Abstract
Key message
The level of stresses of tension wood changes during the gravitropic movement. These changes are induced by the perception of strains experienced by the tree during reorientation to the upright position.
Abstract
In most hardwood species, tension wood is produced to ensure tropic movements in radially growing organs. Tension wood exhibits internal tensional forces (autostresses) greater than those of normal wood, which enable the trunk to restore its verticality. During the gravitropic response, there is a first phase when the trunk curves upwards and a second phase when the trunk decurves to reach a final vertical and straight shape. Tension wood appears to be of varying strength, but the source of these variations remains partly undefined. We set out to assess the involvement of mechanosensing in the regulation of the strength of tension wood. Autostress levels characterise the strength of tension wood and can be indirectly estimated by measuring the associated residual longitudinal maturation strains (rlms) after the autostresses release. The higher the tension, the higher the measured associated shrinkage. To look for the involvement of mechanosensing in the regulation of tension wood strength, rlms were measured in different types of experiments in which the trunk mechanical state was modified. Results showed that (1) bigger trees exhibited higher levels of rlms, (2) there was a quantitative relationship between the rlms and the sum of strains experienced by the trunk, (3) artificial curving induced an increase in rlms and (4) in tilted staked trees, rlms increased towards negative values for 3 weeks and then remained constant. These findings are consistent evidence for the regulation of rlms values by mechanosensing. This brings new insight into gravitropism.
Similar content being viewed by others
References
Bastien R, Bohr T, Moulia B (2012) Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants. PNAS 110:755–760
Clair B, Alméras T, Sugiyama J (2006) Compression stress in opposite wood of angiosperms: observations in chestnut, mani and poplar. Ann For Sci 63:507–510
Cosgrove DJ (1997) Cellular mechanism underlying growth asymmetry during stem gravitropism. Planta 203:130–135
Coutand C (2010) Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci 179:168–182
Coutand C, Moulia B (2000) Biomechanical study of the effect of a controlled bending on tomato stem elongation, II Local strain sensing and spatial integration of the signal. J Exp Bot 51:1825–1842
Coutand C, Jeronimidis G, Chanson B, Loup C (2004) Comparison of mechanical properties of tension and opposite wood in Populus. Wood Sci Tech 38:11–24
Coutand C, Fournier M, Moulia B (2007) The gravitropic response of poplar trunks, key role of prestressed wood regulation and the relative kinetics of cambial growth versus wood maturation. Plant Physiol 144:1166–1180
Coutand C, Martin L, Leblanc-Fournier N, Decourteix M, Julien J-L, Moulia B (2009) Strain mechanosensing quantitatively controls diameter growth and PtaZFP2 gene expression in poplar. Plant Physiol 151:223–232
Coutand C, Chevolot M, Lacointe A, Rowe N, Scotti I (2010) Mechanosensing of stem bending and its interspecific variability in five neotropical rainforest species. Ann Bot 105:341–347
Digby J, Firn R (1995) The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell E 18:1434–1440
Firn R, Digby J (1980) The establishment of tropic curvature in plants. Ann Rev Plant Physiol 31:131–148
Fournier M, Baillères H, Chanson B (1994) Tree biomechanics: growth, cumulative prestresses, and reorientations. Biomimetics 2:229–251
Gril J, Thibaut B (1994) Tree mechanics and wood mechanics, relating hygrothermal recovery of green wood to the maturation process. Ann For Sci 51:329–338
Hamant O, Heisler MG, Jonsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in arabidopsis. Science 322:1650–1655
Jaffe MJ (1973) Thigmomorphogenesis, the response of plant growth and development to mechanical stimulation with reference to Bryonia dioica. Planta 114:143–157
Jourez B, Avella-Shaw T (2003) Effet de la durée d’un stimulus gravitationnel sur la formation de bois de tension et de bois opposé dans de jeunes pousses de peuplier (Populus euramericana cv ‘Ghoy’). Ann For Sci 60:31–41
Jullien D, Gril J (2008) Growth strain assessment at the periphery of small-diameter trees using the two-grooves method: influence of operating parameters estimated by numerical simulations. Wood Sci Technol 42:551–565
Jullien D, Alméras T, Kojima M, Yamamoto H, Cabrolier P (2009) Evaluation of growth stress profiles in tree trunks: comparison of experimental results to a biomechanical model. In: Thibaut B (ed) Proceedings of the sixth Plant Biomechanics Conference, Cayenne, pp 75–82
Moulia B, Fournier M (2009) The power and control of gravitropic movements in plants: a biomechanical and systems biology view. J Exp Bot 6:461–486
Moulia B, Coutand C, Lenne C (2006) Posture control and skeletal mechanical acclimation in terrestrial plants: implications for mechanical modeling of plant architecture. Am J Bot 93:1477–1489
Moulia B, Der Loughian C, Bastien R et al (2010) Integrative mechanobiology of growth and architectural development in changing mechanical environments. In: Wojtaszek P (ed) Mechanical integration of plant cells and plants. Springer, Heidelberg, Dordrecht, London,New-York, pp 269–302
Okuyama T, Sasaki Y, Kikata Y, Kawai N (1981) The seasonal change in growth stress in the tree trunk. Mokuzai Gakkaishi 27:350–355
Pot G, Toussaint E, Coutand C, Le Cam JB (2013) Experimental study of the viscoelastic properties of green poplar wood during maturation. J Mater Sci 48:6065–6073
Scurfield G (1973) Reaction wood, its structure and function. Science 179:647–655
Sierra-De-Grado R, Pando V, Martinez-Zurimendi P et al (2008) Biomechanical differences in the stem straightening process among Pinus pinaster provenances. A new approach for early selection of stem straightness. Tree Physiol 28:835–846
Sinnott EW (1952) Reaction wood and the regulation of tree form. Am J Bot 39:69–78
Tanimoto M, Tremblay R, Colasanto J (2008) Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropisme 5 mutant are associated with reduced starch levels. Plant Mol Biol 67:57–69
Tarui Y, Iino M (1997) Gravitropism of oat and wheat coleoptiles, dependence on the stimulation angle and involvement of autotropic straighthening. Plant Cell Physiol 102:328–335
Telewski FW (2006) A unified hypothesis of mechanoperception in plants. Am J Bot 93:1466–1476
Yamashita S, Yoshida M, Takayama S, Okuyama T (2007) Stem-righting mechanism in gymnosperm trees deduced from limitations in compression wood development. Ann Bot 99:487–493
Yoshida M, Okuda T, Okuyama T (2000) Tension wood and growth stress induced by artificial inclination in Liriodendron tulipifera Linn. and Prunus spachiana Kitamura f. ascendens Kitamura. Ann For Sci 57:739–746
Zandonemi K, Schopfer P (1994) Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 182:96–101
Acknowledgments
We thank Stéphane Ploquin (UMR 547 PIAF, Clermont-Ferrand, France) for help with the measurements, Patrick Chaleil (UMR 547 PIAF, Clermont-Ferrand, France) for tree breeding, Dr. Hervé Cochard, Dr. Bruno Moulia (UMR 547 PIAF, Clermont-Ferrand, France) and Prof. Georges Jeronimidis (University of Reading, United Kingdom) for helpful comments on the manuscript, Dr. André Lacointe for his help with statistical analyses and Mrs Gail Wagman and ATT company for English corrections.
Conflict of interest
Authors declare to have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Fourcaud.
Rights and permissions
About this article
Cite this article
Coutand, C., Pot, G. & Badel, E. Mechanosensing is involved in the regulation of autostress levels in tension wood. Trees 28, 687–697 (2014). https://doi.org/10.1007/s00468-014-0981-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-014-0981-6