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Keywords:

  • CO2 enrichment ;
  • C4 photosynthesis ;
  • water relations

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Despite mounting evidence showing that C4 plants can accumulate more biomass at elevated CO2 partial pressure (p(CO2)), the underlying mechanisms of this response are still largely unclear. In this paper, we review the current state of knowledge regarding the response of C4 plants to elevated p(CO2) and discuss the likely mechanisms. We identify two main routes through which elevated p(CO2) can stimulate the growth of both well-watered and water-stressed C4 plants. First, through enhanced leaf CO2 assimilation rates due to increased intercellular p(CO2). Second, through reduced stomatal conductance and subsequently leaf transpiration rates. Reduced transpiration rates can stimulate leaf CO2 assimilation and growth rates by conserving soil water, improving shoot water relations and increasing leaf temperature. We argue that bundle sheath leakiness, direct CO2 fixation in the bundle sheath or the presence of C3-like photosynthesis in young C4 leaves are unlikely explanations for the high CO2-responsiveness of C4 photosynthesis. The interactions between elevated p(CO2), leaf temperature and shoot water relations on the growth and photosynthesis of C4 plants are identified as key areas needing urgent research.


Abbreviations:
A

CO2 assimilation rate

Ci

intercellular CO2 partial pressure

Cm

mesophyll CO2 partial pressure

Cs

bundle sheath CO2 partial pressure

E

transpiration rate

g

stomatal conductance

gs

bundle sheath cell wall conductance to CO2

[N]

nitrogen concentration

Rubisco

ribulose-1,5-bisphosphate carboxylase/oxygenase

p(CO2)

CO2 partial pressure

PEP

phosphoenolpyruvate

PEPcase

PEP carboxylase

VPDl

leaf-to-air vapour pressure deficit

Vc max

maximum Rubisco activity

Vp max

maximum PEPcase activity

INTRODUCTION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

C4 plants include some of the world’s most important crops (e.g. maize, sorghum), forage and range grasses (e.g. Panicum maximum) and noxious weeds (e.g. Echinochloa and Amaranthus spp.) ( Brown 1999). Although C4 plants represent, floristically, a small proportion of the world’s plant species (approximately 4%), they contribute about 18–21% of global primary productivity, mainly because of the high productivity of C4 grasslands ( Lloyd & Farquhar 1994; Ehleringer, Cerling & Helliker 1997). Due to the importance of grasslands in the global carbon cycle, recognition and understanding of the direct impact of rising atmospheric CO2 partial pressure (p(CO2)) on the growth and function of C4 plants remains a crucial area of interest. This importance is further heightened with some Global Climate Change models predicting an increase in the proportion of the land area covered by grasslands, especially savannas ( Archer 1993). Threatened water resources, anticipated changes in precipitation pattern and global warming are factors certain to interact strongly with the response of C4 plants to rising atmospheric p(CO2) for two main reasons. First, these factors will influence C3/C4 and shrub/grass competitions and land degradation in C4-dominated ecosystems ( Polley et al. 1997 ; Collatz, Berry & Clark 1999; Howden et al. 1999a , b). Secondly, because water and temperature interact directly with the growth response of C4 plants to elevated p(CO2) (e.g. Owensby et al. 1993 ; Alberto et al. 1996 ; Hunt et al. 1996 ; Read & Morgan 1996).

In the last 30 years, an ongoing effort has been dedicated to the study of the direct response of C3 plants to CO2 enrichment. Generally, controlled environment and field studies show that elevated p(CO2) stimulates biomass accumulation of C3 plants in both native and managed ecosystems ( Poorter 1993; Idso & Idso 1994; Drake et al. 1996 ). This growth stimulation is accepted to be primarily due to enhanced leaf CO2 assimilation rate (A). A relatively smaller number of studies have focused on the response of C4 plants to CO2 enrichment (for reviews see Poorter 1993; Poorter, Roumet & Campbell 1996; Wand et al. 1999 ). The under-representation of C4 plants in the CO2 enrichment literature is mainly related to the focus of early research on crop species ( Kimball 1983; Cure & Acock 1986). Maize and sorghum are the two main C4 crops, and they generally tend to show little or no growth response to elevated p(CO2) under well-watered conditions ( Patterson & Flint 1980; Carter & Peterson 1983; Morison & Gifford 1984a; Cure & Acock 1986). Based on these early results and the known CO2 concentrating mechanism of C4 photosynthesis it was generally assumed that C4 plants will not respond to elevated p(CO2) under well-watered conditions ( Berry & Downton 1982; Cure & Acock 1986).

However, more recent studies have found that the growth of many C4 plants respond positively to elevated p(CO2) even under well-watered conditions (e.g. Sionit & Patterson 1984; Riechers & Strain 1988; Ghannoum et al. 1997 ; Ziska & Bunce 1997; Ghannoum & Conroy 1998; Le Cain & Morgan 1998; Seneweera, Ghannoum & Conroy 1998; Ziska, Sicher & Bunce 1999; Wand et al. 1999 ). On average, the growth stimulation of C4 plants in response to a doubling of the current ambient p(CO2) is about 22–33%, compared with 40–44% for C3 plants ( Poorter 1993; Wand et al. 1999a ). The magnitude of the growth stimulation of C4 plants to elevated p(CO2) increases with decreasing soil water availability and increasing leaf-to-air vapour pressure deficit (VPDl), air temperature, light intensity and nitrogen (N) supply ( Sionit & Patterson 1984; Owensby et al. 1993 ; Owensby, Auen & Coyne 1994; Read & Morgan 1996; Samarakoon & Gifford 1996; Ghannoum et al. 1997 ; Ghannoum & Conroy 1998; Seneweera et al. 1998 ). Furthermore, the growth stimulation of C4 weeds is larger than that of C4 crops ( Poorter 1993; Ziska & Bunce 1997). In response to elevated p(CO2), C4 plants exhibit only a limited number of consistent changes; the main ones are reduced stomatal conductance (g) and increased leaf area ( Wand et al. 1999 ). Reduced foliar N concentration ([N]) is reported in some studies ( Owensby et al. 1994 ; Morgan et al. 1994 ; Read & Morgan 1996), but not in others ( Ghannoum et al. 1997 ; Ghannoum & Conroy 1998). Generally, specific leaf area of C4 plants remains unchanged at elevated p(CO2), as opposed to the decreases often observed in C3 plants ( Wand et al. 1999 ). In contrast to C3 plants, elevated p(CO2)-induced reduction in photosynthetic capacity (acclimation) is not usually observed in C4 plants (but see Morgan et al. 1994 ; Le Cain & Morgan 1998).

Despite the accumulation of evidence showing that C4 plants can respond to elevated p(CO2), there is still no clear understanding of the underlying mechanisms. In particular, there are a number of unanswered questions concerning the relative contribution of leaf photosynthesis and plant water relations to the growth response to high p(CO2) of well-watered and water-stressed C4 plants. It is therefore timely to revisit the relevant issues of C4 photosynthesis and plant water relations in the context of the response of C4 plants to elevated p(CO2). Here, we review the current understanding of the underlying mechanisms of the response of C4 plants to elevated p(CO2). We suggest that elevated p(CO2) can affect the growth of C4 plants via several routes ( Fig. 1). First, by raising the intercellular p(CO2) (Ci) and consequently A. Second, by reducing g, and consequently leaf transpiration rate (E). Reduced E can enhance leaf A and growth by conserving soil water, improving shoot water relations and increasing leaf temperature ( Fig. 1). Third, high p(CO2) may reduce mitochondrial respiration and consequently whole plant respiratory losses, which can contribute to biomass in-creases. Elevated p(CO2) reduces mitochondrial respiration in a number of C3 plants ( Drake, Gonzàlez-Meler & Long 1997). However, there is little data on the response of respiration in C4 plants to elevated p(CO2) and no conclusion can yet be drawn ( Poorter et al. 1992 ; Ziska & Bunce 1999). Further research in this area is needed. The influence of the first two factors (leaf A and E) on the growth response of C4 plants to elevated p(CO2) will be discussed in the following sections.

image

Figure 1. Summary of the main mechanisms that contribute to increased biomass accumulation in C4 plants exposed to elevated p(CO2).

