limited by triose-phophate utilization under the highest CO, supply in the A-CO, response curve (Farquhar et al. 1982; Sage et al. 1988). The initial slope of the curve is defined as carboxylation efficiency. The solid lines are connected by two CO, concentrations (ambient and corresponding intercellular CO, concentration), and the initial slope of solid lines is defined as the stomatal conductance ( g c ) . As shown in Fig.-A and B, it is theoretically possible to improve WUE, either through lowering stomatal conductance to water or raising photosynthetic capacity (related to carboxylation efficiency) or a combination of both. In Fig.-A, if stomatal conductance remains unchanged, increased WUE, can be achieved by the enhancement of carboxylation efficiency. In contrast, in Fig.-B, if stomata of a given leaf close and its carboxylation efficiency (the initial slope of a A-c, curve) remains constant, c, decreases and WUE, increases, but it will be at the cost of a reduced assimilation rate because of increasingly limiting substrate levels. However, this is only a potentially desirable outcome and it requires a higher supply of nitrogen and other nutrients per unit leaf biomass. Another possibility to increase WUE, is to control the luxurious transpiration, as shown by Wang and Liu (2003). There was a parabola relationship between CO, assimilation rate and transpiration rate, and the transpiration rate at the maximal CO, assimilation rate was a critical value, therefore it is possible to increase WUE, by controlling this luxurious transpiration without affecting the CO, assimilation rate. As discussed above, although the variation of WUE, at the leaf level is always associated with changes in C,, this can also occur through numerous mechanisms, such as changes in stomatal conductance, carboxylation efficiency etc. Stomata1 regulation is a complex process involving several pathways (Grabov and Blatt 1998; Pei et al. 1998), all of which can condition WUE,. This coordinated control involves stomatal responses to C, (Mott 1990; Leymarie et al. 1998), light (Wang and Liu 2003; Zeiger and Zhu 1998),relative humidity (Grantz 1990; Comstock and Ehleringer 1993; Meinzer et al. 1997), hormonal signals (Hartung et al. 1998; Jia and Zhang 1999), and nutritional status (Guo et al. 2005; Dood et al. 2003; Frederick and James 1997), for example, under ammonium nutrition, rice plants had a higher WUE, than that under the mixture of ammo-
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nium and nitrate and sole nitrate nutrition (Guo et al. 2005). This phenomenon might be caused by the difference of nitrogen accumulation in the leaves between different nitrogen forms of nutrition (Zhou er al. 2006a). Stomata have also been shown to reflect directly to leaf water potential (Saliendra et al. 1995; Fuchs and Livingston 1996; Comstock 2000b). The leaf water potential could affect stomatal behavior either through variation in the water potential-sensing mechanism in the leaf or via changes in the hydraulic architecture of the plant, which determines the functional dependence of leaf water potential on E. The latter includes both relative biomass allocation to different organs, anatomical features (i.e., vessel diameter) of the xylem determining conducting efficiency and cavita.tion vulnerability (Sperry et al. 1998; Mencuccini et al. 2000; Comstock 2000a), and the distribution of aquaporins in the leaf and root tissues (i.e., aquaporin located in the plasma membrane of root tissue plays a key role in root water absorption) (Tyerman et al. 1999, Clarkson et al. 2000). Turgor maintenance by osmotic adjustment is important both as the proximal mechanism of stomatal opening (Talbott and Zeiger 1996; Asai er ul. 2000) and in determining the tolerance of leaf mesophyll tissues to reduced leaf water potential (Zhang et af. 1999). CO, must diffuse inward, beyond the shared pathway of the stomatal pore to reach the chloroplasts. Tissue and subcellular organization and features such as the distribution and amount of carbonic anhydrase (invert CO, into carbonate or bicarbonate) influence the resistance to the liquid-phase movement of CO, to the sites of carboxylation (the resistance of CO, to liquid-phase is 1000 times higher than to air phase) (Evans and von Caemerer 1996; Scartazza et al. 1998). Once CO, has entered the chloroplast, the carboxylation capacity is related to the RuBPCase activity and light-harvesting capacities (Asai et al. 2000). Both of these components are expensive in terms of nitrogen investment, and the RuBPCase alone can be as much as half of all the soluble proteins in the leaf (Farquhar er af. 1980). From Fig., carboxylation efficiency plays an important role in increasing WUE,. Thus, any environmental and nutritional factors that influence RuBPCase content and activity may contribute to WUE,and WUE. Under light drought stress, WUE can be enhanced by the adjustment of nutritional management, even for
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Some Physioloeical Processes Related to Water Use Efficiency of Higher Plants
paddy rice plants (Zhou et af.2005, 2006a). It is therefore estimated that light drought stress may play an important role in increasing WUE. With regard to the plant nutrition, it has been demonstrated that nitrogen, phosphate, and potassium may influence W E , however, it still remains open as to how the mechanism is functioning to adjust the nutritional status in order to increase WUE and WUE, (Zhou et al. 2006b). It is hypothesized that nutritional factors may adjust the process involved in the WUE, such as root depth, leaf area, stomatal conductance, etc.
