Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells

Plant Cell

Volumn 21, Issue 3, 2009, Pages 843-860

  Leitz, Guenther ^a   Kang, Byung Ho ^a   Schoenwaelder, Monica E A ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; COLUMELLA;

EID: 66449120807     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.065052     Document Type: Article

References (85)

1. Aris, R. (1989). Vectors, Tensors, and the Basic Equations of Fluid Mechanics. (New York: Dover Publications).
2. Ashkin, A., and Dziedzic, J.M. (1989). Internal cell manipulation using infrared laser traps. Proc. Natl. Acad. Sci. USA 86: 7914-7918.
3. Autumn, K., Sitti, M., Liang, Y.A., Peattie, A.M., Hansen, W.R., Sponberg, S., Kenny, T.W., Fearing, R., Israelachvili, J.N., and Full, R.J. (2002). Evidence for van der Waals adhesion in gecko setae. Proc. Natl. Acad. Sci. USA 99: 12252-12256.
4. Baluska, F., and Hasenstein, K.H. (1997). Root cytoskeleton: Its role in perception and response to gravity. Planta 203: S69-S78.
5. Belyavskaya, N.A. (1996). Calcium and gravitropism in plants: Inhibitor analysis. Int. Rev. Cytol. 168: 123-185.
6. Bevan, M.A., and Prieve, D.C. (1999). Direct measurement of retarded van der Waals attraction. Langmuir 15: 7925-7936.
7. Blancaflor, E.B., Fasano, J.M., and Gilroy, S. (1998). Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol. 116: 213-222.
8. Blancaflor, E.B., and Masson, P.H. (2003). Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol. 133: 1677-1690.
9. Boal, D. (2002). Mechanics of the Cell. (New York: Cambridge University Press).
10. Boonsirichai, K., Guan, C., Chen, R., and Masson, P.H. (2002). Root gravitropism: An experimental tool to investigate basic cellular and molecular processes underlying mechanosensing and signal transmission in plants. Annu. Rev. Plant Biol. 53: 421-447.
11. Brenner, M.P. (1999). Screening mechanisms in sedimentation. Phys. Fluids 11: 754-772.
12. Chen, R., Guan, C., Boonsirichai, K., and Masson, P.H. (2002). Complex physiological and molecular processes underlying root gravitropism. Plant Mol. Biol. 49: 305-317.
13. Chen, R., Rosen, E., and Masson, P.H. (1999). Gravitropism in higher plants. Plant Physiol. 120: 343-350.
14. Danuser, G., Tran, P.T., and Salmon, E.D. (2000). Tracking differential interference contrast diffraction line images with nanometer sensitivity. J. Microsc. 198: 34-53.
15. Darwin, F. (1907). Lectures on the physiology of movement in plants. New Phytol. 6: 69-76.
16. Davis, R.H., and Acrivos, A. (1985). Sedimentation of noncolloidal particles at low Reynolds numbers. Annu. Rev. Fluid Mech. 17: 91-118.
17. Davis, R.H., Zhao, Y., Galvin, K.P., and Wilson, H.J. (2003). Solid-solid contacts due to surface roughness and their effects on suspension behavior. Philos. Transact. A Math Physiol. Eng. Sci. 361: 871-894.
18. Dean, D.S., and Horgan, R.R. (2006). Renormalization of membrane rigidity by long-range interactions. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73: 011906.
19. Derjaguin, B.V., and Landau, L. (1941). Theory of the stability of strongly charged lyophobic sols and of the adhesion of strongly charged particles in solutions of electrolytes. Acta Physicochimica (USSR) 14: 633-662.
20. Douglass, J.K., Wilkens, L., Pantazelou, E., and Moss, F. (1993). Noise enhancement of information transfer in crayfish mechanore-ceptors by stochastic resonance. Nature 365: 337-340.
21. Driss-Ecole, D., Lefranc, A., and Perbal, G. (2003). A polarized cell: The root statocyte. Physiol. Plant. 118: 305-312.
