Abstract
Photorespiration metabolizes 2-phosphoglyolate (2-PG) to avoid inhibition of carbon assimilation and allocation. In addition to 2-PG removal, photorespiration has been shown to play a role in stress protection. Here, we studied the impact of faster 2-PG degradation through overexpression of 2-PG phosphatase (PGLP) on the abiotic stress-response of Arabidopsis thaliana (Arabidopsis). Two transgenic lines and the wild type were subjected to short-time high light and elevated temperature stress during gas exchange measurements. Furthermore, the same lines were exposed to long-term water shortage and elevated temperature stresses. Faster 2-PG degradation allowed maintenance of photosynthesis at combined light and temperatures stress and under water-limiting conditions. The PGLP-overexpressing lines also showed higher photosynthesis compared to the wild type if grown in high temperatures, which also led to increased starch accumulation and shifts in soluble sugar contents. However, only minor effects were detected on amino and organic acid levels. The wild type responded to elevated temperatures with elevated mRNA and protein levels of photorespiratory enzymes, while the transgenic lines displayed only minor changes. Collectively, these results strengthen our previous hypothesis that a faster photorespiratory metabolism improves tolerance against unfavorable environmental conditions, such as high light intensity and temperature as well as drought. In case of PGLP, the likely mechanism is alleviation of inhibitory feedback of 2-PG onto the Calvin–Benson cycle, facilitating carbon assimilation and accumulation of transitory starch.
Highlights
The characterization of a large set of photorespiratory mutants from a broad collection of phototrophs revealed photorespiration as an essential partner for oxygenic photosynthesis [1,2,3,4,5,6].The photorespiratory pathway represents the only way to metabolize the Rubisco oxygenation reaction product 2-phosphoglycolate (2-PG; [7]) into the Calvin–Benson (CB) cycle intermediate3-phosphoglycerate (3-PGA)
The magnitude of these losses depends mainly on the CO2 and O2 partial pressures in the chloroplast, which can dramatically change under unfavorable environmental conditions, such as high light intensity, drought and high temperatures [12,13,14]
Wild-type and PGLP overexpressor plants were grown under standard conditions (Figure 1A) and used for combined gas exchange and chlorophyll a fluorescence measurements to characterize their response to short-time light and temperature stresses (Figure 1B)
Summary
The characterization of a large set of photorespiratory mutants from a broad collection of phototrophs revealed photorespiration as an essential partner for oxygenic photosynthesis [1,2,3,4,5,6].The photorespiratory pathway represents the only way to metabolize the Rubisco oxygenation reaction product 2-phosphoglycolate (2-PG; [7]) into the Calvin–Benson (CB) cycle intermediate3-phosphoglycerate (3-PGA). The photorespiratory pathway represents the only way to metabolize the Rubisco oxygenation reaction product 2-phosphoglycolate (2-PG; [7]) into the Calvin–Benson (CB) cycle intermediate. The decarboxylation of glycine in the photorespiratory pathway leads to considerable losses of freshly assimilated carbon. The magnitude of these losses depends mainly on the CO2 and O2 partial pressures in the chloroplast, which can dramatically change under unfavorable environmental conditions, such as high light intensity, drought and high temperatures [12,13,14]. Given the CO2 loss during 2-PG recycling, plant research, aims to circumvent photorespiration in order to reduce carbon and energy losses [15,16,17]
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