Mitochondria in photosynthetic cells: Coordinating redox control and energy balance

Igamberdiev, Abir U.; Bykova, Natalia V.

doi:10.1093/plphys/kiac541

Cited by 18 publications

(17 citation statements)

References 132 publications

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“…This ATP buffering activity can be attributed to mitochondrial respiration that utilizes reducing equivalents produced upstream by photosynthesis and transported to the mitochondria through redox shuttles (Igamberdiev and Bykova, 2022), thus maintaining a supply of ATP in the cytosol. Following this hypothesis the decrease of reducing equivalent export from the chloroplast would thus only start impacting cytosolic ATP levels if the dark period exceeded 1.5 minutes.…”

Section: Discussionmentioning

confidence: 99%

Mitochondrial respiration is essential for photosynthesis-dependent ATP supply of the plant cytosol

Vera-Vives,

Novel,

Zheng

et al. 2024

Preprint

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Plants rely on solar energy to synthesize ATP and NADPH for photosynthetic carbon fixation. Since a substantial proportion of cellular ATP is consumed in the cytosol, photosynthesis-derived ATP needs to be supplied there. While the triose phosphate shuttle and mitochondrial respiration can both deliver ATP to the cytosol, the significance of the different mechanismsin vivohas been difficult to assess. Although mitochondrial respiration is essential in plants, whether this is due to heterotrophic bottlenecks during plant development or rather a need for respiration in photosynthetically active cells, has not been resolved. In this study, we examinedin vivochanges of cytosolic ATP concentration in response to light, employing a biosensing strategy in the mossPhyscomitrium patens. Our measurements revealed increased cytosolic ATP concentration caused by photosynthetic activity. Moss tissue depleted of respiratory complex I showed decreased cytosolic ATP accumulation, highlighting a critical role of mitochondrial respiration in light-dependent ATP supply of the cytosol. Consistently, targeting mitochondrial ATP production directly, through the construction of mutants deficient in mitochondrial ATPase (complex V), led to drastic growth reduction, despite only minor alterations in photosynthetic electron transport activity. SinceP. patensis photoautotrophic throughout its development, we conclude that heterotrophic bottlenecks cannot account for the indispensable role of mitochondrial respiration in plants. Instead, our results offer compelling evidence that mitochondrial respiration is essential for ATP provision to the cytosol in actively photosynthesizing cells. Mitochondrial respiration provides metabolic integration, ensuring a reliable supply of cytosolic ATP essential for supporting plant growth and development.

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Section: Discussionmentioning

confidence: 99%

Mitochondrial respiration is essential for photosynthesis-dependent ATP supply of the plant cytosol

Vera-Vives,

Novel,

Zheng

et al. 2024

Preprint

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“…5 ). Indeed, the changes in contents of NADP(H) and NAD(H) also play key roles in regulating energy status in plants (Igamberdiev and Bykova 2023 ). There was obvious difference in NADPH/NADP + between the control and heat stress in either rice plants; A notable decrease in NADH/NAD + were presented in ett1 mutant plants under heat stress compared with control (Fig.…”

Section: Discussionmentioning

confidence: 99%

RGA1 Negatively Regulates Thermo-tolerance by Affecting Carbohydrate Metabolism and the Energy Supply in Rice

Feng¹,

Xu²,

Fu³

et al. 2023

Rice

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Background Signal transduction mediated by heterotrimeric G proteins, which comprise the α, β, and γ subunits, is one of the most important signaling pathways in rice plants. RGA1, which encodes the Gα subunit of the G protein, plays an important role in the response to various types of abiotic stress, including salt, drought, and cold stress. However, the role of RGA1 in the response to heat stress remains unclear. Results The heat-resistant mutant ett1 (enhanced thermo-tolerance 1) with a new allele of the RGA1 gene was derived from an ethane methyl sulfonate-induced Zhonghua11 mutant. After 45 °C heat stress treatment for 36 h and recovery for 7 d, the survival rate of the ett1 mutants was significantly higher than that of wild-type (WT) plants. The malondialdehyde content was lower, and the maximum fluorescence quantum yield of photosystem II, peroxidase activity, and hsp expression were higher in ett1 mutants than in WT plants after 12 h of exposure to 45 °C. The RNA-sequencing results revealed that the expression of genes involved in the metabolism of carbohydrate, nicotinamide adenine dinucleotide, and energy was up-regulated in ett1 under heat stress. The carbohydrate content and the relative expression of genes involved in sucrose metabolism indicated that carbohydrate metabolism was accelerated in ett1 under heat stress. Energy parameters, including the adenosine triphosphate (ATP) content and the energy charge, were significantly higher in the ett1 mutants than in WT plants under heat stress. Importantly, exogenous glucose can alleviate the damages on rice seedling plants caused by heat stress. Conclusion RGA1 negatively regulates the thermo-tolerance in rice seedling plants through affecting carbohydrate and energy metabolism.

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“…In photorespiratory conditions, the direction of the photorespiratory flux of glycerate to sucrose via gluconeogenesis would be preferable over its oxidation in glycolysis since the latter would result in the additional loss of the fixed carbon. The reductant and ATP are generated in mitochondria during oxidation of the photorespiratory glycine, while respiration is suppressed in the light [ 99 , 100 , 101 ]. Sucrose synthesis via gluconeogenesis, on the contrary, keeps carbon in the cell and balances Pi concentration.…”

Section: Gk In Gluconeogenesis and Respirationmentioning

confidence: 99%

Multiple Roles of Glycerate Kinase—From Photorespiration to Gluconeogenesis, C4 Metabolism, and Plant Immunity

Kleczkowski,

Igamberdiev

2024

IJMS

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Plant glycerate kinase (GK) was previously considered an exclusively chloroplastic enzyme of the glycolate pathway (photorespiration), and its sole predicted role was to return most of the glycolate-derived carbon (as glycerate) to the Calvin cycle. However, recent discovery of cytosolic GK revealed metabolic links for glycerate to other processes. Although GK was initially proposed as being solely regulated by substrate availability, subsequent discoveries of its redox regulation and the light involvement in the production of chloroplastic and cytosolic GK isoforms have indicated a more refined regulation of the pathways of glycerate conversion. Here, we re-evaluate the importance of GK and emphasize its multifaceted role in plants. Thus, GK can be a major player in several branches of primary metabolism, including the glycolate pathway, gluconeogenesis, glycolysis, and C4 metabolism. In addition, recently, the chloroplastic (but not cytosolic) GK isoform was implicated as part of a light-dependent plant immune response to pathogen attack. The origins of glycerate are also discussed here; it is produced in several cell compartments and undergoes huge fluctuations depending on light/dark conditions. The recent discovery of the vacuolar glycerate transporter adds yet another layer to our understanding of glycerate transport/metabolism and that of other two- and three-carbon metabolites.

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Mitochondria in photosynthetic cells: Coordinating redox control and energy balance

Cited by 18 publications

References 132 publications

Mitochondrial respiration is essential for photosynthesis-dependent ATP supply of the plant cytosol

Mitochondrial respiration is essential for photosynthesis-dependent ATP supply of the plant cytosol

RGA1 Negatively Regulates Thermo-tolerance by Affecting Carbohydrate Metabolism and the Energy Supply in Rice

Multiple Roles of Glycerate Kinase—From Photorespiration to Gluconeogenesis, C4 Metabolism, and Plant Immunity

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