JXB Advance Access originally published online on November 1, 2005
Journal of Experimental Botany 2005 56(422):3033-3039; doi:10.1093/jxb/eri300
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
Oxygen isotope enrichment (
18O) as a measure of time-averaged transpiration rate
1Department of Crop Physiology, University of Agricultural Sciences, GKVK Campus, Bangalore 560065, India
2Planetary and Geosciences Division, Physical Research Laboratory, Ahmedabad, 380 009, India
3Department of Physics, University of Agricultural Sciences, GKVK Campus, Bangalore 560065, India
* To whom correspondence should be addressed. Fax: +91 80 23636713. E-mail: msheshshayee{at}hotmail.com
Received 1 July 2005; Accepted 26 August 2005
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Experimental evidence is presented to show that the 18O enrichment in the leaf biomass and the mean (time-averaged) transpiration rate are positively correlated in groundnut and rice genotypes. The relationship between oxygen isotope enrichment and stomatal conductance (gs) was determined by altering gs through ABA and subsequently using contrasting genotypes of cowpea and groundnut. The Peclet model for the 18O enrichment of leaf water relative to the source water is able to predict the mean observed values well, while it cannot reproduce the full range of measured isotopic values. Further, it fails to explain the observed positive correlation between transpiration rate and 18O enrichment in leaf biomass. Transpiration rate is influenced by the prevailing environmental conditions besides the intrinsic genetic variability. As all the genotypes of both species experienced similar environmental conditions, the differences in transpiration rate could mostly be dependent on intrinsic gs. Therefore, it appears that the
18O of leaf biomass can be used as an effective surrogate for mean transpiration rate. Further, at a given vapour pressure difference, 18O can serve as a measure of stomatal conductance as well. Key words: ABA, groundnut, mean transpiration rate, 18O enrichment, rice, stomatal conductance
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Plant biomass production is determined by the total water used and the water use efficiency (WUE, ratio of net CO2 assimilation rate to the transpiration rate), especially under water-limited conditions (Passioura, 1976
). Since water availability is the most important constraint, particularly in the semi-arid tropics, increasing WUE is regarded as one of the potential approaches to improve crop yields. Recent efforts in selecting wheat genotypes with improved WUE resulted in higher productivity under water-limited conditions (Condon et al., 2002, Rebetske et al., 2002; Richards et al., 2002). In these genotypes, the higher WUE was achieved through a reduction in stomatal conductance (gs). The gs regulates CO2 entry for photosynthesis besides controlling transpiration rate. Hence when gs is reduced, although transpiration decreases, it also hinders CO2 entry. Most often an increase in WUE is associated with reduced gs which can be counterproductive in terms of biomass accumulation (Udayakumar et al., 1998a; Sheshshayee et al., 2003). Therefore, from the agricultural point of view, it is essential to increase WUE without compromising transpiration. Such genotypes would possess superior mesophyll efficiency to assimilate CO2 and hence need to be identified so as to have a distinct advantage in improving agricultural productivity.
To this end it becomes imperative simultaneously to determine the genetic variability in WUE and transpiration in plants. Carbon isotope discrimination (13C) has been well established as a time-averaged surrogate for WUE (Farquhar and Richards, 1984; Farquhar et al., 1989), The application of the carbon isotope discrimination technique to assess the genetic variability in WUE has been examined and validated in container and field experiments in several crop species such as cowpea (Ashok et al., 1999; Aniya and Herzog, 2004), wheat (Condon and Hall, 1997; Richards et al., 2002; Condon et al., 2004), groundnut (Wright et al., 1988; Rao, et al., 1995; Bindumadhava et al., 2003), and rice (Sheshshayee et al., 2003; Impa et al., 2005).
