The Transcription Factors TCP4 and PIF3 Antagonistically Regulate Organ-Specific Light Induction of SAUR 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 (Arabidopsis thaliana). Chromatin immunoprecipitation sequencing and RNA sequencing analyses indicated that TCP4 targets a number of SMALL AUXIN UPREGULATED RNA (SAUR) 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 SAUR16 and SAUR50 expression in response to light. Light regulates the binding of TCP4 to the promoters of SAUR14, SAUR16, and SAUR50 through PHYTOCHROME-INTERACTING FACTORs (PIFs). PIF3, which accumulates in etiolated seedlings and its levels rapidly decline upon light exposure, also binds to the SAUR16 and SAUR50 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 SAUR16 and SAUR50, which contributes to cotyledon closure and opening before and after de-etiolation.

Arabidopsis PP6 phosphatases dephosphorylate PIF proteins to repress photomorphogenesis

“…However, we observed that PP6 mutations did not further enhance the cotyledon separation of pifq mutant, probably because PP6 may mediate cotyledon development by factors other than PIFs. SAUR genes, which are auxin-responsive genes, have been shown to be the major factors regulating cotyledon opening (29,30). We found that several SAURs were up-regulated to higher levels in pifq than those in f1 f3 (e.g., SAUR51) or down-regulated in f1 f3 (e.g., SAUR14, SAUR16) (Dataset S1), which could be part of the reason why f1 f3 did not further enhance the cotyledon separation phenotype of pifq mutant.…”

Genome-Wide Identification, Characterization and Expression Analysis of TCP Transcription Factors in Petunia

“…Noteworthily, PaTCP21 and PaTCP23 represent a relatively high level of expression in developing fruits, suggesting they may play roles in fruit development. PaTCP9, PaTCP14b, PaTCP20, PaTCP21 and PaTCP23 are transcribed at the highest levels in cotyledons, suggesting their potential roles in cotyledon development, similar to the TCP4-like genes in Arabidopsis [8,33,60].…”

“…Moreover, the transcripts of most putative miR319-regulated PaTCP genes are detected in most tested tissues, including seedlings, cotyledons, leaves, axillary buds, inflorescences and flower buds, suggesting that these PaTCPs may play diverse regulatory roles at multiple developmental processes in petunia. Recently, the TCP4-like genes were proved to play a positive role in light-induced cotyledon opening via directly targeting and transcriptionally activating several SAUR (SMALL AUXIN UPREGULATED RNA) genes in Arabidopsis [60]. AtTCP4 is predominantly expressed in cotyledons and young leaves [8] and regulates the morphogenesis of these organs [33].…”

Transcriptional regulatory network of the light signaling pathways

“…The TFs TCP4 and PIF3 antagonistically regulate the expression of SAUR16/50 to control cotyledon opening during de-etiolation. The opposite effects of TCP4 and PIF3 might help ensure the specific and proper expression of the target genes (Sun et al, 2016;Dong et al, 2019). To date, TCP4-PIF3-SAUR16/50 is the only known regulatory module that mediates the differential growth; additional players and mechanisms have not yet been examined.…”