WUE, AND CARBON ISOTOPE DISCRIMINATION The efficacy of the use of d l T as an indicator of WUE, has been firmly established under both greenhouse and field conditions (Farquhar et af. 1982; Faquhar and Richards 1984; Hubick and Farquharl989). It obviates the prohibitive need for measurements of water budget for a large number of individuals during large-scale screening. This technique, based on the natural abundance of stable carbon isotopes, takes advantage of the naturally occurring variation in the isotopic composition of plants, and does not require specific labeling. Briefly, CO, in air naturally contains two stable isotopes of carbon, I2Cand I3C,in an approximate of 99% to 1 %, and it is in the form of I T , but the isotope ratio, l3C/I2C,is smaller in plant organic carbon than in atmospheric CO, because of the discrimination against I3C (by the dominant enzyme Rubisco) during photosynthetic uptake. The theoretical model describing fractionation during C, photosynthesis was developed by Farquhar et uf. ( I 989). The simplest form of the model is:
A = a + (b-a)'
C
ca
(3)
Where A represents the total difference in isotopic composition between photosynthetically fixed carbon and that in the atmosphere, and a and b are the fractionation constants associated with diffusion versus carboxylation and have values of 4.4 and 27%0(per mill), respectively (Farquhar et af. 1989). It is clearly shown in Eq. 3 that D is positively correlated with the ratio of ci to ca, whereas, as mentioned before, WUE, is nega-
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tively correlated with the ratio of cI to ca.Therefore, D and W E , are negatively correlated. Coming back to the biochemical and physiological process explaining the relationship between D and WLJE,, when the stomata are widely open, there is ample CO, in the stomatal cavities and at the carboxylation site, the photosynthetic enzyme Rubisco can distinguish pronounced ' T O , against l3CO,, and uses '*CO, in preference to ' T O , as the substrate. On the other hand, as stomata are closed, the photosynthetic process is limited by CO, availability at the carboxylation site. Rubisco will fix ' T O , and ' T O , and consequently there is less discrimination, and the measured D in the leaf tissue is higher (Farquhar et al. 1989). The mechanistic validity of the isotopic behavior embodied in &. 3 has been verified for many crops and wild plant species (Hubick et ul. 1988; Ehleringer et al. 1991; Livingston ef al. 1999). The negative linear relation between WUE, and A has also been shown to hold for numerous crops, even when WUE, was measured on potted material at the whole plant level (Farquhar and Richards 1984; Hubick and Farquhar 1989; Martin et af. 1999) or in open field plantings (Knight et af. 1994; Saranga et ul. 1998). Other potential factors, such as variation in the efficiency of respiration in the conversion of photosynthate to new biomass, or nonphotosynthetic water loss will also affect WUE,, or the process of carbon fixation by PEPCase, but variation arising from such traits seems to be smaller than that associated with the photosynthetic process itself.