22. Driss-Ecole, D., Vassy, J., Rembur, J., Guivarc'h, A., Prouteau, M., Dewitte, W., and Perbal, G. (2000). Immunolocalization of actin in root statocytes of Lens culinaris L. J. Exp. Bot. 51: 521-528.
23. Fasano, J.M., Swanson, S.J., Blancaflor, E.B., Dowd, P.E., Kao, T.H., and Gilroy, S. (2001). Changes in root cap pH are required for the gravity response of the Arabidopsis root. Plant Cell 13: 907-921.
24. Friml, J., Wisniewska, J., Benkova, E., Mendger, K., and Palme, K. (2002). Lateral relocation of auxin efflux regulator AtPIN3 mediates tropism in Arabidopsis. Nature 415: 806-809.
25. Gilkey, J.C., and Staehelin, L.A. (1986). Advances in ultrarapid freezing for the preservation of cellular structure. J. Electron Microsc. Tech. 3: 177-210.
26. Gillespie, P.G., and Walker, R.G. (2001). Molecular basis of mechano-sensory transduction. Nature 413: 194-202.
27. Guyon, E., Hulin, J.-P., Petit, L., and Mitescu, C. (2001). Physical Hydrodynamics. (New York: Oxford University Press).
28. Haberlandt, G. (1900). Uber die Perzeption des geotropischen Reizes. Ber. Dtsch. Bot. Ges. 18: 261-272.
29. Hamill, O.P., and Martinac, B. (2001). Molecular basis of mechano-transduction in living cells. Physiol. Rev. 91: 685-740.
30. Hanggi, P. (2002). Stochastic resonance in biology. ChemPhysChem 3: 285-290.
31. 2+ transient induced by extracellular changes in osmotic pressure in Arabidopsis leaves: Differential involvement of cell wall-plasma membrane adhesion. Plant Cell Environ. 29: 661-672.
32. Hejnowicz, Z., Sondag, C., Alt, W., and Sievers, A. (1998). Temporal course of graviperception in intermittently stimulated cress roots. Plant Cell Environ. 21: 1293-1300.
33. Hou, G., Kramer, V.L., Wang, Y.S., Chen, R., Perbal, G., Gilroy, S., and Blancaflor, E.B. (2004). The promotion of gravitropism in Arabidopsis roots upon actin disruption is coupled with the extended alkanization of the columella cytoplasm and a persistent lateral auxin gradient. Plant J. 39: 113-125.
34. Hou, G., Mohamalawari, D.R., and Blancaflor, E.B. (2003). Enhanced gravitropism of roots with a disrupted cap actin cytoskeleton. Plant Physiol. 131: 1360-1373.
35. Janmey, P.A., and Weitz, D.A. (2004). Dealing with mechanics: Mech-anisms of force transduction in cells. Trends Biochem. Sci. 29: 364-370.
36. Joseph, D.D., Liu, Y.J., Poletto, M., and Feng, J. (1994). Aggregation and dispersion of spheres falling in viscoelastic liquids. J. Non-Newt. Fluid Mech. 54: 45-86.
37. 2+ release from intracellular stores in Nitella flexilis. Plant Cell Physiol. 42: 358-365.
38. Kiss, J.Z., and Staehelin, L.A. (1995). High pressure freezing. In Rapid Freezing, Freeze Fracture, and Deep Etching, N.J. Severs, and D.M. Shottons, eds (New York: Wiley-Liss), pp. 89-104.
39. Kiss, J.Z. (2000). Mechanisms of the early phases of plant gravitropism. CRC Crit. Rev. Plant Sci. 19: 551-573.
40. Kuusela, E., Lahtinen, J.M., and Ala-Nissila, T. (2004). Sedimentation dynamics of spherical particles in confined geometries. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 69: 066310.
41. Leitz, G., Schnepf, E., and Greulich, K.O. (1995). Micromanipulation of statoliths in gravity-sensing Chara rhizoids by optical tweezers. Planta 197: 278-288.
