Malate Circulation: Linking Chloroplast Metabolism to Mitochondrial ROS

Abstract

The malate valve has long been proposed to release excess reducing equivalents from the chloroplast, but mutants lacking the proposed key enzyme NADP-dependent malate dehydrogenase show little impairment of chloroplast function, suggesting the involvement of an alternative pathway.New research suggests a central role for a malate valve, employing chloroplast NAD-dependent malate dehydrogenase, which also has additional non-enzymatic functions in chloroplast biogenesis.The new malate circulation model proposes that malate exported from the chloroplast is oxidized in the mitochondrion triggering ROS production, which can modulate growth and ultimately induce cell death.It is proposed that the chloroplast to mitochondrion (CTM) pathway in conjunction with direct import of NAD+ leads to elevated levels of NADH in the mitochondrion. In photosynthetic cells, chloroplasts and mitochondria are the sites of the core redox reactions underpinning energy metabolism. Such reactions generate reactive oxygen species (ROS) when oxygen is partially reduced. ROS signaling leads to responses by cells which enable them to adjust to changes in redox status. Recent studies in Arabidopsis thaliana reveal that chloroplast NADH can be used to generate malate which is exported to the mitochondrion where its oxidation regenerates NADH. Oxidation of this NADH produces mitochondrial ROS (mROS) which can activate signaling systems to modulate energy metabolism, and in certain cases can lead to programmed cell death (PCD). We propose the term ‘malate circulation’ to describe such redistribution of reducing equivalents to mediate energy homeostasis in the cell. In photosynthetic cells, chloroplasts and mitochondria are the sites of the core redox reactions underpinning energy metabolism. Such reactions generate reactive oxygen species (ROS) when oxygen is partially reduced. ROS signaling leads to responses by cells which enable them to adjust to changes in redox status. Recent studies in Arabidopsis thaliana reveal that chloroplast NADH can be used to generate malate which is exported to the mitochondrion where its oxidation regenerates NADH. Oxidation of this NADH produces mitochondrial ROS (mROS) which can activate signaling systems to modulate energy metabolism, and in certain cases can lead to programmed cell death (PCD). We propose the term ‘malate circulation’ to describe such redistribution of reducing equivalents to mediate energy homeostasis in the cell. The chloroplast is considered to be the main site of reactive oxygen species (ROS; see Glossary) production, because photosynthetic electron transfer reactions ultimately generate all the reducing equivalents required for assimilation and biosynthesis in the whole cell. Achieving the balance between the production and consumption of reducing power is vital since excess reducing equivalents result in ROS production, leading to oxidative signaling. Under stressful environmental conditions such as excess light or high temperature, elevated ROS signaling can lead to changes in cell function to adjust to the effects of excess reducing equivalents [1.Van Aken O. Van Breusegem F. Licensed to kill: mitochondria, chloroplasts, and cell death.Trends Plant Sci. 2015; 20: 754-766Abstract Full Text Full Text PDF PubMed Scopus (92) Google Scholar, 2.Czarnocka W. Karpinski S. Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses.Free Radic. Biol. Med. 2018; 122: 4-20Crossref PubMed Scopus (253) Google Scholar, 3.Waszczak C. et al.Reactive oxygen species in plant signaling.Annu. Rev. Plant Biol. 2018; 69: 209-236Crossref PubMed Scopus (459) Google Scholar]. One way in which the chloroplast is thought to dissipate reducing equivalents is by means of the malate valve [4.Scheibe R. Malate valves to balance cellular energy supply.Physiol. Plant. 2004; 120: 21-26Crossref PubMed Scopus (351) Google Scholar,5.Selinski J. Scheibe R. Malate valves: old shuttles with new perspectives.Plant Biol. 2019; 21: 21-30Crossref PubMed Scopus (84) Google Scholar]. It is proposed that excess NADPH is consumed by plastidial NADP-dependent malate dehydrogenase (plNADP-MDH) to produce malate which is exported from the chloroplast for subsequent oxidation. However, mutants lacking plNADP-MDH do not appear to be compromised under conditions of photosynthetic stress, suggesting that other mechanisms can operate [6.Hebbelmann I. et al.Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase.J. Exp. Bot. 2012; 63: 1445-1459Crossref PubMed Scopus (95) Google Scholar, 7.Heyno E. et al.Putative role of the malate valve enzyme NADP-malate dehydrogenase in H2O2 signalling in Arabidopsis.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2014; 36920130228Crossref PubMed Scopus (42) Google Scholar, 8.Selinski J. Scheibe R. Lack of malate valve capacities lead to improved N-assimilation and growth in transgenic A. thaliana plants.Plant Signal. Behav. 