TCP3-mediated regulation of cell expansion in Arabidopsis thaliana

Cell expansion is crucial for organ morphogenesis in multicellular organisms. Apoplast acidification triggers plant cell expansion. Plant hormones and transcription factors such as TEOSINTE BRANCHED, CYCLOIDEA, and PROLIFERATING CELL NUCLEAR ANTIGEN BINDING FACTORs (TCPs) control cell expansion. However, details regarding the regulatory mechanism of cell expansion for organ morphogenesis remain unclear. In this study, we used molecular, biochemical, cellular, genetic, atomic force microscopy, and tensile testing analyses and showed that miR319-targeted TCPs integrated cell expansion with organ morphogenesis in Arabidopsis thaliana. We found that TCPs directly induce the expression of genes encoding cell wall loosening proteins and SMALL AUXIN UP RNAs (SAURs), activators of plasma membrane-localized H+-ATPases. TCP-mediated activation of plasma membrane-localized H+-ATPases stimulates apoplast acidification, reduce cell stiffness, promote cell expansion, and thus exaggerate elongation of the hypocotyl. Ectopic expression of a SAUR gene in sextuple tcp mutant plants substantially recovered the hypocotyl morphology of the tcp mutant, providing genetic evidence of TCP-mediated SAUR regulation. Collectively, our data show that TCPs regulate apoplast acidification for cell expansion.