WUE, AND WATER CHANNEL (AQUAPORIN) The study of plant WUE, is complicated because several processes are involved, not only the leaf parameters (leaf area, transpiration rate, and stomatal conductance), but also the parameters of root and stem such as: root amount and extend, hydraulic conductance of root and stem, the capacity of water uptake of roots, and the pathway of radial water transport across the root. The most important parameters related to plant itself are hydraulic conductance of stem and root, and aquaporin of roots (Maurel and Chrispeels 2001 ; Javot and Maurel2002); however, there is little experimental evidence showing how these parameters influence the plant WUE,. Theoretically, the stem has diverted water
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to the leaf, from where it transpires. Water is delivered to the stem by the root, therefore the capacity of root water uptake and the hydraulic conductivity of root and stem might significantly affect the leaf water status and further stomatal conductance and transpiration rate. For example, with a lower hydraulic conductivity, rice plants suffer from water shortage in the shoot even in flooded fields (Miyamoto et al. 2001). Generally, the increase in hydraulic conductivity is illustrated as being correlated with increased aquaporin activity and gene expression (Clarkson et al. 2000; Maurel and Chrispeels 2001). The capacity of root water uptake depends dominantly on the activity of the water channel (aquaporin)(Chrispeelsand Maurel 1994; Kaldenhoff et al. 1998;Quintero et al. 1999).Aquaporin is a general designation of membrane channel proteins that regulate the water transport across the plasma membrane (Maurel and Chrispeels 2001). The contribution of aquaporin to whole plant water relation may account up to 85%. The water channel activity is regulated by phosphorylation, pH, pCa, osmotic gradients, and some nutrient’s (i.e., N and P) stress (Clarkson et al. 2000). The activity of aquaporin can be reversibly inhibited by HgCl, (Quintero et u1. 1999; Baiges et al. 2002; Zhang and Tyerman 1999). It has been testified that aquaporin plays a significant role in water status in higher plants in response to drought stress (Martre et al. 2002). For example, tobacco plants impaired in NtAQP1 expression (resulting in low aquaporin activity) show reduced root hydraulic conductivity, transpiration rate, and thus lower water stress resistance (Siefritz et ul. 2002), therefore, tobacco plants impaired in NtAQP1 suffer from water stress under wetted soil. It is suggested that under water stress, some root water channels are switched off (North and Nobel 2000), as some root aquaporin (PIP) gene is downregulated. Therefore, it may be argued whether the first responsibility to drought stress could have resulted from stomatal closure or from the expression of aquaporin downregulation. The argument still remains open whether a higher WUE, is associated with a higher activity andor gene expression of aquaporin, as there is a complicated transport pathway of water transport across the roots (Steudle 2000). The assumption based on the associa-
tion between root water absorption and delivery, and leaf transpiration relies on the critical water absorption (Steudle and Henzler 1995).
THE RELATIONSHIP BETWEEN WUE AND YIELD Generally, at the crop and whole plant level, WUE is linearly correlated to the biomass under limited water condition. On the other hand, under a condition of sufficient water supply, W E is not always linearly correlated to the biomass or economic yield. For example, there was a parabola relationship between the grain yield and WUE of maize (Liu 1998), and the maximal WUE came earlier than the maximal yield with a rise in transpiration rate. At the leaf level, the relationship between W E , and yield is variable among crop systems, and depends on environmental factors, such as, water availability limiting the growth and variation in the underlying genetics conditioning the variations in WUE. In many cases examined, A is seen to be positively correlated to the yield and W E itself is negatively correlated, especially under conditions of ample water availability (White et al. 1994). This is what was expected when variation in A was being caused primarily by variation in stomatal opening, and low WUE was associated with greater total water use and higher A (Eqs. 1, 2). Contrasting cases have also been reported where yield was positively correlated with WUE (Musick et al. 1994). This is expected when moderate water deficits make higher efficiency (Martin er al. 1999) and when variation in W E is caused primarily by variation in carboxylation capacity (Livingston et al. 1999; Rao et al. 1995; Virgona and Farquhar 1996).
Acknowledgements This study was supported by the National Basic Research Program of China (2005CB121101), and the National Natural Science Foundation of China (30400279). This paper is in memory of Prof. Dr. Burkhard Sattelmacher (08,6,1947- 1 1,21,2005).
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Agricultural Sciences in China 2006. 5(6): 403-41 1
June 2006
Some Physiological Processes Related to Water Use Efficiency of Higher Plants GUO Shi-wei, ZHOU Yi, SONG Na and SHEN Qi-rong College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R.China
Abstract Water use efficiency (WUE) of higher plants is of vital importance in the dry-land agricultural ecosystem in terms of the development of water-saving agriculture. Of all the approaches used to improve WUE, the intrinsic water use efficiency (WUE,, the ratio of CO, assimilation rate to transpiration rate) can be a right index, as the variation of WUE, is correlated with the physiological and biochemical processes of higher plants. The measurements of leaf gas exchange and carbon isotope discrimination (D I F ) are the two ways to detect the variation in WUE,. This article reviewed some physiological processes related to WUE,, including the relationship between CO, assimilation and stomatal conductance and WUE, and water absorption. The relationship between WUE and aquaporin and the yield are discussed as well.
