Matrix Redox Physiology Governs the Regulation of Plant Mitochondrial Metabolism through Posttranslational Protein Modifications
Møller, Ian & Igamberdiev, Abir & Bykova, Natalia & Finkemeier, Iris & Rasmusson, Allan & Schwarzländer, Markus. (2020). Matrix Redox Physiology Governs the Regulation of Plant Mitochondrial Metabolism through Post-Translational Protein Modifications. The Plant Cell. 10.1105/tpc.19.00535.
Plain language summary
Mitochondria function as the power stations of plant cell metabolism by producing and exporting energy equivalents, which are required by many metabolic pathways and are needed to drive life processes. Mitochondria modulate their metabolism quickly in response to dynamic changes in the requirements of cell for energy and building blocks. An efficient, rapid and direct regulation of mitochondrial function can be achieved by biochemical modification of enzymes involved in mitochondrial metabolism. In this review, the crucial role of redox-driven modifications of mature functional proteins in mitochondrial metabolic regulation is discussed. Several fundamental concepts contributing to redox-associated changes include biological redox reactions of small molecules, amino acid-specific biochemical modifications of proteins identified by sequencing and analysis, and their functional importance. Another concept encompasses the combinatorial role of multiple modifications on the same protein or in the same metabolic pathway that can interact to fine-tune metabolic regulation. Protein modifications also take part in the repair of stress-induced damage as well as adjusting metabolic functions in response to environmental variation, such as changes in light irradiance or oxygen availability. Finally, they form a complex regulatory system that provides the speed and flexibility needed for mitochondrial coordination that cannot be provided by changes in nuclear gene expression alone.
Mitochondria function as hubs of plant metabolism. Oxidative phosphorylation produces ATP, but it is also a central high capacity electron sink required by many metabolic pathways that must be flexibly coordinated and integrated. Here, we review the crucial roles of redox-associated posttranslational protein modifications (PTMs) in mitochondrial metabolic regulation. We discuss several major concepts. First, the major redox couples in the mitochondrial matrix (NAD, NADP, thioredoxin, glutathione, and ascorbate) are in kinetic steady state rather than thermodynamic equilibrium. Second, targeted proteomics have produced long lists of proteins potentially regulated by Cys oxidation/thioredoxin, Met-SO formation, phosphorylation, or Lys acetylation, but we currently only understand the functional importance of a few of these PTMs. Some site modifications may represent molecular noise caused by spurious reactions. Third, different PTMs on the same protein or on different proteins in the same metabolic pathway can interact to fine-tune metabolic regulation. Fourth, PTMs take part in the repair of stress-induced damage (e.g., by reducing Met and Cys oxidation products) as well as adjusting metabolic functions in response to environmental variation, such as changes in light irradiance or oxygen availability. Finally, PTMs form a multidimensional regulatory system that provides the speed and flexibility needed for mitochondrial coordination far beyond that provided by changes in nuclear gene expression alone.