Mechanosensing of stem bending and its interspecific variability in five neotropical rainforest species

Annals of Botany 105: 341 –347, 2010 doi:10.1093/aob/mcp286, available online at www.aob.oxfordjournals.org SHORT COMMUNICATION Mechanosensing of stem bending and its interspecific variability in five neotropical rainforest species Catherine Coutand1,2,*, Malia Chevolot3, André Lacointe1,2, Nick Rowe4,5 and Ivan Scotti3 1 INRA, UMR 547 PIAF, F-63000 Clermont-Ferrand, France, 2Université Blaise Pascal, UMR 547 PIAF, INRA-, F-63000 Clermont-Ferrand, France, 3UMR ECoFoG, BP 709, F-97387 Kourou Cedex, France, 4Université de Montpellier 2, UMR AMAP, F-34000 Montpellier, France and 5CNRS, UMR AMAP, F-34000 Montpellier, France * For correspondence. E-mail † Background and Aims In rain forests, sapling survival is highly dependent on the regulation of trunk slenderness (height/diameter ratio): shade-intolerant species have to grow in height as fast as possible to reach the canopy but also have to withstand mechanical loadings (wind and their own weight) to avoid buckling. Recent studies suggest that mechanosensing is essential to control tree dimensions and stability-related morphogenesis. Differences in species slenderness have been observed among rainforest trees; the present study thus investigates whether species with different slenderness and growth habits exhibit differences in mechanosensitivity. † Methods Recent studies have led to a model of mechanosensing (sum-of-strains model) that predicts a quantitative relationship between the applied sum of longitudinal strains and the plant’s responses in the case of a single bending. Saplings of five different neotropical species (Eperua falcata, E. grandiflora, Tachigali melinonii, Symphonia globulifera and Bauhinia guianensis) were subjected to a regimen of controlled mechanical loading phases (bending) alternating with still phases over a period of 2 months. Mechanical loading was controlled in terms of strains and the five species were subjected to the same range of sum of strains. The application of the sum-of-strain model led to a dose–response curve for each species. Dose–response curves were then compared between tested species. † Key Results The model of mechanosensing (sum-of-strain model) applied in the case of multiple bending as long as the bending frequency was low. A comparison of dose –response curves for each species demonstrated differences in the stimulus threshold, suggesting two groups of responses among the species. Interestingly, the liana species B. guianensis exhibited a higher threshold than other Leguminosae species tested. † Conclusions This study provides a conceptual framework to study variability in plant mechanosensing and demonstrated interspecific variability in mechanosensing. Key words: Mechanosensing, interspecific variability, trees, lianas, rain forest, neotropical species, bending, biomechanics, Bauhinia, Eperua, Symphonia, Tachigali. IN T RO DU C T IO N Interest in mechanical signals is increasing because of their implication in the control of plant morphogenesis (Moulia et al., 2006; Hamant et al., 2008); their effects, which have been described as thigmomorphogenesis since the 1970s (Boyer, 1967; Jaffe, 1973), are also the focus of increasing interest. External mechanical signals generally induce a decrease of elongation and a stimulation of diameter growth. Thigmomorphogenesis has been demonstrated for plants including both herbaceous (for a review see Biddington, 1985) and woody species (Jacobs, 1954; Larson, 1965; Telewski and Pruyn, 1998; Meng et al., 2006; Coutand et al., 2008; reviewed by Telewski, 1995). Although thigmomorphogenetic responses have been attributed to a range of external mechanical stimuli, internal mechanical signals produced by deformations induced by gravity and self-weight lead to responses similar to those of thigmomorphogenesis but have been referred to as gravity resistance (Soga et al., 2006). Telewski (2006) proposed a unified hypothesis of plant mechanosensing including both gravimorphism and thigmomorphogenesis. From an ecological point of view, growth in height is an important functional trait for sapling survival that is linked to light requirements and behaviour. In contrast to shadetolerant species, shade-intolerant species have to reach the canopy as fast as possible to survive, which means that they have to grow in height with a minimum investment of material in diameter growth. However, their survival also depends on their capacity to withstand mechanical loadings due to wind or to their own weight and avoid buckling (Mc Mahon, 1973; Fournier et al., 2006). The control of trunk slenderness (height/diameter ratio) is thus an important, if not essential, factor in the survival of saplings. Biomechanical studies suggest that it is the perception of mechanical signals that is a necessary prerequisite for plants to control their dimensions and their stability-related morphogenesis (Fournier et al., 2006). It is therefore of interest to know how sensitivity of mechanosensing may vary and if it can account for differences in slenderness of different species observed in natural conditions (Jaouen, 2008). Jaffe (1973) found different responses to internode rubbing in a variety of herbaceous species: species such as Hordeum vulgare, Bryonia dioica, Cucumis sativus, # The Author 2009. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: Received: 17 July 2009 Returned for revision: 14 September 2009 Accepted: 28 October 2009 Published electronically: 8 December 2009 342 Coutand et al. — Interspecific variability of mechanosensing D ¼ alnðSumstrains=Sumstrains0 Þ ð1Þ where D is the plant response duration, a the species sensitivity, Sumstrains is the sum of longitudinal applied strains and Sumstrains0 is the stimulus threshold beyond which the level of the sum of strain induces a thigmomorphogenetic response. More recently, the underlying assumptions of the model have been validated by measuring two localized responses of plant stem after a single bending treatment at the loaded zone: the growth in diameter and the level of expression of a primary mechanosensitive gene, PtaZFP2 (Coutand et al., 2009). As it has been validated for different responses and at different scales, the model can thus be used to control the source of variability due to intensity of the mechanical stimulus. The objective of this model is to obtain two parameters, which are independent of stem geometry and mechanical properties and which provide an indication of a species’ intrinsic mechanosensitivity. If a quantitative relationship between the level of applied strains and the plant response could be established for different species and different growth forms, comparisons of dose –response curves could then indicate whether interspecific variability of mechanosensing exists. In addition to quantitative studies based on single bending treatments, other analyses have suggested an accli (...truncated)