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ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

Many workers have noted enhanced leaf A in C4 plants at elevated p(CO2) when measured under well-watered conditions (e.g. Sionit & Patterson 1984; Morgan et al. 1994 ; Ziska & Bunce 1997, 1999; Le Cain & Morgan 1998; Ziska et al. 1999 ; Wand 1999). Although puzzling, this response was perceived as a likely explanation for the growth stimulation observed in well-watered C4 plants at elevated p(CO2). However, a number of studies found a growth response in C4 plants without the concomitant enhancement of leaf A (e.g. Carlson & Bazzaz 1980; Rogers et al. 1983 ; Ghannoum et al. 1997 ) or vice versa (e.g. Le Cain & Morgan 1998; Ziska et al. 1999 ). These results partly reflect the difficulty of inferring growth responses from short-term measurements of A for a number of reasons. First, diurnal variations of A, which may be caused by midday stomatal closure, are rarely measured. Secondly, photosynthetic measurements are often carried out on developmentally advanced plants. It is possible that increases in A at elevated p(CO2) are only apparent during early, but not late, plant development as has been observed with Themeda triandra ( Wand 1999).

Since C4 photosynthesis is almost saturated under current atmospheric p(CO2), the observed responsiveness of growth to elevated p(CO2) was thought to be related to a number of potential mechanisms. These include differences in bundle sheath leakiness, direct CO2 fixation in the bundle sheath and the presence of C3-like photosynthesis in young, developing C4 leaves ( Tremmel & Patterson 1993; Poorter et al. 1996 ; Le Cain & Morgan 1998; Ziska et al. 1999 ). These mechanisms together with the saturation and acclimation of C4 photosynthesis at elevated p(CO2) are discussed below.

CO2 saturation of C4 photosynthesis

During C4 photosynthesis, atmospheric CO2 is initially fixed by phosphoenolpyruvate carboxylase (PEPcase) into C4 acids in the outer mesophyll cells. C4 acids are then decarboxylated in the inner bundle sheath cells with the subsequent release of CO2 and its fixation by ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) ( Hatch 1987). CO2 released in the bundle sheath is concentrated to 3–10 times that of ambient partial pressure because of the very low bundle sheath cell wall conductance to CO2 (gs) ( Hatch 1987; Furbank, Jenkins & Hatch 1989; Jenkins, Furbank & Hatch 1989a; Brown & Byrd 1993). Under the high bundle sheath p(CO2) (Cs), A is largely saturated and photorespiration suppressed. Consequently, raising CO2 above the current ambient partial pressure is expected to have little or no effect on A.

Most gas exchange measurements show that C4 photosynthesis is at near saturation under the current ambient p(CO2) ( Ludlow & Wilson 1971; von Caemmerer et al. 1997 ). However, a number of studies have found that photosynthesis is not completely saturated in many well-watered C4 species under the current ambient p(CO2), with A increasing at elevated p(CO2) ( Wong 1979; Morgan et al. 1994 ; Watling & Press 1997; Ziska & Bunce 1997; Le Cain & Morgan 1998; Wand et al. 1999 ; Ziska et al. 1999 ). The A/Ci response curve of C4 plants is characterized by a steep initial slope and early saturation at relatively low Ci (10–15 Pa). Under high light, saturation of the A/Ci curve depends on Rubisco activity. Under low light, saturation is dependent on the capacity to regenerate PEP and ribulose-1, 5-bisphos-phate (RuBP) (i.e. photosynthetic electron transport) ( Berry & Farquhar 1978; von Caemmerer & Furbank 1999). It is important to note that saturation of A does not occur at a set Ci, but is dependent on a number of environmental conditions. For example, in a number of C4 species, the point of inflection of the A/Ci curve (i.e. the Ci at which saturation occurs) increases with increasing light and N supplies ( Fig. 2a & b; Leegood & von Caemmerer 1989) and temperature (L. Ziska unpublished). At low soil water availability and high VPDl, elevated p(CO2) overcomes the Ci limitation of A imposed by low g that occurs in low p(CO2)-grown plants, thus leading to higher A at elevated p(CO2) ( Samarakoon & Gifford 1995; S. Seneweera & O. Ghannoum unpublished). Overall, the enhancement of C4 photosynthesis at elevated p(CO2) depends on the integration of all these growth conditions. The role of a Ci limitation on photosynthesis and growth at the current atmospheric p(CO2) can be tested by growing C4 plants at a range of p(CO2) rather than ambient and double ambient p(CO2).

image

Figure 2. A/Ci response curves of P. antidotale (C4) grown at a p(CO2) of 36 (□○▵) or 71 Pa (●▴) and receiving 0 (▵▴) or 60 (□○●) mg N kg−1 soil week−1. Measurements were made at 1200 (○●▵▴) μmol quanta m−2 s−1 (a), leaf temperature of 30 °C and VPDl of 2·0 kPa. High [N], low p(CO2)-grown plants were also measured at 400 (□) μmol quanta m−2 s−1 (b). Each plot is the mean of five (high [N], a), three (low [N], a) and two (b) A/Ci curves. Error bars represent two standard errors. The solid lines represent the mathematical fits of the initial slope and saturated rates, within each set of A/Ci curves, using the photosynthetic model of von Caemmerer & Furbank (1999). Arrows indicate a point on the curve corresponding to an ambient p(CO2) of 36 Pa. Adapted from Ghannoum et al. (1997) and Ghannoum & Conroy (1998).

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Leakiness: the suberin lamella and PEPcase/Rubisco

Following the major enzyme catalyzing the decarboxylation of the C4 acids in the bundle sheath, C4 plants are grouped into three biochemical subtypes: NAD malic enzyme (NAD-ME), NADP-ME and PEP carboxykinase (PCK) ( Hatch 1987). Each biochemical subtype is distinguished by a characteristic leaf anatomy ( Hattersley & Watson 1992; Dengler & Nelson 1999). It has been suggested that the differences in the growth response of C4 plants to elevated p(CO2) could be related to the biochemical subtype or more specifically to leakiness [defined as the rate of CO2 leakage out of the bundle sheath divided by the rate of PEP carboxylation ( Farquhar 1983)] of the C4 photosynthetic pathway ( Le Cain & Morgan 1998; Ziska et al. 1999 ). In other words, the growth response to elevated p(CO2) was thought to increase with leakiness.

The relationship between the biochemical subtype and leakiness is based on the interpretation of Hattersley (1982) and Ehleringer & Pearcy (1983) of the differences in the dry matter 13C/12C isotope abundance ratio (δ13C) and the quantum yield of photosynthesis. In particular, Hattersley (1982) proposed that the bundle sheath of NADP-ME species is less ‘leaky’ to CO2 because a suberin lamella is present in the bundle sheath cell walls. Leakiness cannot be directly measured but has been estimated by two laboratories using different techniques. Henderson, von Caemmerer & Farquhar (1992) found no differences in leakiness among the C4 subtypes, using concurrent measurements of carbon isotope discrimination and gas exchange. However, using 14CO2 pulse chase labelling, Hatch, Agostino & Jenkins (1995) calculated leakiness to be highest in NADP-ME type dicots, followed by NADP-ME type monocots, PCK and NAD-ME type, separated by marginal differences. This ranking of leakiness is unrelated to that predicted by either dry matter δ13C or photosynthetic quantum yield measurements. The findings of these two studies cast doubt over the relationship between leakiness and the biochemical subtype.

