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Sodium Hydrosulfide Induces Resistance Against Penicillium expansum in Apples by Regulating Hydrogen Peroxide and Nitric Oxide Activation of Phenylpropanoid Metabolism.

ABSTRACT: As a multifunctional signaling molecule, hydrogen sulfide (H₂S) has been reported to induce plant responses to a variety of abiotic stresses. However, there are no reports on H₂S treatment inducing resistance in apples against Penicillium expansum, a biotic factor, and its possible mechanism of action. In this study, fumigating apples with 5 mM sodium hydrosulfide (NaHS), the exogenous donor of H₂S, for 12 h reduced the diameter of lesions in fruit colonized by P. expansum. NaHS treatment markedly promoted the synthesis of endogenous H₂S, hydrogen peroxide (H₂O₂), and nitrogen oxide (NO). In vivo NaHS treatment enhanced the activities of phenylalanine ammonia-lyase, cinnamate 4-hydroxylase, p-coumarate:coenzyme A ligase isoenzymes, caffeoyl-CoA-O-methyltransferase, caffeic acid-O-methyltransferase, ferulic acid-5-hydroxylase, cinnamyl-CoA reductase, and cinnamyl-alcohol dehydrogenase. The treatment also facilitated the production of specific phenolic acids, such as cinnamic acid, p-coumaric acid, caffeic acid, ferulic acid, and sinapic acid; total phenolic compounds; p-coumaryl alcohol; coniferyl alcohol; sinapyl alcohol; and lignin. NaHS treatment induced resistance against P. expansum in apples through H₂O₂- and NO-mediated activation of phenylpropanoid metabolism.

SUBMITTER: Deng H

PROVIDER: S-EPMC8440896 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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

Sodium Hydrosulfide Induces Resistance Against Penicillium expansum in Apples by Regulating Hydrogen Peroxide and Nitric Oxide Activation of Phenylpropanoid Metabolism.

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