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Coordinated regulation of starch synthesis in maize endosperm by microRNAs and DNA methylation.

Starch synthesis is an essential feature of crop filling, but knowledge of the molecular regulatory mechanism of its synthetic genes' expressions is currently limited to transcription factors (TFs). Here, we obtained transcriptome, small-RNAome and DNA methylome data from maize endosperms, during multiple developmental stages and established a regulatory network atlas of starch synthesis. Transcriptome analysis showed sharp transition at 9-10 DAP, at which starch accumulates rapidly with enrichment of up-regulated genes of starch and sucrose metabolism. Expression pattern analysis established a comprehensive network between starch synthetic genes (SSGs) and TFs. During maize endosperm development, the miRNAs with preferential repression of the expression of TFs, particularly the TFs regulating SSG expression were extensively down-regulated during maize endosperm development. Specifically, ZmMYB138 and ZmMYB115 affected the transcriptional activities of Du1/Wx and Ae1/Bt2 genes at their respective promoters' regions. Remarkably, the two TFs were negatively regulated by the copious expression of Zma-miR159k-3p at post-transcriptional level. This suggests that miRNAs are important regulators of starch synthesis. Moreover, with the exclusion of the TFs, the expressions of both the SSGs and miRNAs were globally regulated by DNA methylation status. Altogether, the present results established the regulatory functions of miRNAs and DNA methylation in starch synthesis, and indicated that DNA methylation was a master switch. Supporting Information.