JXB Advance Access published online on January 31, 2008
Journal of Experimental Botany, doi:10.1093/jxb/erm314
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© 2008 The Author(s).
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RESEARCH PAPER |
Soil water deficits decrease the internal conductance to CO2 transfer but atmospheric water deficits do not
School of Biological Sciences, Heydon-Laurence Building A08, The University of Sydney, Sydney NSW 2006, Australia
* E-mail: charles.warren{at}bio.usyd.edu.au
Received 11 October 2007; Revised 9 November 2007 Accepted 15 November 2007
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Abstract |
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The internal conductance to CO2 supply from substomatal cavities to sites of carboxylation poses a large limitation to photosynthesis. It is known that internal conductance is decreased by soil water deficits, but it is not known if it is affected by atmospheric water deficits (i.e. leaf to air vapour pressure deficit, VPD). The aim of this paper was to examine the responses of internal conductance to atmospheric and soil water deficits in seedlings of the evergreen perennial Eucalyptus regnans F. Muell and the herbaceous plants Solanum lycopersicum (formerly Lycopersicon esculentum) Mill. and Phaseolus vulgaris L. Internal conductance was estimated with the variable J method from concurrent measurements of gas exchange and fluorescence. In all three species steady-state stomatal conductance decreased by
30% as VPD increased from 1 kPa to 2 kPa. In no species was internal conductance affected by VPD despite large effects on stomatal conductance. In contrast, soil water deficits decreased stomatal conductance and internal conductance of all three species. Decreases in stomatal and internal conductance under water deficit were proportional, but this proportionality differed among species, and thus the relationship between stomatal and internal conductance differed among species. These findings indicate that soil water deficits affect internal conductance while atmospheric water deficits do not. The reasons for this distinction are unknown but are consistent with soil and atmospheric water deficits having differing effects on leaf physiology and/or root–shoot communication. Key words: Carbon dioxide, drought, internal conductance, mesophyll conductance, photosynthesis, stomatal conductance, transfer conductance, vapour pressure deficit, water deficit
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConclusionsReferences |
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For photosynthesis (A) to occur, CO2 must diffuse from the atmosphere to the sites of carboxylation. The concentration of CO2 at the sites of carboxylation (Cc) is less than atmospheric (Ca) owing to a series of gas phase (air) and liquid phase (mesophyll cell) resistances. The drawdown in CO2 concentration between the bulk atmosphere and substomatal cavity is largely a function of stomatal conductance (gs), while the drawdown from substomatal cavity (Ci) to chloroplast (Cc) is a function of the internal conductance [gi=A/(Ci–Cc)]. A range of recent studies have shown that internal conductance is finite (i.e. Cc is significantly less than Ci) and this finite internal conductance poses a large limitation to photosynthesis (Evans et al., 1986; Parkhurst and Mott, 1990; Lloyd et al., 1992; Warren, 2004, 2007).
Leaf morphology and anatomy are often correlated with gi (Vitousek et al., 1990; Evans et al., 1994; Kogami et al., 2001), and this has led to suggestions that gi is largely constitutive (Evans et al., 1994; Syvertsen et al., 1995). gi may also be correlated with physiological factors such as rates of photosynthesis and stomatal conductance (von Caemmerer and Evans, 1991; Lloyd et al., 1992; Loreto et al., 1992; Epron et al., 1995; Hanba et al., 2001). Physiological factors such as A and gs are also correlated with anatomical traits, and thus relationships among gi, gs, and A are also consistent with the view that gi is largely constitutive.
Recent studies are highlighting that gi is affected by environmental variables and may change as rapidly as gs (Delfine et al., 1999; Centritto et al., 2003; Warren et al., 2004). For example, many reports have shown that drought and salt stress reduce gs and gi (Delfine et al., 1999; Flexas et al., 2002; Warren et al., 2004; Galmes et al., 2007). One might contrast the well-known effect of soil water deficits on gi with the atmospheric water deficits, for which only one study has examined if they affect gi (Bongi and Loreto, 1989). It is known that atmospheric water deficits (as indicated by leaf to air vapour pressure deficit, VPD) reduce gs (Franks and Farquhar, 1999), and an earlier study showed that VPD decreases gi (Bongi and Loreto, 1989); therefore, this study tests the hypothesis that atmospheric water deficits (like soil water deficits) reduce gi and gs. To test this hypothesis, gi and gs were measured under soil and atmospheric water deficits in three species: the herbaceous plants Solanum lycopersicum (formerly Lycopersicon esculentum) and Phaseolus vulgaris, and seedlings of the evergreen tree species Eucalyptus regnans.
