The CsUVR8-CsPIF3 module contributes to UV-B-induced cold tolerance through flavonoid accumulation in cucumber

Abstract

Cold stress is a major limiting factor for crop production, and modulation of light quality is an effective strategy to enhance plant stress tolerance. However, the molecular mechanism underlying UV-B radiation regulating cold tolerance remains largely unknown. Here, we found that supplemental UV-B is effective for improving cold tolerance without growth penalty in cucumber seedlings. We further identified CsUVR8 as the cucumber UV-B photoreceptor that converts from dimer in the cytosol into monomer in the nucleus upon UV-B radiation. Knockout of CsUVR8 resulted in impaired UV-B response, decreased cold tolerance, reduced flavonoid accumulation and reactive oxygen species homeostasis. Integrated transcriptomic and metabolomic analyses revealed that flavonoid biosynthesis is a key downstream pathway regulated by CsUVR8 under UV-B radiation. CsUVR8 directly interacts with the bHLH transcription factor CsPIF3, a negative regulator of cold tolerance and flavonoid biosynthesis. UV-B-activated CsUVR8 promotes CsPIF3 protein degradation, thereby relieving its transcriptional repression on flavonoid biosynthetic genes, including CsCHS, CsCHI-L, and CsF3H. Moreover, the promotive effect of UV-B through flavonoid biosynthesis on cold tolerance is conserved in other cucurbit crops, including melon and watermelon. Therefore, our study reveals that the CsUVR8-CsPIF3 module links UV-B signaling to flavonoid metabolism and cold tolerance, providing new insights and a practical strategy for improving stress resilience in horticultural crops.