Key words: water use efficiency, gas exchange, carbon isotope discrimination, water channel
INTRODUCTION Water is the single most limiting resource for world agriculture and food production, highly exceeding other key limitations. Large amount of water is used in field production of food crops, leading to a deficit of fresh water resources in many arid or semi-arid areas in the world. The optimization of plant irrigation protocols is essential for saving water and preserving water quality. The goal of optimization is to increase plant dry matter production, yield quantity, and yield quality for a given water volume, which is so-called water use efficiency ( W E ) . WUE by higher plants is of vital importance in the dry-land agricultural ecosystem in terms of the development of water-saving agriculture (Udayakumar et al. 1998). Therefore, in the modern agricultural ecosystem, the established optimal water management is highly regulated to achieve two objectives: ( 1 ) to maximize the water uptake by plants from the soil to compete with water loss (i.e., leakage and evaporation),
and the capacity for water delivery to the foliage, which is related to the water holding capacity of soil, the capacity of root water uptake, and the hydraulic conductivity of the xylem of the root and stem (Davis and Quick 1998); and (2) to optimize the water use efficiency (WUE), which is associated with the economic yield produced and the total water consumed (Kafkafi 1997). To improve W E in field scale, field water managers and plant breeders have achieved much progress, but only several approaches succeeded in raising physiological water use efficiency (Udayakumar et al. 1998), as the complicated factors required. Of all the approaches to improve WUE, the intrinsic water use efficiency (WUE,, the ratio of CO, assimilation rate to transpiration rate) (Stanhill 1986) can be a useful parameter, as the variation of W E T is correlated with the physiological and biochemical processes of higher plants. However, because of the complicated interaction between the parameters of gas exchange and contrary effects of stomatal conductance, transpiration rate and CO, assimilation rate, it is difficult to estimate and study
Received 20 July. 2005 Accepted 19 March, 2006 GUO Shi-wei. Ph D, Associate Professor, Tel: +86-25-84396393. E-mail: sguoBnjau,edu.cn
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water use efficiency in this physiological aspect. Thus, the relationship between the amounts of assimilated CO, and transpired water by improving plant physiological performance is still a matter of trial and error. Of most interest in this article are: (1) the biochemical and physiological processes related to intrinsic water use efficiency, and (2) the relationship between water use efficiency and aquaporin and yield.
DEFINITIONS OF WATER USE EFFICIENCY WUE of higher plants is defined as biomass andor economic yield produced per unit of water consumed. Generally, according to different research objectives and the pathways of water consumption and loss, W E may be defined at three different levels (Stanhill 1986): 1 ) Leaf level. WUE, the so-called intrinsic water use efficiency, is defined as the simultaneous ratio of net carbon assimilation to water transpiration of the stomata from a leaf (WUE,=A/E). This is the WUE, of the photosynthetic process. 2) Whole plant level. WUE is defined as the ratio of the biomass produced to total water used. WUE at this level is always lower than Leaf Level WUE, because of the water loss associated with non-photosynthetic processes and respiratory carbon loss during conversion of initial photosynthate to standing biomass. 3 ) Stand or crop level. WUE is defined as the ratio of the biomass produced to total water inputs to the whole ecosystem (yieldtotal water input). At this level, WUE is further decreased by the fraction of total water inputs from rain or irrigation that is never taken up by the plants. Crop level WUE is of importance for economical considerations, and integrates processes at all levels. Much progress has already been made in improving crop level WUE by irrigation practices that are more efficient in timing, allocation, and delivery of water to minimize secondary runoff, seepage, and unproductive evaporation from the soil surface (Stanhill 1986; Tuong and Bhuiyan 1999). Breeding for plant characteristics that maximize water extraction capabilities, such as deep roots, high hydraulic capacities for water transport, and high stomatal conductance can sometimes increase crop level WUE simply by increasing total productive water use and consequently by decreasing the evaporation
