The TCP4 transcription factor regulates trichome cell differentiation by directly activating GLABROUS INFLORESCENCE STEMS in Arabidopsis thaliana

Abstract

Trichomes are the first cell type to be differentiated during the morphogenesis of leaf epidermis and serve as an ideal model to study cellular differentiation. Many genes involved in the patterning and differentiation of trichome cells have been studied over the past decades, and the majority of these genes encode transcription factors that specifically regulate epidermal cell development. However, the upstream regulators of these genes that link early leaf morphogenesis with cell type differentiation are less studied. The TCP proteins are the plant-specific transcription factors involved in regulating diverse aspects of plant development including lateral organ morphogenesis by modulating cell proliferation and differentiation. Here, we show that the miR319-regulated class II TCP proteins, notably TCP4, suppress trichome branching in Arabidopsis leaves and inflorescence stem by direct transcriptional activation of GLABROUS INFLORESCENCE STEMS (GIS), a known negative regulator of trichome branching. The trichome branch number is increased in plants with reduced TCP activity and decreased in the gain-of-function lines of TCP4. Biochemical analyses show that TCP4 binds to the upstream regulatory region of GIS and activates its expression. Detailed genetic analyses show that GIS and TCP4 work in same pathway and GIS function is required for TCP4-mediated regulation of trichome differentiation. Taken together, these results identify a role for the class II TCP genes in trichome differentiation, thus providing a connection between organ morphogenesis and cellular differentiation.

CIN‐TCP transcription factors: Transiting cell proliferation in plants

“…Trichomes are single‐celled, polyploid, branched structures that arise by differentiation of epidermal cells . The degree of trichome branching was found to be enhanced upon the loss of CIN‐TCP function and reduced with the gain of the CIN‐TCP function . The CIN‐TCP effect on trichome branching was found to be independent of endoreduplication cycles, often correlated with the degree of branching .…”

“…The CIN‐TCP effect on trichome branching was found to be independent of endoreduplication cycles, often correlated with the degree of branching . Instead, TCP4 was found to directly activate the expression of GLABROUS INFLORESCENCE STEMS ( GIS ), a negative regulator of trichome branching known to function in the GA‐signalling pathway . The inhibitory effect of CIN‐TCPs on trichome differentiation is contrary to their general role as differentiation‐inducing factors.…”

“…In addition to the pavement cells that constitute ∼70% of cells in the epidermis, CIN ‐ TCP s also control differentiation of other epidermal cell‐types in Arabidopsis . Trichomes are single‐celled, polyploid, branched structures that arise by differentiation of epidermal cells .…”

“…The inhibitory effect of CIN‐TCPs on trichome differentiation is contrary to their general role as differentiation‐inducing factors. Presence of hyper‐branched and dense trichomes on the surface of developmentally young and immature leaves, as seen in cin‐tcp mutants, may be of adaptive advantage to the plant against biotic stress agents as actively growing cells/tissues are less efficient in mounting strong defense responses as compared to mature tissues . This is attributed to the so‐called growth‐defense trade‐off .…”

Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impact development and defence of Arabidopsis versus maize

“…The latter is also known as the glutamic acid-cysteine-glutamic acid (ECE) clade [29]. PCFs promote cell proliferation, whereas CIN clade TCPs promote leaf and petal cell maturation and differentiation and have antagonistic roles to PCFs [30–33]. The ECE clade includes maize TEOSINTE BRANCHED 1 (TB1) and TB1 homologs of A. thaliana BRANCHED 1 (BRC1) and BRC2, that repress the development of axillary branches in plants [34–37], and CYCLOIDEA (CYC) that control flower symmetry [38].…”