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    Inhibition of photosynthesis by heat stress: Although the catalytic activity of Rubisco increases with temperature, the low affinity of the enzyme for CO2 and its dual nature as an oxygenase limit the possible increase in net photosynthesis with temperature. Inhibition of photosynthesis by moderate heat stress i. However, measurements of chlorophyll fluorescence and metabolite levels at air-levels of CO2. Instead, recent evidence shows that inhibition of net photosynthesis correlates with a decrease in the activation state of Rubisco in both C3 and C4 plants and that this decrease in the amount of active Rubisco can fully account for the temperature response of net photosynthesis. Biochemically, the decrease in Rubisco activation can be attributed to: The net result is that as temperature increases activase becomes less effective in keeping Rubisco catalytically competent. In this opinionated review, we discuss how these processes limit photosynthetic performance under moderate heat stress. Introduction Inhibition of photosynthesis by heat stress is a common occurrence for plants in tropical and subtropical regions and is experienced periodically by plants in the temperate zone Larcher In the field, heat stress often accompanies drought stress, highlighting the importance of water availability for stress avoidance. Plants with access to adequate water keep their stomates open at high temperatures, using evaporative cooling to reduce their leaf temperature. This process works extremely well in hot, arid regions like the desert south-west of the US, where the differential between air and foliar tempera-. In fact, the higher yield of modern cultivars of Pima cotton in these regions has been attributed to a greater capacity for leaf cooling, a direct consequence of increased stomatal control Radin et al.

    That the rate of net photosynthesis in heat stressed leaves increases with increasing CO2 concentration even under non-photorespiratory conditions provides another indication that the capacity for electron transport and RuBP regeneration is in excess under moderate heat stress Crafts-Brandner and Law In fact.

    CO2 and other environmental factors Perchorowicz et al. Law and Crafts-Brandner Rapid extraction and assay of Rubisco has shown that the activation state of Rubisco changes in response to light. When net photosynthesis and chlorophyll fluorescence are measured at air-levels of CO2 in an intact system.

    Recent investigations from our laboratory have re-examined the involvement of RuBP regeneration and Rubisco activation in the inhibition of net photosynthesis by moderate heat stress in both wheat and cotton Feller et al. Bilger et al.

    Havaux This difference represents inhibition of net photosynthesis since it cannot be accounted for by changes in the solubilities of CO2 and O2 and the kinetic properties of Rubisco. At the time. Murakami et al. Sage et al. Inhibition of net photosynthesis by moderate heat stress has often been attributed to the adverse effects of temperature on components of the photosynthetic electron transport. Temperature effects on the activation state of Rubisco Each higher plant-type Rubisco holoenzyme contains eight active sites that appear to function independently of one another reviewed in Spreitzer and Salvucci Feller et al.

    Fm ratio. Since then. Kanechi et al. Yamasaki et al. Rokka et al. Predicted versus observed effects — inhibition of photosynthesis at high temperature The effect of temperature on the kinetic constants of isolated Rubisco can be used to predict the response of photosynthesis to temperature Fig.

    Crafts-Brandner and Law Law and Crafts-Brandner and 14C labelling patterns Weis a. In the normal course of catalysis.

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    The formation of dead-end complexes by the binding of RuBP to decarbamylated sites 2. A third and related property of Rubisco that impacts its activation state is the formation of inhibitory sugar-P by misprotonation of RuBP.

    The first is carbamylation of Rubisco active sites by spontaneous addition of nonsubstrate CO2 to an active site lysine Lorimer In the open conformation. Cleavage of the C-C bond of the reaction intermediate in the last phase of catalysis allows loop 6 to retract. The second property is related to specific conformational changes that accompany the binding of sugar-P Schreuder et al.

    Scheme for de-activation and re-activation of Rubisco. Biochemical mechanism for changes in activation state Detailed biochemical and structural studies have shown that three interrelated properties of Rubisco impact its activation state Fig. The formation of catalytic misfire products asterisk is accelerated at high temperatures. In all three cases.

    RuBP binding triggers extension of loop 6. Extension of loop 6 across the active site. C-C cleavage these sites are very slow to open Duff et al. This binding causes dead-end inhibition because without catalysis and. Carbamylation of this lysine is required for activity since the carbamate participates in metal binding and proton abstraction Cleland et al. Rubisco active sites are represented by the yellow closed conformation or blue open conformation boxes and include loop 6 in red.

    This reaction occurs directly at the active site while the site is in the closed conformation. These changes. The action of activase plus ATP in opening closed sites is indicated by the solid blue arrows. Crafts-Brandner and Salvucci Measurements of chlorophyll fluorescence and metabolite levels at air-levels of CO2 confirm that the potential yield of PSII reaction centres and the availability of RuBP do not decrease at temperatures that inhibit net photosynthesis Law and Crafts-Brandner CraftsBrandner and Law Spreitzer and Salvucci Activase is an AAA1 protein.

    The impact of temperature on these processes has only recently been examined. The carbamylation status was determined by trapping 14CO2 with carboxyarabinitol bisphosphate Edmondson et al. Portis et al. Under non-stress conditions.

