The complementary roles of chloroplast cyclic electron transport and mitochondrial alternative oxidase to ensure photosynthetic performance.

Citation

Chadee A, Alber NA, Dahal K, Vanlerberghe GC* (2021) The complementary roles of chloroplast cyclic electron transport and mitochondrial alternative oxidase to ensure photosynthetic performance. Front. Plant Sci. 10.3389/fpls.2021.748204

Résumé en langage clair

Plants convert light energy to chemical energy in the form of nicotinamide adenine dinucleotide phosphate (NADPH) and adenosine triphosphate (ATP) in a process called photosynthesis. The NADPH and ATP are used as an energy source to produce carbohydrates from carbon dioxide (CO2) inside leaf organs called chloroplasts. Plants use the carbohydrates to build organic compounds, which are essential for their growth and development. Previous studies suggest that when plants are grown under environmental stress, the ratio between these two types of energy is usually not ideal for producing carbohydrates, and cause metabolic imbalances. These imbalances may result in increased generation of reactive oxygen molecules, which can cause irreversible damage to cells, leading to poor photosynthesis and overall plant performance. In our recent studies at University of Toronto, we grew tobacco plants under drought stress. We examined chloroplast cyclic electron transport (CET) and mitochondrial alternative oxidase (AOX), which are specific cell processes. Our study suggested that CET and AOX each plays a key role in preventing oxidative damages in plants grown under drought stress. CET helped in maintaining optimal NADPH level, whereas AOX helped in maintaining optimal ATP level in the cells. Another detailed study using two plant species with enhanced AOX and CET pathways resulted in decreased cell damage by the reactive oxygen molecules, and improved photosynthetic performance under stress. This work is most relevant to improve photosynthesis, and overall plant performance under environmental stress conditions.

Résumé

Chloroplasts use light energy and a linear electron transport (LET) pathway for the coupled generation of NADPH and ATP. It is widely accepted that the production ratio of ATP to NADPH is usually less than required to fulfill the energetic needs of the chloroplast. Left uncorrected, this would quickly result in an over-reduction of the stromal pyridine nucleotide pool (i.e. high NADPH/NADP+ ratio) and under-energization of the stromal adenine nucleotide pool (i.e. low ATP/ADP ratio). These imbalances could cause metabolic bottlenecks, as well as increased generation of damaging reactive oxygen species. Chloroplast cyclic electron transport (CET) and the chloroplast malate valve could each act to prevent stromal over-reduction, albeit in distinct ways. CET avoids the NADPH production associated with LET, while the malate valve consumes the NADPH associated with LET. CET could operate by one of two different pathways, depending upon the chloroplast ATP demand. The NADH dehydrogenase-like pathway yields a higher ATP return per electron flux than the pathway involving PROTON GRADIENT REGULATION5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE1 (PGRL1). Similarly, the malate valve could couple with one of two different mitochondrial electron transport pathways, depending upon the cytosolic ATP demand. The cytochrome pathway yields a higher ATP return per electron flux than the alternative oxidase (AOX) pathway. In both Arabidopsis thaliana and Chlamydomonas reinhardtii, PGR5/PGRL1 pathway mutants have increased amounts of AOX, suggesting complementary roles for these two lesser-ATP yielding mechanisms of preventing stromal over-reduction. These two pathways may become most relevant under environmental stress conditions that lower ATP demands for carbon fixation and carbohydrate export.

Date de publication

2021-09-28

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