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Materials and methods |
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Plant material and experimental protocol
Measurements were made on 6–9-month-old E. regnans (CSIRO ATSC seedlot 15158) grown in a mix of field soil and coarse sand, 3-month-old S. lycopersicum (cv. mini roma) grown in a peat/sand mix, and 2-month-old P. vulgaris (cv. Windsor long pod) also in a peat/sand mix. Plants were grown in a fully sunlit glasshouse at the University of Sydney (Camperdown, NSW, Australia). The VPD response of E. regnans was determined in February 2007, while response to soil water deficits was determined in August and September 2007. All measurements on S. lycopersicum and P. vulgaris were made during August and September 2007. All measurements were made on the youngest fully expanded leaves. In all cases, the same leaf on each plant was used for measurements; this was facilitated by marking leaves so that they could be re-visited for subsequent measurements.
Gas exchange systems
Gas exchange and chlorophyll fluorescence measurements were made with an open gas exchange system (LI-6400, Li-Cor, Lincoln, NE, USA) and either an integrated fluorescence chamber head (LI-6400-40) or a 2x3 cm LED chamber (LI-6400-02B). All measurements were made at a leaf temperature of 25 °C, which was quite similar to the laboratory temperature of 22 °C. The parts of the seedling outside the gas exchange system were illuminated with a 150 W halogen lamp that delivered 150–400 µmol PPFD m–2 s–1 at leaf height.
Data for both gas exchange systems were corrected for diffusion of CO2 into and out of the leaf chamber according to the manufacturer's advice (Anon, 2001). Diffusion leaks are proportional to the gradient in CO2 concentrations between inside and outside of the chamber and the flow rate of air through the chamber. This is accounted for by a diffusion coefficient which was determined by measuring the diffusion of CO2 into an empty chamber (Ca=0 µmol mol–1) as a function of the flow rate of air through the chamber and the inside-outside gradient of CO2. Preliminary tests showed that there was no difference in leakage between an empty chamber and a chamber containing a leaf of E. regnans that had been rapidly killed in a microwave oven (C Warren, unpublished data). Hence, all estimates of leakage were made with an empty chamber. The CO2 concentration of the sample cell was measured by the reference IRGA using the match valve, and the diffusion coefficient was used to recalculate the gas exchange data (Anon, 2001). For measurements under non-photorespiratory conditions, data were corrected for the effect of O2 concentration on the CO2 and H2O sensitivity of the LI-6400.
The effect of VPD on gi and gs
To investigate the effect of VPD on gi and gs, leaves were acclimated to a chamber CO2 concentration of 400 µmol mol–1, leaf temperature of 25 °C, PPFD of 1000 µmol m–2 s–1, and VPD of 1 kPa. Measurements of gas exchange and fluorescence were made every 2 min for at least 30 min or until rates of gas exchange and fluorescence were steady. VPD was then increased rapidly to 2 kPa and measurements continued to be taken every 2 min for at least 60 min or until gs reached a new steady state. VPD was then decreased back to 1 kPa and measurements were made for at least another 30 min.
The effect of soil water deficits on gi and gs
To determine how soil water deficits affect gi and gs, water was withheld from plants. Gas exchange and chlorophyll fluorescence measurements were made the day before water was withheld and then every second day for 8–10 d as pots dried out. Measurements were made between 10 am and 12 noon. On each occasion gas exchange and chlorophyll fluorescence were measured at a chamber CO2 concentration of 400 µmol mol–1, leaf temperature of 25 °C, PPFD of 1000 µmol m–2 s–1, and VPD of 1 kPa.