Similarly, the enrichment of the heavy isotope of oxygen in leaf water (or that of the biomass) relative to the source water is being adopted to assess variations in transpiration rate and stomatal conductance (gs). Although the theory explaining the phenomenon of oxygen isotopic enrichment during the evaporation of water from the ocean surface has been known for almost three decades (Craig and Gordon, 1965), the application of this theory to predict differences in gs and transpiration rate has been fairly recent (Flanagan et al., 1991b, 1994; Farquhar and Lloyd, 1993; Bindumadhava et al., 1999; Bindumadhava, 2000). However, discrepancy between the Craig–Gordon prediction and the measured 
18O of the leaf water has been reported (White et al., 1994; Buhay et al., 1996). Further, the relationship between stomatal conductance and leaf water 18O enrichment has remained equivocal (see Discussion), although increased transpiration has clearly been shown to enrich leaf water 18O (Gonfiantini et al., 1965; DeNiro and Epstein, 1979).
The major objective of the investigation was to show that the 18O enrichment in the biomass can be used as a surrogate for the mean transpiration rate by a re-examination of the relationship between 18O and stomatal conductance. This relationship was tested both under field and growth chamber conditions.
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Plants were grown under well-watered conditions in containers (60x45x30 cm) having 20 kg of red sandy loam and farmyard manure mixed in a 3:1 (v/v) proportion. The containers were arranged randomly in open field conditions, adequate plant nutrients were supplied once a month, and prophylactic measures were taken as and when required to raise healthy plants. All experiments were conducted at the Department of Crop Physiology, GKVK Campus, University of Agricultural Sciences, Bangalore, India (12° 58' N and 77° 35' E).
Alterations in stomatal conductance using abscisic acid (ABA)
Petioles of sunflower (KBSH-1) leaves from 35-d-old plants were excised under water and immediately placed in a test tube containing 15 ml of ABA solution (cis-trans ABA; Sigma, USA). Sets of four leaves were maintained at different ABA concentrations (ranging between 10–4 M and 10–7 M and a control without ABA) and allowed to transpire in a controlled growth chamber under a vapour pressure deficit (VPD) of 15 mbar and a PPFD of 1200 µmol m–2 s–1 (400–700 nm). The leaves were initially allowed to transpire up to 10 ml of the solution to flush out the leaf water. The time taken for leaves to transpire an additional 10 ml of the solution was recorded and transpiration rate was calculated after measuring the leaf area. The leaf water was extracted immediately for determining its 18O. The 18O enrichment in leaf water (18O) relative to that of the distilled water (18O of distilled water was –13.3 
).
Genotypic variations in stomatal conductance among cowpea genotypes
Based on the results of a previous experiment (Sheshshayee, 1998), a few cowpea genotypes with variable gs and transpiration rates were identified and raised in containers under well-watered condition in an open field. Stomatal conductance (gs) and transpiration rate of the third fully expanded leaf from the apex of 45-d-old plants were measured using a portable gas exchange system (LCA-4, ADC, Hoddesdon, EN11, ODB, UK). The temperature and RH of the leaf chamber were maintained close to those of ambient air. The mean natural light intensity was 1600 µmol m–2 s–1. All observations were recorded between 09.00 h and 11.30 h (Indian standard time).
Extraction of leaf water
Immediately after determining gas exchange, holes were punched, avoiding the major veins, and placed in tapering plastic tubes and immediately closed using rubber stoppers. The tubes were purged with pure, dry nitrogen gas and frozen to the liquid nitrogen temperature of –196 °C for 20 min. The tubes were transferred to a hot water bath (80 °C) and, after 10 min of thawing, the tubes were centrifuged at 5000 rpm for 5 min. The leaf water that collected at the tapering end of the tube was drawn out using a syringe and an aliquot of 200 µl was immediately introduced into a 10 ml vacutainer tube (Becton Dickinson vacutainer systems, USA). The tubes were air-tight and all the leaf water was collected instantly; care was taken to keep the fractionation that might occur during the extraction process to be minimal. Unlike the ‘classical’ method of extraction of leaf water by pumping, the present method does not cause significant isotopic fractionation due to incomplete extraction.
Determination of 18O of leaf water
The 18O composition of the leaf water was determined by CO2-equilibration technique (Scrimgeour, 1995). CO2 gas of known oxygen isotopic composition was introduced to the head-space volume of the vacutainer tube containing leaf water and equilibrated overnight at 30 °C. The CO2 was then introduced into the mass spectrometer (Tracermass, PDZ-Europa, UK) for the determination of 18O on a continuous flow mode. The 18O of the source water (used for irrigating the plants) was also similarly determined. The analytical uncertainty was typically ±0.15 .
