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Protoplasma

, Volume 201, Issue 1–2, pp 92–100 | Cite as

Mechanotransduction molecules in the plant gravisensory response: Amyloplast/statolith membranes contain a β1 integrin-like protein

  • Timothy M. Lynch
  • Philip M. Lintilhac
  • David Domozych
Article

Summary

It has been hypothesized that the sedimentation of amyloplasts within root cap cells is the primary event in the plant gravisensory-signal transduction cascade. Statolith sedimentation, with its ability to generate weighty mechanical signals, is a legitimate means for organisms to discriminate the direction of the gravity vector. However, it has been demonstrated that starchless mutants with reduced statolith densities maintain some ability to sense gravity, calling into question the statolith sedimentation hypothesis. Here we report on the presence of a β1 integrin-like protein localized inside amyloplasts of tobacco NT-1 suspension culture, callus cells, and whole-root caps. Two different antibodies to the β1 integrin, one to the cytoplasmic domain and one to the extracellular domain, localize in the vicinity of the starch grains within amyloplasts of NT-1. Biochemical data reveals a 110-kDa protein immunoprecipitated from membrane fractions of NT-1 suspension culture indicating size homology to known β1 integrin in animals. This study provides the first direct evidence for the possibility of integrin-mediated signal transduction in the perception of gravity by higher plants. An integrin-mediated pathway, initiated by starch grain sedimentation within the amyloplast, may provide the signal amplification necessary to explain the gravitropic response in starch-depleted cultivars.

Keywords

Amyloplast Gravity Integrin Mechanotransduction Statolith Tobacco 

Abbreviations

BA

6-benzylaminopurine

ETOH

ethyl alcohol

LP

liquid propane

LR

London Resin

PBST

phosphate-buffered saline with Tween

TEM

transmission electron microscopy

OSM

optical-sectioning microscopy

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References

  1. Barlow PW, Parker JS, Butler R, Brian P (1993) Gravitropism of primary roots ofZea mays L. at different displacement angles. Ann Bot 71: 383–388Google Scholar
  2. Buttrose MS (1962) Ultrastructure of the developing wheat endosperm. Aust J Biol Sci 16: 305–316Google Scholar
  3. Gens SJ, Reuzeau C, Dolittle KW, McNally JG, Pickard BG (1996) Covisualization by computational optical-sectioning microscopy of integrin and associated proteins at the cell membrane of living onion protoplasts. Protoplasma 194: 215–230PubMedGoogle Scholar
  4. Haberlandt G (1884) Physiological plant anatomy, 4th edn, reprint 1965. Today and Tomorrow's Book Agency, New DelhiGoogle Scholar
  5. — (1900) Über die Perzeption des geotropischen Reizes. Ber Dtsch Bot Ges 18: 261–272Google Scholar
  6. Horwitz AF (1997) Integrins and health. Sci Am 276: 68–75Google Scholar
  7. Hush JM, Overall RL (1991) Electrical and mechanical fields orient cortical microtubules in higher plant tissues. Cell Biol Int Rep 15: 551–560Google Scholar
  8. Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11–25PubMedGoogle Scholar
  9. Ingber DE, Dike L, Hansen L, Karp S, Liley H, Manitos A, McNamee H, Mooney D, Plopper G, Sims J, Wang N (1994) Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration, and tissue pattern during morphogenesis. Int Rev Cytol 150: 173–224PubMedGoogle Scholar
  10. Iversen TH, Rommelhoff A (1978) The starch statolith hypothesis and the interaction of amyloplasts and endoplasmic reticulum in root gravitropism. J Exp Bot 29: 1319–1328Google Scholar
  11. Katembe WJ, Swatzell L, Makaroff CA, Kiss JZ (1996) Immunolocalization of integrin-like protein inArabidopsis andChara. Physiol Plant 99: 7–14Google Scholar
  12. Lu Y, Hidaka H, Feldman LJ (1996) Characterization of a calcium/calmodulin-dependent protein kinase homologue from maize roots showing light-regulated gravitropism. Planta 199: 18–24PubMedGoogle Scholar
  13. Lynch TM, Lintilhac PM (1997) Mechanical signals in plant development: a new method for single cell studies. Dev Biol 181: 246–256PubMedGoogle Scholar
  14. Marcantonio E, Hynes RO (1988) Antibodies to the conserved cytoplasmic domain of the integrin β1 subunit react with proteins in vertebrates, invertebrates, and fungi. J Cell Biol 106: 1765–1772PubMedGoogle Scholar
  15. Melkonian B, Burchet M, Kreimer G, Latzko E (1990) Binding and possible function of calcium in the chloroplast. Curr Top Plant Biochem Physiol 9: 38–46Google Scholar
  16. Mina MG, Goldsworthy A (1992) Electrical polarization of tobacco cells by Ca2+ ion channels. J Exp Bot 43: 449–454Google Scholar
  17. Nemec B (1900) Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18: 241–245Google Scholar
  18. Pickard BG, Ding JP (1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control centre? Aust J Plant Physiol 20: 439–459PubMedGoogle Scholar
  19. —, Thimann KV (1966) Geotropic response of wheat coleoptiles in absence of amyloplast starch. J Gen Physiol 49: 1068–1086Google Scholar
  20. Schindler M, Meiners S, Cheresh DA (1989) RGD-dependent linkage between plant cell wall and plasma membrane: consequences for growth. J Cell Biol 108: 1955–1965PubMedGoogle Scholar
  21. Shankar G, Davison I, Helfrich MP, Mason WT, Horton MA (1993) Integrin receptor mediated mobilization of intranuclear calcium in rat osteoclasts. J Cell Sci 105: 61–68PubMedGoogle Scholar
  22. Wayne R, Staves MP, Leopold AC (1992) The contribution of the extracellular matrix to gravisensing in characean cells. J Cell Sci 101: 611–623PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1998

Authors and Affiliations

  • Timothy M. Lynch
    • 1
  • Philip M. Lintilhac
    • 1
  • David Domozych
    • 2
  1. 1.Botany DepartmentUniversity of VermontBurlingtonUSA
  2. 2.Department of BiologySkidmore CollegeSaratoga Springs

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