2014; 9e29057Crossref PubMed Scopus (18) Google Scholar]. New discoveries reveal that excess chloroplast NADH is consumed by plastidial NAD-dependent malate dehydrogenase (plNAD-MDH), and the malate is exported to the mitochondrion. There, malate oxidation generates NADH, which is then oxidized by Complex I (NADH: ubiquinone oxidoreductase), generating ROS which can trigger cell death in extreme circumstances [9.Wu J. et al.Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species.Cell Res. 2015; 25: 621-633Crossref PubMed Scopus (58) Google Scholar,10.Zhao Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. In this opinion article we propose that chloroplast redox stress is linked by a CTM malate transport system that brings about mROS signaling to modulate energy metabolism in the cell under variable environmental conditions. We further propose the term ‘malate circulation’ to describe this form of redistribution of reducing equivalents in the cell. Chloroplast ROS production occurs when electron carriers in the photosynthetic electron transport chain (pETC) become over-reduced. This might happen when the supply of reducing equivalents is greater than their consumption by the cell. Mitochondria provide a means to alleviate over-reduction in the cell by transferring electrons from reductants to molecular oxygen [11.Millar A.H. et al.Organization and regulation of mitochondrial respiration in plants.Annu. Rev. Plant Biol. 2011; 62: 79-104Crossref PubMed Scopus (418) Google Scholar, 12.Noguchi K. Yoshida K. Interaction between photosynthesis and respiration in illuminated leaves.Mitochondrion. 2008; 8: 87-99Crossref PubMed Scopus (237) Google Scholar, 13.Sweetlove L.J. et al.Mitochondrial uncoupling protein is required for efficient photosynthesis.Proc. Natl. Acad. Sci. U. S. 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It is that mROS production occurs the mitochondrial and is particularly with Complex but also with Complex and Complex S. et of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Plant 2016; PubMed Scopus Google Scholar]. In photosynthetic is that the of mitochondria to cellular ROS production is relatively in the light C. et al.Reactive oxygen species in plant signaling.Annu. Rev. Plant Biol. 2018; 69: 209-236Crossref PubMed Scopus (459) Google S. et of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Plant 2016; PubMed Scopus Google Scholar, Plant mitochondria and oxidative electron NADPH and metabolism of reactive oxygen Rev. Plant Plant Biol. PubMed Scopus Google Scholar, et al.Reactive oxygen species in their and scavenging J. Sci. 2011; Scholar, et al.Mitochondrial redox and homeostasis in Plant Sci. Full Text Full Text PDF PubMed Scopus Google Scholar]. Plant mitochondria alternative which provide a means of transferring electrons from ubiquinone to oxygen to mROS production S. et of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Plant 2016; PubMed Scopus Google Plant mitochondria and oxidative electron NADPH and metabolism of reactive oxygen Rev. Plant Plant Biol. PubMed Scopus Google Scholar]. mROS to be important in signaling systems that energy metabolism and stress responses in plants [1.Van Aken O. Van Breusegem F. Licensed to kill: mitochondria, chloroplasts, and cell death.Trends Plant Sci. 2015; 20: 754-766Abstract Full Text Full Text PDF PubMed Scopus (92) Google C. et al.Reactive oxygen species in plant signaling.Annu. Rev. Plant Biol. 2018; 69: 209-236Crossref PubMed Scopus (459) Google S. et of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Plant 2016; PubMed Scopus Google Scholar]. Such mROS has been in the of programmed cell death [1.Van Aken O. Van Breusegem F. Licensed to kill: mitochondria, chloroplasts, and cell death.Trends Plant Sci. 2015; 20: 754-766Abstract Full Text Full Text PDF PubMed Scopus (92) Google E. et cell mitochondria and the plant PubMed Scopus Google Scholar, et in fatty acid leads to cell death and in plant PubMed Scopus Google Scholar, G.C. et of mitochondrial alternative in response to a cell pathway the pathway programmed cell PubMed Scopus Google Scholar, Arabidopsis programmed cell 2006; PubMed Scopus Google Scholar, et Arabidopsis thaliana which the mitochondrial electron transport in stress and Plant. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar]. It is that mROS during stress and in PCD by of the S. et of mitochondrial reactive oxygen species in cellular signaling and stress response in plants.Plant 2016; PubMed Scopus Google Plant mitochondria and oxidative electron NADPH and metabolism of reactive oxygen Rev. Plant Plant Biol. PubMed Scopus Google Scholar]. However, has been that can PCD G.C. et al.Alternative oxidase: a respiratory electron transport chain pathway essential for maintaining photosynthetic performance during drought stress.Physiol. Plant. 