PHYB and PIF3 repress OLE4 expression to regulate hypocotyl length and ABA signaling in Arabidopsis

OLEOSIN proteins (OLEs) are the predominant class of proteins localized on the surface of oil bodies. Previous studies have established that light facilitates the degradation of oil bodies via the action of PHOTOCHROME A/B (PHYA/B). However, the specific roles of OLEs in light signaling pathways and their underlying regulatory mechanisms remain unclear. In this study, we provide evidence that OLE4 inhibits hypocotyl elongation under red light conditions but has no significant effect in the dark. We demonstrated that red light suppressed both the expression and protein accumulation of OLE4. PHYB reduces OLE4 levels, moreover PHYTOCHROME INTERACTING FACTOR 3 (PIF3) directly represses OLE4 by binding to its G-box motifs; this repression is further strengthened by HDA5 and HDA6. Transcriptomic analysis of the ole4 mutant indicated substantial changes in the expression of genes involved in abscisic acid (ABA) signaling, stress responses, and light stimulus pathways. Correspondingly, ABA levels were markedly elevated in OLE4 overexpression lines (OLE4#1), as well as in phyB-9 and pif3-3 mutants under red light exposure. Applying external ABA restored the hypocotyl growth in ole4 mutants and increased the expression of both OLE4 and PIF3. Additionally, the ole4 mutant exhibited heightened sensitivity to ABA under red light and diminished tolerance to salinity and drought stress conditions. Collectively, these results reveal that OLE4 connects the PHYB-PIF3-HDA5/6 signaling pathway with ABA signaling, thereby controlling hypocotyl elongation regulated by red light.