Vital contribution of brassinosteroids to hypoxia-stimulated coleoptile elongation in submerged rice

Abstract

The rapid elongation of rice (Oryza sativa) coleoptile is pivotal for the plant plumule to evade hypoxia stress induced by submergence, a condition often arising from overirrigation, ponding, rainstorms, or flooding. While brassinosteroids (BRs) are recognized for their diverse roles in plant growth and development, their influence on coleoptile elongation under hypoxic conditions remains largely unexplored. In this study, we demonstrate the significant requirement of BRs for coleoptile elongation in deep water. During coleoptile development, Glycogen Synthase Kinase3-Like Kinase2 (GSK2), the central inhibitor of BR signaling in rice, undergoes substantial suppression in deep water but induction in air. In contrast, the dephosphorylated form of BRASSINAZOLE RESISTANT1 (OsBZR1), representing the active form of the key BR signaling transcription factor, is induced in water but suppressed in air. Remarkably, the knockout of GSK3-like kinase genes significantly enhances coleoptile elongation in deep water, strongly indicating a vital contribution of BR response to hypoxia-stimulated coleoptile elongation. Transcriptome analysis uncovers both BR-associated and BR-independent hypoxia responses, implicating substance metabolism, redox reactions, abiotic stress responses, and crosstalk with other hormones in the regulation of BR-induced hypoxia responses. In summary, our findings suggest that rice plumules rapidly elongate coleoptiles through the activation of BR response in deep water, enabling them to escape from submergence-induced hypoxia stress.