Mechanical stress acclimation in plants: Linking hormones and somatic memory to thigmomorphogenesis. (18th January 2022)

• Record Type: Journal Article
• Authors: Brenya, Eric; Pervin, Mahfuza; Chen, Zhong‐Hua; Tissue, David T.; Johnson, Scott; Braam, Janet; Cazzonelli, Christopher I.
• Is Part Of: Plant, cell and environment. Volume 45:Number 4(2022)
• Page Start: 989
• Page End: 1010
• Publication Date: 2022-01-18
• Subjects: defence -- epigenetic -- inheritance -- intergeneration -- mechanoreceptors -- phytohormones -- stress priming -- touch; Plant physiology -- Periodicals; Plant cells and tissues -- Periodicals; Plant communities -- Periodicals; 581.105
• DOI: 10.1111/pce.14252
• Languages: English
• ISSNs: 0140-7791

Abstract

Abstract: A single event of mechanical stimulation is perceived by mechanoreceptors that transduce rapid transient signalling to regulate gene expression. Prolonged mechanical stress for days to weeks culminates in cellular changes that strengthen the plant architecture leading to thigmomorphogenesis. The convergence of multiple signalling pathways regulates mechanically induced tolerance to numerous biotic and abiotic stresses. Emerging evidence showed prolonged mechanical stimulation can modify the baseline level of gene expression in naive tissues, heighten gene expression, and prime disease resistance upon a subsequent pathogen encounter. The phenotypes of thigmomorphogenesis can persist throughout growth without continued stimulation, revealing somatic‐stress memory. Epigenetic processes regulate TOUCH gene expression and could program transcriptional memory in differentiating cells to program thigmomorphogenesis. We discuss the early perception, gene regulatory and phytohormone pathways that facilitate thigmomorphogenesis and mechanical stress acclimation in Arabidopsis and other plant species. We provide insights regarding: (1) the regulatory mechanisms induced by single or prolonged events of mechanical stress, (2) how mechanical stress confers transcriptional memory to induce cross‐acclimation to future stress, and (3) why thigmomorphogenesis might resemble an epigenetic phenomenon. Deeper knowledge of how prolonged mechanical stimulation programs somatic memory and primes defence acclimation could transform solutions to improve agricultural sustainability in stressful environments. Summary Statement: This review describes how the mechanical stimulation of sensory, physiological, phytohormone, molecular and epigenetic processes in plants; (1) regulate transient and/or prolonged transcriptional changes, (2) prime cross‐acclimation to multiple stresses, (3) program somatic‐stress memory, and (4) facilitate thigmomorphogenesis.