Journal of Experimental Botany, Vol. 53, No. 367, pp. 183-193,
February 1, 2002
© 2002 Oxford University Press
Short Papers |
Long-distance CO2 signalling in plants
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
Received 25 September 2001; Accepted 24 October 2001
Abstract
Stomatal numbers are tightly controlled by environmental signals including light intensity and atmospheric CO2 partial pressure. This requires control of epidermal cell development during the early phase of leaf growth and involves changes in both the density of cells on the leaf surface and the proportion of cells that adopt a stomatal fate. This paper reviews the current understanding of how stomata develop and describes recent advances that have given insights into the regulatory mechanisms involved using mutant Arabidopsis plants that implicates a role for long-chain fatty acids in cell-to-cell communication. Evidence is presented which indicates that long-distance signalling from mature to newly developing leaves forms part of the mechanism by which stomatal development responds to environmental cues. Analysis of mutant plants suggests that the plant hormones abscisic acid, ethylene and jasmonates are implicated in the long-distance signalling pathway and that the action may be mediated by reactive oxygen species.
Key words: ABA, Arabidopsis, cell development, CO2, ethylene, jasmonates, leaf development, mutants, plant hormones, ROS, signalling, stomata.
Introduction
On an annual basis 300x1015 g of carbon pass through stomata (40% of the carbon in the atmosphere) and 120x1015 g are assimilated as gross primary production (Ciais et al., 1997
). The pathway of CO2 moving into a plant via stomata is almost universal in vascular land plants, with only few notable exceptions such as Stylites andicola with no stomata (Keely et al., 1984) and species where stomata have been modified for other functions such as the extrafloral nectaries of Cuscuta reflexa (Hibberd et al., 1998). A plentiful supply of CO2 is required as the enzyme responsible for photosynthetic CO2 fixation (Rubisco) has a low affinity for CO2 and is also able to catalyse a second competing and wasteful reaction that uses the much more abundant gas oxygen in a process known as photorespiration. Increased concentrations of CO2, therefore, enhance the photosynthetic rate by increasing the rate of Rubisco carboxylation and decreasing Rubisco oxygenation.
A consequence of having open pores on the surface of a plant is that there is a high rate of water loss, frequently at more than 100 times the rate of CO2 fixation. About 30–40x1018 g of water vapour are transpired annually through stomata, and this exceeds the atmospheric water content of 13x1018 g (Peixoto and Oort, 1992). Water lost through the stomata has to be replaced by uptake from the soil and this, in turn, is totally dependent on water availability that, in many environments, is scarce. The aperture of the stomatal pore must therefore reflect a compromise between the photosynthetic requirement for CO2 and the availability of water (Jarvis and Davies, 1998). This regulation occurs by a variety of mechanisms that allow the stomatal aperture to respond to changes in light intensity, CO2 concentration and water availability. The nature of these signal transduction pathways is outside the scope of this paper but the reader is referred to an excellent recent review (Schroeder et al., 2001).
Stomatal development and cellular signalling
A second and more recent observation is that the number and pattern of stomata within the epidermis of photosynthetic tissues is also tightly controlled (Croxdale, 2000). Leaves develop from cells at the margin of the shoot apical meristem (SAM). Initially, a swelling of this region occurs which is thought to require alterations of cell wall properties to allow cell expansion and ‘slippage’. In dicotyledonous plants, three layers of cells arise and are maintained within the leaf meristem by periclinal cell divisions. These are referred to as L1, L2 and L3 in dicotyledonous plants (McHale, 1993). For monocotyledonous plants this is reduced to two cell layers (L1 and L2). The epidermis is derived from the L1 layer of the leaf meristem, itself derived from peripheral cells of the shoot apical meristem. Control of the planes of cell division lead to an expansion of the leaf meristem and a flattening of the structure, forming an early flattened blade-like structure. After this stage leaf morphogenesis proceeds and sub-domains or sub-organ identities begin to develop. These follow the three major axes of the leaf; abaxial–adaxial, apical–basal and proximal or distal (leaf margin) to the central mid-rib. The adaxial and abaxial leaf-surfaces arise from leaf polarity that develops very early in leaf development (McConnell and Barton, 1998). The abaxial surface (surface facing away from the axis) grows faster and differentiates earlier than the adaxial surface causing the leaf blade to curl around the apical meristem. This curling of developing leaves around the meristem and other developing leaves restricts exposure of these leaves to the atmosphere and, as discussed later, potentially reduces the ability of developing leaves to interpret the surrounding environment correctly. Mutants exist where leaves are ad- or abaxialized. The phantastica mutation of Antirrhinum produces radially symmetrical leaves that are thought to arise due a loss of leaf polarity and hence are completely abaxialized. It is proposed that this gene encodes a product that confers the adaxial identity necessary for the initiation of the leaf-blade structure (Waites and Hudson, 1995). More recently, two genes (phabulosa and phavoluta) have been implicated in determining abaxial/adaxial leaf polarity; mutations of these genes transform abaxial leaf fate into adaxial leaf fate by altering the predicted sterol/lipid-binding domains of two proteins (McConnell et al., 2001). This separation of leaf surfaces is important for subsequent stomatal development as both numbers and density of stomata can vary between the upper and lower surface of a leaf.
