MaMADS1–MaNAC083 transcriptional regulatory cascade regulates ethylene biosynthesis during banana fruit ripening

Abstract

The hormone ethylene is crucial in the regulation of ripening in climacteric fruit, such as bananas. The transcriptional regulation of ethylene biosynthesis throughout banana fruit ripening has received much study, but the cascaded transcriptional machinery of upstream transcriptional regulators implicated in the ethylene biosynthesis pathway is still poorly understood. Here we report that ethylene biosynthesis genes, including MaACS1, MaACO1, MaACO4, MaACO5, and MaACO8, were upregulated in ripening bananas. NAC (NAM, ATAF, CUC) transcription factor, MaNAC083, a ripening and ethylene-inhibited gene, was discovered as a potential binding protein to the MaACS1 promoter by yeast one-hybrid screening. Further in vitro and in vivo experiments indicated that MaNAC083 bound directly to promoters of the five ethylene biosynthesis genes, thereby transcriptionally repressing their expression, which was further verified by transient overexpression experiments, where ethylene production was inhibited through MaNAC083-modulated transcriptional repression of ethylene biosynthesis genes in banana fruits. Strikingly, MaMADS1, a ripening-induced MADS (MCM1, AGAMOUS, DEFICIENS, SRF4) transcription factor, was found to directly repress the expression of MaNAC083, inhibiting trans-repression of MaNAC083 to ethylene biosynthesis genes, thereby attenuating MaNAC083-repressed ethylene production in bananas. These findings collectively illustrated the mechanistic basis of a MaMADS1–MaNAC083– MaACS1/MaACOs regulatory cascade controlling ethylene biosynthesis during banana fruit ripening. These findings increase our knowledge of the transcriptional regulatory mechanisms of ethylene biosynthesis at the transcriptional level and are expected to help develop molecular approaches to control ripening and improve fruit storability.

Acknowledgements

This study was supported by the National Key Research and Development Program of China (grant no. 2022YFD2100103), the National Natural Science Foundation of China (grant no. 32072279), and the China Agriculture Research System of MOF and MARA (grant no. CARS-31).

Author contributions

W.S. conceived and designed the study, while W.W. performed experiments alongside W.S. Data analysis was carried out by a team consisting of W.W., Y.Y.Y, C.J.W, J.F.K., W.J.L., and W.S. The manuscript writing and revision were done by J.Y.C., W.S., and W.W.; all authors participated in manuscript discussions.

Data availability

All study data are incorporated in the submitted article.

Conflict of interest

None declared.

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