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from the surface of the soil (Shan and Xu 1991). Improvements in plant level W E also hold the promise of gains in total crop WUE. WUE of individual C, crop plants often varies two-to-three folds among genotypes grown under common conditions, and even more among wild plants (Rounick and Winterbourn 1986; Brooks el al. 1997). WUE of crops is generally low compared to many wild species (Franks and Farquhar 1999). Despite the obvious opportunities for improved production under water limiting conditions, breeding efforts for plant and leaf level WUE have achieved only limited success (Johnson and Li 1999). One reason why progress is lagging in this area is that some key traits at the leaf level usually have counteracting effects on the opposite parameters, such as the ratio of total water usage to efficient water usage (Udayakumar et al. 1998). For example, maximizing total water use generally involves high stomatal conductance, whereas low stomatal conductance favors high ratio of carbon gain to water loss. Classical selection for yield in field trials most often select to increase total water use, even at the cost of leaf level WUE. Attempts to select high WUE are also directly confounded by unintended side effects (Johnson and Li 1999; Rowe 1995). More effective breeding strategies for WUE require a better understanding of the underlying genetics controlling WUE, and their pleiotropic effects on the related traits of total water capture and/or photosynthetic capacity. In contrast to the W E at whole plant and crop levels, the W E at leaf level represents the physiological parts of the photosynthetic process, and may explain the majority of variance in the whole plant level WUE. Furthermore, to understand how photosynthesis affects WUE, many problematic pleiotropic effects related to the photosynthetic process and WUE must be explained and resolved, for example, how stomata behavior controls the ratio of fixed CO, and lost water vapor.
INSTRINSIC WATER USE EFFICIENCY Water is essential for growth in higher plants, and most of the water absorbed by plants is lost during the gas exchange processes. A normal plant growing in temperate climates requires 700- 1 300 mol H,O for the fixation of I mol CO, (Heldt 1997). However, plants differ in their capacity to regulate the amount of carbon that
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is gained per unit of water lost. Such differences can be referred to as differences in intrinsic water use efficiency, WUE,, which is defined as the ratio of instantaneous rate of CO, assimilation and transpiration (Condon et al. 2002). According to Fick’s law, the intrinsic water use efficiency can be described by a relatively simple equation (Eq. l):
Both A (CO, assimilation rate) and E (transpiration rate) are the product of two factors: stomata conductance (g) for either CO, (gc) or water vapor (g,) and the concentration difference of either CO, (caand ci) or water vapor (wa and wi) between the air outside and inside the leaf. Because H,O and CO, share a common diffusion pathway between the leaf intercellular airspaces and the atmosphere, A/E in leaf level WUE is directly related to the relative magnitudes of the respective diffusion gradients (Farquhar et al. 1989) (Eq.2):
WUET=
ca-ci 1.6 (wi-wa)
Where the factor 1.6 refers to the relative diffusivities of CO, and water vapor in air. In C, plants, the variation in ci is often considered in physiological studies as intrinsic WUE to distinguish this plant trait from the background effects of environ-
2
1
-
IntercellularCOI concentration
mental conditions that also have a strong effect on actual WE,. Because the internal air spaces of a leaf are always close to being saturated with water vapor, wi is determined mainly by leaf temperature. To the first approximation, wi is determined primarily by environmental air temperature, however, wi may also be controlled by the plant itself during the opening and closing of the stomata. It is true that the ca (CO, concentration in atmosphere) is constant and cannot be controlled by plants, then Eq.2 indicates that WUE, is negatively correlated with ci (the intercellular CO, concentration), for a photosynthesizing leaf of nonstressed C, plants, the ratio of ci to ca is typically around 0.7 (Farquhar et al. 1989), this “operating” value of ci/cais determined by the balance between stomatal conductance and photosynthetic capacity. Although stomatal conductance (g,> does not appear explicitly in Eq.2, the ratio of the biochemical potential for carbon fixation to stomatal conductance represents the balance between the supply of CO, and its consumption and determines ci (Farquhar and Sharkey 1982). Therefore, stomatal conductance influences the supply of CO, to the intercellular spaces of leaf, whereas photosynthetic capacity determines the demand for CO,. Fig.-A, B show a typical intercellular CO, response curve (A-ci curve) that is measured under saturating light intensity. Under low CO, supply, the CO, assimilation rate is limited by the activity of Rubisco and under high CO, supply, the CO, assimilation rate is limited by the regeneration rate of RuBP,
L
1
Intercellular CO, concrnlratlon
+
Fig. A schematic illustration demonstrating the dependence of ci on the relationship between stomatal conductance and CO, assimilation rate. Both figures describe the two possible approaches to increase W W . Fig.-A (left) shows increased WUE via increased carboxylation efficiency (initial slope of the A-c, curve) and constant stomatal conductance (the solid line). Fig.-B (right) shows the increased WUE via stomatal closure with constant carboxylation efficiency (Guo 2001).