    To overcome dead-end inhibition of Rubisco. More recently. To our knowledge. Catalytically competent active sites were determined by measuring Rubisco activity Crafts-Brandner and Salvucci As with other AAA1 proteins activase functions as a molecular chaperone. Effect of temperature on carbamylation level and the catalytic competency of Rubisco.

    In vitro measurements have shown that as temperature increases. To understand the mechanism of Rubisco de-activation at high temperature. Rubisco de-activates under catalytic conditions because of increased rates of misfire product formation. In vivo. The results show that. Isolated cotton Rubisco 0. In the absence of activase. Activase rescues Rubisco sites from dead-end inhibition by promoting ATP-dependent conformational changes that open closed sites.

    Effect of temperature on de-activation of Rubisco and its reversal by activase Under steady-state conditions the activation state of Rubisco in leaves represents a dynamic balance between the rates of Rubisco de-activation and re-activation i. Without activase. The shift towards Rubisco de-activation at higher temperatures is not caused by changes in the availability of ATP. The effect is dependent on the concentration of activase with higher amounts of activase counteracting the faster rates of Rubisco de-activation at high temperature CraftsBrandner and Salvucci As discussed above.

    Elucidating the effect of temperature on activation activity will require direct measurement of the actual physical interaction between activase and Rubisco. Considering the exceptional sensitivity of activase to heat inactivation Feller et al. When heat stress is imposed gradually. Because of the high internal CO2 concentration and the marked increase in Rubisco VMax with increasing temperature. Sage concluded that Rubisco activity should not be limiting for C4 photosynthesis when temperatures are optimal or above optimal for photosynthesis.

    For activase. In cotton. As in C3 plants. ATPase and Rubisco activation do not continue to increase with temperature above a relatively low optimum to offset the faster rates of Rubisco de-activation. Portis Kinoshita et al. Although not strictly coupled to Rubisco activation. In some species.

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    These results clearly indicate that Rubisco and not RuBP regeneration limit net photosynthesis at moderately high temperatures. Disruption of the physical interaction between activase and Rubisco could occur because of subunit dissociation.

    ATPase activity is required for Rubisco activation and both activities change in parallel in response to temperature and other conditions Robinson and Portis Law et al. Induction of heat shock proteins and other types of adaptive responses are undoubtedly involved in acclimation to higher growth temperatures. Bukhov et al. Heat stress is known to affect alternative splicing of certain plant genes Lazar and Goodman Measurements of protein aggregation have shown that loss of ATPase activity at temperatures above the optimum may be caused by thermal denaturation of activase Feller et al.

    The temperature response of photosynthesis in C4 plants The temperature optimum of photosynthesis in C4 plants is generally higher than in C3 plants. Burke In many plants. In C4 plants. Higher temperatures generally promote dissociation of oligomers.

    Lorimer GH Mechanism of Rubisco: Itoh Y. Kaneko G. Syngenta Crop Protection. Steady-state rate. Salvucci ME Moderately high temperatures inhibit ribulose 1. Lee JH. Plant Physiol Uchida N.

    Badger MR. References Bernacchi CJ. Plant Cell Physiol Planta This view ignores two important facts. By adjusting the kinetics of Rubisco for changes in activation state.

    Carpentier R Nonphotosynthetic reduction of the intersystem electron transport chain of chloroplasts following heat stress. Singsaas EL.

    Rees D. Ecophysiology and Stress Physiology of Functional Groups. Ogren WL. Reginato RJ. Crafts-Brandner SJ. Radin JW Leaf diffusion resistance and photosynthesis in cotton as related to a foliage temperature based plant water stress index.

    Lange OL Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo L. Andrews TJ Slow inactivation of ribulosebisphosphate carboxylase during catalysis is not due to decarbamylation of the catalytic site. Berry JA Models of photosynthesis. Cell Environ Portis AR Jr. Yasuda T. Salvucci ME Sensitivity of photosynthesis in the C4 plant. Curmi PM The transition between the open and closed states of rubisco is triggered by the interphosphate distance of the bound bisphosphate.

    Physiol Plant Andrews TJ. Lu Z-M. Long SP Improved temperature response functions for models of Rubisco-limited photosynthesis. Edwards GE Influences of leaf temperature on photosynthetic carbon metabolism in wheat. Chem Rev Yamada H.

    Considering that all models of photosynthesis are based on the kinetic properties of Rubisco. O2 and ribulose 1. Watabe S A novel heat stress-responsive gene in the marine diatom Chaetoceros compressum encoding two types of transcripts.

    Gutteridge S. Ann Rev Plant Physiol Condon AG. Farquhar et al. The importance of the Rubisco activation state for predicting the response of photosynthesis to environmental change Understanding the response of photosynthesis to changing environmental conditions is of paramount importance for predicting the effects of global climate change on plant productivity.

    Eur J Biochem We now know that the amount of Rubisco available for photosynthesis i. Law RD Effect of heat stress on the inhibition and recovery of ribulose Yamaguchi T Nonstomatal inhibition associated with inactivation of Rubisco in dehydrated coffee leaves under unshaded and shaded conditions. Photochem Photobiol Schreiber U. Kikuchi K. Samson G. Salvucci ME The two forms of ribulose Crop Sci In the natural environment.

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