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SUMMARY: Flavonoids are a well‐known class of specialized metabolites that play key roles in plant development, reproduction, and survival. Flavonoids are also of considerable interest from the perspective of human health, as both phytonutrients and pharmaceuticals. RNA sequencing analysis of an Arabidopsis null allele for chalcone synthase (CHS), which catalyzes the first step in flavonoid metabolism, has uncovered evidence that these compounds influence the expression of genes associated with the plant circadian clock. Analysis of promoter‐luciferase constructs further showed that the transcriptional activity of CCA1 and TOC1, two key clock genes, is altered in CHS‐deficient seedlings across the day/night cycle. Similar findings for a mutant line lacking flavonoid 3′‐hydroxylase (F3′H) activity, and thus able to synthesize mono‐ but not dihydroxylated B‐ring flavonoids, suggests that the latter are at least partially responsible; this was further supported by the ability of quercetin to enhance CCA1 promoter activity in wild‐type and CHS‐deficient seedlings. The effects of flavonoids on circadian function were also reflected in photosynthetic activity, with chlorophyll cycling abolished in CHS‐ and F3′H‐deficient plants. Remarkably, the same phenotype was exhibited by plants with artificially high flavonoid levels, indicating that neither the antioxidant potential nor the light‐screening properties of flavonoids contribute to optimal clock function, as has recently also been demonstrated in animal systems. Collectively, the current experiments point to a previously unknown connection between flavonoids and circadian cycling in plants and open the way to better understanding of the molecular basis of flavonoid action. Significance Statement: This manuscript presents the novel finding that flavonoids, specialized metabolites that play key roles in plant growth and survival, also influence the plant circadian clock. This discovery, based on genetic, molecular, and physiological evidence, opens new doors to advancing our still remarkably poor understanding of the mode of action of these ubiquitous and abundant plant metabolites. [ABSTRACT FROM AUTHOR]

Plant flavonoid metabolism has served as a platform for understanding a range of fundamental biological phenomena, including providing some of the early insights into the subcellular organization of metabolism. Evidence assembled over the past three decades points to the organization of the component enzymes as a membrane-associated complex centered on the entry-point enzyme, chalcone synthase (CHS), with flux into branch pathways controlled by competitive protein interactions. Flavonoid enzymes have also been found in the nucleus in a variety of plant species, raising the possibility of alternative, or moonlighting functions for these proteins in this compartment. Here, we present evidence that CHS interacts with MOS9, a nuclear-localized protein that has been linked to epigenetic control of R genes that mediate effector-triggered immunity. Overexpression of MOS9 results in a reduction of CHS transcript levels and a metabolite profile that substantially intersects with the effects of a null mutation in CHS. These results suggest that the MOS9-CHS interaction may point to a previously-unknown mechanism for controlling the expression of the highly dynamic flavonoid pathway. [ABSTRACT FROM AUTHOR]