The O2-ZmGRAS11 transcriptional regulatory network orchestrates the coordination of endosperm cell expansion and grain filling in maize

Abstract

Maize (Zea mays) endosperm filling is coordinated with cell expansion to enlarge the grain size, but the mechanism coupling the two processes is poorly understood. Starchy endosperm cells basically contain no visible vacuoles for cell expansion. During grain filling, efficient synthesis of storage compounds leads to reduced cytoplasm and thus lowered cell turgor pressure. Although bioactive gibberellins (GAs) are essential for cell expansion, they accumulate at a low level at this stage. In this study, we identified an endosperm-specific GRAS domain-containing protein (ZmGRAS11) that lacks the DELLA domain and promotes cell expansion in the filling endosperm. The zmgras11 loss-of-function mutants showed normal grain filling but delayed cell expansion, thereby resulting in reduced kernel size and weight. Overexpression of ZmGRAS11 led to larger endosperm cells and therefore increased kernel size and weight. Consistent with this, ZmGRAS11 positively regulates the expression of ZmEXPB12, which is essential for cell expansion, at the endosperm filling stage. Moreover, we found that Opaque2 (O2), a central transcription factor that regulates endosperm filling, could directly bind to the promoter of ZmGRAS11 and activate its expression. Taken together, these results suggest that endosperm cell expansion is coupled with endosperm filling, which is orchestrated by the O2-ZmGRAS11-centered transcriptional regulatory network. Our findings also provide potential targets for maize yield improvement by increasing the storage capacity of endosperm cells.

Keywords: O2; ZmEXPB12; ZmGRAS11; cell expansion; maize endosperm.