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      Mitochondrial redox systems as central hubs in plant metabolism and signaling

      research-article
      Plant Physiology
      Oxford University Press

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          Abstract

          Plant mitochondria are indispensable for plant metabolism and are tightly integrated into cellular homeostasis. This review provides an update on the latest research concerning the organization and operation of plant mitochondrial redox systems, and how they affect cellular metabolism and signaling, plant development, and stress responses. New insights into the organization and operation of mitochondrial energy systems such as the tricarboxylic acid cycle and mitochondrial electron transport chain (mtETC) are discussed. The mtETC produces reactive oxygen and nitrogen species, which can act as signals or lead to cellular damage, and are thus efficiently removed by mitochondrial antioxidant systems, including Mn-superoxide dismutase, ascorbate–glutathione cycle, and thioredoxin-dependent peroxidases. Plant mitochondria are tightly connected with photosynthesis, photorespiration, and cytosolic metabolism, thereby providing redox-balancing. Mitochondrial proteins are targets of extensive post-translational modifications, but their functional significance and how they are added or removed remains unclear. To operate in sync with the whole cell, mitochondria can communicate their functional status via mitochondrial retrograde signaling to change nuclear gene expression, and several recent breakthroughs here are discussed. At a whole organism level, plant mitochondria thus play crucial roles from the first minutes after seed imbibition, supporting meristem activity, growth, and fertility, until senescence of darkened and aged tissue. Finally, plant mitochondria are tightly integrated with cellular and organismal responses to environmental challenges such as drought, salinity, heat, and submergence, but also threats posed by pathogens. Both the major recent advances and outstanding questions are reviewed, which may help future research efforts on plant mitochondria.

          Abstract

          Plant mitochondria are key components of redox homeostasis and play vital roles in regulating cellular metabolism, thereby affecting development and stress tolerance at the whole plant level.

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          Most cited references214

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          How mitochondria produce reactive oxygen species

          The production of ROS (reactive oxygen species) by mammalian mitochondria is important because it underlies oxidative damage in many pathologies and contributes to retrograde redox signalling from the organelle to the cytosol and nucleus. Superoxide (O2 •−) is the proximal mitochondrial ROS, and in the present review I outline the principles that govern O2 •− production within the matrix of mammalian mitochondria. The flux of O2 •− is related to the concentration of potential electron donors, the local concentration of O2 and the second-order rate constants for the reactions between them. Two modes of operation by isolated mitochondria result in significant O2 •− production, predominantly from complex I: (i) when the mitochondria are not making ATP and consequently have a high Δp (protonmotive force) and a reduced CoQ (coenzyme Q) pool; and (ii) when there is a high NADH/NAD+ ratio in the mitochondrial matrix. For mitochondria that are actively making ATP, and consequently have a lower Δp and NADH/NAD+ ratio, the extent of O2 •− production is far lower. The generation of O2 •− within the mitochondrial matrix depends critically on Δp, the NADH/NAD+ and CoQH2/CoQ ratios and the local O2 concentration, which are all highly variable and difficult to measure in vivo. Consequently, it is not possible to estimate O2 •− generation by mitochondria in vivo from O2 •−-production rates by isolated mitochondria, and such extrapolations in the literature are misleading. Even so, the description outlined here facilitates the understanding of factors that favour mitochondrial ROS production. There is a clear need to develop better methods to measure mitochondrial O2 •− and H2O2 formation in vivo, as uncertainty about these values hampers studies on the role of mitochondrial ROS in pathological oxidative damage and redox signalling.
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            Free Radicals in Biology and Medicine

            Free Radicals in Biology and Medicine has become a classic text in the field of free radical and antioxidant research. Now in its fifth edition, the book has been comprehensively rewritten and updated whilst maintaining the clarity of its predecessors. Two new chapters discuss 'in vivo' and 'dietary' antioxidants, the first emphasising the role of peroxiredoxins and integrated defence mechanisms which allow useful roles for ROS, and the second containing new information on the role of fruits, vegetables, and vitamins in health and disease. This new edition also contains expanded coverage of the mechanisms of oxidative damage to lipids, DNA, and proteins (and the repair of such damage), and the roles played by reactive species in signal transduction, cell survival, death, human reproduction, defence mechanisms of animals and plants against pathogens, and other important biological events. The methodologies available to measure reactive species and oxidative damage (and their potential pitfalls) have been fully updated, as have the topics of phagocyte ROS production, NADPH oxidase enzymes, and toxicology. There is a detailed and critical evaluation of the role of free radicals and other reactive species in human diseases, especially cancer, cardiovascular, chronic inflammatory and neurodegenerative diseases. New aspects of ageing are discussed in the context of the free radical theory of ageing. This book is recommended as a comprehensive introduction to the field for students, educators, clinicians, and researchers. It will also be an invaluable companion to all those interested in the role of free radicals in the life and biomedical sciences.
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              Ascorbate and glutathione: the heart of the redox hub.

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                Author and article information

                Journal
                Plant Physiol
                Plant Physiol
                plphys
                Plant Physiology
                Oxford University Press
                0032-0889
                1532-2548
                May 2021
                24 February 2021
                24 February 2021
                : 186
                : 1
                : 36-52
                Affiliations
                Department of Biology, Lund University , Lund, Sweden
                Author notes
                Author for communication: olivier.van_aken@ 123456biol.lu.se

                Senior author.

                Author information
                https://orcid.org/0000-0003-4024-968X
                Article
                kiab101
                10.1093/plphys/kiab101
                8154082
                33624829
                f6af695b-8b5f-49a9-9df1-cf494cc9a1e0
                © The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 October 2020
                : 11 February 2021
                Page count
                Pages: 17
                Funding
                Funded by: Swedish Research Council, DOI 10.13039/501100004359;
                Award ID: 2017-03854
                Funded by: Carl Trygger Foundation, DOI 10.13039/501100002805;
                Award ID: CTS 17: 487
                Categories
                Focus Issue on Plant Redox Biology
                Updates
                AcademicSubjects/SCI02286
                AcademicSubjects/SCI02287
                AcademicSubjects/SCI01270
                AcademicSubjects/SCI01280
                AcademicSubjects/SCI02288

                Plant science & Botany
                Plant science & Botany

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