Abstract
Key message
Periodic bending of young poplars increase the wood production whatever their hydric status; especially in the most highly stressed zones; improving the mechanical behaviour of the stem.
Abstract
The ability of trees to acclimate the building of their structures to windy conditions under various hydric conditions is essential in the context of the predicted climate changes. In this study, we investigated the biomechanical responses of young poplar trees to periodic controlled bending stimulations that mimic the mechanical effect of trees growing under windy conditions. This treatment was conducted for 5 months in well-watered conditions or under hydric stress. Results demonstrate the high impact of thigmomorphogenesis on growth processes, even under the water shortage. While axial growth was reduced by mechanical stimulations and hydric stress, radial growth was strongly increased by the periodic stem bending. The secondary growth was preferentially increased in the direction of highest longitudinal strains leading to the ovalisation of the cross-section. This ovalisation yielded 16%, regardless the hydric condition and generated a huge increase of the bending rigidity of the trees (+ 212%). Further, we observed a differential growth between the side growing under tension and the side growing under compression. A Finite Element model was built to investigate the mechanical benefits of the anisotropic cross-section shapes. This FE model enlightened the modulation of the spatial stress distribution that lead to a reduction of the stress in the weakest zones of the trunk; suggesting an improvement of the mechanical safety margin of wood. Thigmomorphogenesis acclimation appears as a complex and costly, but necessary process for the long-term mechanical support of the trees, even under hydric stress conditions.
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References
Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiol Plant 139:280–288
Awad H, Herbette S, Brunel N, Tixier A, Pilate G, Cochard H, Badel E (2012) No trade-off between hydraulic and mechanical properties in several transgenic poplars modified for lignins metabolism. Environ Exp Bot 77:185–195. https://doi.org/10.1016/j.envexpbot.2011.11.023
Badel E, Ewers F, Cochard H, Telewski FW (2015) Acclimation of mechanical and hydraulic functions in trees: impact of the thigmomorphogenetic process. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00266
Bariska M, Kucera LJ (1985) On the fracture morphology in wood. 2. Macroscopical deformations upon ultimate axial-compression in wood. Wood Sci Technol 19:19–34. https://doi.org/10.1007/bf00354750
Biddington NL (1986) The effects of mechanically induced stress in plants—a review. Plant Growth Regul 4:103–123
Bonnesoeur V, Constant T, Moulia B, Fournier M (2016) Forest trees filter chronic wind-signals to acclimate to high winds. New Phytol. https://doi.org/10.1111/nph.13836
Bornand M, Dejou J, Servant J (1975) Terres noires of Limagne (Massif Central, France)-various soil facies and their place in French classification. C R Hebd Des Seances De L Acad Des Sci Ser D 281:1689–1692
Breda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644
Chauveau M et al (2013) What will be the impacts of climate change on surface hydrology in France by 2070? Houille Blanche Rev Int. https://doi.org/10.1051/lhb/2013027
Coutand C, Moulia B (2000) Biomechanical study of the effect of a controlled bending on tomato stem elongation: local strain sensing and spatial integration of the signal. J Exp Bot 51:1825–1842
Coutand C, Dupraz C, Jaouen G, Ploquin S, Adam B (2008) Mechanical stimuli regulate the allocation of biomass in trees: demonstration with young Prunus avium trees. Ann Bot 101:1421–1432