Cells within the leaf epidermis divide to maintain a sheet-like structure of simple pavement cells that will eventually form the flattened interlocking cells characteristic of the leaf surface. These cells occasionally acquire meristemoid mother cell identity and divide asymmetrically giving rise to a large and a small daughter cell. The smaller is a meristemoid cell, as it now has the ability to differentiate into other cell types including stomata (Croxdale, 2000). In monocotyledonous plants the smaller cell invariably divides symmetrically to form the pair of guard cells that form the stoma; additionally, the four adjacent pavement cells on all sides are induced to divide asymmetrically and the smaller cells form the subsidiary cells that make up the stomatal complex. The initial asymmetric division orientates the smaller daughter cell towards the apex of the leaf causing a uniform pattern of complexes to emerge, giving rise to the files of stomata typical of monocotyledonous leaves (Croxdale, 2000). This pattern of cell division also ensures that stoma are always separated by at least one cell and are never adjacent. Pavement cells always divide in a transverse orientation and the pattern of stomatal development is largely fixed so the number of stomata initials within the leaf surface is determined at an early and particular stage of leaf differentiation when epidermal cells become specified as stomatal progenitors. In dicotyledonous plants the pattern of development is more complex and variable, but is always initiated by an asymmetric division of an epidermal cell. The smaller cell can then undergo further asymmetric divisions. Only one of the progeny (the smaller cell) can subsequently form a guard cell pair after a further symmetrical division. Rarely do stomata appear adjacently on the epidermis. It is proposed that this results from cell-to-cell communication (Geisler et al., 2000), which prohibits cells adjacent to two stomata or their precursors from assuming meristemoid mother cell identity. In situations where two smaller daughter cells do appear next to each other then a correction procedure is employed, whereby subsequent divisions are orientated such that guard cells do not develop adjacent to each other or the fate of one meristemoid mother cell is altered and it differentiates as a pavement cell. These data have been suggested to infer cell-to-cell communication of cell fate (Fenoll and Serna, 2001) and the large number of mutants that have been identified further support this view (see below).
Mutants in stomatal development
Several mutants exist in stomatal development, all of which result in increased stomatal number. The mutants flp and tmm (Yang and Sack, 1995) have distinct phenotypes of clustered stomata, suggesting the spatial cues that normally prevent the formation of adjacent stomata are in some way defective. Two further mutants (hic and sdd1), however, may result from lesions in another stomatal-development signalling pathway. HIC encodes a fatty acid elongase that is involved in the control of stomatal development and, particularly, in the response to environmental signals such as CO2 concentration (Gray et al., 2000). SDD1 encodes a subtilisin-like serine protease which, when mutated, causes up to a 4-fold increase in stomatal density (Berger and Altmann, 2000). Interestingly, subtilisins are also known to catalyse the cleavage of systemin from prosystemin during wound signalling in solanaceous plants (although this pathway does not appear to operate in wound signalling in Arabidopsis) and in the processing of CLAVATA3 that represses cell division in the Arabidopsis shoot apical meristem (Fletcher et al., 1999).
