Strain Mechanosensing Quantitatively Controls Diameter Growth and PtaZFP2 Gene Expression in Poplar

Abstract

Mechanical signals are important factors that control plant growth and development. External mechanical loadings lead to a decrease in elongation and a stimulation of diameter growth, a syndrome known as thigmomorphogenesis. A previous study has demonstrated that plants perceive the strains they are subjected to and not forces or stresses. On this basis, an integrative biomechanical model of mechanosensing was established ("sum-of-strains model") and tested on tomato (Solanum lycopersicum) elongation but not for local responses such as diameter growth or gene expression. The first aim of this interdisciplinary work was to provide a quantitative study of the effect of a single transitory bending on poplar (Populus tremula 3 alba) diameter growth and on the expression level of a primary mechanosensitive transcription factor gene, PtaZFP2. The second aim of this work was to assess the sum-of-strains model of mechanosensing on these local responses. An original bending device was built to study stem responses according to a controlled range of strains. A single bending modified plant diameter growth and increased the relative abundance of PtaZFP2 transcripts. Integrals of longitudinal strains induced by bending on the responding tissues were highly correlated to local plant responses. The sum-of-strains model of mechanosensing established for stem elongation was thus applicable for local responses at two scales: diameter growth and gene expression.

Poplar stem transcriptome is massively remodelled in response to single or repeated mechanical stimuli

“…Poplar stem bending caused a complete cessation of cambial growth during the first hours [4]. The coincidence of early growth cessation in bent poplar and transitory overexpression of genes related to plant defence is consistent with the reported antagonism between plant immunity and growth [41].…”

Regulation of shape and patterning in plant development

“…Although it is difficult to disentangle mechanical effects from other environmental stimuli, such a response might involve as much as 2.5% of the Arabidopsis genome [37] and in particular Ca 2+ -dependent proteins, like TOUCH3 (TCH3). In poplar, the expression of the ZFP2 transcription factor occurs in a few minutes following mechanical stimulation, the level of the protein being quantitatively related to the amount of stem bending [38]. Many mechanosensitive ion channels have been identified [39,40], as well as a plasma membrane protein (MCA1) correlating Ca 2+ influx with mechanostimulation [41], which supports the belief that calcium is central to mechanosensing [40].…”

Physical root–soil interactions

“…Though, the stem elongation zone is far away from the bending site, indicating that the response zone can be at a long distance from the perception zone of the mechanical stimuli [163]. Based on controlled bending experiments, Coutand et al [165] showed that the mechanosensing and responses depend on the load, the mechanical structure of the organ and the mechanosensitive structure, that is the location and amount of mechanosensitive tissues involved in the response. They demonstrated that the variable which is perceived is the strain and that the duration of the plant response is correlated to the spatial sum of longitudinal strains in the bent part.…”