Mechanosensitive control of plant growth: Bearing the load, sensing, transducing, and responding

Frontiers in Plant Science

Volumn 6, Issue FEB, 2015, Pages

  Moulia, Bruno ^a,b   Coutand, Catherine ^a,b   Julien, Jean Louis ^a,b  

^a PIAF   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Biomechanics; Curvature; Mechanobiology; Mechanotransduction; Stress; Thigmomorphogenesis; Turgor pressure; Wind

Indexed keywords

EID: 84923247263     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00052     Document Type: Review

References (82)

1. Almeras, T., Derycke, M., Jaouen, G., Beauchene, J., and Fournier, M. (2009). Functional diversity in gravitropic reaction among tropical seedlings in relation to ecological and developmental traits. J. Exp. Bot. 60, 4397-4410. doi: 10.1093/jxb/erp276
2. Asnacios, A., and Hamant, O. (2012). The mechanics behind cell polarity. Trends Cell Biol. 22, 584-591. doi: 10.1016/j.tcb.2012.08.005
3. Baluska, F., Samaj, J., Wojtaszek, P., Volkmann, D., and Menzel, D. (2003). Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol. 133, 482-491. doi: 10.1104/pp.103.027250
4. Band, L. R., Fozard, J. A., Godin, C., Jensen, O. E., Pridmore, T., Bennett, M. J., et al. (2012). Multiscale systems analysis of root growth and development: modeling beyond the network and cellular scales. Plant Cell 24, 3892-3906. doi: 10.1105/tpc.112.101550
5. Barbacci, A., Diener, J., Hemon, P., Adam, B., Dones, N., Reveret, L., et al. (2014). A robust videogrametric method for the velocimetry of wind-induced motion in trees. Agri. Forest Meteorol. 184, 220-229. doi: 10.1016/j.agrformet.2013.10.003
6. Barbacci, A., Lahaye, M., and Magnenet, V. (2013). Another brick in the cell wall: biosynthesis dependent growth model. PLoS ONE 8:e74400. doi: 10.1371/journal.pone.0074400
7. Baskin, T. I., and Jensen, O. E. (2013). On the role of stress anisotropy in the growth of stems. J. Exp. Bot. 64, 4697-4707. doi: 10.1093/jxb/ert176
8. Bastien, R., Bohr, T., Moulia, B., and Douady, S. (2013). Unifying model of shoot gravitropism reveals proprioception as a central feature of posture control in plants. Proc. Natl. Acad. Sci. U.S.A. 110, 755-760. doi: 10.1073/pnas.1214301109
9. Bastien, R., Douady, S., and Moulia, B. (2014). A unifying modeling of plant shoot gravitropism with an explicit account of the effects of growth. Front. Plant Sci. 5:136. doi: 10.3389/Fpls.2014.00136
10. Bengough, A. G., Mckenzie, B. M., Hallett, P. D., and Valentine, T. A. (2011). Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J. Exp. Bot. 62, 59-68. doi: 10.1093/jxb/erq350
11. Boudaoud, A. (2010). An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci. 15, 353-360. doi: 10.1016/j.tplants.2010.04.002
12. Braam, J. (2005). In touch: plant responses to mechanical stimuli. N. Phytol. 165, 373-389. doi: 10.1111/j.1469-8137.2004.01263.x
13. Brenner, E. D., Stahlberg, R., Mancuso, S., Vivanco, J., Baluska, F., and Van Volkenburgh, E. (2006). Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci. 11, 413-419. doi: 10.1016/j.tplants.2006.06.009
