The Transcription Factors TCP4 and PIF3 Antagonistically Regulate Organ-Specific Light Induction of <i>SAUR</i> Genes to Modulate Cotyledon Opening during De-Etiolation in Arabidopsis

Abstract

Light elicits different growth responses in different organs of plants. These 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 members of the TEOSINTE BRANCHED1, CYCLOIDEA, and PCF (TCP) transcription factor family participate in photomorphogenesis and facilitate light-induced cotyledon opening in Arabidopsis (<i>Arabidopsis thaliana</i>). Chromatin immunoprecipitation sequencing and RNA sequencing analyses indicated that TCP4 targets a number of <i>SMALL AUXIN UPREGULATED RNA</i> (<i>SAUR</i>) genes that 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 <i>SAUR16</i> and <i>SAUR50</i> expression in response to light. Light regulates the binding of TCP4 to the promoters of <i>SAUR14, SAUR16,</i> and <i>SAUR50</i> through PHYTOCHROME-INTERACTING FACTORs (PIFs). PIF3, which accumulates in etiolated seedlings and its levels rapidly decline upon light exposure, also binds to the <i>SAUR16</i> and <i>SAUR50</i> promoters, while suppressing the binding of TCP4 to these promoters in the dark. Our study reveals that the interplay between light-responsive factors PIFs and the developmental regulator TCP4 determines the cotyledon-specific light regulation of <i>SAUR16</i> and <i>SAUR50</i>, which contributes to cotyledon closure and opening before and after de-etiolation.