The 18O enrichment in the leaf water over the source water (18Olw) was computed as follows.
 |
18O is the isotopic composition compared with VSMOW (Vienna-Standard Mean Ocean Water) and the subscripts lw and iw refer to leaf water and irrigation water, respectively (for the experiment with ABA solution the 18O of the distilled water was used).
Gravimetric determination of variability in mean transpiration rate (MTR) in rice and groundnut genotypes
The mean transpiration rate (MTR) was determined gravimetrically (Udayakumar et al., 1998b) in selected genotypes of rice and groundnut in separate experiments. Both the experiments were carried out between January and April 2002. The experimental season was characterized with a mean temperature of 30.6 °C (maximum), 17.2 °C (minimum) and a VPD of 15 mbar. The natural photon flux density was 1600 µmol m–2 s–1. Briefly, the gravimetric method involved weighing the containers daily using a mobile weighing device for a period of 30 d. The container weight was brought back to field capacity daily by adding water. The amount of water added over the experimental period was summed to arrive at the total evapotranspiration (ET). A mobile rain out shelter was moved over the experimental area during nights and rain episodes to maintain a specific water regime in the containers. The soil surface of all the containers was covered with plastic pieces to minimize surface evaporation. Simultaneously, ‘bare’ containers (without plants) were also weighed to quantify the evaporation component (Es) of ET. Cumulative water transpired (CWT) over the experimental period was calculated as the difference between ET and Es. The MTR was computed from the ratio of CWT to the leaf area duration (LAD=(LA1+LA2)/2x30 d, where, LA1 and LA2 are leaf areas at the beginning and end of the experiment, respectively).
Determination of 18O in leaf biomass
The leaves of rice and groundnut genotypes that matured during the experimental period were separately harvested and oven-dried at 70 °C for 72 h). Finely ground dry leaf powder (0.8–1.2 mg) was taken to determine 18Olb by on-line pyrolysis using TC/EA interfaced with an IRMS (Delta Plus, ThermoFinnigan, Bremen, Germany) through a continuous flow device (Conflo-III, ThermoFinnigan, Bremen, Germany) at the National Facility for Stable isotope studies, Department of Crop Physiology, University of Agricultural Sciences, Bangalore, India. The analytical uncertainty of isotope measurements was less than 0.2 .
The 18O enrichment in leaf biomass (18Olb) was computed as follows:
 |
Statistical analysis
Analysis of variance (ANOVA) for all the experiments was computed for a completely randomized design using MSTAT-C software. The geometric mean regression (Model-II) was used to plot all relationships.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Stomatal conductance (gs) and 18O enrichment
The plant hormone abscisic acid (ABA) induces stomatal closure and, accordingly, excised leaves of sunflower (KBSH-1) fed with the highest concentration of ABA (10–4 M) recorded the lowest transpiration rate, which increased as the ABA concentration decreased.
18Olw also showed a very similar pattern. A strong positive correlation between transpiration rate (TR) and 18Olw was evident (Fig. 1).
|
To examine this relationship further, the stomatal conductance of leaves of a few contrasting cowpea genotypes was determined with a gas exchange system. A significant genotypic variability in gs and
18Olw was noticed in this set of cowpea genotypes (Table 1). The 18Olw showed a significant positive relationship with gs (R2=0.90; P <0.05; n=5) reconfirming the stomatal control of 18O enrichment.
|
Genetic variability in
18O, stomatal conductance and mean transpiration rateGas exchange parameters are snap-shot measurements and do not integrate the diurnal as well as the day to-day variations in transpiration rate and gs. Similarly, the 18O composition of the leaf water also varies significantly in time. The transfer of the 18O signature from leaf water into cellulose/biomass has been well elucidated (Sternberg et al., 1986
). The 18O enrichment of the leaf biomass relative to source (18Olb) can serve as a measure of mean (time-integrated) transpiration rate (MTR). The latter was gravimetrically determined for rice and groundnut in separate experiments over an extended period of 30 d. Significant genotypic variability in MTR was noticed in both the crop species (Table 2). Since the biomass formation is continuous, the 18Olb should be a time integrated measure of 18Olw. Therefore, the relationship between the MTR and 18Olb among the genotypes was examined and a significant positive relationship was found (Fig. 2). As the leaf biomass and not the cellulose was analysed, it could be argued that the differences in organic composition among genotypes could possibly account for the observed variability in 18Olb especially in the long-term experiment. However, this can be safely ruled out because (i) the bulk of the dry matter of the leaf (>70%) is cellulose and (ii) the remaining components are not isotopically very different, especially in the same species of plants. It was apparent from Fig. 2 that the slopes of the regression between 18O and MTR were different for groundnut and rice. The difference could arise due to significant variations in the leaf structural composition and architecture of these two species.
