Russian Journal of Plant Physiology

, Volume 61, Issue 5, pp 598–607 | Cite as

Cytophysiological characteristics of Arabidopsis thaliana cultivated cells with disable perception of ethylene signal by the ETR1 receptor

  • A. A. Fomenkov
  • A. V. Nosov
  • V. Yu. Rakitin
  • A. S. Mamaeva
  • G. V. Novikova
Research Papers

Abstract

Contradictory data about ethylene influence on cell growth and division prompted us to investigate cytophysiological characteristics of suspension cultures of Arabidopsis thaliana of wild type Col-0 and ert1-1 mutant carrying a point mutation in the site of ethylene binding by the ETR1 receptor. Some cytophysiological characteristics of the etr1-1 cultivated cells differed from those of Col-0: the growth rate of mutant cells was less and cell sizes were smaller, the culture was committed to the formation of tracheary elements (TE), had a pronounced modal class of nuclei (54%) with the amount of DNA 8C and a tendency to expand the ploidy toward 32C. Despite the absence of ethylene perception by the ETR1 receptor, the cell culture of mutant responded to treatment with ethylene by growth acceleration, an increase in cell viability and in the number of cells in the S-phase of the cell cycle. The inhibitor of ethylene binding to receptors, 1-methylcyclopropene, suppressed growth and viability of the cells of both genotypes. In the etr1-1 cell culture, the inhibitor reduced the number of S-phase nuclei and activated TE formation. All data obtained indicate that ethylene perception and transduction of ethylene signal are required for the maintenance of cell viability and active in vitro growth. It is supposed that the functional activity of the ETR1 receptor is necessary for optimal cell expansion, whereas other receptors are responsible for cell proliferation.

Keywords

Arabidopsis thaliana etr1-1 ethylene 1-methylcyclopropene cell culture growth S-phase tracheary elements DNA cytophotometry 