Leakiness and Cs are best viewed as the result of the integration between leaf anatomy (i.e. gs) and biochemistry (C3 and C4 cycles activity). Although suberization may reduce gs, differences in gs may be closely matched by variations in the activities of the C3 and C4 cycle enzymes, leading to little net effect on leakiness ( Henderson et al. 1992 ; von Caemmerer et al. 1997 ). To better illustrate this point, we used the photosynthetic model of von Caemmerer & Furbank (1999) ( Figs 3 & 4). Figure 3 simulates the CO2-responsiveness of A, Cs and leakiness, for three different combinations of gs and maximum PEPcase (Vp max) and Rubisco (Vc max) activity. Scenario 1 shows a ‘control’ case where consensual values ( Brown & Byrd 1993; He & Edwards 1996; von Caemmerer & Furbank 1999) are given to gs, Vp max and Vc max ( Fig. 3). The first simulation shows that δACi becomes near zero at below current ambient p(CO2) ( Fig. 4). Scenario 2 illustrates a case where gs was increased 10-fold. This change has a substantial impact on the response of A, Cs and leakiness to mesophyll p(CO2) (Cm) ( Fig. 3). However, the saturation profile of the A/Ci response curve is virtually unaffected ( Fig. 4). This shows that large changes in gs and leakiness can have little effect on the CO2-responsiveness of C4 photosynthesis. We therefore do not expect an obligatory relationship between leakiness and the growth response of C4 plants to elevated p(CO2). Growth studies found that NADP-ME species are either more or equally responsive to high p(CO2) than NAD-ME species, whether the distinction was based on the biochemical subtype ( Ghannoum 1997; Le Cain & Morgan 1998; O. Ghannoum unpublished) or leakage rate ( Ziska et al. 1999 ). These findings support the result of our modelling.

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Figure 3. Modelling the response of A (a), bundle sheath p(CO2) (Cs) (b) and leakiness (Φ) (c) during C4 photosynthesis to mesophyll p(CO2) (Cm). Scenario 1 (―) simulates a mature C4 leaf with a maximum PEP carboxylase activity (Vp max) of 75 μmol m−2 s−1, maximum Rubisco activity (Vc max) of 37·5 μmol m−2 s−1, a bundle sheath conductance to CO2 per leaf area (gs) of 1·5 mmol m−2 s−1, leaf mitochondrial respiration = 0 and α (fraction of PSII activity in the bundle sheath) = 0·5 (other parameters are similar to those described in Table 2 of von Caemmerer & Furbank (1999)). Scenarios 2 and 3 use the same parameters as in scenario 1, except for the following changes. In scenario 2 (·····), gs is increased by 10-fold. In scenario 3 (- - -), Vp max/Vc max is reduced by 1·75-fold.

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image

Figure 4. The relationship between the modelled changes of the ratio of the unit change in A per unit CiACi) and Cm during C4 photosynthesis. The scenarios and parameters are the same as used in Fig. 3.

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There are few reports of Rubisco or PEPcase activity in C4 plants at elevated p(CO2). Limited evidence indicates that under well-watered and fertilized conditions, high p(CO2) seems to have little effect on the activity of either enzyme ( Wong 1979; Ghannoum et al. 1997 ; Ziska et al. 1999 ). However, other growth conditions can affect PEPcase and Rubisco activities unequally, thus influencing Cs, leakiness and presumably the CO2-saturation of C4 photosynthesis. Our photosynthetic simulations show that the ratio of PEPcase/Rubisco activity can have a substantial effect on the saturation profile of the A/Ci response curve (scenario 3: Figs 3 & 4). Ranjith et al. (1995) and Saliendra et al. (1996) found that decreasing N and water supplies increase PEPcase/Rubisco activity ratio. According to our modelling, Cs would increase while the saturation point (thus CO2-responsiveness) of C4 photosynthesis decreases (see also von Caemmerer & Furbank 1999). Using transgenic Flaveria bidentis with reduced Rubisco concentration, von Caemmerer et al. (1997) , demonstrated that leakiness increases and photosynthesis saturates at a relatively lower Ci in transgenic compared to wild-type plants. These findings as well as our simulations agree with our gas exchange measurements, which show that low leaf [N] leads to the saturation of the A/Ci response curves at a lower Ci ( Fig. 2a). Low [N] ultimately precluded a growth response to CO2 enrichment in two C4 grasses ( Ghannoum & Conroy 1998). We therefore suggest that environmental factors which affect the relative activities of C3 and C4 cycle enzymes are more important in determining differences in the magnitude of the growth response to elevated p(CO2) than intrinsic differences in the biochemistry or anatomy of the C4 leaf.

Direct CO2 fixation

One potential explanation advanced for enhanced C4 photosynthesis at elevated p(CO2) is direct CO2 fixation by the C3 cycle. The mesophyll of C4 leaves lacks a number of the C3 cycle enzymes ( Sheen & Bogard 1985; Nelson & Langdale 1989; Hudson et al. 1992 ; Dengler & Nelson 1999). Presumably, any direct CO2 fixation must then take place in the bundle sheath. However, there is little evidence to support CO2 uptake via this route. Low gs imposes a substantial barrier in the face of CO2 exchange across the bundle sheath ( Furbank et al. 1989 ; Jenkins et al. 1989a ; Brown & Byrd 1993). This low gs makes the decarboxylation of C4 acids the major source of CO2 for fixation by Rubisco. Indeed, when PEPcase activity was inhibited in a number of C4 grasses or completely lacking in a mutant of Amaranthus edulis, A was reduced by more than 90% of the control rates even under high p(CO2) ( Jenkins, Furbank & Hatch 1989b; Dever et al. 1997 ). Furthermore, there is very little bundle sheath directly exposed to the intercellular air space in C4 leaves ( Dengler et al. 1994 ). Therefore, any CO2 directly fixed in the bundle sheath must diffuse through the intercellular air space and the liquid phase of the mesophyll and part of the bundle sheath ( Evans & von Caemmerer 1996). This constitutes a large diffusive barrier because diffusion of CO2 in the liquid phase is extremely slow (104 fold less than in the gas phase) ( Falkowski & Raven 1997). Nevertheless, Moore, Cheng & Edwards (1986) found that 10 and 0% of labelled 14CO2 is directly fixed by the C3 cycle of 20 and 75% expanded Flaveria trinervia leaves, respectively. No Rubisco activity was detected in mesophyll protoplasts isolated from the young F. trinervia leaves ( Moore et al. 1986 ). Therefore, direct CO2 fixation is clearly insignificant in mature C4 leaves, but may play a role in developing C4 leaves, possibly due to the immaturity of the bundle sheath cell wall. This aspect has yet to be investigated.

Developing C4 leaves

Another proposed explanation for enhanced C4 photosynthesis at high p(CO2) is that young C4 leaves have C3-like characteristics ( Sionit & Patterson 1984; Tremmel & Patterson 1993; Poorter et al. 1996 ; Ziska et al. 1999 ). This hypothesis is based on a few studies concerning the expression of C4 photosynthetic genes early in leaf development ( Nelson & Langdale 1989). A key feature of the C4 syndrome is the spatial distribution of the photosynthetic apparatus between the mesophyll and the bundle sheath ( Dengler & Nelson 1999). A number of studies found that cell-specific accumulation of photosynthetic genes and proteins begins concurrently with the initiation of veins in monocots ( Mayfield & Taylor 1984; Langdale Rothermel & Nelson 1988a; Langdale et al. 1988b ) and dicots ( Wang et al. 1992 , 1993; Dengler et al. 1995 ), well before a Kranz anatomy is visible. However, these molecular changes occur early in leaf development, before a functional photosynthetic system is in place. Dai, Ku & Edwards (1995) found a substantial inhibition of photosynthesis (31%) in young Zea mays leaves, under current ambient p(CO2) when p(O2) was raised from 9·3 to 18·6 kPa. It was argued that this inhibition is related to photorespiration ( Dai et al. 1995 ). These results have been interpreted, in the CO2 enrichment literature, to be indicative of the occurrence of C3 photosynthesis in young C4 leaves. However, careful examination of the results reveals that A of young maize leaves was saturated at very low Ci ( Dai et al. 1995 ). This is a distinctive characteristic of C4 photosynthesis, which contradicts the interpretation that the photosynthesis of young C4 leaves is C3-like. This interpretation is further repudiated by the work of Moore & Edwards (1986) with F. trinervia where the same labelling pattern of C4 acids was obtained throughout leaf expansion. Our work with two C4 grasses, Panicum antidotale and Pancum coloratum, showed that the young C4 leaves had CO2 and light response curves typical of C4 photosynthesis, saturating at below current ambient p(CO2) ( Ghannoum et al. 1998 ). When p(O2) was gradually increased between 2 and 40%, the A of both mature and young C4 leaves was little affected. With the aid of photosynthesis modelling, it was argued that young C4 leaves have lower Cs, brought about by higher gs relative to Vp max and Vc max and/or lower Vp max/Vc max ( Ghannoum et al. 1998 ).

