Riboflavin integrates cellular energetics and cell cycle to regulate maize seed development.

Riboflavin integrates cellular energetics and cell cycle to regulate maize seed development.
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核黄素整合细胞能量学和细胞周期调控玉米种子发育。

DOI:
10.1111/pbi.13826
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发表时间:
2022-08
影响因子:
13.8
通讯作者:
Wang, Guifeng
Wang, Guifeng
中科院分区:
工程技术1区
文献类型:
--
作者:
Tian, Qiuzhen;Wang, Gang;Ma, Xuexia;Shen, Qingwen;Ding, Mengli;Yang, Xueyi;Luo, Xiaoli;Li, Rongrong;Wang, Zhenghui;Wang, Xiangyang;Fu, Zhiyuan;Yang, Qinghua;Tang, Jihua;Wang, Guifeng

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核黄素是多种代谢过程中必需辅因子的前体。与动物不同,植物可以通过细菌和真菌等祖先保守的途径从头产生核黄素。然而,核黄素调节种子发育的机制还知之甚少。在此,我们报道了一种新的玉米(Zea Mays L.)不透明突变体O18,表现为赖氨酸积累增加,但损害胚乳充盈和胚胎发育。O18编码一种限速双功能酶ZmRIBA1,定位于启动核黄素生物合成的叶绿体。O18功能的丧失会特异性地破坏呼吸复合体I和II,但也会减少SDH1的黄素化,进而将线粒体三羧酸(TCA)循环转移到糖酵解。在胚乳发育过程中,细胞能量的丧失导致有丝分裂和内复制的细胞周期停滞在G1期和S期。O18中细胞周期基因的意外上调与H3K4me3水平的增加相关,揭示了在不利环境下H3K4me可能介导的细胞周期进展的表观遗传支持机制。O18的过表达增加了核黄素的产生,并赋予了渗透耐受性。总之,我们的结果证实了核黄素在协调细胞能量和细胞周期以调节玉米胚乳发育方面的关键作用。
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, and 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 up‐regulation of cell‐cycle genes in o18 correlates with the increase of H3K4me3 levels, revealing a possible H3K4me‐mediated epigenetic back‐up mechanism for cell‐cycle progression under unfavourable 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.
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