Mechano-sensing of mechanical oscillations by plants: frequency sensing and accommodation – Senzo

Plants are submitted to repeated and fluctuating wind loads during their growth. In case of extreme winds, lodging or breaking of forest trees or crop plants occur with major economic and ecological consequences. Moreover, scenarii of global climatic changes forecast clear increases in the frequency of high wind occurrence in Europe, raising questions about the way plants may or not acclimate to these changes. A key biological process for such acclimation involves mechanical strain sensing (during wind-induced bending and torsion) and a syndrome of mechano-controlled growth responses called thigmomorphogenesis. However very little is known about the underlying mechanical and biological mechanisms. In particular, the mechanical and biological consequences of wind-induced vibrations have been disregarded up to now. In vertebrates, mechanosensitive responses to vibration frequency and strain rate have been shown to be central, for example for bone growth. Moreover a slower tuning of mechanosensitivity over successive mechanical stimulations was found to be a key process called accommodation. Many clues suggest that frequency dependence and accommodation may also exist in plants. Nevertheless, at the cellular and molecular level, the responses to vibration of MechanoSensors (MS) have not been well documented, whereas the physiological and molecular bases of accommodation remain elusive. Wind-induced vibrations in plants can broadly be separated into two ranges of frequencies: i) 'high' frequencies from 0.5 to 10 Hz, and very low frequencies related to diurnal and weather-induced wind changes (10-5-10-6 Hz). The high frequencies should have major influence on the mechanical dynamics of the plant and hence on their strains and strain rates. The very low frequencies are likely to be involved in the accommodation process. The Senzo project aims at understanding the sensing by plants of wind 'induced vibrations, and the accommodation process over time, as both are central to the thigmomorphogenetic acclimation of plants to wind. . The ambition of Senzo is to make a shifting-up in plant biomechanics and mechanobiology through broad and intensive interdisciplinary collaboration, joining vibration physicists, plant biomechanicists, cytologists, cellular electrophysiologists, molecular physiologists and molecular biophysicists in a focussed project. The plant mechanical structure clearly applies a mechanical filter/amplifier between external fluctuating loads and the mechanical strain regimes stimulating mechanosensitive tissues. By the same token the cellular structure is likely to mechanically influence cell responses. At the other end of the scale, specific genes and proteins may be involved. Two candidates have been selected from the bibliography and from our previous results: i) mechanosensitive channels (MSLs) recently cloned in plants and which bacterial homologs display relaxation time consistent with the 0.5-10 Hz range, ii) a mechanosensitive transcription factor (ZFP2) which expression seems to change over very low frequencies, thus being probably an entry to the genes-transcription-network involved in the accommodation process. However no phenotype has ever been described in the mutants or transgenic plants obtained for these two candidate-genes families, probably due to the lack of relevant stimulations and measurements. Three tasks have been designed to i) investigate the mechanical and biological features influencing the range of vibration that a plant can sense, ii) analyse the cellular and subcellular responses of MSLs to vibrations, and ii) analyse the genes-network involved in accommodation. All these tasks are interdisciplinary and involve a mix of experiments and modelling. The information gathered through these tasks will then be used in the fourth task in an attempt to reveal and assess the influence of the level of expression of the candidate genes (and proteins) on the quantitative phenotype of mutants and transgenic plants. Two contrasted plant systems will be studied, Arabidopsis and poplar (both being model species for genomics). In the field of plant biomechanics and mechanobiology, all this is relevant and completely novel. Even broadening to mechanobiology in Life Sciences, the systematic analysis of frequency-amplitude response of i) mechanosensors and ii) the genes involved in the accommodation of mechanosensitivity has not been conducted yet. Although fundamental in essence, this research may open avenues for more applied uses of mechanosensitive growth control. For example it may ground i) the design of ideotypes and markers of wind acclimation and hardening for plant breeding or ii) innovating chemical-free controls of plant growth and aspect in greenhouse. The project is also likely to foster a totally novel approach for high-rate plant phenotyping (mass, size'), beyond the field of plant biomechanics.