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and this is further limited by triose-phophate utilization under the highest CO, supply in the A-CO, response curve (Farquhar et al. 1982; Sage et al. 1988). The initial slope of the curve is defined as carboxylation efficiency. The solid lines are connected by two CO, concentrations (ambient and corresponding intercellular CO, concentration), and the initial slope of solid lines is defined as the stomatal conductance ( g c ) . As shown in Fig.-A and B, it is theoretically possible to improve WUE, either through lowering stomatal conductance to water or raising photosynthetic capacity (related to carboxylation efficiency) or a combination of both. In Fig.-A, if stomatal conductance remains unchanged, increased WUE, can be achieved by the enhancement of carboxylation efficiency. In contrast, in Fig.-B, if stomata of a given leaf close and its carboxylation efficiency (the initial slope of a A-c, curve) remains constant, c, decreases and WUE, increases, but it will be at the cost of a reduced assimilation rate because of increasingly limiting substrate levels. However, this is only a potentially desirable outcome and it requires a higher supply of nitrogen and other nutrients per unit leaf biomass. Another possibility to increase WUE, is to control the luxurious transpiration, as shown by Wang and Liu (2003). There was a parabola relationship between CO, assimilation rate and transpiration rate, and the transpiration rate at the maximal CO, assimilation rate was a critical value, therefore it is possible to increase WUE, by controlling this luxurious transpiration without affecting the CO, assimilation rate. As discussed above, although the variation of WUE, at the leaf level is always associated with changes in C,, this can also occur through numerous mechanisms, such as changes in stomatal conductance, carboxylation efficiency etc. Stomata1 regulation is a complex process involving several pathways (Grabov and Blatt 1998; Pei et al. 1998), all of which can condition WUE,. This coordinated control involves stomatal responses to C, (Mott 1990; Leymarie et al. 1998), light (Wang and Liu 2003; Zeiger and Zhu 1998),relative humidity (Grantz 1990; Comstock and Ehleringer 1993; Meinzer et al. 1997), hormonal signals (Hartung et al. 1998; Jia and Zhang 1999), and nutritional status (Guo et al. 2005; Dood et al. 2003; Frederick and James 1997), for example, under ammonium nutrition, rice plants had a higher WUE, than that under the mixture of ammo-
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nium and nitrate and sole nitrate nutrition (Guo et al. 2005). This phenomenon might be caused by the difference of nitrogen accumulation in the leaves between different nitrogen forms of nutrition (Zhou er al. 2006a). Stomata have also been shown to reflect directly to leaf water potential (Saliendra et al. 1995; Fuchs and Livingston 1996; Comstock 2000b). The leaf water potential could affect stomatal behavior either through variation in the water potential-sensing mechanism in the leaf or via changes in the hydraulic architecture of the plant, which determines the functional dependence of leaf water potential on E. The latter includes both relative biomass allocation to different organs, anatomical features (i.e., vessel diameter) of the xylem determining conducting efficiency and cavita.tion vulnerability (Sperry et al. 1998; Mencuccini et al. 2000; Comstock 2000a), and the distribution of aquaporins in the leaf and root tissues (i.e., aquaporin located in the plasma membrane of root tissue plays a key role in root water absorption) (Tyerman et al. 1999, Clarkson et al. 2000). Turgor maintenance by osmotic adjustment is important both as the proximal mechanism of stomatal opening (Talbott and Zeiger 1996; Asai er ul. 2000) and in determining the tolerance of leaf mesophyll tissues to reduced leaf water potential (Zhang et af. 1999). CO, must diffuse inward, beyond the shared pathway of the stomatal pore to reach the chloroplasts. Tissue and subcellular organization and features such as the distribution and amount of carbonic anhydrase (invert CO, into carbonate or bicarbonate) influence the resistance to the liquid-phase movement of CO, to the sites of carboxylation (the resistance of CO, to liquid-phase is 1000 times higher than to air phase) (Evans and von Caemerer 1996; Scartazza et al. 1998). Once CO, has entered the chloroplast, the carboxylation capacity is related to the RuBPCase activity and light-harvesting capacities (Asai et al. 2000). Both of these components are expensive in terms of nitrogen investment, and the RuBPCase alone can be as much as half of all the soluble proteins in the leaf (Farquhar er af. 1980). From Fig., carboxylation efficiency plays an important role in increasing WUE,. Thus, any environmental and nutritional factors that influence RuBPCase content and activity may contribute to WUE,and WUE. Under light drought stress, WUE can be enhanced by the adjustment of nutritional management, even for
