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Role of abscisic acid and ethylene in the control of water transport-driving forces in germinating petunia male gametophyte

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Abstract

Data on ABA involvement in osmoregulation of in vitro germinating petunia (Petunia hybrida L.) male gametophyte were obtained. Two potential targets of ABA action in a pollen tube (PT) are identified. These are represented by (1) plasma membrane (PM) H+-ATPase, electrogenic proton pump participating in PM polarization, and (2) Ca-dependent K+-channels localized in the same membrane. It was established that a stimulatory effect of ABA on electrogenic activity of H+-ATPase is mediated by the increase in free Ca2+ level in the cytosol of a PT and reactive oxygen species (ROS) generation. Based on the results obtained on the role of K+ ions in the hormonal control of water transport-driving forces in a PT, the hypothesis suggesting that ABA stimulated pollen grains (PGs) germinating and PT growth by activating K+-channels was put forward. The revealed ABA-induced shift in cytoplasmic pH (pHc) is suggested to be involved in a cascade of the events of the progamic phase of fertilization, including pH-dependent K+-channels functioning. It was established that ABA abolishes the inhibitory effects of ethylene receptors blocker, 1-methylcyclopropene (1-MCP), and blockers of ACC and ABA synthesis (aminooxyacetic acid, AOA, and fluridone, respectively) on PT germination and growth, whereas ethrel blocks the inhibitory effect of fluridone on PT growth. In stigmas pretreated with ABA and AOA before pollination, this phytohormone was found to suppress inhibitory effect of AOA on ACC synthesis in the pollen-pistil system. All these findings, taken together, led us to the conclusion that ABA is involved in petunia male gametophyte osmoregulation interacting with ethylene at the level of ACC synthesis in the progamic phase of fertilization.

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Abbreviations

ABA:

abscisic acid

ACC:

1-aminocyclopropane-1-carboxylic acid

AOA:

aminooxyacetic acid

ACC:

1-amino cyclopropane-1-carbonic acid

1-MCP:

1-methylcyclopropene

PGs:

pollen grains

PTs:

pollen tubes

ROS:

reactive oxygen species

References

  1. Kovaleva, L. and Zakharova, E., Hormonal status of the pollen–pistil system at the progamic phase of fertilization after compatible and incompatible pollination in Petunia hybrida L., Sex. Plant Reprod., 2003, vol. 16, pp. 191–196.

    Article  CAS  Google Scholar 

  2. Kovaleva, L.V., Dobrovolskaya, A., Voronkov, A., and Rakitin, V., Ethylene is involved in the control of male gametophyte development and germination in Petunia, J. Plant Growth Regul., 2011, vol. 30, pp. 64–73.

    Article  CAS  Google Scholar 

  3. Verma, V., Ravindran, P., and Kumar, P.P., Plant hormone- mediated regulation of stress responses, BMC Plant Biol., 2016, vol. 16, p. 86. doi 10.1186/s12870-016- 0771

    Article  PubMed  PubMed Central  Google Scholar 

  4. Rowe, J.H., Topping, J.F., Liu, J., and Lindsey, K., Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin, New Phytol., 2016, vol. 211, pp. 225–239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hopper, D.W., Ghan, R., Schlauch, K.A., and Cramer, G.R., Transcriptomic network analyses of leaf dehydration responses identify highly connected ABA and ethylene signaling hubs in three grapevine species differing in drought tolerance, BMC Plant Biol., 2016, vol. 16, no. 1, p. 118. doi 10.1186/s12870-016-0804-6

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kovaleva, L.V., Zakharova, E.V., Voronkov, A.S., and Timofeeva, G.V., Ethylene and auxin interactions during hormonal regulation at the progamic phase of fertilization in germinating Petunia male gametophyte, Russ. J. Dev. Biol., 2016, vol. 48, pp. 122–129.

    Article  Google Scholar 

  7. Voronkov, A.S., Andreev, I.M., Timofeeva, G.V., and Kovaleva, L.V., Electrogenic activity of plasma membrane H+-ATPase in germinating male gametophyte of Petunia and its stimulation by exogenous auxin: mediatory role of calcium and reactive oxygen species, Russ. J. Plant Physiol., 2010, vol. 57, pp. 401–407.

    Article  CAS  Google Scholar 

  8. Kovaleva, L.V., Voronkov, A.S., and Zakharova, E.V., Role of auxin and cytokinin in the regulation of the actin cytoskeleton in the in vitro germinating male gametophyte of Petunia, Russ. J. Plant Physiol., 2015, vol. 62, pp. 179–186.

