Mitochondrial redox systems as central hubs in plant metabolism and signaling

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.

Figure 1

Plant mitochondria as hubs in redox metabolism, signaling, and plant growth. Plant mitochondria have a typical structure consisting of an outer membrane, inner membrane, and intermembrane space (IMS). The IMM forms large folds called cristae. The MTL complex is important for the formation of cristae at the cristae junction, and potentially interacts with TOM and mtETC components. The cristae lumen is thought to be important for the concentration of protons and protein complexes, improving metabolic efficiency. The TCA cycle uses substrates derived from glycolysis, photosynthesis, and amino acid metabolism to reduce NAD(P)+ to NAD(P)H. NADH is used to drive the mitochondrial electron transport chain (Complexes I–IV and AOXs and NDs), consuming O₂. The cyt c pathway drives proton translocation from the mitochondrial matrix into the IMS, which can flow back via ATP synthase (green complex) to produce ATP or via UCPs without producing ATP. ATP can be exported into the cytosol and acts as a major energy source for a variety of cellular processes. Reductant from photosynthesis is transported to the mitochondria via the malate valve, which may be important to dissipate excess reductant from photosynthesis via the TCA cycle and mtETC. Excess citrate may leave the mitochondria via the citrate valve to be used in cytosolic metabolism. Other TCA cycle intermediates can be exchanged with the cytosol via mitochondrial carrier proteins to support metabolism. A TP-3PGA shuttle is thought to export NADH/ATP equivalents from the chloroplast into the cytosol. The mtETC inevitably produces superoxide as a by-product, especially under stress, which is rapidly scavenged by MnSOD, producing H₂O₂. H₂O₂ is further reduced in the Asc-GSH cycle, or by other peroxidase systems such as GPXs and Prxs. These peroxidase systems are regenerated by the Trx/ NTR system, ultimately using NADPH as a reductant. Mitochondrial GRXs mainly play a role in Fe–S cluster protein biosynthesis. Some of the H₂O₂ may either enter or leave mitochondria (via VDAC or aquaporins), which may have a signaling role. The functional status of mitochondria is communicated to the cellular nucleus via MRR. A key pathway that is activated during mitochondrial dysfunction is mediated by ANAC017-related transcription factors, which are anchored into the endoplasmic reticulum membrane. Upon stress, the NAC transcription factors are thought to be released by proteases and regulate gene expression of alternative mtETC components and other mitochondrial dysfunction stimulon genes. Other ANAC017-independent retrograde pathways are also likely to be active and may steer mitochondrial biogenesis. Overall, plant mitochondria act as redox, metabolism, and signaling hubs that affect all aspects of plant development and stress response.