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

Authors: ZHAO, JIANYU - University Of Wisconsin; BO, KAILIANG - University Of Wisconsin; PAN, YUPENG - University Of Wisconsin; LI, YUHONG - Northwest A&f University; YU, DAOLIANG - Chinese Academy Of Agricultural Sciences; LI, CHUANG - China Agriculture University; CHANG, JIANG - Fujian Agricultural & Forestry University; WU, SHUANG - Fujian Agricultural & Forestry University; WANG, ZHONGYI - China Agriculture University; ZHANG, XIOALAN - China Agriculture University; GU, XINGFANG - Chinese Academy Of Agricultural Sciences; Weng, Yiqun

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/18/2022
Publication Date: 11/25/2022
Citation: Zhao, J., Bo, K., Pan, Y., Li, Y., Yu, D., Li, C., Chang, J., Wu, S., Wang, Z., Zhang, X., Gu, X., Weng, Y. 2022. Phytochrome-interacting factor PIF3 integrates phytochrome B and UVB signaling pathways to regulate gibberellin- and auxin-dependent growth in cucumber hypocotyls. Journal of Experimental Botany. 74(15):4520-4539. https://doi.org/10.1093/plcell/koac335.
DOI: https://doi.org/10.1093/plcell/koac335

Interpretive Summary: Background: After a seedling emerges from the dark in the soil, it goes through a complex process called photomorphogenesis to adapt to the light environment. The molecular mechanisms of light responses to the solar irradiation, especially the red and UV-B lights have been studied extensively in the model plant Arabidopsis, but knowledge gap still exists, not to mention the fact that little is known about these events in crop plants like cucumber. Findings: In this manuscript, we reported cloning and functional characterization of two cucumber hypocotyl mutants, long hypocoty1 (lh1) and lh2). Hypocotyl growth of both mutants are insensitive to red, low dosage UV-B light and dark conditions. The two genes encode the red light photoreceptor Phytochrome B (PhyB), and a key gibberellic acid (GA) biosynthesis enzyme CsGA20ox-2, respectively. We identified several important players in CsPhyB and CsUVR8-mediated light responses. They include the phytochrome interacting factor (PIF) CsPIF4 that physically interacts with both CsPhyB and CsUVR8 (UV-B photoreceptor) to link the red/far-red and UV-B light responses for hypocotyl growth. We identified two working modules, CsPhyB-CsPIF1b and CsPIF3-CsARF18 which mediate CsPhyB-regulated hypocotyl elongation through the phytohomone GA and auxin biosynthesis/signaling pathways. The UV-B induced hypocotyl growth inhibition is controlled by the interaction between CsPIF4 and CsUVR8 whereas UV-B protection/acclimation is controlled by a different model. We also identified a complex regulatory network in control of hypocotyl growth in cucumber. Significance This is the first comprehensive study on molecular mechanisms of hypocotyl growth in responses to red/far-red light and UV-B irradiation during photomorphogenesis in non-model crop plants. This work provides new insights in our understanding of molecular control of hypocotyl growth in a crop plant.

Technical Abstract: In Arabidopsis, the photoreceptors phytochrome B (PhyB)- and 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 two UVB-insensitive, long-hypocotyl mutants, lh1 and lh2 in cucumber that encode CsPhyB, and a key gibberellic acid (GA) biosynthesis enzyme CsGA20ox-2, respectively. We show that the phytochrome interacting factor (PIF) CsPIF4 physically interacts with both CsPhyB and CsUVR8 connecting the red/far-red and UV-B light responses for hypocotyl growth. Two modules, CsPhyB-CsPIF1b and CsPIF3-CsARF18, mediate CsPhyB-regulated hypocotyl elongation through GA and auxin biosynthesis/signaling pathways. CsUVR8-CsPIF4 interaction mediates UV-B induced hypocotyl growth inhibition, which is independent of the CsUVR8-CsCOP1-CsHY5 signaling for UV-B protection/acclimation. Hypocotyl growth in cucumber involves complex interplay of multiple photoreceptor- and phytohormone-mediated signaling pathways that show both conservation with and divergence from those in Arabidopsis.