|
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
The first mechanistic explanation for the evaporative enrichment of 18O in large water bodies was provided by Craig and Gordon (1965)
. This theory was extended by several models to predict the 18O enrichment in leaf water (Flanagan et al., 1991b, 1994; Flanagan, 1993; Farquhar and Lloyd, 1993; Roden and Ehleringer, 1999).
 |
18Oe is the 18O enrichment in the leaf water at the site of evaporation relative to source water, 
* and k are the equilibrium and kinetic (oxygen isotopic) fractionation factors, respectively (expressed in per million units), 18Ov, the 18O enrichment of the atmospheric water vapour relative to the source water, and ea, ei, the partial pressures of water outside and inside the leaf, respectively.
However, it was observed that the actual oxygen enrichment in bulk leaf water (18Olw) was less than that predicted by the Craig–Gordon theory (Allison et al., 1985; Leaney et al., 1985; Flanagan et al., 1991a, b; Wang and Yakir, 1995; Barbour et al., 2002). To explain this discrepancy, several modifications have been attempted. Leaney et al. (1985) considered ‘two pools’ of water in a leaf. The first pool is an enriched fraction due to evaporation and the second, the unfractionated xylem water pool. The ‘Peclet model’ of Farquhar and Lloyd (1993) and Barbour et al. (2000) account for the progressive variation of leaf water enrichment along the leaf mesophyll tissue due to convective and diffusive mixing of the enriched water and the unfractionated xylem water. The ‘string-of-lakes’ model (Gat and Bowser, 1991; Yakir, 1992; Helliker and Ehleringer, 2000, 2002) provides for the spatial variation in 18O across the entire leaf surface. The string-of-lakes model argues that the enriched leaf water would gradually flow into the xylem thus spatially altering the source water isotopic composition. It is to be noted that, in general, (i) all these models deal with steady-state fluxes of water from the stem to the leaf, from the leaf to the boundary layer, from the boundary layer to the atmosphere, and (ii) they do not address the effect of stomatal response to the atmospheric water vapour deficit, unlike Lindroth and Halldin (1986) who suggest an empirical relation. Recently, a non-steady-state model was proposed by Farquhar and Cernusak (2005); according to these authors, the model ‘is less important during the day and hence for determining the 18O enrichment in organic matter’.
In some earlier experiments it was observed that the 18O enrichment in the leaf water was directly proportional to the transpiration rate (Walker et al., 1989; Yakir et al., 1990; Yakir, 1998). Gan et al. (2002) showed that the leaf water as well as the leaf organic matter 18O was significantly higher in the leaves exposed to lower RH, which indicated that the 18O enrichment linearly increased with transpiration rate. A lower stomatal conductance (gs), at a given VPD, is also known to reduce the transpiration rate and hence 18O enrichment (Fig. 1 of Wang and Yakir, 1995). Our results are consistent with these, but they contrast with the trend reported for the relationship between leaf water enrichment and transpiration among wheat genotypes (Barbour et al., 2000).
