Qiuzhen Tian,Gang Wang,Xuexia Ma,Qingwen Shen,Mengli Ding,Xueyi Yang,Xiaoli Luo,Rongrong Li,Zhenhui Wang,Xiangyang Wang,Zhiyuan Fu,Qinghua Yang,Jihua Tang,Guifeng Wang
Plant Biotechnology Journal
DOI:10.1111/pbi.13826
Abstract
Riboflavin is the precursor of essential cofactors for diverse metabolic processes. Unlike animals, plants can de novo produce riboflavin through an ancestrally conserved pathway, like bacteria and fungi. However, the mechanism by which riboflavin regulates seed development is poorly understood. Here we report a novel maize (Zea mays L.) opaque mutant o18, which displays an increase in lysine accumulation but impaired endosperm filling and embryo development. O18 encodes a rate-limiting bifunctional enzyme ZmRIBA1, targeted to plastid where to initiate riboflavin biosynthesis. Loss of function of O18 specifically disrupts respiratory complexes I and II, but also decreases SDH1 flavinylation, in turn shifts the mitochondrial tricarboxylic acid (TCA) cycle to glycolysis. The deprivation of cellular energy leads to cell cycle arrest at G1 and S phases in both mitosis and endoreduplication during endosperm development. The unexpected upregulation of cell cycle genes in o18 correlates with the increase of H3K4me3 levels, revealing a possible H3K4me-mediated epigenetic backup mechanism for cell cycle progression under unfavorable circumstances. Overexpression of O18 increases riboflavin production and confers osmotic tolerance. Altogether, our results substantiate a key role of riboflavin in coordinating cellular energy and cell cycle to modulate maize endosperm development.