2016; 157: 322-337Crossref PubMed Scopus (77) Google J. et of programmed cell death by in Exp. Bot. 2014; PubMed Scopus Google G.C. oxidase: a mitochondrial respiratory pathway to and signaling homeostasis during abiotic and stress in J. Sci. PubMed Scopus Google G.C. et of mitochondrial alternative in response to a cell pathway the pathway programmed cell PubMed Scopus Google of programmed cell death by Exp. Bot. 2011; 62: PubMed Scopus Google Scholar]. The of the reducing equivalents that mROS production in response to stress has been but new suggests that malate a key for an important role for malate in mROS production from of a in chloroplast The Arabidopsis thaliana is by and when is under or high et in fatty acid leads to cell death and in plant PubMed Scopus Google Scholar]. The growth is with cell The the chloroplast enzyme protein This enzyme is a of the fatty acid and an essential reduction in fatty acid biosynthesis et and of protein from of Scopus Google Scholar]. In is by a which in the a acid The leads to a in in from or and the a in et in fatty acid leads to cell death and in plant PubMed Scopus Google Scholar]. this of mutants from a of mutants in the [9.Wu J. et al.Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species.Cell Res. 2015; 25: 621-633Crossref PubMed Scopus (58) Google Scholar]. of the that the a of mitochondrial Complex I. of the which a protein that the of for a of Complex I. mutants with Complex I to the and mROS production [9.Wu J. et al.Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species.Cell Res. 2015; 25: 621-633Crossref PubMed Scopus (58) Google Scholar]. of in mROS levels and cell death et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. the production of mROS by mitochondrial Complex I and Complex that to be a of from the chloroplast to the mitochondrion. the between chloroplast and mitochondrion in further mutants and for with Complex I This to the of further in which mROS and the Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. of key of malate between chloroplast and mitochondrion. are chloroplast and mitochondrial NAD-dependent malate dehydrogenase Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. that in chloroplast NADH is oxidized by to produce malate which is exported in for the and the mitochondrion. Such malate then be oxidized by NADH to as for Complex with mROS production Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. In this proposed ‘malate reducing equivalents are in the form of malate from chloroplasts to the mitochondria with of to the chloroplasts In a new a in mitochondrial NAD+ as a new of et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. In the NADH in mitochondria is with that of and of the mROS and PCD in that in the of malate transported mitochondria is such that additional NAD+ is to the for malate oxidation et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. malate from the chloroplast in this way is to as a malate valve [4.Scheibe R. Malate valves to balance cellular energy supply.Physiol. Plant. 2004; 120: 21-26Crossref PubMed Scopus (351) Google Scholar,5.Selinski J. Scheibe R. Malate valves: old shuttles with new perspectives.Plant Biol. 2019; 21: 21-30Crossref PubMed Scopus (84) Google Scholar]. It is that the chloroplast malate valve plNADP-MDH to dissipate excess NADPH during The plNADP-MDH enzyme is by the system and is thought to be in the excess light and of a malate K. Scheibe R. of chloroplast NADP-malate dehydrogenase produces PubMed Scopus Google Scholar, et of NADP-malate a J. Plant Scholar, et of NADP-malate a for an Plant. Scopus Google Scholar]. However, studies in which plNADP-MDH has been in Arabidopsis that other mechanisms are in the response to chloroplast redox stress [6.Hebbelmann I. et al.Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase.J. Exp. Bot. 2012; 63: 1445-1459Crossref PubMed Scopus (95) Google Scholar]. In to is in all and and its is not is under light and conditions [4.Scheibe R. Malate valves to balance cellular energy supply.Physiol. Plant. 2004; 120: 21-26Crossref PubMed Scopus (351) Google Scholar,5.Selinski J. Scheibe R. Malate valves: old shuttles with new perspectives.Plant Biol. 2019; 21: 21-30Crossref PubMed Scopus (84) Google et NAD-dependent malate dehydrogenase from chloroplasts of Arabidopsis thaliana L.J. Biol. PubMed Scopus Google Scholar]. The enzyme is to a role in the of reducing equivalents from chloroplasts during and from is considered to be a of a malate [4.Scheibe R. Malate valves to balance cellular energy supply.Physiol. Plant. 2004; 120: 21-26Crossref PubMed Scopus (351) Google Scholar,5.Selinski J. Scheibe R. Malate valves: old shuttles with new perspectives.Plant Biol. 2019; 21: 21-30Crossref PubMed Scopus (84) Google Scholar]. The function of has because are S. et NAD-dependent malate dehydrogenase is for and metabolism in 2014; PubMed Scopus Google Scholar, et NAD-dependent malate a protein in chloroplast its with an 2018; PubMed Scopus Google Scholar, J. et NAD-dependent malate dehydrogenase is for energy homeostasis in Arabidopsis thaliana Plant. 2014; Full Text Full Text PDF PubMed Scopus Google of the suggests that an important function in a malate valve in the light in response to elevated NADH Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. are new and The mutants of in Arabidopsis are that this enzyme has an essential function during S. et NAD-dependent malate dehydrogenase is for and metabolism in 2014; PubMed Scopus Google J. et NAD-dependent malate dehydrogenase is for energy homeostasis in Arabidopsis thaliana Plant. 