Coutand C, Martin L, Leblanc-Fournier N, Decourteix M, Julien JL, Moulia B (2009) Strain mechanosensing quantitatively controls diameter growth and PtaZFP2 gene expression in poplar. Plant Physiol 151:223–232. https://doi.org/10.1104/pp.109.138164
Deng Q, Li S, Chen YP (2012) Mechanical properties and failure mechanism of wood cell wall layers. Comput Mater Sci 62:221–226. https://doi.org/10.1016/j.commatsci.2012.05.050
Doube M et al (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079. https://doi.org/10.1016/j.bone.2010.08.023
Fournier M, Stokes A, Coutand C, Fourcaud T, Moulia B (2006) Tree biomechanics and growth strategies in the context of forest functional ecology. Ecology and Biomechanics: a mechanical approach to the ecology of animals and plants. CRC Press–Taylor & Francis Group, Boca Raton
Fournier M, Dlouha J, Jaouen G, Almeras T (2013) Integrative biomechanics for tree ecology: beyond wood density and strength. J Exp Bot 64:4793–4815. https://doi.org/10.1093/jxb/ert279
Gartner BL (1994) Root biomechanics and whole-plant allocation patterns. Responses of tomato plants to stem flexure. J Exp Bot 45:1647–1654
Giovannelli A, Deslauriers A, Fragnelli G, Scaletti L, Castro G, Rossi S, Crivellaro A (2007) Evaluation of drought response of two poplar clones (Populus × canadensis Monch ‘I-214’ and P-deltoides Marsh. ‘Dvina’) through high resolution analysis of stem growth. J Exp Bot 58:2673–2683. https://doi.org/10.1093/jxb/erm117
Haarsma RJ et al (2013) More hurricanes to hit western Europe due to global warming. Geophys Res Lett 40:1783–1788. https://doi.org/10.1002/grl.50360
Jaffe MJ (1973) Thigmomorphogenesis. The response of plant growth and development to mechanical stimulation. Planta 114:143–157
Jaffe MJ, Telewski FW, Cooke PW (1984) Thigmomorphogenesis. On the mechanical properties of mechanically perturbed bean plants. Physiol Plant 62:73–78
Jourez B (1997) Tension wood. 1. Definition and distribution in the tree. BASE 1:100–112
Jourez B, Avella-Shaw T (2003) Effect of gravitational stimulus duration on tension wood formation in young stems of poplar (P-euramericana ev ‘Ghoy’). Ann For Sci 60:31–41. https://doi.org/10.1051/forest:2002071
Kern KA, Ewers FW, Telewski FW, Koehler L (2005) Mechanical perturbation affects conductivity, mechanical properties and aboveground biomass of hybrid poplars. Tree Physiol 25:1243–1251
Krabel D, Meyer M, Solger A, Muller R, Carvalho P, Foulkes J (2015) Early root and aboveground biomass development of hybrid poplars (Populus spp.) under drought conditions. Can J For Res 45:1289–1298. https://doi.org/10.1139/cjfr-2015-0126
Lebourgeois F, Cousseau G, Ducos Y (2004) Climate-tree-growth relationships of Quercus petraea Mill. stand in the Forest of Berce (“Futaie des Clos”, Sarthe, France. Ann For Sci 61:361–372. https://doi.org/10.1051/forest:2004029
Mader M et al (2016) Whole-genome draft assembly of Populus tremula × P-alba clone INRA 717-1B4. Silvae Genet 65:74–79. https://doi.org/10.1515/sg-2016-0019
Merian P, Bontemps JD, Berges L, Lebourgeois F (2011) Spatial variation and temporal instability in climate-growth relationships of sessile oak (Quercus petraea Matt. Liebl.) under temperate conditions. Plant Ecol 212:1855–1871. https://doi.org/10.1007/s11258-011-9959-2
Moulia B, Coutand C, Julien J-L (2015) Mechanosensitive control of plant growth: bearing the load, sensing, transducing and responding. Front Plant Sci 6:20. https://doi.org/10.3389/fpls.2015.00052
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Navi P, Heger F (2005) Approche micromécanique du comportement mécanique du bois. In: Comportement thermo-hydromécanique du bois: applications technologiques et dans les structures. Presses Polytechniques et Universitaires Romandes (PPUR), Lausanne, Suisse, pp 167–215
