Phytochrome-interacting factor PIF3 integrates phytochrome B and UVB signaling pathways to regulate gibberellin- and auxin-dependent growth in cucumber hypocotyls.

Abstract

In Arabidopsis, the photoreceptors phytochrome B- (PhyB) and UVB resistance 8- (UVR8) mediated light responses play a major role in regulating photomorphogenic hypocotyl growth, but how they crosstalk to coordinate this process is not well understood. Here we report map-based cloning and functional characterization of a UVB-insensitive, long-hypocotyl mutant, lh1, and a wild-type-like lh2 mutant in cucumber, Cucumis sativus, which encodes a defective CsPhyB and a key gibberellic acid (GA) biosynthesis enzyme CsGA20ox-2, respectively. The lh2 mutation was epistatic to lh1 and partly suppressed long-hypocotyl phenotype in the lhl1lh2 double mutant. We identified phytochrome interacting factor (PIF) CsPIF3 that played a critical role in integrating the red/far-red and UVB light responses for hypocotyl growth. We show that two modules, CsPhyB-CsPIF3-CsGA20ox-2 (GA oxidase2)-DELLA and CsPIF3-CsARF18 (auxin response factor 18) mediate CsPhyB-regulated hypocotyl elongation through GA and auxin pathways, respectively, in which CsPIF3 binds to the G-/E-box motifs in the promoters of CsGA20ox-2 and CsARF18 to regulate their expression. We also identified a new physical interaction between CsPIF3 and CsUVR8 mediating CsPhyB-dependent, UVB-induced hypocotyl growth inhibition. Our work suggests that hypocotyl growth in cucumber involves a complex interplay of multiple photoreceptor- and phytohormone-mediated signaling pathways that show both conservation with and divergence from those in Arabidopsis.