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Integrative analyses of transcriptome, microRNA-seq and metabolome reveal insights into exogenous melatonin-mediated salt tolerance during seed germination of maize

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Abstract

Melatonin is an important phytohormone influencing plant growth and defense responses. However, the mechanism mediating the regulatory effects of melatonin on the salt tolerance of germinating maize seeds remains unexplored. In this study, the application of exogenous melatonin enhanced the salt tolerance of germinating maize seeds. A transcriptome analysis indicated that complex regulatory pathways may be associated with the melatonin-mediated salt tolerance. Remarkably, antioxidant activities, transcriptional regulation, and phytohormone (e.g., cytokinin and auxin) pathways were induced following the exogenous application of melatonin. The microRNA (miRNA)-seq analysis result indicated that exogenous melatonin obviously altered the expression of a set of miRNAs. Notably, many differentially expressed miRNAs and their target genes, including several transcription factor genes, were revealed to contribute to salt stress responses. According to metabolite profiles, the abundance of diverse metabolites, like secondary metabolites, nucleotides, cofactors, and vitamins, increased significantly after using exogenous melatonin. The combined analysis of the transcriptome and metabolome indicated that several gene–metabolite networks related to amino acid metabolism and secondary metabolite biosynthetic pathways are essential for melatonin-mediated maize tolerance to salt stress. Consistent with these findings, exogenously applied melatonin altered the phytohormone levels and increased the antioxidant enzyme activities and energy supply. Our results reflect the significance of melatonin for enhancing the salt tolerance of germinating maize seeds, which is achieved through the regulation of antioxidant capacity, phytohormone content, and metabolic adaptation.

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Data availability

The RNA-seq data and microRNA-seq data generated as part of the study have been deposited to the NCBI GEO database under the BioProject accession GSE223824. The data underlying this article are available in the article and Supporting Information.

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Funding

This work was supported by the grant from the National Natural Science Foundation of China (32070558, 32061143030, 32301826, 32100448, 32170636), National key research and development program of China (2022YFD1900704), Natural Science Foundation of Jiangsu Province (BK20230570, BK20210799), the China Postdoctoral Science Foundation (2023M731389), A project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), the Seed Industry Revitalization Project of Jiangsu Province (JBGS[2021]009), the Key Research and Development Program of Jiangsu Province (BE2022343), the Shanghai Science and Technology Agriculture Project ([2022] No. 1–6), and the Project of Zhongshan Biological Breeding Laboratory (BM2022008-029).

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Contributions

Z.Y. and R.C. conceived the idea and supervised this study. S.X., S.W., Z.W., Y.L., T.T., Q.H., Z.L., H.W., Y.S. and A.G. performed the experiments. S.X., S.W., Z.W., Y.Z., Y.X., and P.L. participated in the result analysis. S.X., R.C. and Z.Y. wrote the original draft of the manuscript. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Rujia Chen or Zefeng Yang.

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Xu, S., Wang, S., Wang, Z. et al. Integrative analyses of transcriptome, microRNA-seq and metabolome reveal insights into exogenous melatonin-mediated salt tolerance during seed germination of maize. Plant Growth Regul (2024). https://doi.org/10.1007/s10725-024-01138-w

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  • DOI: https://doi.org/10.1007/s10725-024-01138-w

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