Stomatal density is regulated by CO2 concentration
Stomatal development on leaves is measured both as stomatal numbers per unit area (density) and as the fraction of all epidermal cells (index). It has been demonstrated that increases in atmospheric CO2 since the onset of the industrial revolution have occurred in parallel with a decrease in leaf stomatal density (Woodward, 1987). This decrease in density can be replicated experimentally by an increase in atmospheric CO2 concentration of the growth environment (Woodward, 1987; Woodward and Bazzaz, 1988). Stomatal density responses have now been quantified for over 100 species (Woodward and Kelly, 1995). This data set indicates a broad range of responses from decreases to increases in density with CO2 enrichment, although the average response is for a reduction of 30% with a doubling of CO2 concentration (Woodward et al., 2001). The mechanism of this response has remained unknown until recently when a gene (HIC; high carbon dioxide) was identified that was involved in the signal transduction pathway that controls the response of stomatal development to changing CO2 concentration in Arabidopsis (Gray et al., 2000). When the expression of HIC is reduced, plants respond to increasing CO2 by a large increase in stomatal density and index. This contrasts with decreases in stomatal density for wild-type plants grown at elevated CO2. Several other mutants such as tmm and flp (Yang and Sack, 1995) have altered stomatal numbers, however, these invariably result from the formation of stomatal clusters due to impairment of the mechanism that controls stomatal spacing (see above). Changes in density brought about by altered growth CO2 concentration do not result from the formation of stomatal clusters. This suggests that the mechanism for the regulation of stomatal density by the environment is mechanistically different from those cell-to-cell mechanisms that determine stomatal spacing. Perturbation of the HIC gene, which alters the stomatal density response to environmental CO2 concentration, also does not result in the formation of stomatal clusters (Gray et al., 2000) suggesting that this gene may be involved in a separate regulatory pathway.
The CO2 signal is systemic
The question arises as to how and where the CO2 signal is detected and how this integrates with the control of epidermal-cell fate. Although stomatal development continues late into leaf development the vast majority of stomatal formation is complete well before full leaf expansion. It is argued that the generally enclosed nature of developing leaves (see above) precludes them from reliably monitoring atmospheric CO2 concentration as restricted air movement, reduced light intensity, altered humidity, and high respiratory activity would significantly alter the CO2 environment from that encountered by a mature leaf. Mature leaves should best experience and communicate information concerning the nature of the environment to young developing leaves and this would require a systemic signal for the developing leaf. Several long-distance environmental signalling pathways have been identified in plants and include systemic alterations in gene expression in response to high light (Karpinski et al., 2000), wounding (Ryan and Pearce, 1998; Bowles, 1998) and the control of flowering by day length and temperature (Reeves and Coupland, 2000). Systemic signals induced in response to high light signals result in changes of gene expression and biochemical acclimation and are thought to be mediated by the production of hydrogen peroxide (Karpinski et al., 2000). The systemic wound signal is a short peptide, systemin, which is released from prosystemin by a proteolytic cleavage. Systemin is able to travel through the plant and causes production of jasmonate that, together with ethylene, is thought to bring about the wound response (Pearce et al., 1991; O'Donnell et al., 1996). It has recently been demonstrated that a systemic signal is involved in the CO2-mediated changes of stomatal density in Arabidopsis (Lake et al., 2001). Using a gas-tight cuvette system it was possible to maintain mature leaves in environments containing CO2 concentrations different from the newly developing leaves. The stomatal density (Fig. 1a, b) and index (Fig. 1c, d) of newly developed leaves reflected the CO2 concentration experienced by the mature leaves, rather than the environment in which they had developed. This treatment had no effect on leaf expansion (data not shown) or the density of epidermal cells (Fig. 1e, f) indicating that the signal regulating stomatal development controlled, primarily, the extent to which epidermal cells acquired a stomatal fate. The CO2 concentration experienced by the young developing leaves exerted no significant impact on their stomatal index. These data provide clear evidence of a novel long-distance signal that is produced by mature leaves in response to elevated CO2 and that travels to newly developing leaves, affecting their subsequent development. These observations have been verified using a second species, Sinapis alba (Lake, 2001), though it still remains to be established whether this response is common to all plants.
