A Unified Hypothesis of Mechanoperception in Plants1

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A Unified Hypothesis of Mechanoperception in Plants1 American Journal of Botany 93(10): 1466–1476. 2006. A UNIFIED HYPOTHESIS OF MECHANOPERCEPTION IN PLANTS1 FRANK W. TELEWSKI2 W. J. Beal Botanical Garden, Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824 USA The perception of mechanical stimuli in the environment is crucial to the survival of all living organisms. Recent advances have led to the proposal of a plant-specific mechanosensory network within plant cells that is similar to the previously described network in animal systems. This sensory network is the basis for a unifying hypothesis, which may account for the perception of numerous mechanical signals including gravitropic, thigmomorphic, thigmotropic, self-loading, growth strains, turgor pressure, xylem pressure potential, and sound. The current state of our knowledge of a mechanosensory network in plants is reviewed, and two mechanoreceptor models are considered: a plasmodesmata-based cytoskeleton–plasma membrane–cell wall (CPMCW) network vs. stretch-activated ion channels. Post-mechanosensory physiological responses to mechanical stresses are also re- viewed, and future research directions in the area of mechanoperception and response are recommended. Key words: gravitropism; gravity; mechanoperception; sound; thigmomorphogenesis; thigmotropism; turgor pressure; wind. The ability to sense and respond to physical stimuli is of key gravitational field is proposed to induce internal pressure importance to all living things. Among the common differences at the CPMCW interface, which can be considered environmental stimuli detected by living organisms are light, an external mechanical signal (Staves et al., 1997; MacCleery temperature, and a variety of chemical signals. A number of and Kiss, 1999; Balusˇka et al., 2005). Therefore, a more these stimuli appear to be closely related and can be considered broadly unifying mechanism may underlie graviperception in as physical–mechanical stimuli, that is differences in a plants than that evoked by a hypothesis that relies on how the mechanical force or pressure perceived by the living cell. A mechanical signal is initiated; an actual sensory structure cell may perceive gravity; strains caused by self-loading and within the cell may allow for mechanoperception as the plant is internal growth; mechanical loading by snow, ice, and fruit, reoriented with respect to gravity. Supporting the concept of a wind, rainfall, touch, sound; and the state of hydration within a unified hypothesis for mechanical sensing in the gravitropic cell (turgor pressure). All organisms appear to perceive these response is the work of Massa and Gilroy (2003) who reported mechanical signals, regardless of their taxonomic classification when a root cap came in contact with a horizontal glass plate or life habit (sessile vs. motile). The significant differences (inducing thigmotropic stimulus), the root cells behind the between taxonomic groups, specifically plants and animals, are growing tip began to grow horizontally. This allowed the root found in the individual molecular components of the cap to maintain contact with the plate, while the rest of the root microstructure of the internal cellular sensing network (Jaffe grew over and parallel to the obstacle with a step-like growth et al., 2002; Balusˇka et al., 2003) and in the response of an form. The authors suggested that the gravisensitive cells of the individual organism to each mechanical stimulus. root cap also sense the touch and signal the columella cells to alter their gravitropic response, so that they act together to Internal mechanical forces—The sensing of gravitropic redirect root growth to avoid obstacles while continuing a signals by plants has been studied for 200 years (Knight, 1806). general downward pattern of growth. Since the first study, the elucidation of the mechanism of In plants, gravitropism can occur in either primary or gravitropic perception has been researched in a broad array of secondary tissues. In primary growth, the gravitropic curvature plants from algae to trees and in a variety of plant organs. To results from differential cell elongation on opposite sides of the date, two compelling hypotheses exist regarding gravipercep- displaced organ. In the case of secondary growth, the tion in plants: the starch–statolith hypothesis and the gravitropic response includes the formation of reaction wood; hydrostatic model of gravisensing (for reviews, see Sack, tension wood in porous angiosperms and compression wood in 1991, 1997; Balusˇka and Hasenstein, 1997; Staves et al., 1997; nonporous angiosperms and gymnosperms (Timell, 1986a). MacCleery and Kiss, 1999; Boonsirichai et al., 2002; Drøbak et Tension wood forms on the upper side of