Journal of Experimental Botany, Vol. 54, No. 383, pp. 867-874,
February 1, 2003
© 2003 Oxford University Press
Photosynthetic performance of an Arabidopsis mutant with elevated stomatal density (sdd1-1) under different light regimes
Received 2 October 2002; Accepted 17 October 2002
Max-Planck-Institute of Molecular Plant Physiology, Am Muhlenberg 1, D-14424 Golm, Germany
1 Present address and to whom correspondence should be sent: Risø National Laboratory, Plant Research Department, PRD-301, PO Box 49, DK-4000 Roskilde, Denmark. Fax: +45 4677 4122. E-mail: urte.schluter{at}risoe.dk
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Abstract |
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In the Arabidopsis mutant sdd1-1, a point mutation in a single gene (SDD1) causes specific alterations in stomatal density and distribution. In comparison to the wild type (C24), abaxial surfaces of sdd1-1 rosette leaves have about 2.5-fold higher stomatal densities. This mutant was used to study the consequence of stomatal density on photosynthesis under various light regimes. The increased stomatal density in the mutant had no significant influence on the leaf CO2 assimilation rate (A) under constant light conditions. Mutant and wild-type plants contained similar amounts of carbohydrates under these conditions. However, exposure of plants to increasing photon flux densities resulted in differences in gas exchange and the carbohydrate metabolism of the wild type and mutant. Increased stomatal densities in sdd1-1 enabled low-light-adapted plants to have 30% higher CO2 assimilation rates compared to the wild type when exposed to high light intensities. After 2 d under high light conditions leaves of sdd1-1 accumulated 30% higher levels of starch and hexoses than wild-type plants.
Key words: Arabidopsis thaliana, gas exchange, photosynthesis, sdd1-1, stomatal density.
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Introduction |
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Stomata are involved in two of the most important plant processes, photosynthesis and transpiration. Opening and closing of the stomatal pores enables terrestrial plants to adjust their gas exchange (uptake of CO2 and evaporation of water) to suit the environmental and physiological conditions. Plant breeders have always had special interest in improving crops by manipulating their stomatal characteristics (Jones, 1987). In principle, an increase in stomatal density (number of stomata per leaf area) could allow plants under well-watered conditions to increase conductance for gas exchange at the leaf surface and, thus, avoid photosynthetic limitation by sub-optimal CO2 supply. Unfortunately, evidence of such benefit is not strong as no simple relationship between stomatal density, photosynthesis and yield has been found. Depending on plant species, positive (Kundu and Tigerstedt, 1998; Araus et al., 1986; Walton, 1974), negative (Heichel, 1971) or a lack of correlation (Miskin et al., 1972; Teare et al., 1971) has been observed between stomatal density, photosynthetic rate and yield of plants. However, general conclusions from these experiments are difficult to obtain, because a comparison of cultivars and species with different genetic backgrounds or with different growth histories (e.g. the comparison of sun and shade leaves; Masarovicova and Stefancik, 1990) were involved. Strong indications for a major influence of stomatal characteristics on yield have been obtained in studies on Pima cotton cultivars with optimized performance under high temperatures (Lu et al., 1998).
An Arabidopsis mutant (sdd1-1) is available that differs from the wild type only in stomatal density and distribution (Berger and Altmann, 2000; von Groll et al., 2002). The affected gene, SDD1, was identified by map-based cloning and encodes a subtilisin-like serine protease related to prokaryotic and eukaryotic proteins. In comparison to the wild type (C24), sdd1-1 mutants exhibit a 2–4-fold increase in stomatal density in nearly all organs and, in addition, form ‘clustered stomata’ in leaves (c. 10% of the stomata are not separated by intervening pavement cells). The apparent sdd1-1 mutant phenotype is restricted to the epidermis. No differences are detectable in terms of tissue organization, leaf size or leaf form compared with the wild type (Berger and Altmann, 2000). The sdd1-1 mutant, therefore, is an excellent system to study the influence of stomatal density on gas exchange and net photosynthesis under varying environmental conditions.