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Biochemical bases of the long-distance stomatal responses to CO2
The roles of phytohormones (ethylene, abscisic acid, gibberellins, cytokinins) in regulating responses to environmental stimuli have been known for some time (Taiz and Zeiger, 1991). Many studies have elucidated the mechanism by which phytohormones integrate with biochemical signal transduction pathways to regulate plant processes (Kende, 1993; Bleecker and Kende, 2000; Keiber, 1997; Leung and Giraudat, 1998; Richards et al., 2001; Mok and Mok, 2001). In addition, a whole range of new signalling molecules has also been discovered, for example, NO3 (Stitt, 1999), PO4, (Sadka et al., 1994) and sugars (Sheen, 1990). These signalling molecules and the regulatory systems that bring them into play can be cell specific (Chrispeels et al., 1999), involve short distance cell-to-cell communication (Zambryski and Crawford, 2000; Fletcher and Meyerowitz, 2000), and longer distance signalling, for example, leaf-to-leaf or root-to-shoot (Bowles, 1998; Havelange et al., 2000).
The use of mutants showing resistance or susceptibility to a particular stress or environmental cue, through defective or deficient biochemistry, have been useful for identifying pathways involved in environmental and developmental responses of plants (Smeekens, 2000). More recently, molecular and genetic techniques have been applied, at very fine levels, to identify the intricacy of the processes involved, such as by transcription and translation of specific genes. A large number of signal transduction pathway mutants of Arabidopsis thaliana have been characterized that have lesions in particular components of a range of signal transduction pathways. As a first step to elucidating the biochemical basis of the systemic CO2 signalling pathway the screening of a selection of these mutants to identify those pathways that may be critical for the long-distance signalling of stomatal responses to changes in CO2 was undertaken. The available mutants were chosen specifically to cover several aspects of the major biochemical pathways involved in long-distance environmental or developmental responses, but were by no means comprehensive.
Some mutations that do not influence stomata
Changes in stomatal index can arise from changes in density of stomatal complexes alone, changes in epidermal cell density alone, or by a combination of changes in both stomatal and epidermal cell densities, each of which may represent a different response. A number of mutants tested showed no effect on the long-distance signalling pathway, however, several mutants did interfere with stomatal density responses to elevated CO2 (Lake, 2001). A summary of these results is provided in Table 1. The mutants fah-1, jar-1 and ed5 show no effect on the long-distance CO2 signalling pathway when tested using this experimental design. The fah-1 gene encodes the enzyme ferulate-5-hydroxylase that is required for the synthesis of sinapate esters, particularly sinapoylmalate, that accumulate in the adaxial epidermis of leaves and provide resistance against UV-B irradiation (Chapple, 1998). These intermediates are also involved in lignin biosynthesis that is frequently linked with plant defence responses and involved in systemic signalling. jar-1 is a jasmonate-insensitive mutant. Jasmonates are known to regulate a variety of plant developmental responses (Creelman and Mullet, 1997) and also to be induced by pathogen attack or wounding which often leads to the generation of oxidative bursts and the generation of reactive oxygen species (ROS) (Lamb and Dixon, 1997). The systemic nature of plant wounding responses and the volatile nature of jasmonates have linked this compound with systemic signalling, though the precise mechanism for long-distance transport remains unclear. ed5 is an uncharacterized ozone-sensitive mutant (P Conklin, personal communication). Several mutants (vtc) have been identified that are ozone-sensitive and these largely have reduced ascorbic acid concentrations (Smirnoff et al., 2001).
