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

Abstract

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.

An MCIA-like complex is required for mitochondrial complex I assembly and seed development in maize

“…Consistent with the loss of complex I NADH dehydrogenase activity, the NADH/NAD + ratio was higher in crk1-1, consequently resulting in a decrease in ATP abundance (Figure 4H). This scenario is exactly in line with that observed for the maize o18 mutant, which also has defects in complex I function (Tian et al, 2022).…”

“…In humans, complex I dysfunction is responsible for around one-third of mitochondrial diseases, such as Leigh syndrome, lactic acidosis, leukoencephalopathy, and isolated myopathy (Ghezzi and Zeviani, 2018). In contrast, plants lacking complex I exhibit growth and development retardation and/or, commonly, seed abortion (Wang et al, 2017;Ligas et al, 2019;Tian et al, 2022). Nonetheless, some unicellular and multicellular organisms naturally lack complex I but compensate through diverse mechanisms, such as the acquisition of ATP from host cells, degeneration or rearrangement of the respiratory chain, or alternative oxidoreduction (Mayer and Muller, 2014;Raven and Beardall, 2017;Maclean et al, 2018;Senkler et al, 2018).…”

Dynamic atlas of histone modifications and gene regulatory networks in endosperm of bread wheat

“…A well-known example is the progressive repression of FLOWERING LOCUS C (FLC) by H3K27me3 during vernalization 49 . Studies in rice and maize have reported the role of histone modifications in endosperm starch and protein accumulation [24][25][26][27][28] . We mapped H3K27me3, H3K4me3 and H3K9ac in wheat endosperm to explore the role of histone modifications on gene transcription during endosperm development.…”

“…For instance, a large number of genes involved in nutrient metabolic pathway are directly regulated in the endosperm by OsFIE2-catalyzed H3K27me3. Up-regulation of cell cyclerelated genes in maize opaque mutant opaque18 correlates with increased levels of H3K4me3 28 . Moreover, a majority number of paternally expressed imprinted genes and transposable elements are marked by H3K27me3 in maize and Arabisopsis endosperm [29][30][31] .…”

“…Thus, both H3K4me3 and H3K9ac peak regions can be treated as cis-element enriched region for predicting up-stream regulators. Evidence in rice and maize has depicted the role of histone modifications in regulating the transcriptional activity of endosperm-specific genes [24][25][26][27][28] . For instance, a large number of genes involved in nutrient metabolic pathway are directly regulated in the endosperm by OsFIE2-catalyzed H3K27me3.…”