Stomatal morphogenesis is controlled by genetic as well as environmental factors. High light intensities (Gay and Hurd, 1975) or drought (Elias, 1995) can increase stomatal densities in the leaves, while high temperatures and high UV-B (Dai et al., 1995) tend to decrease them. Particularly interesting results have been found for the relationship between stomatal densities and atmospheric CO2 concentrations. It has been demonstrated that a wide range of species show a reduction in stomatal density with CO2 enrichment (Woodward and Kelly, 1995) and that several tree species respond to atmospheric CO2 concentrations by an alteration in stomatal density (Woodward and Bazzaz, 1988; McElwain and Chaloner, 1995; Beerling et al., 1998). Furthermore, responses of stomatal development to light intensity or CO2 concentration have been shown to involve signalling from mature leaves to the developing leaves (Schoch et al., 1980; Lake et al., 2001).
Stomatal densities are determined by environmental conditions prevalent during leaf development, but are fixed after maturation of leaves. Therefore, it is of particular relevance to study the effects of altered stomatal densities under different conditions. Here evidence is presented for increased stomatal densities as an important pre-adaptation of low-light-grown plants for optimal photosynthetic performance under high light conditions.
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Materials and methods |
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Growth conditions
Arabidopsis wild-type (cv. C24) and mutant (sdd1-1) plants were grown in standard soil (Einheitserde GS90, Gebrüder Patzer, Sinntal-Jossa, Germany) at 16/8 h light/dark photoperiod (photon flux density (PFD) about 100–200 µmol m–2 s–1); temperature 18/16 °C; 50–60% relative humidity). After 2 weeks the population was divided into three subsets for further growth in the greenhouse (temperature 20–25 °C) under PFD of 80, 200–250 and 300–400 µmol m–2 s–1, respectively. Experiments with plants under changing PFDs during growth were carried out in growth chambers fixed to 120 or 500 µmol m–2 s–1. All experiments were carried out on source rosette leaves at the stage of bolting.
Stomatal density
Nail polish imprints were taken from the abaxial surface of mature leaves from wild-type (C24) and mutant (sdd1-1) plants. Stomatal densities were determined by light microscopy from leaf imprints of five individual wild-type and mutant plants, respectively. Five independent counts were carried out on each leaf.
Gas exchange
Measurements for gas exchange and chlorophyll fluorescence were carried out in a growth chamber (Noske-Kaeser, Germany), where conditions were set to temperatures of 20 °C, 60–70% relative humidity and a PFD of approximately 400 µmol m–2 s–1 (radiation source: Osram HQI TDW 400). Gas exchange measurements were performed on single rosette leaves in a special custom-designed open system developed in collaboration with Walz Inc. (Germany). This system and the experimental procedures for obtaining light-saturating curves were described by Schlüter et al. (2002).
Assimilation curves of wild type and mutant were compared by linear regression of the double reciprocals and calculation of the maximal photosynthetic capacity under light-saturating conditions. Significant differences were determined by t-test. Because no simple function could be applied to the stomatal conductance curves, significant differences between wild type and mutant were calculated separately for measurements at defined light levels by t-test.
Chlorophyll fluorescence
Chlorophyll fluorescence measurements were done with a PAM-2000 pulse amplitude modulated chlorophyll fluorometer (Walz Inc., Germany). At the start of each measurement, a plant was dark adapted for 20 min for determination of Fo and Fm. Then the first level of PFD (50 µmol m–2 s–1) was applied and a set of values was measured after 30 min. The same procedure was repeated for each PFD level (100, 200, 400, 600, 800, and 1000 µmol m–2 s–1). PFD was increased gradually. Leaf illumination was provided by two cold light sources FL-400 (Walz Inc., Germany).
Carbohydrate content
After approximately 8 h of the photoperiod, 100 mg FW rosette leaves were harvested from randomly selected wild-type and mutant plants. Both genotypes were grown intermixed in the same tray. Samples were frozen in liquid nitrogen immediately after harvest and stored at –80 °C. Hexoses (glucose and fructose), sucrose and starch contents were determined enzymatically as described by Trethewey et al. (1998). Significant differences between the carbohydrate contents were determined by t-test.
