A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production

Vishwakarma, Abhaypratap; Kumari, Arti; Mur, Luis A. J.; Gupta, Kapuganti Jagadis

doi:10.1016/j.freeradbiomed.2018.03.045

Cited by 75 publications

(82 citation statements)

References 41 publications

(51 reference statements)

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“…In contrast, the opposite results were obtained with the RNAi-aox strains. Previous studies with Arabidopsis thaliana have shown that under hypoxic stress, aox can regulate energy metabolism, affect ROS production and enhance resistance [61], and we obtained similar results. The formation of ROS is mainly due to the "single electron leakage" of respiratory chain components, and complexes I and III are considered the main sites of this electron leakage [62].…”

Section: Discussionsupporting

confidence: 86%

Alternative Oxidase Gene Induced by Nitric Oxide is Involved in the Regulation of ROS and Enhance the Resistance of Pleurotus Ostreatus to Heat Stress

Hou¹,

Zhao

Huang

et al. 2020

Preprint

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Background: Pleurotus ostreatus is easily affected by temperature during its cultivation. Nitric oxide (NO) plays an important regulatory role in the response to abiotic stress, and previous studies have found that NO can induce alternative oxidase (aox) in response to heat stress (HS) by regulating aconitase. However, the regulatory pathway of NO is complex, and the function and regulation of the aox gene in the response to HS remain unclear.Results: In this study, we found that NO affected the NADH and ATP levels, reduced the H2O2 and O2- contents, and slowed the production of O2-. Further RNA-Seq results showed that NO regulated the oxidation-reduction process and oxidoreductase activity, affected the cellular respiration pathway and activated aox gene expression. The function of aox was determined by constructing overexpression (OE) and RNA interference (RNAi) strains. The results showed that the OE-aox strains showed obvious advantages in experiencing growth recovery after exposure to HS. During exposure to HS, the OE-aox strains exhibited reduced levels of NADH, the product of the TCA cycle, and decreased synthesis of ATP, which reduced the production and accumulation of ROS, whereas the RNAi-aox strains exhibited the opposite result. In addition, aox mediated the expression of antioxidant enzyme genes in the mycelia of P. ostreatus under HS through the retrograde signaling pathway. Conclusions: This study shows that the aox gene in P. ostreatus mycelia can be induced by NO under HS, regulates the TCA cycle and cell respiration to reduce the production of ROS, and can mediate the retrograde signaling pathway involved in the mycelial response to HS.

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Section: Discussionsupporting

confidence: 86%

Alternative Oxidase Gene Induced by Nitric Oxide is Involved in the Regulation of ROS and Enhance the Resistance of Pleurotus Ostreatus to Heat Stress

Hou¹,

Zhao

Huang

et al. 2020

Preprint

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“…Candidates include: nitric oxide (NO), shown to participate in stress signaling in plants (Delledonne et al ., ; Durner et al ., ; Neill et al ., ; de Pinto et al ., ) and to regulate AOX expression (Feng et al ., ), could serve as a signaling molecule. In A. thaliana , AOX overexpression led to NO increase, while AOX downregulation resulted in NO decrease (Vishwakarma et al ., ). NO accumulates in P. tricornutum cells treated with diatom‐derived aldehydes.…”

Section: Discussionmentioning

confidence: 97%

Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom

et al. 2018

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Diatom dominance in contemporary aquatic environments indicates that they have developed unique and effective mechanisms to cope with the rapid and considerable fluctuations that characterize these environments. In view of their evolutionary history from a secondary endosymbiosis, inter-organellar regulation of biochemical activities may be of particular relevance. Diatom mitochondrial alternative oxidase (AOX) is believed to play a significant role in supplying chloroplasts with ATP produced in the mitochondria. Using the model diatom Phaeodactylum tricornutum we generated AOX knockdown lines, and followed sensitivity to stressors, photosynthesis and transcriptome and metabolome profiles of wild-type and knockdown lines. We show here that expression of the AOX gene is upregulated by various stresses including H O , heat, high light illumination, and iron or nitrogen limitation. AOX knockdown results in hypersensitivity to stress. Knockdown lines also show significantly reduced photosynthetic rates and their chloroplasts are more oxidized. Comparisons of transcriptome and metabolome profiles suggest a strong impact of AOX activity on gene expression, which is carried through to the level of the metabolome. Our data provide evidence for the involvement of mitochondrial AOX in processes central to the cell biology of diatoms, revealing that cross-talk between mitochondria and chloroplasts is crucial for maintaining sensitivity to changing environments.

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“…High concentrations of ascorbate in plant cells facilitates scavenging of superoxide (O2-) moreover, ascorbate peroxidase is also involved in H2O2 scavenging and reduction of NO2- to NO (Alegria et al, 2004). The ability of plants under hypoxia to synthesize ascorbate (Fig 8m) and induction of genes involved in the ascorbate-glutathione cycle (Fig 6) may be one of the reasons for production of reduced peroxynitrite under hypoxia (Vishwakarma et al ., 2018) despite of higher NO production by the mitochondrial COX and AOX (Gupta et al, 2005; Vishwakarma et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Nitric oxide is important for sensing and survival under hypoxia in Arabidopsis

Wany

Brotman

et al. 2018

Preprint

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Nitric oxide (NO) is a free radical molecule that plays an important role in hypoxic stress. We studied the impact of hypoxia-induced NO production on the expression of genes and production of metabolites involved in carbon, oxygen sensing, nitrogen, and antioxidant metabolism using wild type (WT), non-symbiotic haemoglobin-overexpressing (Hb+) and nitrate reductase double mutant (nia1,2) of Arabidopsis. Futher application of NO scavenger cPTIO was used to confirm NO role. We found that imposing hypoxia leads to the increaseof NO and reactive oxygen species (ROS) levels in WT, while the reduced levels of NO and higher levels of ROS were observed in roots of Hb+ and nia1,2 mutant. Expression of the genes encoding oxygen sensing and the enzymes involved in fermentative pathways, their activities and metabolite levels were highly induced in WT suggesting that NO plays a role in the induction of fermentation. Several genes and metabolites involved in the TCA cycle were also induced in WT in comparison to Hb+ and nia mutant line suggesting that NO can accelerate TCA cycle to regenerate reducing equivalents under hypoxia. Interestingly, we found that the genes and metabolites involved in the ascorbate-glutathione cycle were modulated by NO under hypoxia. The alternative oxidasegene (AOX1A) was induced under hypoxia in WTdue to increased levels of NO rather than ROS. Futher, we found that NO improves plant survival. Overall these findings suggest that NO is a major player in plant survival under hypoxia by modulating gene expression and metabolite levels of carbon, nitrogen, oxygen sensing and antioxidant metabolism.HighlightHypoxia-induced nitric oxide plays a central role in activation of genes and metabolites involved in fermentation, TCA cycle, nitrogen and antioxidant metabolism

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A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production

Cited by 75 publications

References 41 publications

Alternative Oxidase Gene Induced by Nitric Oxide is Involved in the Regulation of ROS and Enhance the Resistance of Pleurotus Ostreatus to Heat Stress

Alternative Oxidase Gene Induced by Nitric Oxide is Involved in the Regulation of ROS and Enhance the Resistance of Pleurotus Ostreatus to Heat Stress

Downregulation of mitochondrial alternative oxidase affects chloroplast function, redox status and stress response in a marine diatom

Nitric oxide is important for sensing and survival under hypoxia in Arabidopsis

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