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University of Glasgow (2014)

High temperature stress on cereal photosynthesis : a re-evaluation

Almalki, Najla Abdullah

Titre : High temperature stress on cereal photosynthesis : a re-evaluation

Auteur : Almalki, Najla Abdullah

Université de soutenance : University of Glasgow

Grade : Doctor of Philosophy (PhD) 2014

Under natural conditions, crop plants are likely to experience high leaf temperatures that reduce plant growth, reproduction, and photosynthesis, which impact dramatically on crop yield. Some wild plants such as Agave can withstand prolonged periods of Tleaf in excess of 55⁰C but the mechanisms of thermotolerance are unclear at present. To establish whether there is sufficient genetic diversity to be exploited for developing heat tolerant crops, a comparative study was conducted to assess the effects of high leaf temperatures (Tleaf) on two barley lines (C3, Optic and Local) and two maize lines (C4, Sundance and Katumani) that are routinely grown in temperate and sub-tropical regions, respectively, in addition to the obligate C3 plant Yucca filimentosa that is endemic to hot arid habitats. Gas exchange measurements show light saturated CO2 assimilation rates (Asat) and the carboxylation coefficient (the efficiency of CO2 fixation, CO2) were irreversibly suppressed to approximately 20% of their pre-treatment levels immediately after raising Tleaf to 38.0 (± 0.2 ⁰C) for 3 hours in all lines regardless of their origins (temperate or sub- tropical), and this inhibition was not attributed to stomatal closure. In contrast, Y. filimentosa showed a close correspondence between Asat and stomatal conductance (gs) in response to leaf temperatures between 36° to 40°C with a marked suppression immediately after heat stress and rapid full recovery following one hour of release from stress. Above 40°C however, stomata respond differently by opening and increase gs. This pattern suggested the response of stomata in Y. filimentosa is regulated by temperature. There is a general consensus that the primary site of thermal injury to CO2 assimilation is RuBisCO Activase but this is contentious. In this study the effects of high leaf temperatures (Tleaf) on photosynthetic efficiency of barley were re-investigated. Parallel measurements using a range of techniques confirmed that the suppression of Asat was not attributable to Maximum Quantum Efficiency of PSII (ФPSII), or changes in the light harvesting capacity (leaf absorbance, Chla fluorescence excitation spectra), or in vitro electron transport rates. Metabolomics profiling of heat stressed and control leaves showed that carbon flow between Ribose 5-phosphate (Ri5P) and 3-phosphoglycerate (3-PGA) was severely impaired by heat stress, consistent with the assertion that Asat was suppressed by inhibition of RuBisCO activity. Surprisingly, enzyme-linked assays on RuBisCO prepared from leaves exposed to 38.0° (± 0.2°C) for 3 hours showed unequivocally that RuBisCO activity was not affected suggesting the substrates for RuBisCO (CO2 and/or RuBP), rather than RuBisCO activity itself, accounted for the decrease in carbon flow from Ri5P to 3-PGA. These studies also showed that the standard procedures for isolating RuBisCO from cereal leaves lead to a partial re-activation of RuBisCO resulting in false conclusions on the in vivo activation state of the enzyme. The implications of these results are discussed. In intact barley leaves, the suppression in Asat was not reversed by increasing external CO2 (Ca) to 1000 μmol CO2. mol-1 air suggesting chloroplast CO2 levels were not limiting. In vitro assays demonstrated the activities of Ri5P isomerase and phosphoribulose kinase (PRK) were not affected by these heat stress treatments. In contrast, measurements on leaf ATP levels and in vivo electron transport rate (ETR) showed a parallel and dramatic decline (>75%). Post-illumination chlorophyll fluorescence relaxation (light-to-dark transition) was used to assess the magnitude of the proton motive force (pmf) across the thylakoid membrane of control and heat stressed leaves. Heat stress increased the relaxation half time (t½) from 45 to 180 seconds suggesting a decrease in proton conductance through the ATP synthase, and thus a decrease in leaf ATP levels1. Taken together these results suggest high leaf temperatures lead to a decrease in chloroplast ATP levels and this suppresses the synthesis of Ribulose 1,5-Bisphosphate by the C3 Cycle ; carbon flow through RuBisCO is impaired and thus whole leaf photosynthesis rates decline severely.

Mots clés : Heat stress, photosynthesis, RuBisCO, RuBisCO Activase


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