Acclimation of C4 photosynthesis at elevated p(CO2)

In contrast to C3 plants, elevated p(CO2)-induced photosynthetic acclimation is not commonly observed in C4 plants. In C3 plants, long-term (i.e. weeks, months) exposure to elevated p(CO2) usually, but not always, brings about a reduction in A when the rates are compared at the same p(CO2). This response, termed acclimation or down-regulation, is often accompanied by reduction in foliar [N] and accumulation of non-structural carbohydrates ( Stitt 1991). Although it is clear that acclimation of A in C3 plants is associated with reduced Rubisco and other C3 cycle enzymes, the contribution of the N or C metabolism to the signalling process is still uncertain ( Geiger et al. 1999 ; Stitt & Krapp 1999).

However, the lack of photosynthetic acclimation in C4 plants can be readily explained. There is less Rubisco protein in C4, relative to C3, plants ( Wong 1979; Schmitt & Edwards 1981; Ghannoum et al. 1997 ), and this enzyme operates under high p(CO2) in the bundle sheath ( Hatch 1987). Furbank et al. (1996) and von Caemmerer et al. (1997) showed that Rubisco concentration in F. bidentis is linearly related to A under high light, indicating that there is just enough Rubisco protein to support maximum A in C4 plants under current and elevated p(CO2). Indeed, the observed increases in A at elevated p(CO2) are usually small in C4 plants. Moreover, C4 plants are adapted to fast growth rates. Both their biochemistry (e.g. processing of increased phosphoglycerate flux), and physiology (phloem loading, production of new sinks) are expected to cope with moderate increases in A ( Henderson et al. 1994 ; Grodzinski, Jiao & Leonardos 1998). Generally, mature C4 leaves do not accumulate excess non-structural carbohydrates at elevated p(CO2) ( Wand et al. 1999 ). Hence, the expected ensuing changes in the N and C metabolisms of C4 plants at elevated p(CO2) are likely to be too small to entail the acclimatory response usually observed in C3 photosynthesis. Nevertheless, PEPcase and carbonic anhydrase activities remain potential sites for acclimation in C4 plants. There are a few reports of reduced PEPcase activity at elevated p(CO2) in some C4, especially under limited N supply ( Wong 1979; Fig. 2a; Table 1) and CAM ( Nobel, Israel & Wang 1996) plants. Reduced PEPcase activity may explain some of the strong photosynthetic acclimatory responses reported in a number of C4 species under conditions of low N supply or low temperature ( Morgan et al. 1994 ; Wand 1999). We are unaware of any studies investigating carbonic anhydrase activity of C4 plants at elevated p(CO2).

Table 1.  Effect of CO2 and N fertilization on the maximum PEPcase and Rubisco activities of P. antidotale (C4) estimated from gas exchange measurements. Plants were grown at a p(CO2) of 36 or 71 Pa and supplied with 0 or 60 mg N kg−1 soil week−1. Maximum PEPcase (Vp max) and Rubisco (Vc max) activities were obtained by fitting the initial slope and saturated rates of the A/Ci curves, shown in Fig. 2(a), using von Caemmerer & Furbank (1999) photosynthetic model. Values are means of five (high [N]) or three (low [N]) replicates. Standard errors are shown in parenthesis
Growth p(CO2) (Pa) Growth (mg N kg−1 soil week−1) [N] Vc max (μmol m−2 s−1) Vp max
  1. 71

  2. 60

  3. 87·7 (6·2)

  4. 38·7 (1·9)

36076·2 (3·8)25·0 (0·4)
71049·6 (3·1)27·3 (1·5)
366077·3 (4·4)42·7 (1·9)

ELEVATED P(CO2) AND STOMATAL CONDUCTANCE

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

The discussion in the previous sections focused on the mechanisms by which elevated p(CO2) may directly increase C4 photosynthesis. Greater A leads to increased carbohydrate supply to the growing leaves, stems and roots and consequently, enhances plant growth. In the following sections, we will discuss the mechanisms by which reduced leaf E, brought about by lower g at elevated p(CO2), may affect leaf A and growth in water-stressed and well-watered C4 plants. Three main possibilities are identified: conservation of soil water, improved shoot water status and increased leaf temperature ( Fig. 1).

Conservation of soil water and improved shoot water status

Reduced leaf E at elevated p(CO2) may lead to lower whole plant E, and consequently conservation of soil water ( Fig. 1). This will take place only if increases in leaf temperature and area do not offset the decreases in leaf E ( Morison & Gifford 1984b; Jarvis, Mansfield & Davies 1999). Conservation of soil water in the field depends on additional factors such as wind speed, canopy cover and soil evaporation. Nevertheless, water conservation has been reported in a relatively dry C4 tallgrass prairie system ( Owensby et al. 1997 ). Conservation of soil water at elevated p(CO2) is relevant only under water-limited conditions (e.g. dry fields, small or drying pots) where the development of water stress in plants is delayed due to increased soil water availability. For example, in the C4 grass P. coloratum growing in a drying soil, leaf water potential of the fully expanded leaves of high p(CO2)-grown plants is higher than in their low p(CO2)-grown counterparts, when comparisons are made at the same point in time (S. Seneweera & O. Ghannoum unpublished). Thus, leaf growth at elevated p(CO2) is likely to continue for longer during drought ( Passioura 1988; Davies & Zhang 1991; Kramer & Boyer 1995). In addition, improved leaf water relations can maintain higher A in many plants due to the maintenance of larger cell volume and metabolic integrity ( Lawlor & Fock 1978; Conroy et al. 1988 ; S. Seneweera & O. Ghannoum unpublished). Hence, the active period for photosynthesis and growth under drought is extended at elevated p(CO2), provided other growth conditions, such as temperature and N supply, are still favourable ( Hogan, Smith & Ziska 1991; Tyree & Alexander 1993; S. Seneweera & O. Ghannoum unpublished). There is ample evidence from field and controlled-environment trials with C4 plants showing more pronounced growth stimulation in response to elevated p(CO2) under soil water-limited conditions ( Owensby et al. 1993 , 1994, 1997; Samarakoon & Gifford 1996; Seneweera et al. 1998 ). This is in contrast to well-watered conditions, such as the estuarine tidal marsh system of Chesapeake Bay where Spartina patens (C4) showed no biomass response to long-term CO2 enrichment ( Curtis et al. 1989 ).

