Thigmomorphogenesis: a complex plant response to mechano-stimulation

Journal of Experimental Botany, Vol. 60, No. 1, pp. 43–56, 2009 doi:10.1093/jxb/ern315 Advance Access publication 16 December, 2008 DARWIN REVIEW Thigmomorphogenesis: a complex plant response to mechano-stimulation E. Wassim Chehab, Elizabeth Eich and Janet Braam* Rice University, Biochemistry and Cell Biology, 6100 Main St. Houston, TX 77005, USA Received 2 September 2008; Revised 14 November 2008; Accepted 17 November 2008 Abstract Key words: ABA, auxin, brassinosteroids, calcium, ethylene, jasmonates, nitric oxide, ROS, thigmomorphogenesis, touch. Introduction When animals encounter adverse or life-threatening circumstances, they often react by relocating to a more favourable environment. Plants do not have this luxury of high mobility. They are non-motile organisms that are persistently challenged by a wide spectrum of environmental stresses. These stimuli can be extremely detrimental to plants if they had not evolved mechanisms to sense and respond to their dynamic surroundings (Liscum, 2002). Examples of challenges related to mechanical force include wind, physical barriers, and predation. Initially, plants have to sense these stimuli and subsequently launch appropriate responses by either avoiding obstacles, clinging to supporting structures, or producing toxic chemicals to fend off herbivorous predators. In 1881, Charles Darwin reported on mechanostimulus-induced plant behaviour. In The power of movement in plants, Darwin described in detail directed plant growth in response to external stimuli (Darwin and Darwin, 1881), including how roots of many plant species reorient their growth direction upon making contact with barriers. Such observations were fascinating to Darwin and continue to be an active and intriguing area of research. Mechanical perturbations are among the many environmental stimuli to which plants respond. Plants sense forces ranging from very intense and physically damaging to more subtle, moderate ones. Many studies have focused on plant responses to wounding, a tissue-damaging mechanical perturbation often used to simulate insect and microbe attacks. Plants sense and respond to mechanical stimuli immediately, as well as over time, by synthesizing an array of phytohormones and other chemicals in addition to expressing defencerelated genes that decrease herbivore ability to colonize, feed, and/or reproduce (Green and Ryan, 1972; Karban and Baldwin, 1997; Chen et al., 2005; Chehab et al., 2006, 2008). Similar responses occur in plants stimulated by more subtle mechanical cues including touch. In addition to the production of the phytohormones and expression induction of * To whom correspondence should be addressed: E-mail: ª The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: In nature, plants are challenged with hurricane winds, monsoon rains, and herbivory attacks, in addition to many other harsh mechanical perturbations that can threaten plant survival. As a result, over many years of evolution, plants have developed very sensitive mechanisms through which they can perceive and respond to even subtle stimuli, like touch. Some plants respond behaviourally to the touch stimulus within seconds, while others show morphogenetic alterations over long periods of time, ranging from days to weeks. Various signalling molecules and phytohormones, including intracellular calcium, jasmonates, ethylene, abscisic acid, auxin, brassinosteroids, nitric oxide, and reactive oxygen species, have been implicated in touch responses. Many genes are induced following touch. These genes encode proteins involved in various cellular processes including calcium sensing, cell wall modifications, and defence. Twenty-three per cent of these up-regulated genes contain a recently identified promoter element involved in the rapid induction in transcript levels following mechanical perturbations. The employment of various genetic, biochemical, and molecular tools may enable elucidation of the mechanisms through which plants perceive mechano-stimuli and transduce the signals intracellularly to induce appropriate responses. 44 | Chehab et al. defence-related genes, touched plants also respond physically to the stimulus, but with varying degrees depending on the plant species examined. Some responses are very rapid and highly noticeable due to the presence of specialized cells which constitute part of the plant touch response machinery (Braam, 2005). For example, touching Mimosa pudica will cause leaf folding within 1 s (Fig. 1) and disturbing the trigger hairs on a Venus’ Fly Trap leaf will cause the trap to close within the same time frame. Thigmomorphogenesis Cellular signalling Plant thigmomorphogenetic responses to mechanical stimulations have been reported to be saturable (Beryl and Mitchell, 1977), dose-dependent (Jaffe, 1976), and systemic, i.e. the stimulus and its subsequent response translocate from plant regions directly stressed to non-disturbed distal regions (Erner et al., 1980). Furthermore, perturbed plant symptoms of altered morphology and growth rate can be mimicked or antagonized by applications of specific chemical compounds (Erner and Jaffe, 1982; Boyer et al., 1983; Biro and Jaffe, 1984). Altogether, these data suggest that plant responses to mechanical perturbations are mediated by signalling molecules. Hormones, secondary messengers, nitric oxide (NO), reactive oxygen species (ROS), as well as lipid-derived metabolites have been implicated as potential signalling factors. These factors and the potential implications in plant responses to mechanical perturbations are discussed here. Calcium Calcium (Ca2+) is a universal signal transduction molecule. Its signalling capabilities are implicated in plant responses Fig. 1. Mimosa pudica (sensitive plant). (A) Opened leaves before stimulation. (B) Folded up leaves after touching. Plants without specialized sensory cells also respond to mechanical perturbations. However, they react slowly over time by altering their morphology as well as their growth rate. Salisbury (1963) reported that repeatedly touching the leaves of young cocklebur plants caused a 30% inhibition in growth in addition to an increase in the rate of leaf senescence. Mark Jaffe was the first to introduce the term ‘thigmomorphogenesis’ to describe these mechanically-induced responses (thigma is the Greek word for touch) (Jaffe, 1973). Thigmomorphogenesis in higher plants is generally a slow response occurring over time and, unlike the responses of Mimosa or the Venus Fly Trap, touch-induced morphological changes are not readily apparent immediately after the stimulus (Jaffe, 1973). Among many plant species, a common thigmomorphogenetic response includes a decrease in shoot elongation coupled to an increase in radial expansion (Telewski and Jaffe, 1986; Braam and Davis, 1990; Braam, 2005). An example of thigmomorphogen (...truncated)