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Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds.

ABSTRACT: Seed ageing is a major problem in the conservation of germplasm resources. The involvement of possible signalling molecules during seed deterioration needs to be identified. In this study, we confirmed that nitric oxide (NO), a key signalling molecule in plants, plays a positive role in the resistance of elm seeds to deterioration. To explore which metabolic pathways were affected by NO, an untargeted metabolomic analysis was conducted, and 163 metabolites could respond to both NO and the ageing treatment. The primary altered pathways include glutathione, methionine, and carbohydrate metabolism. The genes involved in glutathione and methionine metabolism were up-regulated by NO at the transcriptional level. Using a biotin switch method, proteins with an NO-dependent post-translational modification were screened during seed deterioration, and 82 putative S-nitrosylated proteins were identified. Eleven of these proteins were involved in carbohydrate metabolism, and the activities of the three enzymes were regulated by NO. In combination, the results of the metabolomic and S-nitrosoproteomic studies demonstrated that NO could activate glycolysis and inhibit the pentose phosphate pathway. In summary, the combination of these results demonstrated that NO could modulate carbohydrate metabolism at the post-translational level and regulate glutathione and methionine metabolism at the transcriptional level. It provides initial insights into the regulatory mechanisms of NO in seed deterioration.

SUBMITTER: He Y

PROVIDER: S-EPMC6184755 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds.

He Yuqi Y Xue Hua H Li Ying Y Wang Xiaofeng X

Journal of experimental botany 20181001 21

Seed ageing is a major problem in the conservation of germplasm resources. The involvement of possible signalling molecules during seed deterioration needs to be identified. In this study, we confirmed that nitric oxide (NO), a key signalling molecule in plants, plays a positive role in the resistance of elm seeds to deterioration. To explore which metabolic pathways were affected by NO, an untargeted metabolomic analysis was conducted, and 163 metabolites could respond to both NO and the ageing ...[more]

PMID: 30053069

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Project description:Hydrogen peroxide (H2O2) and nitric oxide (NO·) are toxic metabolites that immune cells use to attack pathogens. These antimicrobials can be present at the same time in phagosomes, and it remains unclear how bacteria deal with these insults when simultaneously present. Here, using Escherichia coli, we observed that simultaneous exposure to H2O2 and NO· leads to prioritized detoxification, where enzymatic removal of NO· is impeded until H2O2 has been eliminated. This phenomenon is reminiscent of carbon catabolite repression (CCR), where preferred carbon sources are catabolized prior to less desirable substrates; however, H2O2 and NO· are toxic, growth-inhibitory compounds rather than growth-promoting nutrients. To understand how NO· detoxification is delayed by H2O2 whereas H2O2 detoxification proceeds unimpeded, we confirmed that the effect depended on Hmp, which is the main NO· detoxification enzyme, and used an approach that integrated computational modeling and experimentation to delineate and test potential mechanisms. Plausible interactions included H2O2-dependent inhibition of hmp transcription and translation, direct inhibition of Hmp catalysis, and competition for reducing equivalents between Hmp and H2O2-degrading enzymes. Experiments illustrated that Hmp catalysis and NAD(P)H supply were not impaired by H2O2, whereas hmp transcription and translation were diminished. A dependence of this phenomenon on transcriptional regulation parallels CCR, and we found it to involve the transcriptional repressor NsrR. Collectively, these data suggest that bacterial regulation of growth inhibitor detoxification has similarities to the regulation of growth substrate consumption, which could have ramifications for infectious disease, bioremediation, and biocatalysis from inhibitor-containing feedstocks.IMPORTANCE Bacteria can be exposed to H2O2 and NO· concurrently within phagosomes. In such multistress situations, bacteria could have evolved to simultaneously degrade both toxic metabolites or preferentially detoxify one over the other. Here, we found that simultaneous exposure to H2O2 and NO· leads to prioritized detoxification, where detoxification of NO· is hampered until H2O2 has been eliminated. This phenomenon resembles CCR, where bacteria consume one substrate over others in carbon source mixtures. Further experimentation revealed a central role for transcriptional regulation in the prioritization of H2O2 over NO·, which is also important to CCR. This study suggests that regulatory scenarios observed in bacterial consumption of growth-promoting compound mixtures can be conserved in bacterial detoxification of toxic metabolite mixtures.

Dataset Information

Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds.

Publications

Nitric oxide alleviates cell death through protein S-nitrosylation and transcriptional regulation during the ageing of elm seeds.

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