The explanation for the growth response of water-stressed C4 plants to CO2 enrichment is evidently linked to stomatal closure. However, the growth response of well-watered C4 plants to elevated p(CO2) seems more difficult to explain ( Samarakoon & Gifford 1996; Ghannoum et al. 1997 ; Le Cain & Morgan 1998; Seneweera et al. 1998 ; Ziska & Bunce 1999; Ziska et al. 1999 ). Water stress may arise as a result of either soil or atmospheric water deficit, both of which are known to limit plant growth through their effect on shoot water status ( Passioura 1988; Grantz 1990; Ben Haj Salah & Tardieu 1996; Seneweera et al. 1998 ). Under most field and controlled environment conditions (e.g. high midday radiation and high temperatures), C4 plants may experience substantial evaporative demands that lead to the development of transient shoot water stress with adverse effects on leaf growth. Elevated p(CO2) can enhance plant growth by reducing leaf E and hence, alleviating the negative effects of transient water stress on leaf growth. Consequently, the average daily leaf expansion rates may increase at elevated p(CO2) independently of its effect on A ( Fig. 1). This hypothesis is supported by the observations of Ben Haj Salah & Tardieu (1996), who found that the evaporative demand affects leaf extension rates, independently of leaf temperature and soil water availability, of maize growth in both the field and controlled environments ( Ben Haj Salah & Tardieu 1996).

A good example of how elevated p(CO2) can alleviate the negative effects of high VPDl on the growth of a C4 grass, P. coloratum is shown in Fig. 5. Changes in growth (shoot dry mass and leaf area) were negatively correlated with whole plant E, whether the changes were brought about by varying VPDl or p(CO2). In this experiment, soil water content was controlled at 100% pot capacity, and any effect of high p(CO2) was independent of soil water availability ( Fig. 5). Therefore, under well-watered conditions, elevated p(CO2) and low VPDl had similar effects on E, and consequently shoot growth ( Fig. 5). This response is particularly relevant in C4 plants, because stomatal closure at elevated p(CO2), under well-watered conditions, influences mainly leaf E, with little effect on A, due to the CO2 saturation characteristics of C4 photosynthesis ( Bunce 1993; von Caemmerer & Furbank 1999). It is worth noting that when the evaporative demand was low, elevated p(CO2) had little effect on whole plant E and growth ( Fig. 5). This reinforces our hypothesis that part of the growth response observed in C4 plants at elevated p(CO2) is due to the alleviation of the negative effect of high evaporative demands on leaf growth. However, this positive effect may disappear under very high VPDl, when stomata close little in response to high p(CO2) ( Bunce 1993). The underlying mechanism of the link between leaf E, growth and p(CO2), or VPDl, remains unclear. Although there is some agreement about the general mechanism of action and the signal transduction pathway of soil water deficit, the sensing and mode of action of atmospheric water deficit is unknown ( Grantz 1990; Davies & Zhang 1991). Available evidence seems to implicate water vapour fluxes through the leaf as both a sensor and an effector, through their direct effect on shoot water status ( Grantz 1990; Ben Haj Salah & Tardieu 1996). However, changes in leaf E may also influence leaf temperature. Hence, it is often impossible to distinguish between the effects of these two factors (i.e. E and temperature) on leaf growth. The interaction between the evaporative demand and the growth response of C4 plants to elevated p(CO2) warrants further research.

image

Figure 5. The relationship between shoot dry mass (a) and leaf area (b) and whole plant E of P. coloratum (C4). Plants were grown for 34 d at a p(CO2) of either 36 (○▵) or 100 (●▴) Pa, exposed to a VPDl of either 0·9 (○●) or 2·1 (▵▴) kPa and watered to 100% pot capacity daily. The solid lines are linear regression fits and error bars represent 2SE. Adapted from Seneweera et al. (1998) .

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Increased leaf temperature

Another important consideration in the growth response of C4 plants to elevated p(CO2), is the likely effect of reduced E on leaf temperature. As a direct consequence of reduced E, leaf temperature may rise ( Fig. 1). A number of studies compared the interaction of increased air temperature (simulating global warming) and elevated p(CO2) on the growth and photosynthesis of C4 plants (e.g. Morgan et al. 1994 ; Read & Morgan 1996; Alberto et al. 1996 ). However, little attention has been given to the effect of high p(CO2)-induced stomatal closure on leaf temperature. Data are severely lacking in this area, despite the strong dependence of C4 photosynthesis and growth on temperature ( Ludlow & Wilson 1971; Watts 1971; Wardlaw 1979; Berry & Björkman 1980; Ben Haj Salah & Tardieu 1995; Long 1999). The temperature optimum for C4 photosynthesis is between 30 and 40 °C ( Ludlow & Wilson 1971; Wardlaw 1979; Berry & Björkman 1980; Mjwara & Botha 1993; Long 1999) and that for growth of C4 plants is between 30 and 35 °C ( Watts 1971; Wardlaw 1979). Hence, the temperature response of both A and leaf growth remains strong under growth temperatures experienced in most controlled environments and some occasions in the field. Consequently, in the short term, small increases in leaf temperature could lead to significant increases in A and leaf expansion rates ( Fig. 1). Leaf energy balance calculations predict increases of 1–1·5 °C with a doubling of current ambient p(CO2), and direct measurements using C3 plants seem to confirm this prediction ( Idso, Kimball & Mauney 1987; Jarvis et al. 1999 ). This rise is rarely captured in gas exchange measurements because they are conducted under controlled conditions. Our work with four C4 grasses showed that between 20 and 36 °C, a rise of 1 °C in leaf temperature at both ambient and elevated p(CO2) leads to an average of 2·0 μmol CO2 m−2 s−1 increase in A (O. Ghannoum unpublished). Furthermore, at temperatures between 13 and 30 °C, leaf expansion rates of field- and controlled-environment-grown maize plants, are linearly related to the leaf meristem temperature with a Q10 of approximately 3 ( Ben Haj Salah & Tardieu 1995). The authors concluded that temperature enhances leaf expansion rate by simultaneously increasing cell division and cell wall expansion rates ( Ben Haj Salah & Tardieu 1995). These small increases in leaf CO2 assimilation and expansion rates, that may occur due to leaf warming at elevated p(CO2), can substantially enhance biomass accumulation in the long term due to the compound effect of these processes on plant growth. However, the interaction between elevated p(CO2) and leaf and air temperatures on A and leaf growth depends on factors such as nutrition, light intensity, water supply, species habit and adaptation (see Morison & Lawlor 1999). These factors will not only determine the extent to which leaf temperature may rise at elevated p(CO2), but also the translation of this rise into a growth response. Moreover, an increase in leaf temperature will, in turn, increase VPDl, feeding back on leaf E. For example, a temperature rise of several degrees in maize leaves increased VPDl by up to 1–2 kPa ( Ben Haj Salah & Tardieu 1997). Research into the role of leaf temperature in the growth response of C4 plants to elevated p(CO2) is needed.

CONCLUDING REMARKS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

The growth response of C4 plants to elevated p(CO2) is particularly interesting. The near saturation of C4, as opposed to C3, photosynthesis at current ambient p(CO2) and the lack of acclimation at elevated p(CO2) offer an excellent opportunity to explore the more subtle effects of shoot water relations and leaf temperature on the growth response of plants to CO2 enrichment. The main areas requiring further research are the interaction of leaf and air temperature, as well as shoot water relations, with elevated p(CO2) on diurnal C4 photosynthesis and growth. We conclude from available data that CO2 enrichment can increase leaf A and growth of C4 plants via increases in Ci, changes in diurnal CO2 fixation patterns, improvements of shoot water relations and increases in leaf temperature.

ACKNOWLEDGMENTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES

We thank Stephanie Wand for critically reading this manuscript. O.G. was supported by a research grant funded by the Australian Research Council (SPIRT program) with the Bureau of Resource Sciences (Canberra) and Pacific Power International (Australia) as industry partners.