Measurement of Ci* and Rd
The substomatal CO2 photocompensation point (Ci*) and Rd were estimated using the Laisk (1977) method on one leaf from each of six E. regnans seedlings at a VPD of 1 kPa and 2 kPa. These initial measurements showed that Ci* and Rd were unaffected by VPD; hence, with S. lycopersicum and P. vulgaris, measurements were made only at a VPD of 1 kPa. Measurements were made with the 2x3 cm broadleaf chamber at a flow rate of 200 µmol s–1. One leaf (per seedling) was carefully placed inside the chamber and exposed to a near-saturating PPFD of 500 µmol m–2 s–1 for at least 15 min or until rates of gas exchange and fluorescence were steady. Ci* and Rd were estimated from three partial CO2 response curves (40–125 µmol mol–1 CO2) measured at PPFDs of 75, 200, and 500 µmol m–2 s–1. These light intensities were chosen following preliminary trials to ensure a large difference in slope of the three A–Ci curves. Each partial CO2 response curve comprised at least six points, although sometimes only four or five points were used in regressions because at the lowest PPFD there was sometimes curvature in the A–Ci relationship above 100 µmol mol–1 CO2. The intersection of the three lines identified Ci* (x-axis) and Rd (y-axis).
Calculation of gi via the variable J method
gi was estimated with the ‘variable J method’:
 | (1) |
A and Ci were measured directly by gas exchange, and Ja was estimated from chlorophyll fluorescence (see Fig. 1 and below). Ci* was used as a proxy for 
*.
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Chlorophyll fluorescence can estimate rates of linear electron transport (Jf) from the photochemical efficiency of photosystem II (PSII) (Genty et al., 1989), but due to a number of uncertainties such estimates may not be strictly related to the actual rate of linear electron transport (Ja). To overcome this limitation of chlorophyll fluorescence and obtain truly quantitative estimates, it is necessary to calibrate the relationship between Jf and Ja. The empirical relationships of Jf with Ja were determined for each leaf by measuring light response curves under non-photorespiratory conditions (1% O2, 1000 µmol CO2 mol–1). This allowed the actual rate of linear electron transport (Ja) to be calculated from gross photosynthesis [i.e. Ja=4(A+Rd)], where Rd is the rate of mitochondrial respiration in the light as determined by the Laisk method. It is possible that VPD affects the relationship of electron transport with chlorophyll fluorescence, so to test for this possibility measurements with E. regnans were made at VPDs of 1 kPa and 2 kPa. There was no evidence that VPD affects the relationship of Jf with Ja in E. regnans (Fig. 1). Hence, measurements of S. lycopersicum and P. vulgaris were made solely at a VPD of 1 kPa. Reference gas was supplied from a cylinder of 1% O2 in N2 (BOC Gases, Australia) and CO2 was added to 1000 µmol mol–1 using the CO2 mixer of the LI-6400. Leaf temperature was controlled at 25 °C, and leaf to air VPD was maintained at 1 kPa or 2 kPa. Leaves were acclimated to a PPFD of 1500 µmol m–2 s–1 for at least 30 min, or until stomatal conductance, net photosynthesis, and fluorescence were steady. Thereafter, PPFD was decreased, stepwise, from 1500 µmol m–2 s–1 to 0 µmol m–2 s–1. At each PPFD, leaves were acclimated for at least 5 min until stomatal conductance, net photosynthesis, and fluorescence reached a steady state, and then gas exchange and fluorescence parameters were recorded.
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Results |
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Relationship of chlorophyll fluorescence with electron transport
There were strong positive relationships between rates of linear electron transport estimated from chlorophyll fluorescence (Jf) and rates of linear electron transport estimated from gas exchange (Ja) (Fig. 1). In E. regnans, relationships did not differ between VPDs of 1 kPa and 2 kPa [analysis of covariance (ANCOVA), P >0.05]. Hence, in S. lycopersicum and P. vulgaris, measurements were only made at a VPD of 1 kPa. Because relationships differed somewhat among replicate plants and species, individual Jf–Ja relationships were used when calculating gi. In all cases, these individual plant-specific relationships were highly linear (R2
0.99).
