Summary: 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.

Cytosolic malate dehydrogenase (MDH) is a key enzyme that regulates the interconversion between malate and oxaloacetate (OAA). However, its role in modulating storage compound accumulation in maize endosperm is largely unknown. Here, we characterized a novel naturally occurring maize mdh4‐1 mutant, which produces small, opaque kernels and exhibits reduced starch but enhanced lysine content. Map‐based cloning, functional complementation and allelism analyses identified ZmMdh4 as the causal gene. Enzymatic assays demonstrated that ZmMDH4 predominantly catalyses the conversion from OAA to malate. In comparison, the activity of the mutant enzyme, which lacks one glutamic acid (Glu), was completed abolished, demonstrating that the Glu residue was essential for ZmMDH4 function. Knocking down ZmMdh4 in vivo led to a substantial metabolic shift towards glycolysis and a dramatic disruption in the activity of the mitochondrial complex I, which was correlated with transcriptomic alterations. Taken together, these results demonstrate that ZmMdh4 regulates the balance between mitochondrial respiration and glycolysis, ATP production and endosperm development, through a yet unknown feedback regulatory mechanism in mitochondria.

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The grain filling rate is closely associated with final grain yield of maize during the period of maize grain filling. To identify the key microRNAs (miRNAs) and miRNA-dependent gene regulation networks of grain filling in maize, a deep-sequencing technique was used to research the dynamic expression patternsof miRNAs at four distinct developmental grain filling stages in Zhengdan 958, which is an elite hybrid and cultivated widely in China. The sequencing result showed that the expression amount of almost all miRNAs was changing with the development of the grain filling and formed in seven groups. After normalization, 77 conserved miRNAs and 74 novel miRNAs were co-detected in these four samples. Eighty-one out of 162 targets of the conserved miRNAs belonged to transcriptional regulation (81, 50%), followed by oxidoreductase activity (18, 11%), signal transduction (16, 10%) and development (15, 9%). The result showed that miRNA 156, 393, 396 and 397, with their respective targets, might play key roles in the grain filling rate by regulating maize growth, development and environment stress response. The result also offered novel insights into the dynamic change of miRNAs during the developing process of maize kernels and assistedin the understanding of how miRNAs are functioning about the grain filling rate.