REFERENCES

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. ELEVATED P(CO2) AND C4 PHOTOSYNTHESIS
  5. ELEVATED P(CO2) AND STOMATAL CONDUCTANCE
  6. CONCLUDING REMARKS
  7. ACKNOWLEDGMENTS
  8. REFERENCES
  • Alberto A.M.P., Ziska L.H., Cervancia C.R., Manalo P.A. (1996) The influence of increasing carbon dioxide and temperature on competitive interactions between a C3 crop, rice (Oryza sativa) and a C4 weed (Echinochloa glabrescens). Australian Journal of Plant Physiology 23, 795 802.
  • Archer S. (1993) Climate change and grasslands: a life-zone and biota perspective. In Grasslands for Our World (ed. M.J. Baker), pp. 396 402. SIR Publishing, Wellington.
  • Ben Haj Salah H. & Tardieu F. (1995) Temperature affects expansion rate of maize leaves without change in spatial distribution of cell length. Analysis of the coordination between cell division and cell expansion. Plant Physiology 109, 861 870.
  • Ben Haj Salah H. & Tardieu F. (1996) Quantitative analysis of the combined effects of temperature, evaporative demand and light on leaf elongation rate in well-watered field and laboratory-grown maize plants. Journal of Experimental Botany 47, 1689 1698.
  • Ben Haj Salah H. & Tardieu F. (1997) Control of leaf expansion rate of droughted maize plants under fluctuating evaporative demand. A superposition of hydraulic and chemical messages? Plant Physiology 114, 893 900.
  • Berry J.A. & Björkman O. (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 31, 491 543.
  • Berry J.A. & Downton J.S. (1982) Environmental regulation of photosynthesis. In Photosynthesis, Development, Carbon Metabolism and Plant Productivity (ed. Govindgee), pp. 263 343. Academic Press, New York.
  • Berry J.A. & Farquhar G.D. (1978) The CO2 concentrating function of C4 photosynthesis. A biochemical model. In Proceedings of the Fourth International Congress on Photosynthesis (eds D.O. Hall, J. Coombs & T.W. Goodwin), pp. 119 131. The Biochemical Society, London.
  • Brown R.H. (1999) Agronomic implications of C4 photosynthesis. In C4 Plant Biology (eds R.F. Sage & R.K. Monson), pp. 473 507. Academic Press, San Diego.
  • Brown R.H. & Byrd G.T. (1993) Estimation of bundle sheath cell conductance in C4 species and O2 insensitivity of photosynthesis. Plant Physiology 103, 1183 1188.
  • Bunce J.A. (1993) Effects of doubled atmospheric carbon dioxide concentration on the response of assimilation and conductance to humidity. Plant, Cell and Environment 16, 189 197.
  • Carlson R.W. & Bazzaz F.A. (1980) The effects of elevated CO2 concentrations on growth, photosynthesis, transpiration, and water use efficiency of plants. In Environmental and Climatic Impacts of Coal Utilization (eds J.J. Singh & A. Deepak), pp. 609 622. Academic Press, New York.
  • Carter D.R. & Peterson K.M. (1983) Effects of a CO2-enriched atmosphere on the growth and competitive interaction of a C3 and a C4 grass. Oecologia 58, 188 193.
  • Collatz G.J., Berry J.A., Clark J.S. (1999) Effects of climate and atmospheric CO2 partial pressure on the global distribution of C4 grasses: present, past and future. Oecologia 114, 441 454.DOI: 10.1007/s004420050468
  • Conroy J.P., Virgona J.M., Smillie R.M., Barlow E.W.R. (1988) Influence of drought acclimation and CO2 enrichment on osmotic adjustment and chlorophyll a fluorescence of sunflower during drought. Plant Physiology 86, 1108 1115.
  • Cure J.D. & Acock B. (1986) Crop responses to carbon dioxide doubling: a literature survey. Agricultural and Forest Meteorology 38, 127 145.
  • Curtis P.S., Drake B.G., Leadley P.W., Arp W.J., Whigham D.F. (1989) Growth and senescence in plant communities exposed to elevated CO2 concentrations on an estuarine marsh. Oecologia 78, 20 29.
  • Dai Z., Ku M.S.B., Edwards G.E. (1995) C4 photosynthesis. The effects of leaf development on the CO2-concentrating mechanism and photorespiration in maize. Plant Physiology 107, 815 825.
  • Davies W. & Zhang J. (1991) Root signals and the regulation of growth and development of plants in drying soil. Annual Review of Plant Physiology and Plant Molecular Biology 45, 55 76.
  • Dengler N.G. & Nelson T. (1999) Leaf structure and development in C4 plants. In C4 Plant Biology (eds R.F. Sage & R.K. Monson), pp. 133 172. Academic Press, San Diego, CA.
  • Dengler N.G., Dengler R.E., Donnelly P.M., Hattersley P.W. (1994) Quantitative leaf anatomy of C3 and C4 grasses (Poaceae): bundle sheath and mesophyll surface area relationships. Annals of Botany 73, 241 255.DOI: 10.1006/anbo.1994.1029
  • Dengler N.G., Dengler R.E., Donnelly P.M., Filosa M.F. (1995) Expression of the C4 pattern of photosynthetic enzyme accumulation during leaf development in Atriplex rosea (Chenopodiaceae). American Journal of Botany 82, 318 327.
  • Dever L.V., Bailey K.J., Leegood R.C., Lea P.J. (1997) Control of photosynthesis in Amaranthus edulis mutants with reduced amounts of PEP carboxylase. Australian Journal of Plant Physiology 24, 469 476.
  • Drake B.G., Gonzàlez-Meler M.A., Long S.P. (1997) More efficient plants: a consequence of rising atmospheric CO2. Annual Review of Plant Physiology and Plant Molecular Biology 47, 609 637.
  • Drake B.G., Peresta G., Beugling E., Matamala R. (1996) Long-term elevated CO2 exposure in a Chesapeake Bay wetland: ecosystem gas exchange, primary production, and tissue nitrogen. In Carbon Dioxide and Terrestrial Ecosystems (eds G.W. Koch & H.A. Mooney), pp. 179 214. Academic Press, San Diego, CA.
  • Ehleringer J. & Pearcy R.W. (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiology 73, 555 559.
  • Ehleringer J.R., Cerling T.E., Helliker B.R. (1997) C4 photosynthesis, atmospheric CO2 and climate. Oecologia 112, 285 299.DOI: 10.1007/s004420050311
  • Evans J.R. & Von Caemmerer S. (1996) Carbon dioxide diffusion inside leaves. Plant Physiology 110, 339 346.
  • Falkowski P. & Raven J. (1997) Carbon acquisition and assimilation. In Aquatic Photosynthesis (eds P. Falkowski & J. Raven), pp. 128 162. Blackwell Science, Oxford.
  • Farquhar G.D. (1983) On the nature of carbon isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, 205 226.
  • Furbank R.T., Chitty J.A., Von Caemmerer S., Jenkins L.D.C. (1996) Antisense RNA inhibition of rbcsS gene expression reduces Rubisco levels and photosynthesis in the C4 plant Flaveria bidentis. Plant Physiology 111, 725 734.
  • Furbank R.T., Jenkins C.L.D., Hatch M.D. (1989) CO2 concentrating mechanism of C4 photosynthesis. Permeability of isolated bundle sheath cells to inorganic carbon. Plant Physiology 91, 1364 1371.
  • Geiger M., Haake V., Ludewig F., Sonnewald U., Stitt M. (1999) The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco. Plant, Cell and Environment 22, 1177 1199.DOI: 10.1046/j.1365-3040.1999.00466.x
  • Ghannoum O. (1997) Responses of C3 and C4Panicum grasses to CO2 enrichment, PhD Thesis. University of Western Sydney, Hawkesbury, Australia.
  • Ghannoum O. & Conroy J.P. (1998) Nitrogen deficiency precludes a growth response to CO2 enrichment in C3 and C4Panicum grasses. Australian Journal of Plant Physiology 25, 627 636.
  • Ghannoum O., Siebke K., Von Caemmerer S., Conroy J.P. (1998) The photosynthesis of young C4Panicum leaves is not C3-like. Plant, Cell and Environment 21, 1123 1131.
