Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO ₂

Abstract

Net photosynthesis (Pn) is inhibited by moderate heat stress. To elucidate the mechanism of inhibition, we examined the effects of temperature on gas exchange and ribulose 1,5-bisphosphate carboxylase͞oxygenase (Rubisco) activation in cotton and tobacco leaves and compared the responses to those of the isolated enzymes. Depending on the CO 2 concentration, Pn decreased when temperatures exceeded 35-40°C. This response was inconsistent with the response predicted from the properties of fully activated Rubisco. Rubisco deactivated in leaves when temperature was increased and also in response to high CO 2 or low O2. The decrease in Rubisco activation occurred when leaf temperatures exceeded 35°C, whereas the activities of isolated activase and Rubisco were highest at 42°C and >50°C, respectively. In the absence of activase, isolated Rubisco deactivated under catalytic conditions and the rate of deactivation increased with temperature but not with CO 2. The ability of activase to maintain or promote Rubisco activation in vitro also decreased with temperature but was not affected by CO 2. Increasing the activase͞Rubisco ratio reduced Rubisco deactivation at higher temperatures. The results indicate that, as temperature increases, the rate of Rubisco deactivation exceeds the capacity of activase to promote activation. The decrease in Rubisco activation that occurred in leaves at high CO 2 was not caused by a faster rate of deactivation, but by reduced activase activity possibly in response to unfavorable ATP͞ADP ratios. When adjustments were made for changes in activation state, the kinetic properties of Rubisco predicted the response of Pn at high temperature and CO 2.C urrent models of global climate predict a gradual increase in the atmospheric concentrations of greenhouse gases over the next century and associated increases in global temperature (1). The resulting effects on net photosynthesis will have significant ecological and agricultural consequences. For temperate C3 plants, the rate of photosynthesis under current atmospheric conditions exhibits a broad temperature optimum, with the maximum rate occurring near the daytime temperature under which the plants are grown (2). The broad temperature optimum for photosynthesis has been attributed to differential changes in the solubility of CO 2 and O 2 with temperature (3, 4) and to specific changes in the kinetic properties of ribulose 1,5-bisphosphate carboxylase͞oxygenase (Rubisco) (4-6). Increasing the CO 2 concentration above ambient generally increases the temperature optimum for photosynthesis by several degrees (2, 4).Models of photosynthesis have been developed to explain the response of photosynthesis to environmental conditions (7,8). These models make a clear distinction between limitations attributable to Rubisco and those attributable to factors that limit the rate of ribulose-1,5-bisphosphate (RuBP) regeneration, but they usually do not include changes in the activation state of Rubisco among the factors that influence the rate of photosynthesis. Th...

Interactions between temperature, drought and stomatal opening in legumes

“…Previously, elevated temperatures were shown to negatively affect photosynthesis (Feller et al, 1998;Law and Crafts-Brandner, 1999;Haldimann and Feller, 2004), influencing leaf metabolism primarily through Rubisco activase properties and Rubisco activation state (Feller et al, 1998;Crafts-Brandner and Salvucci, 2000;Feller, 2004, 2005). It was also demonstrated that plants increase stomatal conductance under high temperatures (Salvucci and Crafts-Brandner, 2004).…”

Photosynthetic Characteristics of Antisense Transgenic Rice Expressing Reduced Levels of Rubisco Activase

“…In addition to the Rubisco activation activity, Rubisco activase has ATPase activity, and the ATPase activity is inhibited by ADP (Robinson and Portis, 1989b). The ATP/ADP ratio generally decreases under a higher CO 2 condition by an increase in ATP consumption (Gardestrom and Wigge, 1988), and this could down-regulate the activation state of Rubisco under elevated CO 2 conditions (Crafts-Brandner and Salvucci, 2000). Rubisco as well as Rubisco activase levels are considered to become excessive for photosynthesis under high CO 2 condition.…”

“…Rubisco activase is also involved in inhibition of photosynthesis by heat stress. Depending on plant species, the heat stress induces denaturation of Rubisco activase (Crafts-Brandner and Salvucci, 2000;Salvucci et al, 2001), association of Rubisco activase with the thylakoid membrane (Rokka et al, 2001), and appearance of new Rubisco activase isoform (Sánchez et al, 1995;Law et al, 2001), and these result in decreased photosynthetic rates.…”

Two Residues of Rubisco Activase Involved in Recognition of the Rubisco Substrate

“…Cotton Activase-Procedures for the purification and assay of cotton Rubisco and the ␤-form of recombinant cotton activase have been described in detail previously (28,31,32). Point mutations were introduced into the cotton activase cDNA using the Gene Tailor kit according to the manufacturer's instructions (Invitrogen).…”