Ci* and Rd
In E. regnans, neither the rate of mitochondrial respiration in the light (Rd) nor the substomatal CO2 photocompensation point (Ci*) was affected by VPD, and thus data for 1 kPa and 2 kPa are combined. In S. lycopersicum and P. vulgaris, measurements were only made at a VPD of 1 kPa. Ci* was 42 µmol mol–1 or 43 µmol mol–1 in all three species, while Rd varied from 0.46 to 0.73 µmol m–2 s–1.
Effect of VPD on gas exchange
Stomatal conductance of E. regnans responded to changes in VPD within 5–10 min (Fig. 2). There was no evidence that VPD affected the internal conductance to CO2 transfer (gi), either transiently (Fig. 2) or in the longer term (Table 2). VPD elicited similar changes in stomatal conductance of S. lycopersicum and P. vulgaris, but as with E. regnans there was no effect on gi.
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In all three species, steady-state gs decreased by
30% as VPD was increased from 1 kPa to 2 kPa (Table 2). This large decrease in gs at high VPD led to a small decrease in substomatal CO2 concentrations (Ci), and a small (10%) decrease in the rate of net photosynthesis. gi and chloroplast CO2 concentrations (Cc) were unaffected by VPD, despite large differences in gs. There was no relationship between gi and gs among or within species when measured at VPDs of 1 kPa and 2 kPa (Fig. 3).
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Effect of soil water deficits on gas exchange
Soil water deficit, in contrast to atmospheric water deficit, decreased A, gs, and gi (Table 3; Figs 4 and 5). In E. regnans and S. lycopersicum, water stress caused large decreases in A, gs, gi, Ci, and Cc (Fig. 4; Table 3). In P. vulgaris, there were also decreases in A, gs, and gi, but these were not matched by decreases in Ci and Cc.
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Because soil water deficits decreased gs and gi, there were strong positive relationships between gs and gi (Fig. 5). However, these relationships differed among species. In S. lycopersicum, the onset of drought led to a large reduction in gs that was not matched by a reduction in gi, but as drought progressed there were (linear) reductions in gs and gi. In P. vulgaris, decreases in gi were
1.5 times as large as those in gs, while in E. regnans gi decreased at 0.7 times the rate of gs. In the case of S. lycopersicum, if the initial large drop in gs is ignored, then decreases in gi were 2.3 times faster than those in gs. |
Discussion |
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There is a strong positive correlation between gi and gs among species (Loreto et al., 1992), within the canopy of trees (e.g. due to foliage age or light environment: Piel et al., 2002; Ethier et al., 2006), and in species under drought or salt stress (Fig. 5, and see also Cornic et al., 1989; Centritto et al., 2003; Warren et al., 2004). However, results of this study show that the positive relationship of gi with gs is not ubiquitous. The relationship differs substantially among different species subjected to soil water deficits (Fig. 5) and there is no relationship of gi with gs when gs is modulated by atmospheric water deficits (Fig. 3).
Stomatal and internal conductances are both reduced by soil water deficits (Figs 4, 5, and see also Flexas et al., 2002; Centritto et al., 2003; Warren et al., 2004; Galmes et al., 2007), and thus it seemed reasonable to propose that atmospheric water deficits (i.e. VPD) would reduce gi. This is especially the case as a previous study had shown that VPD reduces gi (Bongi and Loreto, 1989), and atmospheric and soil water deficits have similar effects on leaf and whole-plant water relations. However, in three disparate species there was no evidence that VPD affected gi, despite large effects on gs (Table 2; Fig. 2). There are a couple of explanations as to why Bongi and Loreto (1989) working with Olea europea found reductions in gi due to VPD whereas these were not found in the present experiments. One explanation is that this could simply reflect nothing more than inherent species differences. A more probable explanation is that Bongi and Loreto (1989) used more extreme VPD treatments that caused a 21% difference in A, whereas here differences in A of only 10% were observed.