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Results |
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Stomatal density
Stomatal density, stomatal index and other parameters describing leaf morphology of the sdd1-1 mutant were examined in an earlier paper (Berger and Altmann, 2000). Stomatal density of sdd1-1 rosette leaves was found to be elevated 2–4-fold in all plant organs. Increases in light supply during growth lead to parallel increases in both adaxial and abaxial stomatal density of rosette leaves, values for the abaxial surface were about 20% higher than for the adaxial surface (Berger, 1997). When grown under 150 µmol m–2 s–1, the stomatal index (SI) on the abaxial surfaces of primary leaves was shifted from 25% in the wild type to 37% in sdd1-1. In these experiments, plants were grown under three different light regimes (low light, 80 µmol m–2 s–1; intermediate light, 250 µmol m–2 s–1; high light, 300–400 µmol m–2 s–1) and the effects of light intensity on abaxial stomatal densities were checked. Stomatal densities on the abaxial leaf surface of mature rosette leaves were, in sdd1-1, at least doubled when compared with the wild type under all conditions (Table 1). Furthermore, increasing light intensities caused an increase in stomatal density of the abaxial leaf surface of both wild-type and mutant plants (Table 1).
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Gas exchange
Under all three constant light treatments, the conductance curve of the mutant with increased stomatal density lay above the conductance curve of the wild type (Fig. 1A–C). These differences were most pronounced for the medium- and high-light-adapted leaves, where significant differences in stomatal conductance of wild-type and mutant were determined under PFDs of 400–800 µmol m–2 s–1 (P
0.05). It should be kept in mind that, as shown in Table 1, growth under high irradiance caused increases in stomatal densities of both wild-type and mutant plants of about 50–60% when compared with those that grew under low light. Furthermore, there were differences in the shape of the conductance curves. In the wild type, stomatal conductance rose under increasing PFD reaching a maximal level under saturating light conditions, while conductance in sdd1-1 leaves seemed to drop again under saturating light conditions.
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CO2 uptake rates for the wild type and sdd1-1 mutant did not show a uniform picture under the three constant light treatments applied (Fig. 1E–G). There were no differences in the assimilation response of the wild type and mutant when grown under low light conditions. When adapted to medium light conditions the sdd1-1 mutant plants seemed to have higher assimilatory capacity than the wild type, especially above a PFD of 200–250 µmol m–2 s–1. However, calculated maximal photosynthetic rates for the mutant and the wild type just failed to be significantly different (P=0.059). The increased stomatal conductance in high-light-adapted plants did not correlate with substantial changes in the assimilatory performance.
Stomatal limitation can play a major role in photosynthetic performance under fluctuating environmental conditions or under stress. CO2 assimilation rate curves obtained under intermediate light indicated that elevated stomatal density could stimulate photosynthesis in plants shifted to higher photon flux densities. The potential advantages of the mutant sdd1-1 were, therefore, checked when plants were precultured under constant light intensities of 120 µmol m–2 s–1 and subsequently shifted for 2 d to high light conditions (500 µmol m–2 s–1). Because mature leaves finished their development before the transfer to higher light intensities their morphology was not altered further. Leaves of sdd1-1 and wild-type plants possessed stomatal densities comparable to those of low-light-grown plants (Table 1). However, 2 d under high light conditions allowed the plants to undergo biochemical adaptation. Under these conditions the calculated maximal photosynthetic capacity of sdd1-1 was indeed significantly increased by 30% in comparison to the wild type (P=0.009; Fig. 1H). Stomatal conductance under saturating light levels on the other hand was increased in the mutant but failed to be significantly altered (P=0.12; Fig. 1D). The high conductance, especially in the mutant, at the start of the experiment is probably due to insufficient adaptation of the leaves to the conditions in the measuring chamber.