Neel PL, Harris RW (1971) Motion-induced inhibition of elongation and induction of dormancy in Liquidambar. Science 173:58. https://doi.org/10.1126/science.173.3991.58
Niklas KJ (1996) Differences between Acer saccharum leaves from open and wind-protected sites. Ann Bot 78:61–66. https://doi.org/10.1006/anbo.1996.0096
Osorio J, Osorio ML, Chaves MM, Pereira JS (1998) Water deficits are more important in delaying growth than in changing patterns of carbon allocation in Eucalyptus globulus. Tree Physiol 18:363–373
Perbal G, Drissecole D (1993) Microgravity and root gravitropism. Acta Bot Gall 140:615–632. https://doi.org/10.1080/12538078.1993.10515642
Petit JR et al (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399:429–436. https://doi.org/10.1038/20859
Pruyn ML, Ewers BJ, Telewski FW (2000) Thigmomorphogenesis: changes in the morphology and mechanical properties of two Populus hybrids in response to mechanical perturbation. Tree Physiol 20:535–540
Ritchie GA, Hinckley TM (1975) The pressure chamber as an instrument for ecological research. In: MacFadyen A (ed) Advances in ecological research, vol 9. Academic Press, Cambridge, pp 165–254. https://doi.org/10.1016/S0065-2504(08)60290-1
Roignant J, Badel E, Leblanc-Fournier N, Brunel-Michac N, Ruelle J, Moulia B, Decourteix M (2018) Feeling stretched or compressed? The multiple mechanosensitive responses of wood formation to bending. Ann Bot. https://doi.org/10.1093/aob/mcx211
Rosner S, Klein A, Muller U, Karlsson B (2008) Tradeoffs between hydraulic and mechanical stress responses of mature Norway spruce trunk wood. Tree Physiol 28:1179–1188
Ruelle J (2014) Morphology, anatomy and ultrastructure of reaction wood. In: Gril J, BGJBPS (ed) The biology of reaction wood. Springer, Berlin, pp 13–35
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants—negative hydrostatic pressure can be measured in plants. Science 148:339–339+. https://doi.org/10.1126/science.148.3668.339
Silva FCE, Shvaleva A, Maroco JP, Almeida MH, Chaves MM, Pereira JS (2004) Responses to water stress in two Eucalyptus globulus clones differing in drought tolerance. Tree Physiol 24:1165–1172. https://doi.org/10.1093/treephys/24.10.1165
Telewski FW (1989) Structure and function of flexure wood in Abies fraseri. Tree Physiol 5:113–121
Telewski FW (1995) Wind-induced physiological and developmental responses in trees. In: Coutts MP, Grace J (eds) Wind and trees. Cambridge University Press, Cambridge, pp 237–263
Telewski FW (2016) Flexure wood: mechanical stress induced secondary xylem formation. In: Secondary xylem biology: origins, functions, and applications. Academic Press, Cambridge, pp 73–91
Telewski FW, Pruyn ML (1998) Thigmomorphogenesis: a dose response to flexing in Ulmus americana seedlings. Tree Physiol 18:65–68
Timoshenko SP (1930a) Strength of materials, vol 1. D. Van Nostrand Company, Inc, Princeton
Timoshenko SP (1930b) Strength of materials, vol 2, D. Van Nostrand Company, Inc, Princeton
Acknowledgements
The authors thank Christelle Boisselet, Patrice Chaleil, Pierre Conchon, Aline Faure, Brigitte Girard, Stéphane Ploquin and Romain Souchal (UMR UCA-INRA PIAF) for their technical support and Evelyne Toussaint and Joseph Gril (UMR UCA-Institut Pascal) for constructive discussions and suggestions. This work was supported by grants from the Auvergne-Rhônes-Alpes Regional Council and from EFPA department of National Institute for Agronomic Research (INRA).
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Niez, B., Dlouha, J., Moulia, B. et al. Water-stressed or not, the mechanical acclimation is a priority requirement for trees. Trees 33, 279–291 (2019). https://doi.org/10.1007/s00468-018-1776-y
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DOI: https://doi.org/10.1007/s00468-018-1776-y