The Ca2+-Regulation of the Mitochondrial External NADPH Dehydrogenase in Plants Is Controlled by Cytosolic pH

Hao, Meng; Jensen, Anna M.; Boquist, Ann Sofie; Liu, Yun Jun; Rasmusson, Allan G.

doi:10.1371/journal.pone.0139224

Cited by 16 publications

(8 citation statements)

References 70 publications

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“…A particularly striking example for intracellular pH regulation in plant cells is provided by the external mitochondrial NAD(P)H DEHYDROGENASE B1, which contributes to the alternative respiratory pathway and was shown to be stimulated by increases in [Ca 2+ ] cyt . However, biochemical data revealed that the enzyme is only sensitized to Ca 2+ regulation by a coincident decrease of pH (Hao et al, 2015). Our data now reveal that, in vivo, those changes coincide, providing the physiological basis for active regulation of the NADPH oxidation pathway to occur.…”

Section: Discussionsupporting

confidence: 51%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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Ca 2+ play a key role in cell signaling across organisms. The question of how a simple ion can mediate specific outcomes has spurred research into the role of Ca 2+ signatures and their encoding and decoding machinery. Such studies have frequently focused on Ca 2+ alone and our understanding of how Ca 2+ signaling is integrated with other responses is poor. Using in vivo imaging with different genetically encoded fluorescent sensors in Arabidopsis (Arabidopsis thaliana) cells, we show that Ca 2+ transients do not occur in isolation but are accompanied by pH changes in the cytosol. We estimate the degree of cytosolic acidification at up to 0.25 pH units in response to external ATP in seedling root tips. We validated this pH-Ca 2+ link for distinct stimuli. Our data suggest that the association with pH may be a general feature of Ca 2+ transients that depends on the transient characteristics and the intracellular compartment. These findings suggest a fundamental link between Ca 2+ and pH dynamics in plant cells, generalizing previous observations of their association in growing pollen tubes and root hairs. Ca 2+ signatures act in concert with pH signatures, possibly providing an additional layer of cellular signal transduction to tailor signal specificity.

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Section: Discussionsupporting

confidence: 51%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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“…4B). Figure 4C shows that NADPH dehydrogenase activity did not respond to high concentrations of calcium, as occurs in other fungal systems such as N. crassa and some plants [41,44]. As both the mRNA and the protein with the calcium binding domain (um03669) were synthesized in the four culture conditions, the lack of an effect of calcium on the respiratory activity of permeabilized cells is in agreement with the absence of critical residues in the putative calcium binding domain of this protein.…”

Section: Primerssupporting

confidence: 68%

Expression of alternative NADH dehydrogenases (NDH‐2) in the phytopathogenic fungus Ustilago maydis

et al. 2018

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Type 2 alternative NADH dehydrogenases ( NDH ‐2) participate indirectly in the generation of the electrochemical proton gradient by transferring electrons from NADH and NADPH into the ubiquinone pool. Due to their structural simplicity, alternative NADH dehydrogenases have been proposed as useful tools for gene therapy of cells with defects in the respiratory complex I. In this work, we report the presence of three open reading frames, which correspond to NDH ‐2 genes in the genome of Ustilago maydis . These three genes were constitutively transcribed in cells cultured in YPD and minimal medium with glucose, ethanol, or lactate as carbon sources. Proteomic analysis showed that only two of the three NDH ‐2 were associated with isolated mitochondria in all culture media. Oxygen consumption by permeabilized cells using NADH or NADPH was different for each condition, opening the possibility of posttranslational regulation. We confirmed the presence of both external and internal NADH dehydrogenases, as well as an external NADPH dehydrogenase insensitive to calcium. Higher oxygen consumption rates were observed during the exponential growth phase, suggesting that the activity of NADH and NADPH dehydrogenases is coupled to the dynamics of cell growth.

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“…The oxidation of NADH was shown to specifically require Ca 2+ (Møller et al, 1981b) and NADPH oxidation was also inhibited by chelators of divalent cations Edwards, 1979, 1980;Møller and Palmer, 1981). The activities of NADH and NADPH oxidation are regulated by submicromolar and micromolar concentrations of cytosolic free Ca 2+ , respectively, and activation of NADPH oxidation by Ca 2+ depends on the cytosolic pH (Hao et al, 2015). The concentration of the second messenger Ca 2+ , which has a central role in plant metabolism (Hetherington and Brownlee, 2004), also changes with cytosolic pH (Behera et al, 2018).…”

Section: External Nad(p)h Dehydrogenasesmentioning

confidence: 97%

Plant mitochondria – past, present and future

2021

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The study of plant mitochondria started in earnest around 1950 with the first isolations of mitochondria from animal and plant tissues. The first 35 years were spent establishing the basic properties of plant mitochondria and plant respiration using biochemical and physiological approaches. A number of unique properties (compared to mammalian mitochondria) were observed: (i) the ability to oxidize malate, glycine and cytosolic NAD (P)H at high rates; (ii) the partial insensitivity to rotenone, which turned out to be due to the presence of a second NADH dehydrogenase on the inner surface of the inner mitochondrial membrane in addition to the classical Complex I NADH dehydrogenase; and (iii) the partial insensitivity to cyanide, which turned out to be due to an alternative oxidase, which is also located on the inner surface of the inner mitochondrial membrane, in addition to the classical Complex IV, cytochrome oxidase. With the appearance of molecular biology methods around 1985, followed by genomics, further unique properties were discovered: (iv) plant mitochondrial DNA (mtDNA) is 10-600 times larger than the mammalian mtDNA, yet it only contains approximately 50% more genes; (v) plant mtDNA has kept the standard genetic code, and it has a low divergence rate with respect to point mutations, but a high recombinatorial activity; (vi) mitochondrial mRNA maturation includes a uniquely complex set of activities for processing, splicing and editing (at hundreds of sites); (vii) recombination in mtDNA creates novel reading frames that can produce male sterility; and (viii) plant mitochondria have a large proteome with 2000-3000 different proteins containing many unique proteins such as 200-300 pentatricopeptide repeat proteins. We describe the present and fairly detailed picture of the structure and function of plant mitochondria and how the unique properties make their metabolism more flexible allowing them to be involved in many diverse processes in the plant cell, such as photosynthesis, photorespiration, CAM and C4 metabolism, heat production, temperature control, stress resistance mechanisms, programmed cell death and genomic evolution. However, it is still a challenge to understand how the regulation of metabolism and mtDNA expression works at the cellular level and how retrograde signaling from the mitochondria coordinates all those processes.

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The Ca2+-Regulation of the Mitochondrial External NADPH Dehydrogenase in Plants Is Controlled by Cytosolic pH

Cited by 16 publications

References 70 publications

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Expression of alternative NADH dehydrogenases (NDH‐2) in the phytopathogenic fungus Ustilago maydis

Plant mitochondria – past, present and future

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The Ca2+-Regulation of the Mitochondrial External NADPH Dehydrogenase in Plants Is Controlled by Cytosolic pH

Cited by 16 publications

References 70 publications

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Expression of alternative NADH dehydrogenases (NDH‐2) in the phytopathogenic fungus Ustilago maydis

Plant mitochondria – past, present and future

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Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants