Advertisement

Journal of Plant Research

, Volume 126, Issue 5, pp 589–596 | Cite as

Resistance of plants to gravitational force

  • Kouichi SogaEmail author
Current Topics in Plant Research

Abstract

Developing resistance to gravitational force is a critical response for terrestrial plants to survive under 1 × g conditions. We have termed this reaction “gravity resistance” and have analyzed its nature and mechanisms using hypergravity conditions produced by centrifugation and microgravity conditions in space. Our results indicate that plants develop a short and thick body and increase cell wall rigidity to resist gravitational force. The modification of body shape is brought about by the rapid reorientation of cortical microtubules that is caused by the action of microtubule-associated proteins in response to the magnitude of the gravitational force. The modification of cell wall rigidity is regulated by changes in cell wall metabolism that are caused by alterations in the levels of cell wall enzymes and in the pH of apoplastic fluid (cell wall fluid). Mechanoreceptors on the plasma membrane may be involved in the perception of the gravitational force. In this review, we discuss methods for altering gravitational conditions and describe the nature and mechanisms of gravity resistance in plants.

Keywords

Cell wall rigidity Gravity resistance Growth anisotropy Hypergravity Mechanoreceptor Microgravity 

Notes

Acknowledgments

The author is grateful to numerous colleagues and collaborators. Thanks are also due to Professor T. Hoson and Dr. K. Wakabayashi of Osaka City University for critical reading of the manuscript and valuable suggestions. The present study was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Grant for Ground-based Research for Space Utilization from Japan Space Forum, and by Sasakawa Scientific Research Grant from the Japan Science Society.

References

  1. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215:150–171PubMedCrossRefGoogle Scholar
  2. Bouquin T, Mattsson O, Naested H, Foster R, Mundy J (2003) The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J Cell Sci 116:791–801PubMedCrossRefGoogle Scholar
  3. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–827PubMedGoogle Scholar
  4. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30PubMedCrossRefGoogle Scholar
  5. Caspar T, Huber SC, Somerville CR (1985) Alterations in growth, photosynthesis, and respiration in starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79:11–17PubMedCrossRefGoogle Scholar
  6. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861PubMedCrossRefGoogle Scholar
  7. Erhardt M, Stoppin-Mellet V, Campagne S, Canaday J, Mutterer J, Fabian T, Sauter M, Muller T, Peter C, Lambert AM, Schmit AC (2002) The plant Spc98p homologue colocalizes with γ-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115:2423–2431PubMedGoogle Scholar
  8. Fitzelle KJ, Kiss JZ (2001) Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. J Exp Bot 52:265–275PubMedCrossRefGoogle Scholar
  9. Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430PubMedCrossRefGoogle Scholar
  10. Hamada T (2007) Microtubule-associated proteins in higher plants. J Plant Res 120:79–98PubMedCrossRefGoogle Scholar
  11. Hayashi T (1989) Xyloglucans in the primary cell wall. Annu Rev Plant Physiol Plant Mol Biol 40:139–168CrossRefGoogle Scholar
  12. Hayashi T, Kaida R (2011) Functions of xyloglucan in plant cells. Mol Plant 4:17–24PubMedCrossRefGoogle Scholar
  13. Hoson T (1993) Regulation of polysaccharide breakdown during auxin-induced cell wall loosening. J Plant Res 106:369–381CrossRefGoogle Scholar
  14. Hoson T, Soga K (2003) New aspects of gravity responses in plant cells. Int Rev Cytol 229:209–244PubMedCrossRefGoogle Scholar
  15. Hoson T, Nishitani K, Miyamoto K, Ueda J, Kamisaka S, Yamamoto R, Masuda Y (1996) Effects of hypergravity on growth and cell wall properties of cress hypocotyls. J Exp Bot 47:513–517PubMedCrossRefGoogle Scholar
  16. Hoson T, Soga K, Mori R, Saiki M, Wakabayashi K, Kamisaka S, Kamigaichi S, Aizawa S, Yoshizaki I, Mukai C, Shimazu T, Fukui K, Yamashita M (1999) Morphogenesis of rice and Arabidopsis seedlings in space. J Plant Res 112:477–486PubMedCrossRefGoogle Scholar
  17. Hoson T, Soga K, Mori R, Saiki M, Nakamura Y, Wakabayashi K, Kamisaka S (2002) Stimulation of elongation growth and cell wall loosening in rice coleoptiles under microgravity conditions in space. Plant Cell Physiol 43:1067–1071PubMedCrossRefGoogle Scholar
  18. Hoson T, Saito Y, Soga K, Wakabayashi K (2005) Signal perception, transduction, and response in gravity resistance. another graviresponse in plants. Adv Space Res 36:1196–1202CrossRefGoogle Scholar
  19. Jiang CJ, Sonobe S (1993) Identification and preliminary characterization of a 65 kDa higher-plant microtubule-associated protein. J Cell Sci 105:891–901Google Scholar
  20. Kasahara H, Shiwa M, Takeuchi Y, Yamada M (1995) Effects of hypergravity on elongation growth in radish and cucumber hypocotyls. J Plant Res 108:59–64PubMedCrossRefGoogle Scholar
  21. Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39CrossRefGoogle Scholar
  22. Kiss JZ (2000) Mechanisms of the early phases of plant gravitropism. Crit Rev Plant Sci 19:551–557PubMedCrossRefGoogle Scholar
  23. Kotake T, Hirata N, Kitazawa K, Soga K, Tsumuraya Y (2009) Arabinogalactan-proteins in the evolution of gravity resistance in land plants. Biol Sci Space 23:143–149CrossRefGoogle Scholar
  24. Kraft TFB, van Loon JJWA, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211:415–422PubMedCrossRefGoogle Scholar
  25. Masuda Y (1990) Auxin-induced cell elongation and cell wall changes. Bot Mag Tokyo 103:345–370CrossRefGoogle Scholar
  26. Masuda Y, Kamisaka S, Hoson T (1998) Growth behavior of rice coleoptiles. J Plant Physiol 152:180–188CrossRefGoogle Scholar
  27. Matsumoto S, Kumasaki S, Soga K, Wakabayashi K, Hashimoto T, Hoson T (2010) Gravity-induced modifications to development in hypocotyls of Arabidopsis tubulin mutants. Plant Physiol 152:918–926PubMedCrossRefGoogle Scholar
  28. Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720PubMedCrossRefGoogle Scholar
  29. Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol 7:961–968PubMedCrossRefGoogle Scholar
  30. Nakabayashi I, Karahara I, Tamaoki D, Masuda K, Wakasugi T, Yamada K, Soga K, Hoson T, Kamisaka S (2006) Hypergravity stimulus enhances primary xylem development and decreases mechanical properties of secondary cell walls in inflorescence stems of Arabidopsis thaliana. Ann Bot 97:1083–1090PubMedCrossRefGoogle Scholar
  31. Nakamura M, Ehrhardt DW, Hashimoto T (2010) Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat Cell Biol 12:1064–1070PubMedCrossRefGoogle Scholar
  32. Ooume K, Inoue Y, Soga K, Wakabayashi K, Fujii S, Yamamoto R, Hoson T (2009) Cellular basis of growth suppression by submergence in azuki bean epicotyls. Ann Bot 103:325–332PubMedCrossRefGoogle Scholar
  33. Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, Evrard JL, Schmit AC, Guerche P, Bouchez D (2006) γ-Tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18:1412–1425PubMedCrossRefGoogle Scholar
  34. Sawano M, Shimmen T, Sonobe S (2000) Possible involvement of 65 kDa MAP in elongation growth of azuki bean epicotyls. Plant Cell Physiol 41:968–976PubMedCrossRefGoogle Scholar
  35. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
  36. Sedbrook JC (2004) MAPs in plant cells: delineating microtubule growth dynamics and organization. Curr Opin Plant Biol 7:632–640PubMedCrossRefGoogle Scholar
  37. Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Ann Rev Plant Physiol Plant Mol Biol 45:527–544CrossRefGoogle Scholar
  38. Sievers A, Heyder-Caspers L (1983) The effect of centrifugal accelerations on the polarity of statocytes and on the graviperception of cress roots. Planta 157:64–70PubMedCrossRefGoogle Scholar
  39. Sievers A, Buchen B, Volkmann D, Hejnowicz Z (1991) Role of the cytoskeleton in gravity perception. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 169–182Google Scholar
  40. Skagen EB, Iversen TH (1999) Simulated weightlessness and hyper-g results in opposite effects on the regeneration of the cortical microtubule array in protoplasts from Brassica napus hypocotyls. Physiol Plant 106:318–325PubMedCrossRefGoogle Scholar
  41. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Ann Rev Cell Develop Biol 21:271–295CrossRefGoogle Scholar
  42. Soga K (2010) Gravity resistance in plants. Biol Sci Space 24:129–134CrossRefGoogle Scholar
  43. Soga K, Wakabayashi K, Hoson T, Kamisaka S (1999a) Hypergravity increases the molecular size of xyloglucans by decreasing xyloglucan-degrading activity in azuki bean epicotyls. Plant Cell Physiol 40:581–585PubMedCrossRefGoogle Scholar
  44. Soga K, Harada K, Wakabayashi K, Hoson T, Kamisaka S (1999b) Increased molecular mass of hemicellulosic polysaccharides is involved in growth inhibition of maize coleoptiles and mesocotyls under hypergravity conditions. J Plant Res 112:273–278PubMedCrossRefGoogle Scholar
  45. Soga K, Wakabayashi K, Hoson T, Kamisaka S (2000a) Changes in the apoplastic pH are involved in regulation of xyloglucan breakdown of azuki bean epicotyls under hypergravity conditions. Plant Cell Physiol 41:509–514PubMedCrossRefGoogle Scholar
  46. Soga K, Wakabayashi K, Hoson T, Kamisaka S (2000b) Hypergravity-induced increase in the apoplastic pH and its possible involvement in suppression of β-glucan breakdown in maize seedlings. Aust J Plant Physiol 27:967–972PubMedGoogle Scholar
  47. Soga K, Wakabayashi K, Hoson T, Kamisaka S (2001) Gravitational force regulates elongation growth of Arabidopsis hypocotyls by modifying xyloglucan metabolism. Adv Space Res 27:1011–1016PubMedCrossRefGoogle Scholar
  48. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2002) Stimulation of elongation growth and xyloglucan breakdown in Arabidopsis hypocotyls under microgravity conditions in space. Planta 215:1040–1046PubMedCrossRefGoogle Scholar
  49. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2003) Growth restoration in azuki bean and maize seedlings by removal of hypergravity stimuli. Adv Space Res 31:2269–2274PubMedCrossRefGoogle Scholar
  50. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2004) Graviperception in growth inhibition of plant shoots under hypergravity conditions produced by centrifugation is independent of that in gravitropism and may involve mechanoreceptors. Planta 218:1054–1061PubMedCrossRefGoogle Scholar
  51. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2005a) Mechanoreceptors rather than sedimentable amyloplasts perceive the gravity signal in hypergravity-induced inhibition of root growth in azuki bean. Funct Plant Biol 32:175–179PubMedCrossRefGoogle Scholar
  52. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2005b) Hypergravity inhibits elongation growth of azuki bean epicotyls independently of the direction of stimuli. Adv Space Res 36:1269–1276CrossRefGoogle Scholar
  53. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2006) Hypergravity induces reorientation of cortical microtubules and modifies growth anisotropy in azuki bean epicotyls. Planta 224:1485–1494PubMedCrossRefGoogle Scholar
  54. Soga K, Wakabayashi K, Kamisaka S, Hoson T (2007a) Effects of hypergravity on expression of XTH genes in azuki bean epicotyls. Physiol Plant 131:332–340PubMedGoogle Scholar
  55. Soga K, Arai K, Wakabayashi K, Kamisaka S, Hoson T (2007b) Modifications of xyloglucan metabolism in azuki bean epicotyls under hypergravity conditions. Adv Space Res 39:1204–1209CrossRefGoogle Scholar
  56. Soga K, Kotake T, Wakabayashi K, Kamisaka S, Hoson T (2008) Transient increase in the transcript levels of ϒ-tubulin complex genes during reorientation of cortical microtubules by gravity in azuki bean (Vigna angularis) epicotyls. J Plant Res 121:493–498PubMedCrossRefGoogle Scholar
  57. Soga K, Kotake T, Wakabayashi K, Kamisaka S, Hoson T (2009) The transcript level of katanin gene is increased transiently in response to changes in gravitational conditions in azuki bean epicotyls. Biol Sci Space 23:23–28CrossRefGoogle Scholar
  58. Soga K, Yamaguchi A, Kotake T, Wakabayashi K, Kamisaka S, Hoson T (2010) Transient increase in the levels of γ-tubulin complex and katanin are responsible for reorientation by ethylene and hypergravity of cortical microtubules. Plant Signal Behav 5:1480–1482PubMedCrossRefGoogle Scholar
  59. Soga K, Kotake T, Wakabayashi K, Hoson T (2012) Changes in the transcript levels of microtubule-associated protein MAP65-1 during reorientation of cortical microtubules in azuki bean epicotyls. Acta Physiol Plant 34:533–540CrossRefGoogle Scholar
  60. Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657CrossRefGoogle Scholar
  61. Tasaka M, Kato T, Fukaki H (2001) Genetic regulation of gravitropism in higher plants. Int Rev Cytol 206:135–154PubMedCrossRefGoogle Scholar
  62. Volkmann D, Baluška F (2006) Gravity: one of the driving forces for evolution. Protoplasma 229:143–148PubMedCrossRefGoogle Scholar
  63. Wakabayashi K, Soga K, Kamisaka S, Hoson T (2005) Increase in the level of arabinoxylan-hydroxycinnamate network in cell walls of wheat coleoptiles grown under continuous hypergravity conditions. Physiol Plant 125:127–134CrossRefGoogle Scholar
  64. Wakabayashi K, Soga K, Hoson T (2009a) Modification of cell wall architecture in gramineous plants under altered gravity conditions. Biol Sci Space 23:137–142CrossRefGoogle Scholar
  65. Wakabayashi K, Nakano S, Soga K, Kamisaka S, Hoson T (2009b) Cell wall-bound peroxidase activity and lignin formation in azuki bean epicotyls grown under hypergravity conditions. J Plant Physiol 166:947–954PubMedCrossRefGoogle Scholar
  66. Walczak CE, Shaw SL (2010) A MAP for bundling microtubules. Cell 142:364–367PubMedCrossRefGoogle Scholar
  67. Waldron KW, Brett CT (1990) Effects of extreme acceleration on the germination, growth and cell wall composition of pea epicotyls. J Exp Bot 41:71–77CrossRefGoogle Scholar
  68. Wayne R, Staves MP (1997) A down-to earth model of gravisensing. Gravi Space Biol Bull 10:57–64Google Scholar
  69. Wymer CL, Wymer SA, Cosgrove DJ, Cyr RJ (1996) Plant cell responds to external forces and the response requires intact microtubules. Plant Physiol 110:425–430PubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2013

Authors and Affiliations

  1. 1.Department of Biology and Geosciences, Graduate School of ScienceOsaka City UniversityOsakaJapan

Personalised recommendations