Interaction of methionine sulfoxide reductase B5 with SlMYC2 stimulates the transcription of MeJA-mediated autophagy-related genes in tomato fruit

Abstract

Methyl jasmonate (MeJA) has been shown to induce autophagy in various plant stress responses and metabolic pathways. MYC2 is involved in MeJA-mediated postharvest fruit biological metabolism, but it is unclear how it affects MeJA-induced fruit autophagy. In this study, we noticed that silencing SlMYC2 significantly reduced the increase in autophagy-related genes (SlATGs) expression induced by MeJA. SlMYC2 could also bind to the promoters of several SlATGs, including SlATG13a, SlATG13b, SlATG18a, and SlATG18h, and activate their transcript levels. Moreover, SlMsrB5, a methionine sulfoxide reductase, could interact with SlMYC2. Methionine oxidation in SlMYC2 and mimicking sulfoxidation in SlMYC2 by mutation of methionine-542 to glutamine reduced the DNA-binding ability and transcriptional activity of SlMYC2, respectively. SlMsrB5 partially repaired oxidized SlMYC2 and restored its DNA-binding ability. On the other hand, silencing SlMsrB5 inhibited the transcript levels of SlMYC2-targeted genes (SlATG13a, SlATG13b, SlATG18a, and SlATG18h). Similarly, dual-luciferase reporter (DLR) analysis revealed that SlMsrB5–SlMYC2 interaction significantly increased the ability of SlMYC2-mediated transcriptional activation of SlATG13a, SlATG13b, SlATG18a, and SlATG18h. These findings demonstrate that SlMsrB5-mediated cyclic oxidation/reduction of methionine in SlMYC2 influences SlATGs expression. Collectively, these findings reveal the mechanism of SlMYC2 in SlATGs transcriptional regulation, providing insight into the mechanism of MeJA-mediated postharvest fruit quality regulation.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 32172278) and the Shandong Province Natural Science Foundation (ZR2020KC011). We are grateful to City Hills Proofreading for their assistance in editing this manuscript.

Author contributions

D.M., F.L., and X.Z. conceived and designed experiments; D.M., J.L., and X.F. conducted the experiment; D.M., Y.S., J.D., and X.L analysed the data; D.M. and F.L. wrote the manuscript; X.Z. and F.L. revised the manuscript. N.J. provided technical support. M.A. improved the language. X.Z. supervised the experiment. All authors read and approved the manuscript.

Data availability

All data generated and analysed during this study are included in this article (and supplementary file).

Conflicts of interest statement

The authors declare no conflict of interest.

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