ELONGATED HYPOCOTYL 5 and miR156d orchestrate axillary meristem maturation and AHL15-mediated plant longevity

Abstract

Plant development in Arabidopsis thaliana transitions through various stages influenced by environmental cues and internal processes. ELONGATED HYPOCOTYL 5 (HY5), a critical light-signaling transcription factor, plays a key role in plant development; however, its function in flowering and vegetative phase change (VPC) remains unclear. Our study reveals that HY5 directly regulates the expression of microRNA156d (miR156d) by binding to G-box-like motifs in the miR156d promoter. This interaction inversely modulates the expression of miR156d and SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes between wild-type and hy5 mutant plants. Notably, the miR156d overexpression (miR156dOX/hy5) plants exhibited delayed flowering, extended vegetative phases, and increased longevity, primarily due to a delay in the maturation of the axillary meristem associated with elevated levels of AT-HOOK MOTIF NUCLEAR LOCALIZED 15 (AHL15), a target of SPL genes. To investigate the role of AHL15, we developed knockdown lines for AHL15 in a miR156dOX background. Interestingly, the AHL15 knockdown combined with miR156dOX in hy5 plants (AHL15CR/miR156dOX/hy5) displayed hypersensitivity, bolting substantially earlier than other genotypes. This finding highlights the regulatory balance between HY5, miR156d, and AHL15. Overall, this interplay is crucial for controlling the transition from the vegetative to reproductive stages and influencing plant lifespan, providing essential insights into the molecular regulation of plant life history.