14. Burian, A., Ludynia, M., Uyttewaal, M., Traas, J., Boudaoud, A., Hamant, O., et al. (2013). A correlative microscopy approach relates microtubule behaviour, local organ geometry, and cell growth at the Arabidopsis shoot apical meristem. J. Exp. Bot. 64, 5753-5767. doi: 10.1093/jxb/ert352
15. Coutand, C. (2010). Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view.Plant Sci. 179, 168-182. doi: 10.1016/j.plantsci.2010.05.001
16. Coutand, C., and 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. doi: 10.1093/jexbot/51.352.1825
17. Coutand, C., Chevolot, M., Lacointe, A., Rowe, N., and Scotti, I. (2010). Mechanosensing of stem bending and its interspecific variability in five neotropical rainforest species. Ann. Bot. 105, 341-347. doi: 10.1093/aob/mcp286
18. Coutand, C., Julien, J. L., Moulia, B., Mauget, J. C., and Guitard, D. (2000). Biomechanical study of the effect of a controlled bending on tomato stem elongation: global mechanical analysis. J. Exp. Bot. 51, 1813-1824. doi: 10.1093/jexbot/51.352.1813
19. Coutand, C., Martin, L., Leblanc-Fournier, N., Decourteix, M., Julien, J. L., and Moulia, B. (2009). Strain mechanosensing quantitatively controls diameter growth and PtaZFP2 gene expression in poplar. Plant Physiol. 151, 223-232. doi: 10.1104/pp.109.138164
20. Coutand, C., Mathias, J. D., Jeronimidis, G., and Destrebecq, J. F. (2011). TWIG: a model to simulate the gravitropic response of a tree axis in the frame of elasticity and viscoelasticity, at intra-annual time scale. J. Theor. Biol. 273, 115-129. doi: 10.1016/j.jtbi.2010.12.027
21. Couturier, E., Brunel, N., Douady, S., and Nakayama, N. (2012). Abaxial growth and steric constraints guide leaf folding and shape in acer pseudoplatanus. Am. J. Bot. 99, 1289-1299. doi: 10.3732/ajb.1100325
22. De Langre, E. (2008). Effects of wind on plants. Annu. Rev. Fluid Mech. 40, 141-168. doi: 10.1146/annurev.fluid.40.111406.102135
23. Der Loughian, C., Tadrist, L., Allain, J.-M., Diener, J., Moulia, B., and De Langre, E. (2014). Measuring local and global vibration modes in model plants. C. R. Mécanique 342, 1-7. doi: 10.1016/j.crme.2013.10.010
24. Ding, J. P., and Pickard, B. G. (1993). Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J. 3, 713-720. doi: 10.1111/j.1365-313X.1993.00713.x
25. Ditengou, F. A., Tealea, W. D., Kochersperger, P., Flittner, K. A., Kneuper, I., Van Der Graaff, E., et al. (2008). Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 105, 18818-18823. doi: 10.1073/pnas.0807814105
26. Dumais, J. (2013). Modes of deformation of walled cells. J. Exp. Bot. 64, 4681-4695. doi: 10.1093/jxb/ert268
27. Elowitz, M. B., Levine, A. J., Siggia, E. D., and Swain, P. S. (2002). Stochastic gene expression in a single cell. Science297, 1183-1186. doi: 10.1126/science.1070919
28. Fourcaud, T., Zhang, X., Stokes, A., Lambers, H., and Korner, C. (2008). Plant growth modelling and applications: the increasing importance of plant architecture in growth models. Ann. Bot. 101, 1053-1063. doi: 10.1093/aob/mcn050
29. Fournier, M., Baillères, H., and Chanson, B. (1994). Tree biomechanics: growth, cumulative prestresses, and reorientations. Biomimetics 2, 229-251.
