In the heat of the night: wheat respiration and photosynthesis in a warming world

Abstract

Temperature is crucial in determining the efficiency of plant respiration and photosynthesis. Given ongoing trends of rising global average temperature, warming nights, and longer and hotter heatwaves, understanding how these key processes respond to high temperature is increasingly important. This rings particularly true for crops, because efforts to improve yields must contend with the consequences of warming. In this thesis, measurements of leaf gas-exchange, chlorophyll fluorescence, gene expression and protein thermostability were used to characterise the responses of respiration and photosynthesis to warming in field and controlled environment grown wheat. Among 20 wheat genotypes grown over multiple seasons in the Australian wheat belt, elevated growth temperature coincided with reduced leaf dark respiration rate (Rdark) when measured as O2 consumption (Rdark-O2) at a common temperature, reflecting the predicted acclimation response. However, warming was not associated with declines in either Rdark when measured as CO2 release (Rdark-CO2) or CO2 assimilation rate. The critical temperature at which photosystem II becomes damaged (Tcrit) was also used to quantify wheat photosynthetic heat tolerance and acclimation. Tcrit varied dynamically with time of day and phenological stage, rising from heading to anthesis and grain-fill. Acclimation of Tcrit to a 36C heat shock was rapid (within two hours of heat stress), before reaching an upper threshold of approximately 43.7C after three-to-five days. A systematic review of wheat Tcrit data highlighted a 20C variation in wheat leaf Tcrit, though this was unrelated to the latitude of genotype origin. Controlled environment experiments were also conducted to examine the effects of night versus day warming on Rdark. Wheat leaf Rdark-O2 measured at a common temperature again declined with warming, though this only coincided with night warming rather than day warming. Night warming also led to a lack of acclimation of leaf Rdark-CO2, decreased plant biomass at maturity, and an increased capacity of the non-ATP producing alternative oxidase electron transport pathway. Taken together, this illustrated a predominant effect of night warming in reducing wheat growth, potentially via reduced ATP demand. Gene and protein-level analyses explored biochemical mechanisms underpinning physiological responses to elevated night temperature and daytime heatwave. A five-day 38C daytime heatwave elicited a large and rapid increase in gene expression for heat shock proteins 70 and 90 (HSP70 and HSP90), as well as for the heat tolerant isoform of Rubisco activase (Rca1-b). Elevated night growth temperature seemed to prime these responses; warm night-grown plants increased their expression of HSP70, HSP90, and Rca-1b more rapidly during the heatwave. Additionally, after five days of heatwave, the Rubisco activase of warm night-grown plants displayed a higher thermostability than that of the cool-grown plants. Overall, the results in this thesis demonstrate the dynamic and rapid responses of wheat respiration and photosynthesis to high temperature, as well as highlighting that night warming exerts greater influence over wheat energy metabolism than daytime warming does. These findings provide a framework for future efforts to improve wheat growth under elevated temperature, and also carry implications for the modelling of leaf carbon flux in a future, warmer world.