Chlorophyll fluorescence
The control of stomatal density on primary photosynthetic reactions was investigated via measurements of chlorophyll fluorescence (electron transport rate, ETR, and non-photochemical quenching, qN). Measurements of chlorophyll fluorescence were generally in line with the results obtained for CO2 assimilation (Fig. 2). When grown under low light conditions no differences occurred in fluorescence parameters between mutant and wild-type plants. Low levels of electron transport rates (ETR) in both mutant and wild-type leaves support the hypothesis that the capacity of photosynthetic electron transport and carbon assimilation was limiting for photosynthesis under these conditions. The increased photosynthetic capacity of plants grown at intermediate light intensities was also reflected in the fluorescence measurements by increased ETR at saturating photon flux density. Leaves of sdd1-1 displayed ETRs increased by up to 25% compared to wild-type plants under these conditions (Fig. 2B). Leaves of wild-type plants on the other hand dissipated more energy via non-photochemical reactions as shown by measurements of qN (Fig. 2D–F). High-light-grown plants did not show any significant differences in ETR or qN. A slight reduction of ETR in sdd1-1 plants when compared to the wild type was only observed at saturating photon flux densities.
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Carbohydrate content of leaves
Carbohydrate levels in leaves were generally increased with increased photon flux density during growth, but leaves from mutant and wild-type plants accumulated similar amounts of carbohydrates in the constant light level treatments (Fig. 3).
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In plants which were shifted from low to high light conditions for 2 d, the increased CO2 fixation rates of the mutant also resulted in enhanced carbohydrate accumulation. Leaves of sdd1-1 accumulated about 30% higher amounts of hexoses (P=0.01) and starch (P=0.004) under these circumstances (Fig. 3D). Interestingly, both wild-type and mutant plants, which were transferred from low to high light conditions, contained significantly increased amounts of carbohydrates when compared with plants which grew continuously under high light intensities. Factors such as carbohydrate partitioning or differences in metabolic activity could be responsible for this discrepancy.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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Mutation of the SDD1 gene results in a 2.5-fold increase of stomatal density in Arabidopsis rosette leaves, but no other apparent features of leaf morphology are altered (Berger and Altmann, 2000). The enhancement of stomatal density could be observed under various environmental conditions. Exposure to increasing light intensities causes a parallel increase in the stomatal density of the wild type and the mutant. This shows that the mechanisms responsible for light-dependent adjustment of stomatal density are still active in the mutant and are, therefore, independent of SDD1 activity. These results indicate that environmental parameters may influence stomatal density through a different signalling pathway, or be downstream of SDD1 within the same signalling cascade. Recently, an Arabidopsis gene (HIC for high carbon dioxide) has been identified which is involved in regulation of stomatal densities under elevated CO2 (Gray et al., 2000). In contrast to SDD1 the HIC gene did not seem to be involved in mechanisms that prevent the formation of stomata that directly contact one another and no clusters occurred (Serna and Fenoll, 2000). It is, therefore, likely that SDD1 is involved in general stomatal pattern formation, but is not responsible for environmentally mediated regulation of stomatal density.
Plants usually optimize their gas exchange by long-term (e.g. stomatal density) and short-term (stomatal opening and closing) adaptation. For the first time now there was a possibility to investigate the performance of mutant plants with enhanced stomatal density under various environmental conditions. In the first experiment, mutant and wild-type plants were exposed to constant growth conditions under three different light regimes. Carbon assimilation rates measured at the light intensities used during growth were not significantly different in wild-type and mutant plants despite the enhancement of stomatal density. This indicates that stomatal limitation of photosynthesis does not represent a major regulatory factor for CO2 assimilation in Arabidopsis plants under constant environmental conditions and factors different from the CO2 supply seem crucial for photosynthetic restriction under these conditions.
Plants which grew under 80 µmol m–2 s–1 received only low light quantities during their development of the photosynthetic apparatus. The synthesis of many proteins involved in photosynthesis, for example, Rubisco, depends on stimulation by light and it is, therefore, likely that the capacity of Rubisco and the following electron transport were limiting under these conditions, rather than CO2 restriction. Therefore, mutant and wild-type plants were affected in the same manner, and the curves for CO2 assimilation were similar. Under low light conditions the elevated stomatal density in the mutant caused only minimal differences in stomatal conductance. It is conceivable that control mechanisms were active in leaves of the mutant plants to balance elevated stomatal density by enhanced stomatal closure. Increased contents of ABA in the leaves of sdd1-1 (up to 3-fold; C Rock, personal communication) also support the hypothesis that regulatory pathways initiating stomatal closure were active.