30. Gandrillon, O., Kolesnik-Antoine, D., Kupiec, J. J., and Beslon, G. (2012). Special Issue: chance at the heart of the cell. Prog. Biophys. Mol. Biol. 110, 1-4. doi: 10.1016/j.pbiomolbio.2012.05.006
31. Gardiner, B., Byrne, K., Hale, S., Kamimura, K., Mitchell, S. J., Peltola, H., et al. (2008). A review of mechanistic modelling of wind damage risk to forests. Forestry 81, 447-463. doi: 10.1093/forestry/cpn022
32. Gibson, L. J. (2013). The hierarchical sturcture and mechanics of plant materials. J. R. Soc. Interface 9, 2749-2766. doi: 10.1098/rsif.2012.0341
33. Gibson, L. J., Ashby, M. F., and Easterling, K. E. (1988). Structure and mechanics of the iris leaf. J. Mater. Sci. 23, 3041-3048. doi: 10.1007/BF00551271
34. Hamant, O. (2013). Widespread mechanosensing controls the structure behind the architecture in plants. Curr. Opin. Plant Biol. 16, 654-660. doi: 10.1016/j.pbi.2013.06.006
35. Hamant, O., Heisler, M. G., Jonsson, H., Krupinski, P., Uyttewaal, M., Bokov, P., et al. (2008). Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655. doi: 10.1126/science.1165594
36. Haswell, E. S., Peyronnet, R., Barbier-Brygoo, H., Meyerowitz, E. M., and Frachisse, J. M. (2008). Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18, 730-734. doi: 10.1016/j.cub.2008.04.039
37. Heisler, L. K., and Lam, D. D. (2010). 5-HT2C receptor ligands in the treatment of obesity and type 2 diabetes. Eur. Neuropsychopharmacol. 20, S182-S182. doi: 10.1016/S0924-977X(10)70171-1
38. Jaffe, M. J. (1980a). Morphogenetic responses of plants to mechanical stimuli or stress. Bioscience 30, 239-243.
39. Jaffe, M. J. (1980b). Morphogenetic responses of plants to mechanical stimuli or stress. Bioscience 30, 239-243. doi: 10.2307/1307878
40. Jin, K., Shen, J. B., Ashton, R. W., Dodd, I. C., Parry, M. A. J., and Whalley, W. R. (2013). How do roots elongate in a structured soil? J. Exp. Bot. 64, 4761-4777. doi: 10.1093/Jxb/Ert286
41. Jonsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M., and Mjolsness, E. (2006). An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. U.S.A. 103, 1633-1638. doi: 10.1073/pnas.0509839103
42. Kwiatkowska, D. (2008). Flowering and apical meristem growth dynamics. J. Exp. Bot. 59, 187-201. doi: 10.1093/jxb/erm290
43. Landrein, B., and Hamant, O. (2013). How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J. 75, 324-338. doi: 10.1111/tpj.12188
44. Leblanc-Fournier, N., Coutand, C., Crouzet, J., Brunel, N., Lenne, C., Moulia, B., et al. (2008). Jr-ZFP2, encoding a Cys2/His2-type transcription factor, is involved in the early stages of the mechano-perception pathway and specifically expressed in mechanically stimulated tissues in woody plants. Plant Cell Environ. 31, 715-726. doi: 10.1111/j.1365-3040.2008.01785.x
45. Leblanc-Fournier, N., Martin, L., Lenne, C., and Decourteix, M. (2014). To respond or not to respond, the recurring question in plant mechanosensitivity. Front. Plant Sci. 5:401. doi: 10.3389/fpls.2014.00401
