Corepressor AtSDR4L and its paralog regulate hormonal and hypoxia responses in multiple <i>Arabidopsis</i> seed compartments

Development is a series of decision-making events. Success of seed plants at individual and population levels strongly depends on the timing of germination and the rapidness of seedling establishment. Arabidopsis thaliana SEED DORMANCY 4-LIKE (AtSDR4L) and its paralog Dynamic Influencer of Gene Expression 2 (DIG2) are transcriptional corepressors that promote seed-to-seedling phase transition. Their regulatory roles in promoting germination at the temporal and tissue-specific scales remain elusive. We show that strong germination arrest of Atsdr4l dig2 is alleviated by ABA antagonists. Isolated mutant embryos develop faster than intact seeds but still exhibit delayed growth. Atsdr4l dig2 seeds show extensive changes in gene expression in both the seed coat and the embryo, with a subset of the genes differentially expressed tissue-specifically. MIKC-type MADS-box genes are the top-enriched transcription factor family among upregulated genes in both seed compartments of Atsdr4l dig2, and AGAMOUS-LIKE44 (AGL44) is a direct target of both AtSDR4L and DIG2. Many hormonal genes and hypoxia-responsive genes are misregulated in the double mutant seeds, accompanied by an overaccumulation of abscisic acid, auxin, and their derivatives, as well as the immediate precursor of ethylene. Together, these results provide mechanistic insights into how AtSDR4L and DIG2 work in concert to coordinate multiple pathways and prepare seeds for germination.