Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum

Journal of Experimental Botany, Feb 2005

The balance between the capacities of RuBP (ribulose-1,5-bisphosphate) carboxylation (Vcmax) and RuBP regeneration (expressed as the maximum electron transport rate, Jmax) determines the CO2 dependence of the photosynthetic rate. As it has been suggested that this balance changes depending on the growth temperature, the hypothesis that the seasonal change in air temperature affects the balance and modulates the CO2 response of photosynthesis was tested. Vcmax and Jmax were determined in summer and autumn for young and old leaves of Polygonum cuspidatum grown at two CO2 concentrations (370 and 700 μmol mol−1). Elevated CO2 concentration tended to reduce both Vcmax and Jmax without changing the Jmax:Vcmax ratio. The seasonal environment, on the other hand, altered the ratio such that the Jmax:Vcmax ratio was higher in autumn leaves than summer leaves. This alternation made the photosynthetic rate more dependent on CO2 concentration in autumn. Therefore, when photosynthetic rates were compared at growth CO2 concentration, the stimulation in photosynthetic rate was higher in young-autumn than in young-summer leaves. In old-autumn leaves, the stimulation of photosynthesis brought by a change in the Jmax:Vcmax ratio was partly offset by accelerated leaf senescence under elevated CO2. Across the two seasons and the two CO2 concentrations, Vcmax was strongly correlated with Rubisco and Jmax with cytochrome f content. These results suggest that seasonal change in climate affects the relative amounts of photosynthetic proteins, which in turn affect the CO2 response of photosynthesis.

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Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum

Yusuke Onoda 0 Kouki Hikosaka 0 Tadaki Hirose 0 0 Graduate School of Life Sciences, Tohoku University , Aoba, Sendai 980-8578, Japan The balance between the capacities of RuBP (ribulose1,5-bisphosphate) carboxylation (Vcmax) and RuBP regeneration (expressed as the maximum electron transport rate, Jmax) determines the CO2 dependence of the photosynthetic rate. As it has been suggested that this balance changes depending on the growth temperature, the hypothesis that the seasonal change in air temperature affects the balance and modulates the CO2 response of photosynthesis was tested. Vcmax and Jmax were determined in summer and autumn for young and old leaves of Polygonum cuspidatum grown at two CO2 concentrations (370 and 700 lmol mol21). Elevated CO2 concentration tended to reduce both Vcmax and Jmax without changing the Jmax:Vcmax ratio. The seasonal environment, on the other hand, altered the ratio such that the Jmax:Vcmax ratio was higher in autumn leaves than summer leaves. This alternation made the photosynthetic rate more dependent on CO2 concentration in autumn. Therefore, when photosynthetic rates were compared at growth CO2 concentration, the stimulation in photosynthetic rate was higher in young-autumn than in young-summer leaves. In old-autumn leaves, the stimulation of photosynthesis brought by a change in the Jmax:Vcmax ratio was partly offset by accelerated leaf senescence under elevated CO2. Across the two seasons and the two CO2 concentrations, Vcmax was strongly correlated with Rubisco and Jmax with cytochrome f content. These results suggest that seasonal change in climate affects the relative amounts of photosynthetic proteins, which in turn affect the CO2 response of photosynthesis. Introduction Because CO2 is a substrate for photosynthesis, elevation of atmospheric CO2 concentration is expected to increase the carbon assimilation of plants (Mott, 1990). Many studies have focused on the photosynthetic response to elevated CO2 concentration with short- and long-term experiments (for a review see Cure and Acock, 1986; Poorter, 1993; Gunderson and Wullschleger, 1994; Curtis, 1996; Curtis and Wang, 1998; Wand et al., 1999). CO2 responses of photosynthesis are determined by stomatal conductance, and the capacity of RuBP (ribulose-1,5-bisphosphate) carboxylation and RuBP regeneration (Farquhar et al., 1980; Mott, 1990). Stomatal conductance regulates the CO2 concentration in the leaf, while RuBP carboxylation and RuBP regeneration limit the photosynthetic rate at low and high CO2 concentrations, respectively. Transition of the limitation from RuBP carboxylation to RuBP regeneration usually occurs between an ambient and a twice-ambient CO2 concentration (Stitt, 1991). Long-term treatment of elevated CO2 modulates the leaf traits and stimulates photosynthesis to various extents (Poorter, 1993; Gunderson and Wullschleger, 1994; Curtis, 1996). Plants grown in elevated CO2 tend to have a lower stomatal conductance (reviewed by Drake et al., 1997; Medlyn et al., 2001) and a lower photosynthetic rate than those grown in ambient CO2 when compared at a given CO2 concentration (for a review see Stitt, 1991; Gunderson and Wullschleger, 1994; Sage, 1994). The lower rate of photosynthesis has been ascribed to a reduction in the capacity of RuBP carboxylation (Vcmax) and/or RuBP regeneration (expressed as the maximum electron transport rate, Jmax) (Sage, 1994). Reduction in Vcmax is usually attributed to decreased amounts of Rubisco (RuBP carboxylase/oxygenase) (Jacob et al., 1995; Nakano et al., 1997; Tissue et al., 1999), and sometimes to a low activation state (Sage et al., 1989; Cook et al., 1998). The mechanism of lowering in Jmax, on the other hand, is less clear, because the capacity of RuBP regeneration is determined through many biochemical steps in electron transport (von Caemmerer and Farquhar, 1981; Evans and Terashima, 1987; Sudo et al., 2003) and the Calvin cycle (Strand et al., 2000; Sudo et al., 2003). Changes in the balance between Vcmax and Jmax also affect the CO2 stimulation of photosynthesis, because the CO2 dependence of the photosynthetic rate is greater when the rate is limited by RuBP carboxylation than by RuBP regeneration (Fig. 2). As Vcmax and Jmax limit the photosynthetic rate at low and high concentrations, respectively, an increase in the Jmax:Vcmax ratio increases the ratio of the photosynthetic rate at high CO2 to that at low CO2 concentrations (Webber et al., 1994; Sage, 1994; Medlyn, 1996; Hikosaka and Hirose, 1998). This indicates that the increase in the Jmax:Vcmax ratio enhances the CO2 stimulation of photosynthesis. Although higher Jmax:Vcmax ratios were reported in several studies in plants grown with elevated CO2 (Sage et al., 1989; Lewis et al., 1996), many studies found no change in the ratio (reviewed by Medlyn et al., 1999). Hence, the effects of changes in the Jmax:Vcmax ratio have been largely discounted in studies of plant response to elevated CO2. Rece (...truncated)


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Yusuke Onoda, Kouki Hikosaka, Tadaki Hirose. Seasonal change in the balance between capacities of RuBP carboxylation and RuBP regeneration affects CO2 response of photosynthesis in Polygonum cuspidatum, Journal of Experimental Botany, 2005, pp. 755-763, 56/412, DOI: 10.1093/jxb/eri052