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Some Physioloeical Processes Related to Water Use Efficiency of Higher Plants
paddy rice plants (Zhou et af.2005, 2006a). It is therefore estimated that light drought stress may play an important role in increasing WUE. With regard to the plant nutrition, it has been demonstrated that nitrogen, phosphate, and potassium may influence W E , however, it still remains open as to how the mechanism is functioning to adjust the nutritional status in order to increase WUE and WUE, (Zhou et al. 2006b). It is hypothesized that nutritional factors may adjust the process involved in the WUE, such as root depth, leaf area, stomatal conductance, etc.
WUE, AND CARBON ISOTOPE DISCRIMINATION The efficacy of the use of d l T as an indicator of WUE, has been firmly established under both greenhouse and field conditions (Farquhar et af. 1982; Faquhar and Richards 1984; Hubick and Farquharl989). It obviates the prohibitive need for measurements of water budget for a large number of individuals during large-scale screening. This technique, based on the natural abundance of stable carbon isotopes, takes advantage of the naturally occurring variation in the isotopic composition of plants, and does not require specific labeling. Briefly, CO, in air naturally contains two stable isotopes of carbon, I2Cand I3C,in an approximate of 99% to 1 %, and it is in the form of I T , but the isotope ratio, l3C/I2C,is smaller in plant organic carbon than in atmospheric CO, because of the discrimination against I3C (by the dominant enzyme Rubisco) during photosynthetic uptake. The theoretical model describing fractionation during C, photosynthesis was developed by Farquhar et uf. ( I 989). The simplest form of the model is:
A = a + (b-a)'
C
ca
(3)
Where A represents the total difference in isotopic composition between photosynthetically fixed carbon and that in the atmosphere, and a and b are the fractionation constants associated with diffusion versus carboxylation and have values of 4.4 and 27%0(per mill), respectively (Farquhar et af. 1989). It is clearly shown in Eq. 3 that D is positively correlated with the ratio of ci to ca, whereas, as mentioned before, WUE, is nega-
407
tively correlated with the ratio of cI to ca.Therefore, D and W E , are negatively correlated. Coming back to the biochemical and physiological process explaining the relationship between D and WLJE,, when the stomata are widely open, there is ample CO, in the stomatal cavities and at the carboxylation site, the photosynthetic enzyme Rubisco can distinguish pronounced ' T O , against l3CO,, and uses '*CO, in preference to ' T O , as the substrate. On the other hand, as stomata are closed, the photosynthetic process is limited by CO, availability at the carboxylation site. Rubisco will fix ' T O , and ' T O , and consequently there is less discrimination, and the measured D in the leaf tissue is higher (Farquhar et al. 1989). The mechanistic validity of the isotopic behavior embodied in &. 3 has been verified for many crops and wild plant species (Hubick et ul. 1988; Ehleringer et al. 1991; Livingston ef al. 1999). The negative linear relation between WUE, and A has also been shown to hold for numerous crops, even when WUE, was measured on potted material at the whole plant level (Farquhar and Richards 1984; Hubick and Farquhar 1989; Martin et af. 1999) or in open field plantings (Knight et af. 1994; Saranga et ul. 1998). Other potential factors, such as variation in the efficiency of respiration in the conversion of photosynthate to new biomass, or nonphotosynthetic water loss will also affect WUE,, or the process of carbon fixation by PEPCase, but variation arising from such traits seems to be smaller than that associated with the photosynthetic process itself.
