Arabidopsis chromatin remodeler SPLAYED is required for abscisic acid-mediated post-germination growth arrest

The phytohormone abscisic acid (ABA) promotes seed dormancy, inhibits seed germination, and induces post-germination growth arrest. It remains unclear how chromatin remodeling influences ABA responses during early seedling establishment. In this study, an artificial microRNA targeting 2 sucrose nonfermenting 2 (SNF2)-family chromatin remodeling ATPases, SPLAYED (SYD) and PHOTOPERIOD-INDEPENDENT EARLY FLOWERING1 (PIE1), was identified through unbiased forward genetic screening of artificial microRNA (amiRNA)-expressing pooled seed libraries exhibiting ABA insensitivity during the seed-to-seedling transition. T-DNA insertional mutants of syd and pie1, along with amiRNA-expressing knockdown lines amiR-SYD and amiR-PIE1, confirmed that SYD is required for ABA inhibition of post-germination growth. Transcriptomic analyses revealed that, under ABA treatment, amiR-SYD mutant seeds exhibited increased expression of the ABA catabolism gene CYP707A3 and the gibberellin (GA) biosynthesis genes GA20OX2, GA20OX3, GA3OX1, GA3OX2, and GA3OX4. Concurrently, the ABA-responsive genes KIN1 and EM6 were less strongly induced, whereas the GA-responsive genes GASA4 and GASA6 were more strongly induced. The ABA hyposensitivity observed in amiR-SYD mutants was reversed by treatment with uniconazole, an inhibitor of ABA catabolism and GA biosynthesis. These findings suggest that the SYD-associated chromatin remodeling complex positively regulates ABA-mediated post-germination growth arrest by modulating the balance between ABA and GA responses, in contrast to its close homolog BRAHMA (BRM), which negatively regulates ABA responses through an ABI5-mediated checkpoint.