The Complementary Roles of Chloroplast Cyclic Electron Transport and Mitochondrial Alternative Oxidase to Ensure Photosynthetic Performance

Abstract

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 the ATP demands for carbon fixation and carbohydrate export.

Fine Tuning of ROS, Redox and Energy Regulatory Systems Associated with the Functions of Chloroplasts and Mitochondria in Plants under Heat Stress

“…To adapt to stress conditions including heat stress, it is necessary for plant cells to properly balance amounts of ATP, reductants and carbon via modulating functions of the chloroplasts and mitochondria ( Figure 3 ) [ 145 ]. In the chloroplasts, conditions that accelerate the oxygenase activity of RUBISCO lead to high demand of ATP relative to NADPH [ 146 , 147 , 148 ].…”

“…In the chloroplasts, conditions that accelerate the oxygenase activity of RUBISCO lead to high demand of ATP relative to NADPH [ 146 , 147 , 148 ]. In this case, a shortage of ATP relative to NADPH generation by the electron transport chain in the chloroplasts results in excess accumulation of stromal NADPH [ 145 ]. To shuttle excess reductants from the stroma of the chloroplasts, NADPH is consumed by the reduction of oxaloacetate to form malate.…”

“…To shuttle excess reductants from the stroma of the chloroplasts, NADPH is consumed by the reduction of oxaloacetate to form malate. Then, malate transported from the chloroplasts to the cytosol is oxidized back to oxaloacetate (OAA) and returns to the chloroplasts [ 145 ]. This malate oxidation generates NADH, whose conversion to NAD + might depend on the mitochondrial electron transport chain [ 145 ].…”

“…Then, malate transported from the chloroplasts to the cytosol is oxidized back to oxaloacetate (OAA) and returns to the chloroplasts [ 145 ]. This malate oxidation generates NADH, whose conversion to NAD + might depend on the mitochondrial electron transport chain [ 145 ]. Thus, functions of the mitochondria to oxidize reductants excessively accumulated in the stroma of the chloroplasts might be essential to maintain redox status in cells.…”

The colonization of land was a likely driving force for the evolution of mitochondrial retrograde signalling in plants

“…The transition had its many challenges for the land plants, forcing them to evolve again and again through key innovations, for instance evolution of specialized cells, tissues, and organs, to enhance their survival chances and reproduction ( Bowman, 2013 ). Mitochondria are essential double-membrane-bound subcellular compartments that are often regarded as the cell’s ‘powerhouse’, since the majority of the energy required to maintain cellular activities is provided by mitochondria through aerobic respiration in the form of ATP; however, in green plants, chloroplasts and mitochondria work in tight coordination to provide cellular energy ( Chadee et al , 2021 ). At present we have sufficient evidence to believe that eukaryotes are the product of a fusion between an aerobic prokaryotic cell, a relative of modern α-proteobacteria, and a host archaeon ( Martijn et al , 2018 ).…”