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: vitamin C (ascorbate)-deficient, ascorbate pathway mutant (Conklin et al., 1996Involvement of the jasmonate signalling pathway
fad-4, a chloroplastic fatty-acid desaturase-deficient mutant has a mutation in the bi-directional pathway controlling the generation of jasmonates via lipoxygenase (LOX) from linolenic acid. The mutant is devoid of LOX and is therefore jasmonic acid-deficient. Results of the long-distance signalling experiments with the mutant fad-4 suggest that the major LOX-controlled jasmonate cascades, associated with defence and pathogen attack, are involved in the long-term stomatal responses to CO2. This contrasts with the jar-1 mutant which exhibits wild-type stomatal responses to CO2, thereby suggesting that insensitivity to jasmonate and LOX levels does not affect the capacity of plants to acclimate to elevated CO2, with respect to stomatal numbers. The fad-4 mutant, however, does implicate the LOX-controlled pathway by showing a lack of stomatal index response, of both leaf surfaces, indicating a loss of normal responses. As a LOX and therefore, jasmonate-deficient mutant, this suggests that a fully functioning jasmonate pathway may be necessary for these particular responses. The fad-4 mutant also implicates the linolenic acid-derived part of the jasmonate fatty acid pathway, mediated by HPL (hydroperoxide lyase). An interesting study of the fate of fatty acid composition in isolated chloroplasts of Nicotiana tabaccum grown at 700 ppm. CO2, shows that the degree of saturation of fatty acids is generally increased compared to controls; in particular, the accumulation of C16:0 (palmitic acid) and the transition of C16:0 to C16:1 (hexadecanoic acid, the function of the fad-4 desaturase; McCourt et al., 1985) is increased (Radunz et al., 2000). The results here suggest that the fad-4 mutation in some way disrupts this pattern of fatty acid metabolism at elevated CO2, which may affect developmental signalling and processes. The two component parts of fatty-acid metabolism (JA and HPL) have recently been shown to act independently during an investigation of volatile compound release in lime bean in response to wounding, and also that the initial steps of the octadecanoid pathway (lipid peroxidation) occur within chloroplasts (Koch et al., 1999). One part of the pathway may act secondarily to the other in order to differentiate between particular response mechanisms. Interestingly, the recent work by Gray et al., also implicates fatty acid metabolism in the long-term stomatal responses to CO2 enrichment, with the negatively regulating gene, HIC, encoding for a component of the guard cell fatty-acid condensing enzyme (Gray et al., 2000). Other wax biosynthesis mutants (cer1, cer6) also have altered stomatal index (Gray et al., 2000). The fad-4 mutant exhibits a wild-type stomatal density response to CO2, but a lack of response of both leaf surfaces via an epidermal cell density-induced change in stomatal index. This indicates that epidermal cell development has been disrupted. The hic mutant exhibits an increase in stomatal index with elevated CO2 without a concomitant change in epidermal cell density, suggesting that the HIC gene affects stomatal development independently of epidermal cell development, supporting the hypothesis of differential control of these cell types in response to CO2. The fdh (fiddlehead) mutant of Arabidopsis produces aberrant epidermal cell development and is also thought to encode for condensing enzymes of fatty acid metabolism (Yephremov et al., 1999), providing further evidence for the role of fatty acids in regulating epidermal cell development. Several ketoacyl CoA synthase (KCS) genes have now been identified that are associated with fatty acid metabolism and while some KCS gene products appear to be associated with the production of waxes, for example, KCS1, and seed storage lipids (e.g. FAE1) it is becoming clear that other KCS genes, including HIC, play a role in developmental regulation. For example, FDH is involved in controlling the number of trichomes that develop in the epidermis (Yephremov et al., 1999), and CUT1 is necessary for normal stem morphology and pollen fertility (Millar et al., 1999).
