Malate valves: old shuttles with new perspectives

Selinski, Jennifer; Scheibe, Renate

doi:10.1111/plb.12869

Cited by 186 publications

(175 citation statements)

References 101 publications

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“…The cellular NADPH pool is provided by a diverse range of NADPH-generating enzymes located in different subcellular compartments including the cytosol, chloroplasts, mitochondria and peroxisomes (Wakao and Benning 2005, Chai et al 2006, Maier et al 2011, Munekage 2016, Hýsková et al 2017, Corpas and Barroso 2018, Selinski and Scheibe 2018. During sweet pepper fruit ripening, these organelles undergo significant biochemical changes; e.g.…”

Section: Nadph Supply Is Mainly Provided By 6pgdh and Nadp-me Activitmentioning

confidence: 99%

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Muñoz‐Vargas

González‐Gordo

Palma

et al. 2019

Physiologia Plantarum

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NADPH is an essential cofactor in many physiological processes. Fruit ripening is caused by multiple biochemical pathways in which, reactive oxygen and nitrogen species (ROS/RNS) metabolism is involved. Previous studies have demonstrated the differential modulation of nitric oxide (NO) and hydrogen sulfide (H2S) content during sweet pepper (Capsicum annuum L.) fruit ripening, both of which regulate NADP‐isocitrate dehydrogenase activity. To gain a deeper understanding of the potential functions of other NADPH‐generating components, we analyzed glucose‐6‐phosphate dehydrogenase (G6PDH) and 6‐phosphogluconate dehydrogenase (6PGDH), which are involved in the oxidative phase of the pentose phosphate pathway (OxPPP) and NADP‐malic enzyme (NADP‐ME). During fruit ripening, G6PDH activity diminished by 38%, while 6PGDH and NADP‐ME activity increased 1.5‐ and 2.6‐fold, respectively. To better understand the potential regulation of these NADP‐dehydrogenases by H2S, we obtained a 50–75% ammonium‐sulfate‐enriched protein fraction containing these proteins. With the aid of in vitro assays, in the presence of H2S, we observed that, while NADP‐ME activity was inhibited by up to 29–32% using 2 and 5 mM Na2S as H2S donor, G6PDH and 6PGDH activities were unaffected. On the other hand, NO donors, S‐nitrosocyteine (CysNO) and DETA NONOate also inhibited NADP‐ME activity by 35%. These findings suggest that both NADP‐ME and 6PGDH play an important role in maintaining the supply of NADPH during pepper fruit ripening and that H2S and NO partially modulate the NADPH‐generating system.

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Section: Nadph Supply Is Mainly Provided By 6pgdh and Nadp-me Activitmentioning

confidence: 99%

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Muñoz‐Vargas

González‐Gordo

Palma

et al. 2019

Physiologia Plantarum

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“…In chloroplasts, ATP and NADPH can be used in the CBBC to reduce carbon dioxide to triose phosphate (triose-P), whereas reductant (NADPH) can also be used to synthesize malate (MAL) from oxaloacetate (OAA). Plants and algae have a MAL-OAA shuttle that can move electrons between chloroplasts and mitochondria (11,90). A key enzyme for the operation of the shuttle is malate dehydrogenase (MDH), which catalyzes the interconversion of MAL and OAA coupled to the oxidation/reduction of NAD(H)/NADP(H).…”

Section: Energetic Interactions Between Chloroplast and Mitochondriamentioning

confidence: 99%

“…A key enzyme for the operation of the shuttle is malate dehydrogenase (MDH), which catalyzes the interconversion of MAL and OAA coupled to the oxidation/reduction of NAD(H)/NADP(H). Vascular plants and C. reinhardtii contain multiple MDHs that have been detected in chloroplasts, mitochondria, the cytosol, and peroxi- somes (21,90). The MAL/OAA translocator, another important component of the shuttle, is involved in transporting MAL and OAA across the envelope membranes of organelles.…”

Section: Energetic Interactions Between Chloroplast and Mitochondriamentioning

confidence: 99%

The mitochondrial alternative oxidase from Chlamydomonas reinhardtii enables survival in high light

