Touch-triggered bZIP translocation regulates elongation and secondary wall biosynthesis

Abstract

AbstractPlant growth is mediated by the integration of internal and external cues, perceived by cells and transduced into a developmental program that gives rise to cell division, elongation, and wall thickening. Extra-, inter-, and intra- physical cellular forces contribute to this regulation. Across the plant kingdom thigmomorphogenesis is widely observed to alter plant morphology by reducing stem height and increasing stem diameter. The transcriptome is highly responsive to touch, including components of calcium signaling pathways and cell wall modification. One aspect of this cascade involves gibberellins (GA) and bZIP family transcription factors. Here, we present data connecting thigmomorphogenesis with secondary cell wall synthesis by GA inactivation and bZIP translocation into the nucleus. Brachypodium distachyon SECONDARY WALL INTERACTING bZIP (SWIZ) protein translocated into the nucleus in response to mechanical stimulation. This translocation was mitigated by supplementing with exogenous bioactive GA, and induced by chemical inhibition of GA synthesis. Misregulation of SWIZ expression resulted in plants with reduced stem and root elongation, and following mechanical stimulation, increased secondary wall thickness. Classical touch responsive genes were upregulated in B. distachyon following touch, and we observe significant induction of the glycoside hydrolase 17 family, which may be indicative of a facet of grass thigmomorphogenesis. SWIZ protein binding to an E-box variant in exons and introns was associated with immediate activation followed by repression of gene expression. Thus, SWIZ is a transcriptional regulatory component of thigmomorphogenesis, which includes the thickening of secondary cell walls.