Abbreviations

2C

DNA amount in the diploid chromosome set

EdU

5-ethynyl-2′-deoxiuridine

1-MCP

1-methylcyclopropene

PBS

phosphate buffered saline

TE

tracheary elements

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Abeles, F.B., Morgan, P.W., and Salveit, M.E., Ethylene in Plant Biology, San Diego: Academic, 1992.Google Scholar
  2. 2.
    Grierson, D., 100 years of ethylene — a personal view, Annu. Plant Rev., 2012, vol. 44, pp. 1–17.Google Scholar
  3. 3.
    Ji, Y. and Guo, H., From endoplasmic reticulum (ER) to nucleus: EIN2 bridges the gap in ethylene signaling, Mol. Plant, 2013, vol. 6, pp. 11–14.PubMedCrossRefGoogle Scholar
  4. 4.
    Bleecker, A.B., Estelle, M.A., Somerville, C., and Kende, H., Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana, Science, 1988, vol. 241, pp. 1086–1089.PubMedCrossRefGoogle Scholar
  5. 5.
    Chang, C., Kwok, S.F., Bleecker, A.B., and Meyerowitz, E.M., Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators, Science, 1993, vol. 262, pp. 539–545.PubMedCrossRefGoogle Scholar
  6. 6.
    Hua, J., Chang, C., Sun, Q., and Meyerowitz, E.M., Ethylene insensitivity conferred by the Arabidopsis ERS gene, Science, 1995, vol. 269, pp. 1712–1714.PubMedCrossRefGoogle Scholar
  7. 7.
    Hua, J., Sakai, H., Nourizadeh, S., Chen, Q.G., Bleecker, A.B., Ecker, J.R., and Meyerowitz, E.M., EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis, Plant Cell, 1998, vol. 10, pp. 1321–1332.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Sakai, H., Hua, J., Chen, Q.G., Chang, C., Medrano, L.J., Bleecker, A.B., and Meyerowitz, E.M., ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis, Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 5812–5817.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 9.
    Hall, A.E., Chen, Q.G., Findell, J.L., Schaller, G.E., and Bleecker, A.B., The relationship between ethylene binding and dominant insensitivity conferred by mutant forms of the ETR1 ethylene receptor, Plant Physiol., 1999, vol. 121, pp. 291–299.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Binder, B.M., Chang, C., and Schaller, G.E., Perception of ethylene by plants — ethylene receptors, Annu. Plant Rev., 2012, vol. 44, pp. 117–145.Google Scholar
  11. 11.
    Hall, A.E. and Bleecker, A.B., Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent, Plant Cell, 2003, vol. 15, pp. 2032–2041.PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Qu, X., Hall, B.P., Gao, Z., and Schaller, G.E., A strong constitutive ethylene-response phenotype conferred on Arabidopsis plants containing null mutations in the ethylene receptor ETR1 and ERS1, BMC Plant Biol., 2007, vol. 7, no. 3, doi: 10.1186/1471-2229-7-3Google Scholar
  13. 13.
    Moshkov, I.E., Novikova, G.V., Hall, M.A., and George, E.F., Plant growth regulators III: Gibberellins, ethylene, abscisic acid, their analogues and inhibitors; miscellaneous compounds, Plant Propagation by Tissue Culture, vol. 1, The Background, George, E.F., Hall, M.A., and de Klerk, G.J., Eds., Dordrecht: Springer, 2008, pp. 227–281.Google Scholar
  14. 14.
    Schenk, R.U. and Hildebrandt, A.C., Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures, Can. J. Bot., 1972, vol. 50, pp. 199–204.CrossRefGoogle Scholar
  15. 15.
    Greilhuber, J., Intraspecific variation in genome size in angiosperms: identifying its existence, Ann. Bot., 2005, vol. 95, pp. 91–98.PubMedCrossRefGoogle Scholar
  16. 16.
    Zoriniants, S.E., Nosov, A.V., Monforte-Gonzalez, M., Mendes-Zeel, M., and Loyola-Vargas, V.M., Variation of nuclear DNA content during somatic embryogenesis and plant regeneration of Coffea arabica L. using cytophotometry, Plant Sci., 2003, vol. 164, pp. 141–146.CrossRefGoogle Scholar
  17. 17.
    Kotogány, E., Dudits, D., Horváth, G.V., and Ayaydin, F., A rapid and robust assay for detection of S-phase cell cycle progression in plant cells and tissues by using ethynyl deoxyuridine, Plant Methods, 2010, vol. 6, no. 5, doi: 10.1186/1746-4811-6-5Google Scholar
  18. 18.
    Rakitin, V.Yu. and Rakitin, L.Yu., Determination of gas exchange and ethylene, carbon dioxide, and oxygen contents in plant tissues, Sov. Plant Physiol., 1986, vol. 33, pp. 403–413.Google Scholar
  19. 19.
    Sisler, E.C. and Serek, M., Inhibitors of ethylene responses in plants at the receptor level: recent developments, Physiol. Plant., 1997, vol. 100, pp. 577–582.CrossRefGoogle Scholar
  20. 20.
    Stepanchenko, N.S., Fomenkov, A.A., Moshkov, I.E., Rakitin, V.Yu., Novikova, G.V., and Nosov, A.V., Phytohormone interplay controls proliferation of in vitro cultivated cells of Arabidopsis thaliana ethylene-insensitive mutants, Dokl. Biol. Sci., 2012, vol. 442, pp. 46–49.PubMedCrossRefGoogle Scholar
  21. 21.
    Barow, M. and Meister, A., Endopolyploidy in seed plant is differently correlated to systematic, organ, life strategy and genome size, Plant Cell Environ., 2003, vol. 26, pp. 571–584.CrossRefGoogle Scholar
  22. 22.
    Dan, H., Imaseki, H., Wasteneys, G.O., and Kazama, H., Ethylene stimulates endoreduplication but inhibits cytokinesis in cucumber hypocotyl epidermis, Plant Physiol., 2003, vol. 133, pp. 1726–1731.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Saibo, N.J.M., Vriezen, W.H., Beemster, G.T.S., and van der Straeten, D., Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins, Plant J., 2003, vol. 33, pp. 989–1000.PubMedCrossRefGoogle Scholar
  24. 24.
    Pierik, R., Tholen, D., Poorter, H., Visser, E.J.W., and Voesenek, L.A.C.J., The Janus face of ethylene: growth inhibition and stimulation, Trends Plant Sci., 2006, vol. 11, pp. 176–183.PubMedCrossRefGoogle Scholar
  25. 25.
    Polko, J.K., Voesenek, L.A.C.J., Peeters, A.J.M., and Pierik, R., Petiole hyponasty: an ethylene-driven, adaptive response to changes in the environment, AoB Plants, 2011: plr031, doi 10.1093/aobpla/plr031Google Scholar
  26. 26.
    Apelbaum, A. and Burg, S.P., Effect of ethylene on celldivision and deoxyribonucleic acid synthesis in Pisum sativum, Plant Physiol., 1972, vol. 50, pp. 117–124.PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Love, J., Björklund, S., Vahala, J., Hertzberg, M., Kangasjärvi, J., and Sundberg, B., Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus, Proc. Natl. Acad. Sci. USA, 2009, vol. 106, pp. 5984–5989.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Sugimoto-Shirasu, K. and Roberts, K., “Big it up”: endoreduplication and cell-size control in plants, Curr. Opin. Plant Biol., 2003, vol. 6, pp. 544–553.PubMedCrossRefGoogle Scholar
  29. 29.
    Jackson, M.B., Ethylene-promoted elongation: an adaptation to submergence stress, Ann. Bot., 2008, vol. 101, pp. 229–248.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Shakeel, S.N., Wang, X., Binder, B.M., and Schaller, G.E., Mechanisms of signal transduction by ethylene: overlapping and non-overlapping signaling roles in a receptor family, AoB Plants, 2013, vol. 5: plt010, doi: 10.1093/aobpla/plt010PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • A. A. Fomenkov
    • 1
  • A. V. Nosov
    • 1
  • V. Yu. Rakitin
    • 1
  • A. S. Mamaeva
    • 1
  • G. V. Novikova
    • 1
  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

Personalised recommendations