That gi does not respond to atmospheric water deficits suggests that gi is not affected by some or all of the same things that affect gs (e.g. leaf water potential, xylem tension, relative water content, Ci: Sperry et al., 1998; Messinger et al., 2006). For example, it might be the case that gi responds to soil water deficits due to some root-borne signal, whereas there is no such signal with atmospheric water deficits. Once better knowledge is available of what determines or limits gi, we will be better placed to explain why it does respond to soil water deficits but not to atmospheric water deficits.
Another possible reason why gi did not respond to atmospheric water deficits but did respond to soil water deficits could be that atmospheric water deficits were imposed on a small proportion of the plant whereas soil water deficits affected the whole plant. If we accept that the reduction in gi due to soil water deficits is a consequence of changes in leaf water status that decrease the activity of carbonic anhydrase or aquaporins (Price et al., 1994; Terashima and Ono, 2002; Uehlein et al., 2003; Hanba et al., 2004; Flexas et al., 2006c), then we would expect elevated VPD also to reduce gi due to its hypothesized similar effect on leaf-level water status. There can be little doubt that leaf water status was affected by soil water deficits, but there is not the same certainty with atmospheric water deficits. The VPD treatment was imposed on a small leaf area, perhaps <10% of the total leaf area, and thus it is possible that leaf water status of the treated leaf area was unaffected because it was connected hydraulically to the remainder of the plant. Future studies should include accurate measurements of leaf water status (e.g. water potential and relative water content) because these might shed some light on the (apparent) disparity between atmospheric and soil water deficits. Future studies might also like to impose atmospheric water deficit treatments on the entire plant so as to discount the possibility that the absence of a response to VPD is an artefact of imposing treatments on a small leaf area.
Reductions of gi and gs by soil water deficits have been reported in other studies (Roupsard et al., 1996; Flexas et al., 2002, 2006b; Warren et al., 2004; Galmes et al., 2007), but there is no consensus as to the precise form of these relationships. In one of the few multispecies data sets, Galmes and co-workers (2007) found that 10 species shared a common linear relationship between gi and gs under soil water deficits, while other studies have reported curvilinear relationships (Flexas et al., 2002). The results of the present study support the idea that there is a diversity of relationships between gi and gs under soil water deficits. In some species the relationship is linear (E. regnans, P. vulgaris), while in others it is curvilinear (S. lycopersicum). Even when analysis is restricted to the linear portion of these relationships, it is apparent that relationships differ among species. In some species gi is more sensitive to soil water deficits than gs (e.g. P. vulgaris), whereas in others gi is less affected by soil water deficits than gs (e.g. E. regnans). At present no mechanistic explanation is available for why species differ in the relative sensitivity of gi and gs to water deficits. It may be a function of the relative limitation of gi by anatomical versus biochemical traits.
Species differed not only in the relationship between gi and gs under soil water deficits (Fig. 5). but also in the extent to which gi and gs explained reductions in net photosynthesis (Table 3; Fig. 4). It is now fairly well accepted that decreased gs and gi are the principal causes of reduced net photosynthesis under moderate soil water deficits (Flexas et al., 2006a; Galmes et al., 2007). The logic is that decreased gs and gi reduce Cc and this reduces photosynthesis. Two species, E. regnans and S. lycopersicum, fitted this pattern quite well, with large reductions in Cc being the likely cause of reductions in A. In P. vulgaris, however, A was reduced from 17 to 9 µmol m–2 s–1, but neither Ci nor Cc was reduced by soil water deficits. This suggests that in P. vulgaris biochemical factors (e.g. the Calvin cycle) were at least partially responsible for reduced photosynthesis.
An interesting consequence of the differential responses of gs and gi to soil versus atmospheric water deficits is their effect on net photosynthesis. It has just been seen that in two out of three species (and much of the literature: Flexas et al., 2006a; Galmes et al., 2007), the combined effects of decreased gs and gi on Cc are the primary cause of reduced photosynthesis under soil water deficits. This may be contrasted with the small reduction in photosynthesis due to atmospheric water deficits (Table 2). This reduction may be a function of reduced gs but cannot be a function of gi since it was unaffected (Table 2). In other words, internal conductance can at least partially explain reductions in photosynthesis due to drying soil, but cannot explain reductions in photosynthesis due to drying air.
