TCP4 and PIF3 antagonistically regulate organ-specific light induction of SAUR16/50 to modulate cotyledon opening during de-etiolation in Arabidopsis

Light elicits different growth responses in different organs, and those organ-specific responses are prominently displayed during de-etiolation. While major light responsive components and early signaling pathways in this process have been identified, this information has yet to explain how organ-specific light responses are achieved. Here we report that the developmental regulator TCP (TEOSINTE BRANCHED1, CYCLOIDEA, and PCF) family of transcription factors participate in photomorphogenesis and facilitate light-induced cotyledon-opening. ChIP-seq and RNA-seq analyses indicate that TCP4 targets a number of SAUR (Small Auxin Up RNA) genes, which have previously been shown to exhibit organ-specific light responsive expression. We demonstrate that TCP4-like transcription factors, which are predominantly expressed in the cotyledons of both light and dark grown seedlings, activate SAUR16 and SAUR50 in response to light. Light regulates the binding of TCP4 to the promoters of SAUR14/16/50 through PIFs (PHYTOCHROME-INTERACTING FACTORs). We show that PIF3, which accumulates in etiolated seedlings and whose levels rapidly decline upon light exposure, also binds to the SAUR16/50 promoter while suppressing TCP4 promoter-binding in darkness. Our study reveals that the interplay between light responsive factors PIFs and the developmental regulator TCP4 determines the cotyledon-specific light regulation of SAUR16/50, which contributes to cotyledon closure and opening before and after de-etiolation.