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

Abstract

SUMMARYStarch synthesis is an essential feature of crop filling, but knowledge of the molecular mechanisms regulating the expression of starch synthesis genes (SSGs) is currently limited to transcription factors (TFs). Here, we obtained transcriptome, small RNAome, and DNA methylome data from maize (Zea mays) endosperms during multiple developmental stages and established a regulatory network atlas of starch synthesis. Transcriptome analysis showed a sharp transition at 9–10 days after pollination, when genes involved in starch and sucrose metabolism are upregulated and starch accumulates rapidly. Expression pattern analysis established a comprehensive network between 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 downregulated. Specifically, ZmMYB138 and ZmMYB115 affected the transcriptional activities of Du1/Wx and Ae1/Bt2 genes at their respective promoter regions. Remarkably, the two TFs were negatively regulated by the copious expression of Zma‐miR159k‐3p at the post‐transcriptional level. This suggests that miRNAs are important regulators of starch synthesis. Moreover, with the exclusion of the TFs, the expression of both SSGs and miRNAs was globally regulated by DNA methylation. Altogether, the present results (i) establish the regulatory functions of miRNAs and DNA methylation in starch synthesis and (ii) indicate that DNA methylation functions as a master switch.

Starch biosynthesis in cereal endosperms: An updated review over the last decade

“…Previous studies have shown that genes preferentially expressed in the rice endosperm, including SSRGs, usually show reduced expression because of methylation, indicating that methylation is also involved in the regulation of starch synthesis ( Zemach et al., 2010 ). Recently, similar overall methylation patterns were found in the SSRGs expressed in the maize endosperm ( Hu et al., 2021 ). In the developing maize endosperm, the coding regions of low-expression SSRGs are highly methylated, and expression levels of SBE1 and Su1 correlate significantly and negatively with predicted DNA methylation marks ( Hu et al., 2021 ).…”

“…Recently, similar overall methylation patterns were found in the SSRGs expressed in the maize endosperm ( Hu et al., 2021 ). In the developing maize endosperm, the coding regions of low-expression SSRGs are highly methylated, and expression levels of SBE1 and Su1 correlate significantly and negatively with predicted DNA methylation marks ( Hu et al., 2021 ). Thus, DNA methylation may act as a switch in the global regulation of starch biosynthesis.…”

“…Furthermore, the maize MYB TF ZmMYB14 binds to the promoters of multiple SSRGs, including ZmBT1 , to activate their expression ( Xiao et al., 2017 ). ZmMYB138 and ZmMYB115 are candidate TFs involved in the regulation of starch synthesis in the maize endosperm, as suggested by expression correlation analysis ( Hu et al., 2021 ). ZmABI4, ZmEREB156, and HvSUSIBA2 are TFs related to the modulation of SSRGs such as SSIIIa , SSI , and ISA1 by abscisic acid (ABA) and/or sugar signaling ( Sun et al., 2003 ; Hu et al., 2012 ; Huang et al., 2016 ).…”

Identification of miRNAs-mediated seed and stone-hardening regulatory networks and their signal pathway of GA-induced seedless berries in grapevine (V. vinifera L.)

“…Similar cases were reported by previous studies [ 35 ]. For example, ZmMYB138 and ZmMYB115 for ZmmiR159k regulated the endosperm development of corn seeds by affecting the transcriptional activities of Du1/Wx and Ae1/Bt2 genes [ 36 ]. MYB89 was expressed predominantly in developing seeds during maturation, which inhibited seed oil accumulation by directly repressing WRI1 [ 37 ].…”

Molecular Functions and Pathways of Plastidial Starch Phosphorylase (PHO1) in Starch Metabolism: Current and Future Perspectives

“…A limited set of transcription factors have been identified to date [ 106 ] that contribute to the regulation of storage starch synthesis mainly in Oryza sativa [ 107 , 108 ], Triticum aestivum [ 109 ], and Zea mays [ 110 , 111 , 112 ]. NAM, ATAF1/2, and CUC2 (NAC) are the major families of plant-specific transcription factors (TFs) [ 111 , 113 , 114 ], which are reportedly involved directly (physical binding) or indirectly (functional interaction attributed to other binding partners) in the regulation of starch biosynthesis through modulating the starch biosynthetic enzymes [ 115 ]. Based on previously reported work on Zea mays , ZmEREB156 was found to actively modulate the SSIII [ 10 , 107 , 116 ].…”