Methodological limitations
The variable J method requires knowledge of Ja, A, Ci, *, and Rd. Errors associated with estimation of Ja from Jf are probably small given that coefficients of determination (R2) were 0.99 or better (Fig. 1). In E. regnans this relationship was unaffected by VPD and thus it was assumed that the Ja–Jf relationship would be similarly unaffected in S. lycopersicum and P. vulgaris. Additional tests with E. regnans also showed that Ja–Jf relationships were the same with CO2 concentrations of 1000 µmol mol–1 and 400 µmol mol–1 (data not shown). The possible effect of soil water deficits on the Ja–Jf relationship was not examined because previous studies have shown that this relationship is unaffected by soil water deficits (Warren et al., 2004). At any rate, slight differences in the Ja–Jf relationship could not explain the several-fold decreases in gi under soil water deficits.
Cuticular conductance was not measured but is probably at least two orders of magnitude smaller than gs in well-watered plants and thus will have minimal effects on estimates of Ci. In drought-stressed plants, cuticular conductance becomes more important and may have led to significant overestimation of Ci (Boyer et al., 1997). If cuticular conductance to water is 0.01 mol m–2 s–1, ignoring cuticular conductance will lead to underestimation of the true gi by 10% in water-stressed plants and by <5% in well-watered plants. Hence, the effect of cuticular conductance is rather modest in comparison with the several-fold decreases in gi under soil water deficits. One additional factor that may have affected estimates of Ci, and thus gi, is if patchy stomatal closure occurred when VPD was suddenly changed (Mott et al., 1993) and/or drought was imposed (Terashima et al., 1988). However, as with the effect of cuticular conductance, any effects of patchy stomatal closure will be small in comparison with the large effects of soil water deficits on gi and the clear absence of any effect of VPD.
Some uncertainty surrounds the true value of Rd and whether it can be determined accurately with the Laisk method (Pinelli and Loreto, 2003); however, realistic changes in Rd have a minimal effect on gi estimates. Estimates of Rd with the Laisk method were unaffected by VPD in E. regnans. In P. vulgaris and S. lycopersicum, the (possible) effects of VPD on Rd were not tested. At any rate, uncertainties in Rd will not affect any of the conclusions drawn here because if Rd is underestimated by 30%, gi is underestimated by 5%. Conversely if Rd is overestimated by 30%, gi is overestimated by 5%.
The substomatal CO2 photocompensation concentration (Ci*) was used as a surrogate for the chloroplastic value (*), and this is the largest possible source of error in this study. In any case, Ci* would seem to be a reasonable surrogate for * because Ci* in all three species was 42–43 µmol mol–1, which is slightly smaller than the in vitro * estimate of Jordan and Ogren (1984) and somewhat greater than in vivo estimates (von Caemmerer et al., 1994; Bernacchi et al., 2002). Slight errors in * will not affect any of the trends shown here; the only thing that will affect trends is if * is affected by atmospheric or soil water deficits. Ci* in E. regnans was unaffected by VPD and thus it is unlikely that * is affected by VPD in any of the three species. It was not tested whether * (or Ci*) was affected by soil water deficits, but this seems unlikely given that previous studies have shown in vitro that * is unaffected by drought (Galmes et al., 2006).
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Conclusions |
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The results of this study show that while gi is reduced by soil water deficits, it is unaffected by atmospheric water deficits. The clear absence of any response to atmospheric water deficits is not because the three species are in any way odd or unusual. The absence of a response to atmospheric water deficits may well be ubiquitous given the trends observed in three unrelated species that are in all respects normal in terms of their response to soil water deficits. At present there is no ready explanation as to why gi responds to soil water deficits but not atmospheric water deficits.
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Acknowledgements |
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CW acknowledges the financial support of the Australian Research Council in the form of a QEII Fellowship and Discovery grant, and the University of Sydney for a major equipment grant. Comments from two anonymous reviewers served to improve this manuscript greatly.
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