2014; Full Text Full Text PDF PubMed Scopus Google Scholar]. a transgenic with from chloroplasts and an important function of plant S. et NAD-dependent malate dehydrogenase is for and metabolism in 2014; PubMed Scopus Google et NAD-dependent malate a protein in chloroplast its with an 2018; PubMed Scopus Google NAD+ malate dehydrogenase is essential for chloroplast 2018; PubMed Scopus Google Scholar]. of such that chloroplast is in the of Arabidopsis NAD-dependent from the mitochondrion or not the when to the that not This when of by and to the et NAD-dependent malate a protein in chloroplast its with an 2018; PubMed Scopus Google Scholar]. the not its enzyme is required for that a with protein which is a of with the chloroplast et NAD-dependent malate a protein in chloroplast its with an 2018; PubMed Scopus Google Scholar]. This is proposed to as the import that functions with the of the of to the The protein also with of metabolism, suggesting that has additional in function et NAD-dependent malate a protein in chloroplast its with an 2018; PubMed Scopus Google Scholar]. that has important in and in the CTM malate studies the of NADH in the The and mutants reveal that NADH metabolism is important in chloroplasts in the It that the of fatty acid synthesis in is since the in leads to the of reducing equivalents to trigger PCD mROS production [9.Wu J. et al.Deficient plastidic fatty acid synthesis triggers cell death by modulating mitochondrial reactive oxygen species.Cell Res. 2015; 25: 621-633Crossref PubMed Scopus (58) Google Scholar,10.Zhao Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google et in fatty acid leads to cell death and in plant PubMed Scopus Google et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. The plastidial dehydrogenase produces NADH for fatty acid biosynthesis with a of The and NADH are consumed by and et and of protein from of Scopus Google et of core in fatty acid and Plant Biol. 2008; 8: PubMed Scopus Google Scholar]. The other reduction in fatty acid is to NADPH et from PubMed Scopus Google et of with the of the J. PubMed Scopus Google Scholar]. of NADH is chloroplast dehydrogenase which by the reduction However, and are in than in et of the the metabolism and of plastidial dehydrogenase J. PubMed Scopus Google J. et dehydrogenase leads to and the and acid balance in PubMed Scopus Google and of the chloroplast pathway has been to the of and in chloroplasts, a pathway in et in Arabidopsis PubMed Scopus Google Scholar, et plant Sci. PubMed Scopus Google Scholar, et to is essential for and in Arabidopsis PubMed Scopus Google Scholar]. It is proposed that is the chloroplast and to for the production of and NADH for fatty acid synthesis et plant Sci. PubMed Scopus Google Scholar]. is in chloroplasts, generate further NADH that is not consumed in fatty acid in which provide a means to excess NADH, leading to malate from the This brings to the of malate by This malate is exported in for by the in the malate because is such a However, in the malate exported from the chloroplast to the malate that as a for in the mitochondrion Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. This the about other for The Arabidopsis NAD-dependent in to are mitochondrial and and and are to be and C. Malate dehydrogenase cellular and role in the of between the and cell PubMed Scopus Google Scholar, I. et malate dehydrogenase functions in but not in the J. PubMed Scopus Google Scholar, et al.Mitochondrial malate dehydrogenase respiration and and plant growth in PubMed Scopus Google Scholar]. The malate from the chloroplast be and oxidized by to produce NADH to the in et and Plant Sci. Full Text Full Text PDF PubMed Scopus Google J. et and 2012; PubMed Scopus Google Scholar]. This is a core that in the with to malate and NADH. in the the in the reduction to The of of the has not mutants of or This might be because is in and However, such mutants might be to the reducing of the and the the the by NADH production from malate the mitochondrion. We can further that is not to for the of Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google et al.Mitochondrial malate dehydrogenase respiration and and plant growth in PubMed Scopus Google et of mitochondrial malate dehydrogenase metabolism and growth in 2016; Google Scholar]. mitochondrial but has not been This brings to the of the CTM of malate the in a than that of suggesting that has an important function under conditions Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google Scholar]. However, when plants in light greater growth than the and levels of This suggests that conditions leading to excess reducing power in the chloroplast lead to of reducing equivalents malate with subsequent mROS with mutants in and suggesting that the CTM malate pathway can its in plants is to be Y. et al.Malate transported from chloroplast to mitochondrion triggers production of ROS and PCD in Arabidopsis thaliana.Cell Res. 2018; 28: 448-461Crossref PubMed Scopus (73) Google et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. We that plNADP-MDH and can operate the in chloroplasts to generate malate for It that in the in fatty biosynthesis might lead to elevated NADPH levels which malate production by However, the chloroplast has other to NADPH such as electron transport and system [6.Hebbelmann I. et al.Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase.J. Exp. Bot. 2012; 63: 1445-1459Crossref PubMed Scopus (95) Google NADPH might not be as as NADH. The for the reduction of to and the of for malate from the chloroplast is also to the of malate to and its the mitochondrion. In the the malate is oxidized by and the NADH as the for Complex I. malate is a in reactions in the its from the chloroplast in the light its in the which in lead to its import the mitochondrion. We that malate might provide an of the chloroplast redox The is malate oxidation lead to mROS production, since the mitochondrion has in which this be such as by of can induce the and of can mROS production by maintaining electron the and can stress G.C. oxidase: a mitochondrial respiratory pathway to and signaling homeostasis during abiotic and stress in J. Sci. PubMed Scopus Google et al.Alternative and plant stress Signal. Behav. 2016; PubMed Scopus Google J. et al.Alternative is for plant Plant Sci. 2018; Full Text Full Text PDF PubMed Scopus Google Scholar]. of the of the in the and levels by mROS from I and and of this mROS production and PCD J. et of programmed cell death by in Exp. Bot. 2014; PubMed Scopus Google of programmed cell death by Exp. Bot. 2011; 62: PubMed Scopus Google Scholar]. than in but of in alleviate mROS and PCD et of mitochondrial NAD+ is essential for NADH homeostasis and ROS production in Sci. 2019; 62: PubMed Scopus Google Scholar]. the role of mROS as a for in a mitochondrial regulation by which mitochondria provide about their to the This can then lead to to to plant growth and stress is that such responses of the chloroplast protein import such as or under stressful and that a direct role in mechanisms of mROS signaling further as do of malate and The for a CTM system the of a signaling a of fatty acid metabolism, which from to the other to trigger mROS The and molecular that malate is from chloroplast to mitochondrion by means of malate and that this malate as a of redox in the Malate to mitochondria with the import of NAD+ leads to mROS production which plant and under extreme circumstances can lead to are to the role of malate circulation under variable growth and to the responses that are by since provide a key to the growth of plants to the environmental that production is the of the production and consumption of NADH in chloroplasts and how is this with plastidial fatty acid a role in the regulation of protein import chloroplasts under stress by the function of the protein import malate mitochondria, and mitochondrial functions or provide signaling do mitochondrial I and generate ROS and also mediate ROS are the mechanisms by which ROS signaling from mitochondria to the is mitochondrial alternative to modulate mitochondrial ROS production, ROS to cellular and ultimately other in chloroplasts also ROS production in mitochondria malate are the of malate in cells under conditions and how this to changes in synthesis and is the of the production and consumption of NADH in chloroplasts and how is this with plastidial fatty acid a role in the regulation of protein import chloroplasts under stress by the function of the protein import malate mitochondria, and mitochondrial functions or provide signaling do mitochondrial I and generate ROS and also mediate ROS are the mechanisms by which ROS signaling from mitochondria to the is mitochondrial alternative to modulate mitochondrial ROS production, ROS to cellular and ultimately other in chloroplasts also ROS production in mitochondria malate are the of malate in cells under conditions and how this to changes in synthesis and This by the of and the of the of and the the protein of the mitochondrial electron transport chain with It electrons from NADH to and the but also has the to generate a protein that fatty acid biosynthesis from and a protein with and with an protein to which the fatty acid chain is a cellular system that reducing equivalents for the redox reactions in and cellular redox by malate consumption and The transport of reducing equivalents from the to the is by malate In this mROS as a of cellular redox to the responses to various a system for the transport of reducing equivalents cellular by the of This system malate and in cellular the of malate and with the reduction or oxidation of the malate and a by which reducing equivalents are exported from the in the form of malate dehydrogenase by reducing to which is exported in for from the can malate to NADH in the a that leads to the death of It is considered to provide an to the for as a of or as a that than and oxygen

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