Mechanically induced localization of SECONDARY WALL INTERACTING bZIP is associated with thigmomorphogenic and secondary cell wall gene expression

Abstract

Plant 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 signalling pathways and cell wall modification. One aspect of this cascade involves gibberellins and bZIP family transcription factors. Here, we present data connecting thigmomorphogenesis with secondary cell wall synthesis by gibberellin (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 supplement with exogenous bioactive GA, and induced by chemical inhibition of GA synthesis. Misregulation of SWIZ expression resulted in plants hypersensitive to mechanical stimulation, with reduced height and 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 grass specific facet of thigmomorphogenesis. SWIZ 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.

The wild grass Brachypodium distachyon as a developmental model system

“…Importantly, most of the work we will describe would not have been possible without the resources described above. There are a number of additional developmental processes being studied in B. distachyon; important contributions include for example, cell wall biology (see Coomey et al, 2020) and references therein), vascular development (Sakai et al, 2021;Smertenko et al, 2019), pleiotropic genes like the NOOT-BOP-COCH-LIKE genes (Magne et al, 2020), seed germination (Wolny et al, 2018), species-specific aspects of abscission zone formation (Yu et al, 2020), and even thigmomorphogenesis-the developmental response to touch (Coomey et al, 2021). We apologize for not being able to cover all the developmental work done with B. distachyon due to space limitations.…”

Anatomical Characteristics and Variation Mechanisms on the Thick-Walled and Dwarfed Culm of Shidu Bamboo (Phyllostachys nidularia f. farcta)

“…The changes in cell wall structure and components were another important factor affecting cell elongation (Scheible and Pauly, 2004 ; Coomey et al, 2021 ; Li et al, 2021 ; Wang et al, 2021 ). In Shidu bamboo, corresponding signs, such as the thinning of its fiber cell wall and the decrease in lignin, cellulose, and hemicellulose content in the culm wall compared with the prototype plant ( Table 1 ; Figures 5B–D ), indicate that its cell wall exhibits abnormal development.…”

Shoring up the base: the development and regulation of cortical sclerenchyma in grass nodal roots

“…Maize inbred B73 and wheat cultivar Kronos were grown as described above. The mechanical stimulus apparatus used to make contact every 90 min, is previously described (Coomey et al, 2023). In the B. distachyon mechanical stimulus experiment, plants were grown for 2 weeks prior to treatment onset.…”

“…Gibberellic acid (GA) phytohormone signaling is implicated in both secondary wall regulation and plant mechanoperception (Jiang et al, 2008;Wang et al, 2017;Singh et al, 2019;Coomey et al, 2023;Wu et al, 2023). To test whether GA is a component of the perception or transduction pathways that modulate cortical sclerenchyma thickening, we treated hydroponically grown plants with GA3, or the GA biosynthesis inhibitor, paclobutrazol.…”

“…Using a de novo k-mer approach to motif discovery, we next identified sequence motifs enriched in the cis-regulatory regions of genes in each cluster (Supplementary Table 5). Cluster 1, which contains the most distinct touch responsive expression pattern, showed significant enrichment for the Rapid Stress Response Element , P-box, G/A-box, AC element, and FAR1 binding sites, all of which have been implicated in transcriptional responses to mechanical forces (Walley et al, 2007;Van Moerkercke et al, 2019;Coomey et al, 2023). In Cluster 2, we also identified several distinct touch responsive elements including P-box, G-box, and site II elements which have been reported as a response to mechanical stimulus as well as several other motifs not associated with wall thickening.…”