42. Li, X., and Logan, B.E. (1997). Collision frequencies of fractal aggregates with small particles by differential sedimentation. Environ. Sci. Technol. 31: 1229-1236.
43. Li, X., and Yuan, Y. (2002). Settling velocities and permeabilities of microbial aggregates. Water Res. 36: 3110-3120.
44. Lin, B., Yu, J., and Rice, S.A. (2000). Direct measurements of constrained Brownian motion of an isolated sphere between two walls. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 62: 3909-3919.
45. Ma, Z., and Hasenstein, K.H. (2006). The onset of gravisensitivity in the embryonic root of flax. Plant Physiol. 140: 159-166.
46. 2+ influx and touch sensing in roots. Proc. Natl. Acad. Sci. USA 104: 3639-3644.
47. Nemec, B. (1900). Uber die Art der Wahrnehmung des Schwerkraft- reizes bei den Pflanzen. Ber. Dtsch. Bot. Ges. 18: 241-245.
48. Otegui, M.S., Mastronarde, D.N., Kang, B.-H., Bednarek, S.Y., and Staehelin, L.A. (2001). Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13: 2033-2051.
49. Ottenschlager, I., Wolff, P., Wolverton, C., Bhalerao, R.P., Sandberg, G., Ishikawa, H., Evans, M., and Palme, K. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 100: 2987-2991.
50. Pashley, R.M., and Karaman, M.E. (2004). Applied Colloid and Surface Chemistry. (West Sussex, UK: Wiley & Sons).
51. Perbal, G., and Driss-Ecole, D. (1989). Polarity of statocytes in lentil seedling roots grown in space (Spacelab D1 Mission). Physiol. Plant. 75: 518-524.
52. Perbal, G., and Driss-Ecole, D. (2002). Contributions of space experiments to the study of gravitropism. J. Plant Growth Regul. 21: 156-165.
53. Perbal, G., and Driss-Ecole, D. (2003). Mechanotransduction in grav-isensing cells. Trends Plant Sci. 8: 498-504.
54. Perbal, G., Jeune, B., Lefranc, A., Carnero-Diaz, E., and Driss-Ecole, D. (2002). The dose-response curve of the gravitropic reaction: A re-analysis. Physiol. Plant. 114: 336-342.
55. Perbal, G., Lefranc, A., Jeune, B., and Driss-Ecole, D. (2004). Mechanotransduction in root gravity sensing cells. Physiol. Plant. 120: 303-311.
56. Perozo, E., Kloda, A., Cortes, D.M., and Martinac, B. (2002). Physical principles underlying the transduction of bilayer deformation forces during mechanosensitive channel gating. Nat. Struct. Biol. 9: 696-703.
57. Persson, S., and Harper, J. (2006). The ER and cell calcium. In The Plant Endoplasmic Reticulum, Plant Cell Monographs, D.G. Robinson, ed (Heidelberg, New York: Springer-Verlag), pp. 251-278.
58. Pickard, W.F. (2003). The role of cytoplasmic streaming in symplastic
59. transport. Plant Cell Environ. 26: 1-15.
60. Plieth, C. (2005). Calcium: Just another regulator in the machinery of
61. life? Ann. Bot. (Lond.) 96: 1-8. Plieth, C., and Trewavas, A.J. (2002). Reorientation of seedlings in the earth's gravitational field induces cytosolic calcium transients. Plant Physiol. 129: 786-796.
62. Sack, F.D. (1991). Plant gravity sensing. Int. Rev. Cytol. 127: 193-252.
63. Sack, F.D. (1997). Plastids and gravitropic sensing. Planta 203: S63-S68.
64. Sack, F.D., and Kiss, J.Z. (1989). Root cap structure in wild type and in a starchless mutant of Arabidopsis. Am. J. Bot. 76: 454-464.