46. Legay, J. M. (1997). L'expérience et Le Modèle, Un Dicours Sur La Méthode. Paris: Quae Editions.
47. Lopez-Rodriguez, A. M., Venkataraman, G., and Holmgren, M. (2014). Shaker Kv Channel's sugar remotion in real-time. Biophys. J. 106, 537a. doi: 10.1016/j.bpj.2013.11.2996
48. Martin, L., Leblanc-Fournier, N., Azri, W., Lenne, C., Henry, C., Coutand, C., et al. (2009). Characterization and expression analysis under bending and other abiotic factors of PtaZFP2, a poplar gene encoding a Cys2/His2 zinc finger protein. Tree Physiol. 29, 125-136. doi: 10.1093/treephys/tpn011
49. Martin, L., Leblanc-Fournier, N., Julien, J. L., Moulia, B., and Coutand, C. (2010). Acclimation kinetics of physiological and molecular responses of plants to multiple mechanical loadings. J. Exp. Bot. 61, 2403-2412. doi: 10.1093/jxb/erq069
50. Mattheck, C., and Bethge, K. (1998). The mechanical survival strategy of trees. Arboric. J. 22, 369-386. doi: 10.1080/03071375.1998.9747222
51. Milani, P., Braybrook, S. A., and Boudaoud, A. (2013). Shrinking the hammer: micromechanical approaches to morphogenesis. J. Exp. Bot. 64, 4651-4662. doi: 10.1093/jxb/ert169
52. Monshausen, G. B., and Haswell, E. S. (2013). A force of nature: molecular mechanisms of mechanoperception in plants. J. Exp. Bot. 64, 4663-4680. doi: 10.1093/jxb/ert204
53. Moulia, B. (2000). Leaves as shell structures: double curvature, auto-stresses, and minimal mechanical energy constraints on leaf rolling in grasses. J. Plant Growth Regul. 19, 19-30. doi: 10.1007/s003440000004
54. Moulia, B. (2013). Plant biomechanics and mechanobiology are convergent paths to flourishing interdisciplinary research. J. Exp. Bot. 64, 4617-4633. doi: 10.1093/jxb/ert320
55. Moulia, B., Fournier, M., and Guitard, D. (1994). Mechanics and form of the maize leaf: in vivo qualification of flexural behavior. J. Mater. Sci. 29, 2359-2366. doi: 10.1007/Bf00363427
56. Moulia, B., and Fournier, M. (1997). Mechanics of the maize leaf: a composite beam model of the midrib. J. Mater. Sci. 32, 2771-2780. doi: 10.1023/A:1018604012754
57. Moulia, B., and Fournier, M. (2009). The power and control of gravitropic movements in plants: a biomechanical and systems biology view. J. Exp. Bot. 60, 461-486. doi: 10.1093/jxb/ern341
58. Moulia, B., Coutand, C., and 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. doi: 10.3732/ajb.93.10.1477
59. Moulia, B., Der Loughian, C., Bastien, R., Martin, L., Rodriguez, M., Gourcilleau, D., et al. (2011). "Integrative mechanobiology of growth and architectural development in changing mechanical environments," in Mechanical Integrative of Plant Cells and Plants ed P. Wojtaszek (Berlin: Springer-Verlag), 269-302.
60. Nakayama, N., Smith, R. S., Mandel, T., Robinson, S., Kimura, S., Boudaoud, A., et al. (2012). Mechanical regulation of auxin-mediated growth. Curr. Biol. 22, 1468-1476. doi: 10.1016/j.cub.2012.06.050editors
61. Nick, P. (2011). "Mechanics of the cytoskeleton," in Mechanical Integration of Plant Cells and Plants, ed P. Wojtaszek (Berlin; Heidelberg: Springer), 53-90.
62. Niklas, K. J., and Spatz, H. C. (2012). Mechanical properties of wood disproportionately increase with increasing density. Am. J. Bot. 99, 169-170. doi: 10.3732/ajb.1100567
63. Peaucelle, A., Braybrook, S. A., Le Guillou, L., Bron, E., Kuhlemeier, C., and Hofte, H. (2011). Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol. 21, 1720-1726. doi: 10.1016/j.cub.2011.08.057
64. Pivato, D., Dupont, S., and Brunet, Y. (2014). A simple tree swaying model for forest motion in windstorm conditions. Trees 28, 281-293. doi: 10.1007/s00468-013-0948-z
