The TCP4 Transcription Factor Directly Activates TRICHOMELESS1 and 2 and Suppresses Trichome Initiation1[OPEN]

Trichomes are the first line of defense on the outer surface of plants against biotic and abiotic stresses. Because trichomes on leaf surfaces originate from the common epidermal progenitor cells that also give rise to pavement cells and stomata, their density and distribution are under strict genetic control. Regulators of trichome initiation have been identified and incorporated into a biochemical pathway wherein an initiator complex promotes trichome fate in an epidermal progenitor cell, while an inhibitor complex suppresses it in the neighboring cells. However, it is unclear how these regulator proteins, especially the negative regulators, are induced by upstream transcription factors and integrated with leaf morphogenesis. Here, we show that the Arabidopsis (Arabidopsis thaliana) class II TCP proteins activate TRICHOMELESS1 (TCL1) and TCL2, the two established negative regulators of trichome initiation, and reduce trichome density on leaves. Loss-of-function of these TCP proteins increased trichome density whereas TCP4 gain-of-function reduced trichome number. TCP4 binds to the upstream regulatory elements of both TCL1 and TCL2 and directly promotes their transcription. Further, the TCP-induced trichome suppression is independent of the SQUAMOSA PROMOTER BINDING PROTEIN LIKE family of transcription factors, proteins that also reduce trichome density at later stages of plant development. Our work demonstrates that the class II TCP proteins couple leaf morphogenesis with epidermal cell fate determination. The class II TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR group of proteins suppresses trichome initiation on leaf surface.