Mechanism for deactivation of Rubisco under moderate heat stress

Abstract

Photosynthesis is particularly sensitive to direct inhibition by heat stress. This inhibition is closely associated with the inactivation of ribulose‐1,5‐bisphosphate carboxylase/oxygenase (Rubisco). To develop a more complete understanding of the mechanism of inactivation of Rubisco under moderate heat stress, various aspects of the process were examined both in vivo and in vitro. Experiments with isolated Rubisco revealed that the rate of synthesis of the catalytic misfire product, xylulose‐1,5‐bisphosphate, increased with temperature. Activated Rubisco, produced by reaction with activase at a control temperature of 25°C or by incubation with high CO2, deactivated when the temperature of the reaction exceeded temperatures that were equivalent to the optimum for activase adenosine triphosphatase (ATPase) activity. Measurements of the activation state of Rubisco in cotton and tobacco leaves showed that Rubisco inactivated within 7 s of imposing a heat stress. Thus, elevated temperature had an opposite effect on the two processes that ultimately determine the activation state of Rubisco, decreasing activase activity but stimulating the catalytic misfire reaction that inactivates Rubisco. These data support a mechanism for the inactivation of Rubisco at high temperature involving an inability of activase to overcome the inherently faster rates of Rubisco inactivation. That the net effect of elevated temperatures on Rubisco activation is similar both in vivo and under controlled conditions in vitro argues for a direct effect of temperature on the activation of Rubisco by activase and against the proposal that the deactivation of Rubisco under moderate heat stress is a secondary consequence of perturbations in the thylakoid membrane.

Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism

“…The cellular respiration was assessed using 2,3,5 triphenyl tetrazolium chloride (TTC) reduction assay that indicates cellular respiration. The respiration may get affected at supra-optimal temperatures due to direct inhibitory effects of heat stress on enzymes (Salvucci and Crafts-Brandner 2004). The decrease in viability of leaf tissue at 45/40°C in our case is in agreement with the observations on wheat (Wang and Nguyen 1989) and potato (Coria et al 1998) plants exposed to heat stress.…”

“…The elevation of enzymes at 40/35°C might possibly be due to activation of defense mechanisms against oxidative stress, which at higher degree appear to fail leading to damage to membranes, chlorophyll and hence growth. The decrease in activity of these antioxidants possibly occurred due to their denaturation by high temperature (Salvucci and Crafts-Brandner 2004) and is similar to the findings on wheat (Almeselmani et al 2009) and mulberry (Chaitanya et al 2001) plants growing at high temperatures.…”

The Costs of Photorespiration to Food Production Now and in the Future

“…Additionally, the carbon dioxide level can affect how much of the Rubisco is active: The activation state of Rubisco decreased with carbon dioxide concentration in sweet potato (19). The activation state also decreased with temperature above the thermal optimum at each measurement of carbon dioxide concentration in these experiments, likely because of the limited thermotolerance of Rubisco activase, a vital chaperone for Rubisco activity (66). Despite this relationship between Rubisco activation state and temperature, it is still debated whether this results directly in the decrease in photosynthetic rate at elevated temperature or leads to other limitations becoming more dominant (65,66).…”

“…The activation state also decreased with temperature above the thermal optimum at each measurement of carbon dioxide concentration in these experiments, likely because of the limited thermotolerance of Rubisco activase, a vital chaperone for Rubisco activity (66). Despite this relationship between Rubisco activation state and temperature, it is still debated whether this results directly in the decrease in photosynthetic rate at elevated temperature or leads to other limitations becoming more dominant (65,66). Changes in Rubisco quantity or activation state affect absolute rates of V o but have only a slight impact on the V o /V c ratio under identical atmospheric carbon dioxide concentrations.…”

Effects of 2,4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress

“…The chlorophyll a fluorescence transients were obtained by 2 s saturating red light and analyzed with the 2011; Suzuki et al 2014). As the primary limiting factor of net photosynthesis (Salvucci and Crafts-Brandner 2004;, the activation state of Rubisco (ribulose-1,5-bisphosphate carboxylase/oxygenase) is regulated by Rubisco activase (RCA) via the maintenance of Rubisco catalytic sites in the active state at a high level (Tcherkez 2013). Furthermore, introducing more thermostable RCA into Ar abidopsis thaliana L. increases photosynthesis and the growth rate under moderate heat stress (Kurek et al 2007), which demonstrates that RCA is extremely thermolabile.…”