Involvement of the ethylene signalling pathway
The mutant ein2 is a strongly ethylene-insensitive mutant, lacking the normal ethylene-induced triple response and showing increased susceptibility to pathogen attack. This mutant is also insensitive to abscisic acid (ABA) (Woest and Keiber, 1998). The ein2 component of the pathway is thought to be membrane bound and central to ethylene-induced and ethylene cross-talking responses, although the cellular location remains unknown (Alonso et al., 1999). Ethylene signalling has been implicated in the development of root epidermal characteristics (Dolan and Roberts, 1995) and in the stomatal patterning of Arabidopsis (Serna and Fenoll, 1997). Results of the ein2 long-distance signalling experiments (Table 1
) show a wild-type response for stomatal density, but a lack of response in stomatal index on the abaxial leaf surface only. Stomatal index of the adaxial leaf surface shows a wild-type response. Epidermal cell density, as in the mutant fad-4, is reduced on both leaf surfaces. A lack of stomatal index response on the abaxial surface suggests that no change in stomatal numbers has occurred relative to epidermal cell numbers, i.e. a lack of stomatal response. A reduction in stomatal index on the adaxial surface suggests the presence of a stomatal response as well as a reduction in epidermal cell numbers. The results obtained with the ein2 mutant therefore indicate that ethylene signalling has an effect on epidermal cell numbers, causing a reduction when mature leaves are supplied with elevated CO2, to both leaf surfaces, but more specifically, ethylene is required for normal stomatal responses on the abaxial leaf surface, independently of an adaxial response.
Differential responses of abaxial and adaxial leaf surfaces, with respect to both development and physiological activity are known. Studies involving mutants of Arabidopsis (Bowman, 2000; McConnell and Barton, 1998) and Antirrhinum majus (Waites and Hudson, 1995) illustrate the independent control of development of each leaf surface. Stomatal aperture control is also independent for each leaf surface, as shown in the amphistomatous species, Rumex obtusifolius, when grown at ambient and elevated CO2 (Pearson et al., 1995). These findings support the view that abaxial and adaxial stomatal development may also be under independent control. Evidence for ethylene-regulated responses specific to the abaxial leaf surface comes from a study of the accumulation of ethylene-induced chitinase and ß-1,3-glucanase proteins, associated with fungal and pathogen attack and normal floral development. Distribution of these products following exogenous ethylene application was confined to the lower epidermis and along vascular strands in bean leaves (Mauch et al., 1992). Berger and Altmann suggested that ethylene may play a regulatory role in stomatal developmental responses, as Arabidopsis seedlings treated with ACC (the ethylene precursor) caused clustering of stomata (Serna and Fenoll 1997), which may be the result of disrupted epidermal cell development, rather than stomatal development (Berger and Altmann, 2000). One ethylene-induced developmental response is the inhibition of cell expansion in leaves (Johnson and Ecker, 1998), which the ein2 phenotype does not exhibit, therefore, the reduction in epidermal cell number in ein2, at elevated CO2, may be due to a lack of inhibition of cell expansion (i.e. cells continue to expand) and implies ethylene-regulation of epidermal cell expansion in the wild-type response.
Involvement of ascorbate and the ROS signalling pathway
The vtc-1 (ascorbate-deficient) mutant exhibits two interesting results when mature leaves are supplied with elevated CO2. The first shows diminished stomatal density (7% decrease compared to 21% decrease in the wild type) and index (4% decrease compared with 8% in the wild type) responses of the abaxial leaf surface, compared to the wild type (Table 1). As the mutant produces only 
30% of wild-type levels of ascorbate (Conklin et al., 1997), the responses of stomatal density and index to CO2 of the abaxial surface may be regulated in part by ascorbate concentrations. The second result is a lack of stomatal density and index responses of the adaxial surface. Epidermal cell densities, although slightly higher than wild-type levels, are not significantly different between ambient and elevated CO2-treated plants. These results again suggest that both stomatal and epidermal numbers of each leaf surface may be regulated independently. The vtc-1 mutant, lacking ascorbate, will exert less control over the detoxification of ROS, and H2O2 in particular. Plants perceive accumulation of H2O2 as a signal of environmental change (Noctor and Foyer, 1998). As a diffusible molecule, H2O2 is now implicated in long distance, or systemic, signalling of several response mechanisms including pathogen-induced systemic acquired resistance (Noctor and Foyer, 1998), drought, heavy metal toxicity, extremes of temperature and atmospheric pollutants (May et al., 1998), and excess light (Karpinski et al., 2000), which appear to be concentration dependent (Foyer et al., 1997).