65. Pot, G., Toussaint, E., Coutand, C., Le Cam, J. B., and Saudreau, M. (2014). A model to simulate the gravitropic response and internal stresses in trees, considering the progressive maturation of wood. Trees 28, 1235-1248. doi: 10.1007/s00468-014-1033-y
66. Robinson, S., Burian, A., Couturier, E., Landrein, B., Louveaux, M., Neumann, E. D., et al. (2013). Mechanical control of morphogenesis at the shoot apex. J. Exp. Bot. 64, 4729-4744. doi: 10.1093/jxb/ert199
67. Rodriguez, M., De Langre, E., and Moulia, B. (2008). A scaling law for the effects of architecture and allometry on tree vibration modes suggests a biological tuning to modal compartmentalization. Am. J. Bot. 95, 1523-1537. doi: 10.3732/ajb.0800161
68. Routier-Kierzkowska, A. L., Weber, A., Kochova, P., Felekis, D., Nelson, B. J., Kuhlemeier, C., et al. (2012). Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiol. 158, 1514-1522. doi: 10.1104/pp.111.191460
69. Sato, K., Adachi, T., Matsuo, M., and Tomita, Y. (2005). Quantitative evaluation of threshold fiber strain that induces reorganization of cytoskeletal actin fiber structure in osteoblastic cells. J. Biomech. 38, 1895-1901. doi: 10.1016/j.jbiomech.2004.08.012
70. Schriefer, J., Warden, S., Saxon, L., Robling, A., and Turner, C. (2005). Cellular accomodation and the response of bone to mechanical loading. J. Biomech. 38, 1838-1845. doi: 10.1016/j.jbiomech.2004.08.017
71. Sellier, D., Brunet, Y., and Fourcaud, T. (2008). A numerical model of tree aerodynamic response to a turbulent airflow. Forestry 81, 279-297. doi: 10.1093/forestry/cpn024
72. Sierra-De-Grado, R., Pando, V., Martinez-Zurimendi, P., Penalvo, A., Bascones, E., and Moulia, B. (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. doi: 10.1093/treephys/28.6.835
73. Silk, W. K., and Erickson, R. O. (1980). Local biosynthesis rates of cytoplasmic constituents in growing tissue. J. Theor. Biol. 83, 701-703. doi: 10.1016/0022-5193(80)90197-6
74. Sotomayor, M., and Shulten, K. (2014). Molecular dynamics study of gating in the mechanosensitive channel of small conductance MscS. Biophys. J. 87, 3050-3065. doi: 10.1529/biophysj.104.046045
75. Supatto, W., Debarre, D., Moulia, B., Brouzes, E., Martin, J. L., Farge, E., et al. (2005). In vivo modulation of morphogenetic movements in Drosophila embryos with femtosecond laser pulses. Proc. Natl. Acad. Sci. U.S.A. 102, 1047-1052. doi: 10.1073/pnas.0405316102
76. Tardieu, F. (2003). Virtual plants: modelling as a tool for the genomics of tolerance to water deficit. Trends Plant Sci. 8, 9-14. doi: 10.1016/S1360-1385(02)00008-0
77. Telewski, F. W. (2006). A unified hypothesis of mechanoperception in plants. Am. J. Bot. 93, 1466-1476. doi: 10.3732/ajb.93.10.1466
78. Telewski, F. W., and Pruyn, M. L. (1998). Thigmomorphogenesis: a dose response to flexing in Ulmus americana seedlings. Tree Physiol. 18, 65-68. doi: 10.1093/treephys/18.1.65
79. Tixier, A., Badel, E., Franchel, J., Lakhal, W., Leblanc-Fournier, N., Moulia, B., et al. (2014). Growth and molecular responses to long-distance stimuli in poplars: bending vs flame wounding. Physiol. Plant. 150, 225-237. doi: 10.1111/ppl.12089
80. Traas, J., and Hamant, O. (2009). From genes to shape: understanding the control of morphogenesis at the shoot meristem in higher plants using systems biology. C. R. Biol. 332, 974-985. doi: 10.1016/j.crvi.2009.09.008
81. Traas, J., and Moneger, F. (2010). Systems biology of organ initiation at the shoot apex. Plant Physiol. 152, 420-427. doi: 10.1104/pp.109.150409
82. Villaverde, A. F., and Banga, J. R. (2014). Reverse engineering and identification in systems biology: strategies, perspectives and challenges. J. R. Soc. Interface 11:20130505. doi: 10.1098/Rsif.2013.0505