Adaptation to high light resulted in increased stomatal densities of both the wild type and the mutant (Table 1). Under these conditions, stomatal conductance was elevated in the mutant, but assimilatory rates were similar to the wild type. Presumably, the regeneration of RuBP became the pace-making step in photosynthesis of wild-type and mutant plants (von Caemmerer and Farquar, 1981). The advantages of increased stomatal conductance have been described for Pima cotton lines that grew under high temperatures. Increased conductance probably has no direct influence on the photosynthetic rate, but it is supposed to improve viability in certain plant species under high temperatures by better leaf cooling via transpiration (Lu et al., 1998). In the present experiments, the viability of plants did not differ between the wild type and mutant. The shape of the conductance curves might indicate differences in the stomatal behaviour of the wild type and mutant under high light conditions. However, no clear picture could be drawn from the results presented here and the stomatal behaviour of the mutant with extremely high stomatal density under high light conditions will be an interesting subject for further investigation.
Differences for assimilation and stomatal conductance were observed when mutant and wild-type plants were grown under 200–250 µmol m–2 s–1 and exposed to increasing light intensities. The experiment revealed that, under these conditions, wild-type plants perform photosynthesis close to CO2 limitation. Only mutant plants could use the additionally supplied light for elevated CO2 fixation, as indicated by enhanced assimilatory rates and enhanced ETR. Wild-type plants on the other hand dissipated more energy by non-photochemical quenching.
Growth under constant environmental conditions in the greenhouse is, however, quite artificial. In nature, plants have to cope with frequently changing conditions. In a second experiment, the possible consequences of elevated stomatal densities in sdd1-1 were inspected when plants were grown under low light intensities and subsequently moved to high light conditions for 2 d. Under these conditions, decreased conductance in the wild type correlated with reduced CO2 uptake rates, indicating that, under these conditions, wild-type plants could have faced stomatal limitation. Mutant plants with increased stomatal densities on the other hand converted enhanced amounts of CO2 into stored carbohydrates. These results underline the great importance of light intensities during early leaf development for the final stomatal density of a leaf. It has been shown for several species that modified light regimes for periods as short as 1 d modulate stomatal initiation (Schoch et al., 1980) and can be of major importance for the final stomatal density in mature leaves. Light intensities during stomatal initiation could, therefore, be of particular importance for plants where leaves develop over a relatively short period, but serve much longer as a source of carbohydrates. For deciduous trees, short periods in spring with sub-optimal light conditions could be responsible for periods of non-saturating CO2 supply over the whole of the following growth period.
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Summary |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionSummaryReferences |
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The present data show that, under constant environmental conditions, Arabidopsis possesses a high capacity of morphological, physiological and biochemical adaptation to avoid the stomatal limitation of photosynthesis. However, under conditions where the biochemical capacity of photosynthesis is not yet limiting and light exposure is saturating, insufficient CO2 conductance can become the major cause of photosynthetic limitation. Under natural conditions with fluctuating environmental parameters, this might happen more often than expected, even if only for short periods. An artificial increase of stomatal density via genetic engineering without influencing any other parameter may, therefore, improve productivity in certain species under field conditions. The discovery that, in Arabidopsis, the synthesis of a single protein (SDD1) has such remarkable effects on stomatal density might provide a tool for the further investigation of the effects of stomatal characteristics on the photosynthetic adaptation of plants to various environmental conditions.
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Acknowledgements |
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Special thanks go to Dr Joachim Fisahn for critical reading of the manuscript. The work was carried out at the Max-Planck-Institute for Molecular Plant Physiology in Golm and funded by the Deutsche Forschungsgesellschaft (DFG; Sonderforschungs-bereich 429. We would also like to thank Dietmar Kropp and the gardeners’ team for helping us with the establishment of various growth conditions.
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References |
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