A simplified Peclet model developed by Fraquhar and his coworkers (Barbour and Farquhar, 2000) was obtained from Dr Margaret Barbour and the predicted 18O was determined. Several input parameters such as fractionation caused during diffusion through stomata (32 ) and through the boundary layer (21 ) were considered (Cappa et al., 2003) in the model. The source water of the GKVK tube well used for irrigation was –3.7 . The oxygen isotopic enrichment over the source water was estimated using the model. Figure 3 clearly demonstrates that the mean groundnut and rice values of the predicted 18Olb (31.7 and 31.7 ) and the measured 18Olb (32.1 and 31.9 ), respectively, match very well. However, the model is unable to account for the full range of values: the predicted values lie in a narrow range of 30–33 , whereas the observed values vary from 26–38 . A possible reason could be that several parameters used as inputs in the Peclet model, such as leaf and air temperatures, relative humidity, boundary layer and stomatal conductances, were measured at one single instance during the day. These values are known to fluctuate considerably diurnally and hence would influence the 18O enrichment in the leaf biomass in a cumulative fashion. Thus the measured 18O would vary more than that predicted by the model.
|
Even though the mean values are predicted well by the model, the observed positive correlation between transpiration rate and 18O enrichment in the leaf biomass (Fig. 2) cannot be explained by it. Buhay et al. (1996)
showed that k and gb depend on the nature of the boundary layer, influenced by wind speed and leaf temperature, while the shape/area of the leaf is also important. In this study's experiments all plants experienced the same wind speed and air temperature. The shapes of the leaves are also comparable within species. The dependence of the leaf water isotopic composition on the leaf temperature is of a small magnitude (Majoube, 1971). Therefore, it appears necessary to modify existing models to incorporate the stomatal response to changing VPD naturally. |
Conclusion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
In this work, it has been shown experimentally that there is a positive correlation between the transpiration rate (caused by stomatal conductance) and the oxygen isotope enrichment in leaf biomass in groundnut and rice genotypes that contrast with the observations of Barbour and Farquhar (2000)
. Transpiration rate can increase either because of increased stomatal conductance or when the vapour pressure difference between the leaf and air is increased. When the transpiration rate was altered by inducing differential stomatal closure through ABA, the 18Olw closely followed the changes in transpiration rate (Fig. 1). In addition, the genotypes varying in stomatal conductance showed similar variations in mean transpiration rate. The 18Olb, an integrated measure of the leaf water 18O values, showed a significant positive relationship with mean transpiration rate (Fig. 2). These results suggest that the 18Olb is a good time integrated measure of stomatal conductance. Existing models (such as the Peclet model) need to be modified to explain the observed positive correlation between transpiration rate and 18O enrichment in leaf biomass. |
Acknowledgements |
|---|
The authors thank two anonymous referees for constructive suggestions. Dr Anura V Kurpad, Head, Nutrition Division, Department of Physiology, St John's Medical College, Bangalore is thanked for his help during the initial stages of this work and Mr Shashidhar, G and Ms Impa S Muttappa for the help in conducting the groundnut and rice experiments. This work was funded by the Department of Science and Technology (DST), in the form of a Young Scientist project to MSS (HR/OY/B-03/96) and CSIR in the form of Senior Research Fellowship to HB [9/271(51)/96-EMR-1]. Financial assistance by DST and DBT (SP/IO/LF-01/98; BT/IS/06/004/98) is acknowledged. The assistance of Mr Nagabhushana and Mr A Ramesha in sample preparation and isotope analysis is acknowledged. Special thanks to Mr Ram Mhatre, of Thermo-electron for the maintenance of the IRMS.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionReferences |
|---|
Allison GB, Gat JR, Leaney FWJ. 1985. The relationship between deuterium and oxygen-18 delta values in leaf water. Chemical Geology 58, 145–156.
Aniya AO, Herzog H. 2004. Water use efficiency, leaf area and leaf gas exchange of cowpeas under midseason drought. European Journal of Agronomy 20, 327–339.[CrossRef]
Ashok RS, Aftab Hussain IS, Prasad TG, Udayakumar M, Nageswararao RC, Wright GC. 1999. Variations in transpiration efficiency and carbon isotope discrimination in cowpea (Vigna unguiculata (L.) Walp.) genotypes. Australian Journal of Plant Physiology 26, 503–510.
Barbour MM, Schurr U, Henry BK, Wong SC, Farquhar GD. 2000. Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean: evidence in support of the Peclet-effect. Plant Physiology 123, 671–679.
Barbour MM, Farquhar GD. 2000. Relative humidity and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant, Cell and Environment 23, 473–485.