Research into ozone damage and acclimation responses reveal that ROS are produced apoplastically by the pollutant causing the production of ROS by the plant (Kettunen et al., 1999), again suggesting that ROS concentration may be utilized to differentiate between stresses and produce variable responses. It is also known that some ozone-treated plant species exhibit a change in stomatal density, generally increasing with increasing amounts of ozone. Minnocci et al. found an increase of 37% in stomatal density with a leaf area decrease of 19% and stomatal aperture decrease of 63% in olive plants treated with 100 ppb ozone (Minnocci et al., 1999), whilst Pääkkönen et al. found significant increases in stomatal density of two Betula species in response to increased ozone exposure (Pääkkönen et al., 1997). The results of the vtc-1 mutant support the view that concentration-dependent control of ROS is the most likely effect on stomatal development in these experiments.
The aba-1 mutant response shows a significant increase in stomatal density and index of both leaf surfaces, with no change in epidermal cell numbers when mature leaves are supplied with elevated CO2. The overall stomatal density (400 mm-2) is almost twice that of the wild type. This suggests that abscisic acid may exert a regulatory role over stomatal development in response to CO2. Although in this set of experiments it was not possible to include the parental wild-type, Landsberg, previous work suggests that Landsberg is largely non-responsive under CO2 enrichment, with respect to changes in stomatal density (Woodward et al., 2001). The aba-1 mutant results, however, are of interest in that ABA and elevated CO2 concentration can have synergistic effects on stomatal closure in Arabidopsis, whereby ABA responses are enhanced (Leymarie et al., 1999). Differential roles of ABA in signalling stomatal aperture responses to soil water potential and atmospheric water vapour pressure were found using ABA-deficient and ABA-insensitive mutants (Assmann et al., 2000), suggesting that ABA control is subtle and specific to particular environmental cues.
Involvement of the sugar signalling pathway
The rate of photosynthesis is enhanced under elevated CO2 due to direct effects on the rates of Rubisco carboxylation and oxygenation. This leads to an increase in the rate of carbohydrate production. Plants grown at elevated CO2 often do not sustain this increase in photosynthesis and frequently a down-regulation of photosynthetic gene expression reduces photosynthetic capacity. Carbohydrate accumulation (Van der Kooij et al., 1999) and subsequent repression of photosynthetic gene expression (Cheng et al., 1998) is typically observed in Arabidopsis. Whether this regulation is due to sugar-mediated control of gene expression (Smeekens, 2000) or due to induction of accelerated senescence (Ludewig and Sonnewald, 2000) is unclear. Sugar signalling has recently been identified as a major pathway involved in many responses including up- or down-regulation of photosynthetic capacity (associated with changes in CO2 concentration), and developmental responses, including regulation of the cell-cycle and therefore, growth rate (Riou-Khamlichi et al., 2000). This developmental response is known to be sensitive to CO2 in populations of Dactylis glomerata (Kinsman et al., 1997). Sugar-induced pathways also interact with other signal transduction pathways including ethylene and PAL, as well as integrating responses with ABA and other hormones (Smeekens, 2000). An involvement of sugar-mediated signalling in the systemic signalling of CO2 concentration cannot be ruled out given the direct effect of CO2 on photosynthetic carbohydrate production. However, evidence from variegated leaves where achlorophyllous portions of leaves have functional stomata (Lafray et al., 1991) and much reduced carbohydrate content compared to neighbouring photosynthetic regions (Madore, 1990) show normal reductions in stomatal density in response to elevated CO2 (Beerling and Woodward, 1995). This would suggest that local sugar concentrations were not influencing systemic control of stomatal development. Further, stomatal density is generally lower in the achlorophyllous regions of variegated leaves (Salisbury, 1927; Virgin, 1957) analogous to the effect of increased CO2 despite contrasting concentrations of carbohydrates that prevail in these conditions. A schematic that summarizes our findings with these mutants of Arabidopsis is shown in Fig. 2.