  • Ghannoum O., Von Caemmerer S., Barlow E.W.R., Conroy J.P. (1997) The effect of CO2 enrichment and irradiance on the growth, morphology and gas exchange of a C3 (Panicum laxum) and a C4 (Panicum antidotale) grass. Australian Journal of Plant Physiology 24, 227 237.
  • Grantz D.A. (1990) Plant response to atmospheric humidity. Plant, Cell and Environment 13, 667 679.
  • Grodzinski B., Jiao J., Leonardos E.D. (1998) Estimating photosynthesis and concurrent export rates in C3 and C4 species at ambient and elevated CO2. Plant Physiology 117, 207 215.
  • Hatch M.D. (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81 106.
  • Hatch M.D., Agostino A., Jenkins C.L.D. (1995) Measurement of leakage of CO2 from bundle sheath cells of leaves during C4 photosynthesis. Plant Physiology 108, 173 181.
  • Hattersley P.W. (1982) δ13C values in C4 types in grasses. Australian Journal of Plant Physiology 9, 139 154.
  • Hattersley P.W. & Watson L. (1992) Diversification of photosynthesis. In Grass Evolution and Diversification (ed. G.P. Chapman), pp. 38 116. Cambridge University Press, Cambridge.
  • He D. & Edwards G.E. (1996) Estimation of diffusive resistance of bundle sheath cells to CO2 from modelling of C4 photosynthesis. Photosynthesis Research 49, 195 208.
  • Henderson S., Hattersley P.W., Von Caemmerer S., Osmond C.B. (1994) Are C4 pathway plants threatened by global climate change. In Ecological Studies, Vol. 100 (Ecophysiology of Photosynthesis) (eds E.-D. Schulze & M. Caldwell), pp. 529 549. Springer-Verlag, New York.
  • Henderson S., Von Caemmerer S., Farquhar G.D. (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Australian Journal of Plant Physiology 19, 263 285.
  • Hogan K.P., Smith A.P., Ziska L.H. (1991) Potential effects of elevated CO2 and changes in temperature on tropical plants. Plant, Cell and Environment 14, 763 778.
  • Howden S.M., McKeon G.M., Carter J.O., Beswick A. (1999a) Potential global change impacts on C3-C4 distributions in eastern Australian rangelands. In People and Rangelands: Building the Future. Proceedings of the VI International Rangeland Congress, Townsville, Australia (eds D. Eldridge & D. Freudenberger), pp. 41 43. International Rangeland Congress, Ait Kenvale, Australia.
  • Howden S.M., McKeon G.M., Walker L., Carter J.O., Conroy J.P., Hall W.B., Ash A.J., Ghannoum O. (1999b) Global change impacts on native pasture in south-east Queensland, Australia. Environmental Modelling & Software 14, 307 316.DOI: 10.1016/s1364-8152(98)00082-6
  • Hudson G.S., Dengler R.E., Hattersley P.W., Dengler N.G. (1992) Cell-specific expression of Rubisco small subunit and Rubisco activase genes in C3 and C4 species of Atriplex. Australian Journal of Plant Physiology 19, 89 96.
  • Hunt H.W., Elliott E.T., Detling J.K., Morgan J.A., Chen D.-X. (1996) Responses of a C3 and a C4 perennial grass to elevated CO2 and temperature under different water regimes. Global Change Biology 2, 35 47.
  • Idso K.E. & Idso S.B. (1994) Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years. Agricultural and Forest Meteorology 69, 153 203.
  • Idso S.B., Kimball B.A., Mauney J.R. (1987) Atmospheric carbon dioxide enrichment effects on cotton midday foliage temperature: implications for plant water use and crop yield. Agronomy Journal 79, 667 672.
  • Jarvis A.J., Mansfield T.A., Davies W.J. (1999) Stomatal behaviour, photosynthesis and transpiration under rising CO2. Plant, Cell and Environment 22, 639 648.DOI: 10.1046/j.1365-3040.1999.00407.x
  • Jenkins C.L.D., Furbank R.T., Hatch M.D. (1989a) Inorganic carbon diffusion between C4 mesophyll and bundle sheath cells. Direct bundle CO2 assimilation in intact leaves in the presence of an inhibitor of the C4 pathway. Plant Physiology 91, 1356 1363.
  • Jenkins C.L.D., Furbank R.T., Hatch M.D. (1989b) Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxyphosphinoylmethyl) propenoate on photosynthesis. C4 selectivity and studies on C4 photosynthesis. Plant Physiology 89, 1231 1237.
  • Kimball B.A. (1983) Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agronomy Journal 75, 779 788.
  • Kramer J.P. & Boyer J.S. (1995) Growth. In Water Relations of Plants and Soils (eds P.J. Kramer & J.S. Boyer), pp. 344 376. Academic Press, San Diego. CA.
  • Langdale J.A., Rothermel B.A., Nelson T. (1988a) Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes and Development 2, 106 115.
  • Langdale J.A., Zelitch I., Miller E., Nelson T. (1988b) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO Journal 7, 3643 3651.
  • Lawlor D.W. & Fock H. (1978) Photosynthesis, respiration, and carbon assimilation in water-stressed maize at two oxygen concentrations. Journal of Experimental Botany 29, 579 593.
  • Le Cain D.R. & Morgan J.A. (1998) Growth, gas exchange, leaf nitrogen and carbohydrate concentrations in NAD-ME and NADP-ME C4 grasses grown in elevated CO2. Physiologia Plantarum 102, 297 306.
  • Leegood R.C. & Von Caemmerer S. (1989) Some relationships between contents of photosynthetic intermediates and the rate of photosynthetic carbon assimilation in leaves of Zea mays L. Planta 178, 258 266.
  • Lloyd J. & Farquhar G.D. (1994) 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99, 201 215.
  • Long S.P. (1999) Environmental responses. In C4 Plant Biology (eds R.F. Sage & R.K. Monson), pp. 215 249. Academic Press, San Diego, CA.
  • Ludlow M.M. & Wilson G.L. (1971) Photosynthesis of tropical pasture plants. I. Illuminance, carbon dioxide concentration, leaf temperature, and leaf-air vapour pressure difference. Australian Journal of Biological Sciences 24, 449 470.
  • Mayfield S.P. & Taylor W.C. (1984) The appearance of photosynthetic proteins in developing maize leaves. Planta 161, 481 486.
  • Mjwara J.M. & Botha C.E.J. (1993) The interactive effects of light, temperature and CO2/O2 ratio on photosynthesis of Coix lachryma-jobi L. South African Journal of Botany 59, 377 384.
  • Moore B.D. & Edwards G.E. (1986) Photosynthetic induction in a C4 dicot, Flaveria trinervia, of products of 14CO2 fixation after different illumination times. Plant Physiology 81, 669 673.
  • Moore B.D., Cheng S.-H., Edwards G.E. (1986) The influence of leaf development on the expression of C4 metabolism in Flaveria trinervia, a C4 dicot. Plant Cell Physiology 27, 1159 1167.
  • Morgan J.A., Hunt H.W., Monz C.A., Le Cain D.R. (1994) Consequences of growth at two carbon dioxide concentrations and two temperatures for leaf gas exchange in Pascopyrum smithii (C3) and Bouteloua gracilis (C4). Plant, Cell and Environment 17, 1023 1033.
  • Morison J.I.L. & Gifford R.M. (1984a) Plant growth and water use with limited water supply in high CO2 concentrations. II. Plant dry weight, partitioning and water use efficiency. Australian Journal of Plant Physiology 11, 375 384.
  • Morison J.I.L. & Gifford R.M. (1984b) Plant growth and water use with limited water supply in high CO2 concentrations. I. Leaf area, water use and transpiration. Australian Journal of Plant Physiology 11, 361 374.
  • Morison J.I.L. & Lawlor D.V. (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant, Cell and Environment 22, 659 682.DOI: 10.1046/j.1365-3040.1999.00443.x