65. Sack, F.D., Suyemoto, M.M., and Leopold, A.C. (1985). Amyloplast sedimentation kinetics in gravistimulated maize roots. Planta 165: 295-300.
66. Sack, F.D., Suyemoto, M.M., and Leopold, A.C. (1986). Amyloplast sedimentation and organelle saltation in living corn columella cells. Am. J. Bot. 73: 1692-1698.
67. Saito, C., Morita, M.T., Kato, T., and Tasaka, M. (2005). Amyloplasts and vacuolar membrane dynamics in the living gravireceptive cell of the Arabidosis inflorescence stem. Plant Cell 17: 548-558.
68. Scott, A.C., and Allen, N.S. (1999). Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol. 121: 1291-1298.
69. 2+ pump in the endoplasmic reticulum of the Lepidium root be the trigger for rapid changes in membrane potential after gravistimulation? J. Plant Physiol. 114: 195-200.
70. Sievers, A., Buchen, B., Volkmann, D., and Hejnowicz, Z. (1991). Role of the cytoskeleton in gravity perception. In The Cytoskeletal Basis of Plant Growth and Form, C.W. Lloyd, ed (London: Academic Press), pp. 169-182.
71. Sievers, A., and Volkmann, D. (1972). Verursacht differentieller Druck der Amyloplasten auf ein komplexes Endomembransystem die Geo- perzeption in Wurzeln? Planta (Berl.) 102: 160-172.
72. Sinclair, W., and Trewavas, A.J. (1997). Calcium in gravitropism. A re- examination. Planta 203: S85-S90.
73. Smith, J.D., Todd, P., and Staehelin, L.A. (1997). Modulation of statolith mass and grouping in white clover (Trifolium repens) grown in 1-g, microgravity and on the clinostat. Plant J. 12: 1361-1373.
74. Sukharev, S.I., Blount, P., Martinac, B., Blattner, F.R., and Kung, C. (1994). A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 368: 265-268.
75. Toyota, M., Furuichi, T., Tatsumi, H., and Sokabe, M. (2008). Cyto-plasmic calcium increases in response to changes in the gravity vector in hypocotyls and petioles of Arabidopsis seedlings. Plant Physiol. 146: 505-514.
76. 2+ pump inhibitor, thapsigargin, inhibits root gravitropism in Arabidopsis thali-ana. Biol. Res. 39: 289-296.
77. Verwey, E.J.W., and Overbeek, J.T.G. (1948). Theory of the Stability of Lyophobic Colloids. (Amsterdam: Elsevier).
78. Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow. (Princeton, NJ: Princeton University Press).
79. Vogel, S. (2003). Comparative Biomechanics: Life's Physical World. (Princeton, NJ: Princeton University Press).
80. Volkmann, D., and Sievers, A. (1979). Graviperception in multicellular organs. In Encyclopedia of Plant Physiology, New Series, Physiology of Movements, W. Haupt and M.E. Feinleib, eds (Berlin: Springer-Verlag), pp. 573-600.
81. Yamamoto, K., and Kiss, J.Z. (2002). Disruption of the actin cytoskel-eton results in the promotion of gravitropism in inflorescence stems and hypocotyls of Arabidopsis. Plant Physiol. 128: 669-681.
82. Yang, T., and Poovaiah, B.W. (2003). Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci. 10: 505-512. Yoder, T.L., Zheng, H.-Q., Todd, P., and Staehelin, L.A. (2001). Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiol. 125: 1045-1060.
83. Yoshimura, H., Tada, T., and Iida, H. (2004). Subcellular localization and oligomeric structure of the yeast putative stretch-activated Ca2+ channel component Mid1. Exp. Cell Res. 293: 185-195.
84. Zhang, W., Fan, L.-M., and Wu, W.-H. (2007). Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol. 143: 1140-1151.
85. Zheng, H.-Q., and Staehelin, L.A. (2001). Nodal ER, a novel form of ER found exclusively in gravity-sensing columella cells. Plant Physiol. 125: 252-265.