Barbour MM, Walcroft AS, Farquhar GD. 2002. Seasonal variation in 13C and 18O of cellulose from growth rings of Pinus radiata. Plant, Cell and Environment 25, 1483–1499.[CrossRef]
Bindumadhava H, Sheshshayee MS, Devendra R, Prasad TG, Udayakumar M. 1999. Oxygen (18O) isotopic enrichment in the leaves as a potential surrogate for transpiration and stomatal conductance. Current Science 76, 1427–1428.
Bindumadhava H. 2000. Oxygen (18O) and carbon (13C) isotope composition in plants: an approach to quantify transpiration and mesophyll factors associated with water use efficiency. Unpublished PhD thesis, University of Agricultural Science, Bangalore. India.
Bindumadhava H, Sheshshayee MS, Shankar AG, Prasad TG, Udayakumar M. 2003. Use of SPAD chlorophyll meter to assess transpiration efficiency in peanut. In: Breeding of drought-resistant peanuts. ACIAR Proceedings, 112, 3–9.
Buhay WM, Edwards TWD, Aravena R. 1996. Evaluating kinetic fractionation factors used for ecologic and paleoclimatic reconstructions from oxygen and hydrogen isotope ratios in plant water and cellulose. Geochimica et Cosmochimica Acta 60, 2209–2218.[CrossRef][Web of Science]
Cappa CD, Hendricks MB, DePaulo DJ, Cohen RL. 2003. Isotopic fractionation of water during evaporation. Journal of Geophysical Research 108, 4525–4534.[CrossRef]
Condon AG, Richards RA, Rebetzke GT, Farquhar GD. 2002. Improving intrinsic water use efficiency and crop yield. Crop Science 42, 128–133.
Condon AG, Hall KT. 1997. Adaptation to adverse environment; variation in water use efficiency within crop species; In: Jackson LE, ed. Ecology in agriculture. San Diego, USA: Academic Press, 79–116.
Craig L, Gordon LI. 1965. Deuterium and oxygen-18 variations in the ocean and the marine atmosphere. In: Tongiorgi E, ed. Proceedings of a conference on stable isotopes in oceanographic studies and paleotemperatures. Spoleto, Italy, 9–130.
DeNiro MJ, Epstein S. 1979. Relationship between oxygen isotope ratios of terrestrial plant cellulose, carbon dioxide and water. Science 204, 51–53.
Farquhar GD, Cernusak LA. 2005. On the isotopic composition of leaf water in the non-steady state. Functional Plant Biology 32, 293–303.[CrossRef]
Farquhar GD, Ehleringer JR, Hubick KT. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.[CrossRef][Web of Science]
Farquhar GD, Lloyd J. 1993. Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In: Ehleringer JR, Hall AE, Farquhar GD, eds. Stable isotopes and plant carbon-water relations. San Diego: Academic Press, 47–70.
Farquhar GD, Richards RA. 1984. Isotopic composition of plant carbon correlates with water use efficiency of wheat cultivars. Australian Journal of Plant Physiology 11, 539–552.[Web of Science]
Flanagan LB. 1993. Environmental and biological influence on the stable oxygen and hydrogen isotopic composition of leaf water. In: Ehleringer JR, Hall AE, Farquhar GD, eds. Stable isotopes and plant carbon-water relations. San Diego: Academic Press, 71–90.
Flanagan LB, Bain JF, Ehleringer JR. 1991a. Stable oxygen and hydrogen isotope composition of leaf water in C3 and C4 plant species under field conditions. Oecologia 88, 394–400.[CrossRef]
Flanagan LB, Comstock JP, Ehleringer JR. 1991b. Comparison of modelled and observed environmental influences on stable oxygen and hydrogen composition of leaf water in Phaseolus vulgaris L. Plant Physiology 96, 588–596.
Flanagan LB, Philips SL, Ehleringer JR, Farquhar GD. 1994. Effect of changes in leaf water oxygen isotopic composition on discrimination against C18O16O during photosynthetic gas exchange. Australian Journal of Plant Physiology 21, 221–234.
Gan KS, Wong SC, Yong JWH, Farquhar GD. 2002. 18O spatial patterns of vein xylem water, leaf water and dry matter in cotton leaves. Plant Physiology 130, 1008–1021.