Kaye¹,

Huang²,

Clowez

et al. 2019

Journal of Biological Chemistry

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Edited by Ursula JakobPhotosynthetic organisms often experience extreme light conditions that can cause hyper-reduction of the chloroplast electron transport chain, resulting in oxidative damage. Accumulating evidence suggests that mitochondrial respiration and chloroplast photosynthesis are coupled when cells are absorbing high levels of excitation energy. This coupling helps protect the cells from hyper-reduction of photosynthetic electron carriers and diminishes the production of reactive oxygen species (ROS). To examine this cooperative protection, here we characterized Chlamydomonas reinhardtii mutants lacking the mitochondrial alternative terminal respiratory oxidases, CrAOX1 and CrAOX2. Using fluorescent fusion proteins, we experimentally demonstrated that both enzymes localize to mitochondria. We also observed that the mutant strains were more sensitive than WT cells to high light under mixotrophic and photoautotrophic conditions, with the aox1 strain being more sensitive than aox2. Additionally, the lack of CrAOX1 increased ROS accumulation, especially in very high light, and damaged the photosynthetic machinery, ultimately resulting in cell death. These findings indicate that the Chlamydomonas AOX proteins can participate in acclimation of C. reinhardtii cells to excess absorbed light energy. They suggest that when photosynthetic electron carriers are highly reduced, a chloroplast-mitochondria coupling allows safe dissipation of photosynthetically derived electrons via the reduction of O 2 through AOX (especially AOX1)-dependent mitochondrial respiration.

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“…redox valves, redox-regulated transporters) coordinate cellular functions during stress and developmental stages. There are two main redox valves in photosynthetic plant cells, the chloroplastic malate valve driven by photosynthetically produced NADPH that increases subcellular (in mitochondria, peroxisomes, cytosol, and plastids) NADH/NAD + ratios (Krömer and Scheibe, 1996;Selinski and Scheibe, 2019), and the mitochondrial citrate valve, driven by increased reduction level in mitochondria, that reduces subcellular NADP pools (Igamberdiev and Gardeström, 2003). In addition, the mitochondrial malate-aspartate shuttle transfers reducing equivalents from cytoplasm to mitochondria while coupling the TCA cycle to nitrogen assimilation by interconversion and shuttling of oxaloacetate (OAA), aspartate (Asp), glutamate (Glu), a-ketoglutarate (a-KG) and malate.…”

Section: Introductionmentioning

confidence: 99%

Primary Metabolite Responses to Oxidative Stress in Early-Senescing and Paraquat Resistant Arabidopsis thaliana rcd1 (Radical-Induced Cell Death1)

et al. 2020

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Rcd1 (radical-induced cell death1) is an Arabidopsis thaliana mutant, which exhibits high tolerance to paraquat [methyl viologen (MV)], herbicide that interrupts photosynthetic electron transport chain causing the formation of superoxide and inhibiting NADPH production in the chloroplast. To understand the biochemical mechanisms of MVresistance and the role of RCD1 in oxidative stress responses, we performed metabolite profiling of wild type (Col-0) and rcd1 plants in light, after MV exposure and after prolonged darkness. The function of RCD1 has been extensively studied at transcriptomic and biochemical level, but comprehensive metabolite profiling of rcd1 mutant has not been conducted until now. The mutant plants exhibited very different metabolic features from the wild type under light conditions implying enhanced glycolytic activity, altered nitrogen and nucleotide metabolism. In light conditions, superoxide production was elevated in rcd1, but no metabolic markers of oxidative stress were detected. Elevated senescence-associated metabolite marker levels in rcd1 at early developmental stage were in line with its early-senescing phenotype and possible mitochondrial dysfunction. After MV exposure, a marked decline in the levels of glycolytic and TCA cycle intermediates in Col-0 suggested severe plastidic oxidative stress and inhibition of photosynthesis and respiration, whereas in rcd1 the results indicated sustained photosynthesis and respiration and induction of energy salvaging pathways. The accumulation of oxidative stress markers in both plant lines indicated that MV-resistance in rcd1 derived from the altered regulation of cellular metabolism and not from the restricted delivery of MV into the cells or chloroplasts. Considering the evidence from metabolomic, transcriptomic and biochemical studies, we propose that RCD1 has a negative effect on reductive metabolism and rerouting of the energy production pathways. Thus, the altered, highly active reductive metabolism, energy salvaging pathways and Frontiers in Plant Science | www.frontiersin.org redox transfer between cellular compartments in rcd1 could be sufficient to avoid the negative effects of MV-induced toxicity.

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Malate valves: old shuttles with new perspectives

Cited by 186 publications

References 101 publications

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

The mitochondrial alternative oxidase from Chlamydomonas reinhardtii enables survival in high light

Primary Metabolite Responses to Oxidative Stress in Early-Senescing and Paraquat Resistant Arabidopsis thaliana rcd1 (Radical-Induced Cell Death1)

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Malate valves: old shuttles with new perspectives

Cited by 186 publications

References 101 publications

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits

The mitochondrial alternative oxidase from Chlamydomonas reinhardtii enables survival in high light

Primary Metabolite Responses to Oxidative Stress in Early-Senescing and Paraquat Resistant Arabidopsis thaliana rcd1 (Radical-Induced Cell Death1)

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Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits

Inhibition of NADP‐malic enzyme activity by H₂S and NO in sweet pepper (Capsicum annuum L.) fruits