ClPIF3-ClHY5 Module Regulates ClPSY1 to Promote Watermelon Fruit Lycopene Accumulation Earlier under Supplementary Red Lighting

Lycopene content is one of the important factors for determining watermelon fruit quality. In this study, a small-type watermelon was grown in a greenhouse with supplementary red lighting for 10 h per day. The results showed that the content of lycopene in the flesh was increased 6.3-fold after 25 days of supplementary red lighting. qRT-PCR analysis showed that PHYTOENE SYNTHASE 1(ClPSY1) is the major gene that responds to red light within the lycopene synthesis pathway. Moreover, we identified two key transcription factors that were involved in light signal transduction PHYTOCHROME INTERACTING FACTORS 3 (ClPIF3) and LONG HYPOCOTYL 5 (ClHY5) in watermelon flesh. The interaction experiments showed that ClHY5, a potent ClPIF3 antagonist, regulated ClPSY1 expression by directly targeting a common promoter cis-element (G-box). Collectively, our findings identified that ClHY5 and ClPIF3 formed an activation-suppression transcriptional module that is responsive to red light and, through this model, regulated watermelon lycopene accumulation in greenhouse winter cultivation.