WUE, AND WATER CHANNEL (AQUAPORIN) The study of plant WUE, is complicated because several processes are involved, not only the leaf parameters (leaf area, transpiration rate, and stomatal conductance), but also the parameters of root and stem such as: root amount and extend, hydraulic conductance of root and stem, the capacity of water uptake of roots, and the pathway of radial water transport across the root. The most important parameters related to plant itself are hydraulic conductance of stem and root, and aquaporin of roots (Maurel and Chrispeels 2001 ; Javot and Maurel2002); however, there is little experimental evidence showing how these parameters influence the plant WUE,. Theoretically, the stem has diverted water
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to the leaf, from where it transpires. Water is delivered to the stem by the root, therefore the capacity of root water uptake and the hydraulic conductivity of root and stem might significantly affect the leaf water status and further stomatal conductance and transpiration rate. For example, with a lower hydraulic conductivity, rice plants suffer from water shortage in the shoot even in flooded fields (Miyamoto et al. 2001). Generally, the increase in hydraulic conductivity is illustrated as being correlated with increased aquaporin activity and gene expression (Clarkson et al. 2000; Maurel and Chrispeels 2001). The capacity of root water uptake depends dominantly on the activity of the water channel (aquaporin)(Chrispeelsand Maurel 1994; Kaldenhoff et al. 1998;Quintero et al. 1999).Aquaporin is a general designation of membrane channel proteins that regulate the water transport across the plasma membrane (Maurel and Chrispeels 2001). The contribution of aquaporin to whole plant water relation may account up to 85%. The water channel activity is regulated by phosphorylation, pH, pCa, osmotic gradients, and some nutrient’s (i.e., N and P) stress (Clarkson et al. 2000). The activity of aquaporin can be reversibly inhibited by HgCl, (Quintero et u1. 1999; Baiges et al. 2002; Zhang and Tyerman 1999). It has been testified that aquaporin plays a significant role in water status in higher plants in response to drought stress (Martre et al. 2002). For example, tobacco plants impaired in NtAQP1 expression (resulting in low aquaporin activity) show reduced root hydraulic conductivity, transpiration rate, and thus lower water stress resistance (Siefritz et ul. 2002), therefore, tobacco plants impaired in NtAQP1 suffer from water stress under wetted soil. It is suggested that under water stress, some root water channels are switched off (North and Nobel 2000), as some root aquaporin (PIP) gene is downregulated. Therefore, it may be argued whether the first responsibility to drought stress could have resulted from stomatal closure or from the expression of aquaporin downregulation. The argument still remains open whether a higher WUE, is associated with a higher activity andor gene expression of aquaporin, as there is a complicated transport pathway of water transport across the roots (Steudle 2000). The assumption based on the associa-
tion between root water absorption and delivery, and leaf transpiration relies on the critical water absorption (Steudle and Henzler 1995).
THE RELATIONSHIP BETWEEN WUE AND YIELD Generally, at the crop and whole plant level, WUE is linearly correlated to the biomass under limited water condition. On the other hand, under a condition of sufficient water supply, W E is not always linearly correlated to the biomass or economic yield. For example, there was a parabola relationship between the grain yield and WUE of maize (Liu 1998), and the maximal WUE came earlier than the maximal yield with a rise in transpiration rate. At the leaf level, the relationship between W E , and yield is variable among crop systems, and depends on environmental factors, such as, water availability limiting the growth and variation in the underlying genetics conditioning the variations in WUE. In many cases examined, A is seen to be positively correlated to the yield and W E itself is negatively correlated, especially under conditions of ample water availability (White et al. 1994). This is what was expected when variation in A was being caused primarily by variation in stomatal opening, and low WUE was associated with greater total water use and higher A (Eqs. 1, 2). Contrasting cases have also been reported where yield was positively correlated with WUE (Musick et al. 1994). This is expected when moderate water deficits make higher efficiency (Martin er al. 1999) and when variation in W E is caused primarily by variation in carboxylation capacity (Livingston et al. 1999; Rao et al. 1995; Virgona and Farquhar 1996).
Acknowledgements This study was supported by the National Basic Research Program of China (2005CB121101), and the National Natural Science Foundation of China (30400279). This paper is in memory of Prof. Dr. Burkhard Sattelmacher (08,6,1947- 1 1,21,2005).
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