Gat JR, Browser C. 1991. The heavy isotope enrichment of water in coupled evaporative systems. In: Taylor HP, O'Neil JR, Kaplan IR, eds. Stable isotope geochemistry: a tribute to Samuel Epstein. Lancaster, UK: The Geochemical Society, 159–168.
Gonfiantini R, Gratziu S, Tongiorgi E. 1965. Oxygen isotopic composition in leaves. In: Use of isotopes and radiations in soil-plant nutrition studies. Technical Report Series No. 206. Isotopic Atomic Energy Commission, Vienna, 405–410.
Helliker BR, Ehleringer R. 2000. Establishing a grassland signature in veins: 18O in the leaf water of C3 and C4 grasses. Proceedings of National Academy of Sciences, USA 97, 7894–7898.
Helliker BR, Ehleringer R. 2002. Differential 18O enrichment of leaf cellulose in C3 versus C4 grasses. Functional Plant Biology 29, 435–442.[CrossRef]
Impa SM, Nadaradjan S, Boominathan P, Shashidhara G, Bindumadhava H, Sheshshayee MS. 2005. Carbon isotope discrimination accurately reflects variability in WUE measured at a whole plant level in rice (Oryza sativa L.). Crop Science (in press).
Leaney F, Osmond C, Allison G, Ziegler H. 1985. Hydrogen-isotope composition of leaf water in C3 and C4 plants: its relationship to the hydrogen isotope composition of dry matter. Planta 164, 215–220.[CrossRef]
Lindroth A, Halldin S. 1986. Numerical analysis of pine forest evaporation and surface resistance. Agricultural and Forest Meteorology 38, 59–79.[CrossRef]
Majoube M. 1971. Fractionnement en oxygene 18 et en deuterium entre l'eau et sa vapeur. Journal of de Chimie Physique et de Physico-Chimie Biologique 58, 1423–1436.
Passioura JB. 1976. Physiology of grain yield in wheat growing on stored water. Australian Journal of Plant Physiology 3, 559–565.
Rao RCN, Udayakumar M, Farquhar GD, Talwar HS, Prasad TG. 1995. Variations in carbon isotope discrimination and its relationship with specific leaf area and Rubisco content in groundnut genotypes. Australian Journal of Plant Physiology 22, 545–551.
Rebetzke GJ, Condon G, Richards RA, Farquhar GD. 2002. Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rain-fed bread wheat. Crop Science 42, 122–127.
Richards RA, Rebetzke GJ, Condon AG, van Herwaarden AF. 2002. Breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereals. Crop Science 42, 111–121.
Roden JS, Ehleringer JR. 1999. Observations of hydrogen and oxygen isotopes in leaf water confirm the Craig–Gordon model under wide-ranging environmental conditions. Plant Physiology 120, 1165–1173.
Scrimgeour CM. 1995. Measurement of plant and soil water isotope composition by direct equilibration methods. Journal of Hydrology 172, 261–274.[CrossRef][Web of Science]
Sheshshayee MS. 1998. Dual isotope ratio (13C and 18O): an approach to assess mesophyll factors associated with WUE. Project report presented at group monitoring workshop in March 1998. Tiruvanathapuram, India: Tropical Botanical Garden and Research Institute.
Sheshshayee MS, Bindumadhava H, Shankar AG, Prasad, TG, Udayakumar M. 2003. Breeding strategies to exploit water use efficiency for crop improvement. Journal of Plant Biology 30, 253–268.
Sternberg LSL, DeNiro MJ, Savidge RA. 1986. Oxygen isotope exchange between metabolites and water during biochemical reactions leading to cellulose synthesis. Plant Physiology 82, 423–427.
Udayakumar M, Rao RCN, Wright GC, Ramaswamy GC, Ashok RS, Gangadhar GC, Aftab Hussain IS. 1998b. Measurement of transpiration efficiency in field conditions. Journal of Plant Physiology and Biochemistry 1, 69–75.
Udayakumar M, Sheshshayee MS, Nataraj KN, Bindumadahava H, Devendra R, Aftab Hussain IS, Prasad TG. 1998a. Why has breeding for water use efficiency not been successful? An analysis and alternate approach to exploit this trait for crop improvement. Current Science 74, 994–1000.
