GRF5 mediates circadian clock to gate seed quality in soybean

Circadian rhythm is an evolutional strategy to govern cellular processes to adapt to periodic environmental conditions. The mechanism of circadian clock regulation of cellular metabolism is well known and widely applied in animals and human, but poor in plants. Here, to elucidate an environmental, genetic and metabolic circadian-integration mechanism in plants, we comprehensively investigated phase- and tissue-specific transcript and metabolite clusters in soybean pods and found that pod walls and seeds are gifted with diverse circadian rhythms and perform distinct cellular activities. Then, we identified chronologically-identical or -dominant pathways and metabolisms in pod walls and seeds, respectively. We genetically and biochemically confirmed that GmGRF5a (and maybe with GmGRF5b) are directly controlled by clock genes and in turn immediately target genes of protein and oil syntheses. Both mutation and overexpression of GmGRF5 disturb transcriptome and metabolome and alter seed quality and size. During soybean domestication, GmGRF5a and GmGRF5b synergistically satisfy both the latitude (agroecological driver) and human (social driver) by shuffling threonine and isoleucine residues in their functional domains to produce various elites. Our results uncovered a mechanism underlying circadian gating of seed quality and opened a window for high-resolution chronoagriculture studies on seed metabolism and crop breeding targets.