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Conclusion
Following the experimental investigations into long-term stomatal responses to CO2 it is clear that long-term changes in stomatal numbers in the Arabidopsis ecotype Columbia involve signal mechanisms from mature to newly developing leaves. These mechanisms are utilized in responses to both CO2 concentration and irradiance (Lake et al., 2001). The biochemical signal transduction pathways implicated in responses to CO2 suggest that stomatal development is controlled independently from epidermal cell development, both of which operate to optimize stomatal spacing within the epidermis, and that abaxial and adaxial leaf surfaces are also independently controlled. Fatty acid metabolism is strongly implicated in regulating developmental processes of both the abaxial and adaxial epidermis as evidenced by the inhibition of systemic CO2 signalling in the fad-4 mutant and the disruption of stomatal responses to CO2 in the hic mutant (Gray et al., 2000). It is conceivable therefore, that fatty acids may play a crucial, even primary, role in the response pathways of stomatal regulation by CO2 that may involve the LOX-mediated signalling system. A further role in this process for ABA is suggested by a lack of normal wild-type responses of systemic CO2 signalling in the ABA-deficient (aba-1) mutant. It is intriguing that ABA, a hormone central to the biochemical functioning of stomata, may also influence stomatal development. Ascorbate also appears to play an important role in this signalling response albeit on the adaxial surface; its role in the detoxification of ROS could suggest that the concentration of ascorbate could modulate cellular responses to these signalling molecules by altering their concentration in the apoplast. These results would support the recent evidence for the role of ROS in systemic signalling in plants. ROS, and H2O2 in particular, and their control appear to be an important component of the long-distance signal-response to CO2 and ozone (Foyer et al., 1997). Hydroxy fatty acids are known to elicit H2O2 production (Fauth et al., 1998), which is also implicated as a signal molecule in responses to light (Karpinski et al., 1997, 2000) thereby providing a potential signalling link between systemic stomatal responses to both light and CO2 (Lake et al., 2001) and to the involvement of fatty acid metabolism. A role for ethylene in this signal transduction pathway is demonstrated by the inhibition of stomatal response to CO2 in the ethylene-insensitive ein-2 mutant, although this mutant is also known to be ABA-insensitive. This is in line with a previous suggestion for a direct effect of ethylene on stomatal development (Serna and Fenoll, 1997). Further, the specificity of the ethylene response for the abaxial surface provides two pathways for regulating stomatal development independently on both surfaces of the leaf, a phenomenon well known in the literature. A model that illustrates the results obtained from our studies of these signal transduction mutants is shown in Fig. 3; this is clearly preliminary and much more work is required to elucidate the precise nature of these signal transduction pathways. Many more mutants with lesions in different pathways will need to be examined before the entire gambit of signalling pathways is exhausted and the true nature of the systemic CO2 signalling pathway is identified.
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Finally, the question of how plants sense CO2 is one that has not been addressed here thus far, probably because it is the most difficult to answer; however a recent review has discussed this question (Assmann, 1999
) and so this is only briefly mentioned here. No CO2 receptors have yet been identified in any organism, yet it is apparent that many organisms have the ability to respond to CO2, including cyanobacteria (Sultemeyer et al., 1998), algae (Fukuzawa et al., 2001), insects (Keil, 1996), and mammals (Ofelia et al., 1999). The mechanism by which this occurs is still uncertain and whether a true CO2-receptor exists or whether equilibrium of dissolved CO2 with the bicarbonate pool causes pH-induced changes has yet to be established. However, electrophysiological data demonstrates that CO2 can have direct effects on ion channels located in the plasmamembrane (Brearley et al., 1997). Direct evidence for CO2 involvement in signal transduction pathways is at present tenuous, however, a regulatory protein (CCM1) was recently identified from Chlamydomonas that is required for the CO2-mediated induction of the carbon concentration pathway (Fukuzawa et al., 2001), protein phosphorylation is thought to be involved in this induction in cyanobacteria (Sultemeyer et al., 1998) and CO2 activation of HCO3- uptake in mammals has been shown to involve the mitogen-activated protein kinases (MAPK) signal transduction pathway (Ofelia et al., 1999).
Acknowledgments
We would like to thank Dr Julie E Gray for critical reading of the manuscript and Dr P Conklin for donation of seeds. The authors are grateful to the BBSRC (50/P15690) and NERC (ROA13734) for financial support of this work.
Notes
1 To whom correspondence should be addressed. Fax: +44 (0)114 222 0002. E-mail: p.quick{at}sheffield.ac.uk 
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