Walker CD, Leaney FW, Dighton JC, Allison GB. 1989. The influence of transpiration on the equilibration of leaf water with atmospheric water vapour. Plant, Cell and Environment 12, 221–234.[CrossRef]
Wang XF, Yakir D. 1995. Temporal and spatial variations in the oxygen-18 content of leaf water in different plant species. Plant, Cell and Environment 18, 1377–1385.[CrossRef]
White JWC, Lawrence JR, Broecker WS. 1994. Modeling and interpreting D/H ratios in tree rings: A test case of white pine in the Northeastern United States. Geochimica et Cosmochimica Acta 58, 851–862.[CrossRef][Web of Science]
Wright GC, Hubick KT, Farquhar GD. 1988. Discrimination in carbon isotopes of leaves correlate with water use efficiency of field-grown peanut cultivars. Australian Journal of Plant Physiology 15, 815–825.
Yakir D. 1992. Water compartmentation in plant tissue: isotopic evidence. In: Somero GN, Osmond CB, Bolis L, eds. Water and life. Berlin; Heidelberg, Germany: Springer-Verlag, 205–222.
Yakir D. 1998. Oxygen-18 of leaf water: a crossroads for plant associated isotopic signals: In: Griffiths H, ed. Stable isotopes: integration of biological and geochemical process. Oxford: BIOS Scientific Publishers, 147–168.
Yakir D, DeNiro MJ, Gat JR. 1990. Natural deuterium and oxygen-18 enrichment in leaf water of cotton plants grown under wet and dry conditions: evidence for water compartmentation and its dynamics. Plant, Cell and Environment 13, 49–56.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  L. Cabrera-Bosquet, G. Molero, S. Nogues, and J. L. Araus Water and nitrogen conditions affect the relationships of {Delta}13C and {Delta}18O to gas exchange and growth in durum wheat J. Exp. Bot., April 1, 2009; 60(6): 1633 - 1644. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. J. Hasselquist and M. F. Allen Increasing demands on limited water resources: Consequences for two endangered plants in Amargosa Valley, USA Am. J. Botany, March 1, 2009; 96(3): 620 - 626. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. A. Cernusak, K. Winter, J. Aranda, and B. L. Turner Conifers, Angiosperm Trees, and Lianas: Growth, Whole-Plant Water and Nitrogen Use Efficiency, and Stable Isotope Composition ({delta}13C and {delta}18O) of Seedlings Grown in a Tropical Environment Plant Physiology, September 1, 2008; 148(1): 642 - 659. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. S. Nemali and M. W van Iersel Physiological Responses to Different Substrate Water Contents: Screening for High Water-use Efficiency in Bedding Plants J. Amer. Soc. Hort. Sci., May 1, 2008; 133(3): 333 - 340. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J.I.L Morison, N.R Baker, P.M Mullineaux, and W.J Davies Improving water use in crop production Phil Trans R Soc B, February 12, 2008; 363(1491): 639 - 658. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. A. Cernusak, K. Winter, J. Aranda, B. L. Turner, and J. D. Marshall Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility J. Exp. Bot., October 1, 2007; 58(13): 3549 - 3566. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Karaba, S. Dixit, R. Greco, A. Aharoni, K. R. Trijatmiko, N. Marsch-Martinez, A. Krishnan, K. N. Nataraja, M. Udayakumar, and A. Pereira Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene PNAS, September 25, 2007; 104(39): 15270 - 15275. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. J. Thompson, J. Andrews, B. J. Mulholland, J. M.T. McKee, H. W. Hilton, J. S. Horridge, G. D. Farquhar, R. C. Smeeton, I. R.A. Smillie, C. R. Black, et al. Overproduction of Abscisic Acid in Tomato Increases Transpiration Efficiency and Root Hydraulic Conductivity and Influences Leaf Expansion Plant Physiology, April 1, 2007; 143(4): 1905 - 1917. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. D. Farquhar, L. A. Cernusak, and B. Barnes Heavy Water Fractionation during Transpiration Plant Physiology, January 1, 2007; 143(1): 11 - 18. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||