  • Nelson T. & Langdale J.A. (1989) Patterns of leaf development in C4 plants. Plant Cell 1, 3 13.
  • Nobel P.S., Israel A.A., Wang N. (1996) Growth, CO2 uptake, and responses of the carboxylating enzymes to inorganic carbon in two highly productive CAM species at current and doubled CO2 concentrations. Plant, Cell and Environment 19, 585 592.
  • Owensby C.E., Auen L.M., Coyne P.L. (1994) Biomass production in a nitrogen-fertilized, tallgrass prairie ecosystem exposed to ambient and elevated levels of CO2. Plant and Soil 165, 105 113.
  • Owensby C.E., Coyne P.I., Ham J.M., Auen L.M., Knapp A.K. (1993) Biomass production in a tallgrass prairie ecosystem exposed to ambient and elevated CO2. Ecological Applications 3, 644 653.
  • Owensby C.E., Ham J.M., Knapp A.K., Bremer D., Auen L.M. (1997) Water vapour fluxes and their impact under elevated CO2 in a C4-tallgrass prairie. Global Change Biology 3, 189 195.
  • Passioura J.B. (1988) Root signals control leaf expansion in wheat seedlings growing in drying soils. Australian Journal of Plant Physiology 15, 687 693.
  • Patterson D.T. & Flint E.P. (1980) Potential effects of global atmospheric CO2 enrichment on the growth and competitiveness of C3 and C4 weeds and crop plants. Weed Science 28, 71 75.
  • Polley H.W., Mayeux H.S., Johnson H.B., Tischler C.R. (1997) Viewpoint: atmospheric CO2, soil water and shrub/grass ratios on rangelands. Journal of Range Management 50, 278 284.
  • Poorter H. (1993) Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104/105, 77 97.
  • Poorter H., Gifford R.G., Kriedemann P.E., Wong S.C. (1992) A quantitative analysis of dark respiration and carbon content as factors in the growth response of plants to elevated CO2. Australian Journal of Botany 40, 501 513.
  • Poorter H., Roumet C., Campbell B.D. (1996) Interspecific variation in the growth response of plants to elevated CO2: A search for functional types . In Carbon Dioxide, Populations, and Communities (eds C. Körner & F.A. Bazzaz), pp. 375 412. Academic Press, New York.
  • Ranjith S.A., Meinzer F.C., Perry M.H., Thom M. (1995) Partitioning of carboxylase activity in nitrogen-stressed sugarcane and its relation to bundle sheath leakiness to CO2, photosynthesis and carbon isotope discrimination. Australian Journal of Plant Physiology 22, 903 911.
  • Read J.J. & Morgan J.A. (1996) Growth and partitioning in Pascopyrum smithii (C3) and Bouteloua gracilis (C4) as influenced by carbon dioxide and temperature. Annals of Botany 77, 487 496.DOI: 10.1006/anbo.1996.0059
  • Riechers G.H. & Strain B.R. (1988) Growth of blue grama (Bouteloua gracilis) in response to atmospheric CO2 enrichment. Canadian Journal of Botany 66, 1570 1573.
  • Rogers H.H., Bingham G.E., Cure J.D., Smith J.M., Surano K.A. (1983) Responses of selected plant species to elevated carbon dioxide in the field. Journal of Environmental Quality 12, 569 574.
  • Saliendra N.Z., Meinzer F.C., Perry M., Thom M. (1996) Associations between partitioning of carboxylase activity and bundle sheath leakiness to CO2, carbon isotope discrimination, photosynthesis, and growth in sugarcane. Journal of Experimental Botany 47, 907 914.
  • Samarakoon A.B. & Gifford R.M. (1995) Soil water content under plants at high CO2 concentration and interactions with the direct CO2 effects: a species comparison. Journal of Biogeography 22, 193 202.
  • Samarakoon A.B. & Gifford R.M. (1996) Elevated CO2 effects on water use and growth of maize in wet and drying soil. Australian Journal of Plant Physiology 23, 53 62.
  • Schmitt M.R. & Edwards G.E. (1981) Photosynthetic capacity and nitrogen use efficiency of maize, wheat and rice: a comparison between C3 and C4 photosynthesis. Journal of Experimental Botany 32, 459 466.
  • Seneweera S.P., Ghannoum O., Conroy J. (1998) High vapour pressure deficit and low soil water availability enhance shoot growth responses of a C4 grass (Panicum coloratum cv. Bambatsi) to CO2 enrichment. Australian Journal of Plant Physiology 25, 287 292.
  • Sheen J.-Y. & Bogard L. (1985) Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiology 79, 1072 1076.
  • Sionit N. & Patterson D.T. (1984) Responses of C4 grasses to atmospheric CO2 enrichment. I. Effect of irradiance. Oecologia 65, 30 34.
  • Stitt M. (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell and Environment 14, 741 762.
  • Stitt M. & Krapp A. (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant, Cell and Environment 22, 583 621.DOI: 10.1046/j.1365-3040.1999.00386.x
  • Tremmel D.C. & Patterson D.T. (1993) Responses of soybean and five weeds to CO2 enrichment under two temperature regimes. Canadian Journal of Plant Science 73, 1249 1260.
  • Tyree M.T. & Alexander J.D. (1993) Plant water relations and the effects of elevated CO2: a review and suggestions for future research. Vegetatio 104/105, 47 62.
  • Von Caemmerer S. & Furbank R.T. (1999) The modelling of C4 photosynthesis. In C4 Plant Biology (eds R.F. Sage & R.K. Monson), pp. 173 211. Academic Press, San Diego, CA.
  • Von Caemmerer S., Ludwig M., Millgate A., Farquhar G.D., Price D., Badger M.R., Furbank R.T. (1997) Carbon isotope discrimination during C4 photosynthesis: insights from transgenic plants. Australian Journal of Plant Physiology 24, 487 493.
  • Wand S.J.E. (1999) Ecophysiological responses of Themeda triandra Forsk. & other Southern African C4 grasses to increases in atmospheric CO2 concentrations. PhD Thesis. University of Cape Town, South Africa.
  • Wand S.J.E., Midgley G.F., Jones M.H., Curtis P.S. (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a test of current theories and perceptions. Global Change Biology 5, 723 741.
  • Wang J.-L., Klessing D.F., Berry J.O. (1992) Regulation of C4 gene expression in developing Amaranth leaves. Plant Cell 4, 173 184.
  • Wang J.-L., Turgeon R., Carr J.P., Berry J.O. (1993) Carbon sink-to-source transition is coordinated with establishment of cell-specific gene expression in a C4 plant. Plant Cell 5, 289 296.
  • Wardlaw I.F. (1979) The physiological effects of temperature on plant growth. Proceedings of the Agronomy Society of New Zealand 9, 39 48.
  • Watling J.R. & Press M.C. (1997) How is the relationship between the C4 cereal Sorghum bicolor and the C3 root hemi-parasites Striga hermonthica and Striga asiatica affected by elevated CO2. Plant, Cell and Environment 20, 1292 1300.
  • Watts W.R. (1971) Role of temperature in the regulation of leaf extension in Zea mays. Nature 229, 46 47.
  • Wong S.C. (1979) Elevated atmospheric partial pressure of CO2 and plant growth. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 44, 68 74.
  • Ziska L.H. & Bunce J.A. (1997) Influence of increasing carbon dioxide concentration on the photosynthetic and growth stimulation of selected C4 crops and weeds. Photosynthesis Research 54, 199 208.
  • Ziska L.H. & Bunce J.A. (1999) Effect of elevated carbon dioxide concentration at night on the growth and gas exchange of selected C4 species. Australian Journal of Plant Physiology 26, 71 77.
  • Ziska L.H., Sicher R.C., Bunce J.A. (1999) The impact of elevated carbon dioxide on the growth and gas exchange of three C4 species differing in CO2 leak rates. Physiologia Plantarum 105, 74 80.