a displaced stem and al., 2004). Both hypotheses ultimately rely on the sensing of a is characterized by the formation of gelatinous fibers with mechanical signal at the cytoskeleton–plasma membrane–cell lower lignin content, smaller diameter, and fewer vessels and wall interface (CPMCW) interface. In the case of statoliths, by a realignment of cellulose microfibrils into a vertical falling starch grains or other organelles impact the plasma orientation within the gelatinous layer, which forms inside a membrane thus inducing an internal mechanical signal (Sack, partially developed and lignified S2 layer of secondary cell 1991, 1997; Balusˇka and Hasenstein, 1997; Perbal et al., 2004). walls of gelatinous fibers. Compression wood forms in Similarly, the reorientation of a plant organ within a response to gravity on the lower side of displaced stems and is characterized by tracheids with a thickened secondary cell wall with higher lignin content, a round cross section, 1 Manuscript received 31 March 2006; revision accepted 16 August 2006. The author thanks J. S. Kilgore, L. Koehler, and two anonymous intracellular spaces at cell corners, and a realignment of reviewers for critically evaluating this manuscript. The research was cellulose microfibrils in the S2 layer to a 458 to 608 orientation supported by the National Research Initiative of the USDA Cooperative with respect to the axis of the stem. State Research, Education and Extension Service, grant nos. 2002-35103- The formation of reaction wood in stems, branches, and 11701 and 2005-35103-15269. roots is not an exclusive response to gravity in woody plants. 2 E-mail: [email protected] The formation of reaction wood has also been observed to 1466 October 2006] TELEWSKI—MECHANOPERCEPTION IN PLANTS 1467 develop in branches and stems as a means of reshaping crowns further supported by a study on wood formation in Arabidopsis and as a possible phototropic response (Engler, 1924). Tension in which the application of weight, and thus a compressive wood has been reported to form in the vertical stems of rapidly force on the stem, induced secondary growth in a species that growing poplar (Populus) trees (for a review, see Telewski et only produces herbaceous growth under ‘‘normal’’ environ- al., 1996). Timell (1986c) suggested that the reaction wood mental conditions (Ko et al., 2004). Ko et al. suggested that the may form to keep woody plants in balance with their physical mechanical stimulus of self-weight is perceived by the stem environment (e.g., gravity, wind, and light), subsequently and induces the differentiation of a secondary vascular generating internal growth strains that result in the physical cambium and subsequent formation of secondary xylem and reorientation of woody plant organs. that self-weight may play a more important role in the The maturation of xylem cells in the cambial zone involves development of the woody plant growth habit. the alteration of individual cell lengths. In many instances, there The self-loading induced by the bearing of fruit has been is intrusive growth in which the cells elongate within the shown to influence growth in branches (Alme´ras et al., 2004; relatively rigid structure of the stem, inducing internal Vaast et al., 2005). The forces associated with the bearing of compressive forces (Boyd, 1985; Archer, 1987; Fournier et fruit are primarily perceived in branches and at branch bases al., 1991a, b; Larson, 1994). In other cases, the cells shrink upon and consist of an alternate compressive force on the lower side maturation inducing a tensile force within the stem. The of the branch and a tensile force on the upper side of the branch generation of these internal growth strains is responsible for the so that the branch acts like a cantilever (Wainwright et al., realignment of stems in the gravitropic response, with 1976; Niklas, 1992). The additional load will stimulate compression wood developing a compressive growth strain increased reaction wood formation in the branches. and tension wood forming a tensile growth strain (Wilson, Each living cell within a plant, with its organelles and 1981; Alme´ras et al., 2005). Growth strains also develop in protoplasm, functions mechanically like a water-filled balloon stems aligned vertically with respect to gravity and may (hydrostat), exerting a circumferential tensile force and radial function to maintain mechanical balance within woody plants as compressive force within the plasma membrane and pressing part of a phototropic response, self-loading, or from differential against the surrounding cell wall. The plasma membrane loading caused by crown asymmetry (Archer, 1987). controls turgor by regulating the flow of water and solutes Within a vertically aligned stem, there are two potential between the apoplast and
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