    Article  CAS  Google Scholar 

  9. Skorobogatova, I.V., Zakharova, E.V., Karsunkina, N.P., Kurapov, P.B., Sorkina, G.L., and Kislin, E.N., Phytohormones content changes in barley seedlings during ontogenesis and in the presence of growth stimulators, Agrokhimiya, 1999, no. 8, pp. 49–53.

    Google Scholar 

  10. Rakitin, V.Yu. and Rakitin, L.Yu., Determination of gas exchange and the content of ethylene, carbon dioxide, and oxygen in the tissues of higher plants, Sov. Plant Physiol., 1986, vol. 33, pp. 403–413.

    CAS  Google Scholar 

  11. Lizada, M.C. and Yang, S., A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid, Anal. Biochem., 1979, vol. 100, pp. 140–145.

    Article  CAS  PubMed  Google Scholar 

  12. The Molecular Probes Handbook: A Guide to Fluorescent Probes and Labeling Technologies, Johnson, I. and Spence, M.T.Z., Eds., Life Technology, 2010.

  13. Becker, D., Geiger, D., Dunkel, M., Roller, A., Bertl, A., Latz, A., Carpaneto, A., Dietrich, P., Roelfsema, M.R., Voelker, C., Schmidt, D., Mueller-Roeber, B., Czempinski, K., and Hedrich, R., Attpk4, an Arabidopsis tandem-pore K+ channel, poised to control the pollen membrane voltage in a pH- and Ca2+-dependent manner, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 15621–15626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Rehman, S. and Yun, S.J., Developmental regulation of K+ accumulation in pollen, anthers, and papillae: are anther dehiscence, papillae hydration, and pollen swelling leading to pollination and fertilization in barley (Hordeum vulgare L.) regulated by changes in K+ concentration? J. Exp. Bot., 2006, vol. 57, pp. 1315–1321.

    Article  CAS  PubMed  Google Scholar 

  15. Matveeva, N.P., Voitsek, O.O., Andreyuk, D.S., and Ermakov, I.P., Role of H+-ATPase and alternative oxidase in regulation of intracellular pH at different stages of development of the tobacco male gametophyte, Russ. J. Dev. Biol., 2002, vol. 33, no. 6, pp. 355–361.

    Article  CAS  Google Scholar 

  16. Andreev, I.M., Timofeeva, G.V., Minkina, Yu.V., and Kovaleva, L.V., Effects of exogenous phytohormones on intracellular pH of Petunia hybrida pollen grains, Russ. J. Plant Physiol., 2007, vol. 54, pp. 626–632.

    Article  CAS  Google Scholar 

  17. Firon, N., Nepi, M., and Pacini, E., Water status and associated processes mark critical stages in pollen development and functioning, Ann. Bot., 2012, vol. 109, pp. 1201–1214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Potocky, M., Jones, M.A., Bezvoda, R., Smirnoff, N., and Zarsky, V., Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth, New Phytol., 2007, vol. 174, pp. 742–751.

    Article  CAS  PubMed  Google Scholar 

  19. Bright, J., Hiscock, S.J., James, P.E., and Hancock, J.T., Pollen generates nitric oxide and nitrite: a possible link to pollen-induced allergic responses, Plant Physiol. Biochem., 2009, vol. 47, pp. 49–55.

    Article  CAS  PubMed  Google Scholar 

  20. Lang, V., Pertl-Obermeyer, H., Safiarian, M.J., and Obermeyer, G., Pump up the volume—a central role for the plasma membrane H(+) pump in pollen germination and tube growth, Protoplasma, 2014, vol. 251, pp. 477–488.

    Article  CAS  PubMed  Google Scholar 

  21. Hsu, S.W., Cheng, C.L., Tzen, T.C.J., and Wang, C.S., Rop GTPase and its target Cdc42/Rac-interactive binding motif-containing protein genes respond to desiccation during pollen maturation, Plant Cell Physiol., 2010, vol. 51, pp. 1197–1209.

    Article  CAS  PubMed  Google Scholar 

  22. Nibau, C., Tao, L., and Levasseur, K., The Arabidopsis small GTPase AtRAC7/ROP9 is a modulator of auxin and abscisic acid signaling, J. Exp. Bot., 2013, vol. 64, pp. 3425–3437.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Li, B., Feng, Z., Xie, M., Sun, M., Zhao, Y., Liang, L., Liu, G., Zhang, J., and Jig, W., Modulation of the rootsourced ABA signal along its way to the shoot in Vitis riparia x Vitis labrusca under water deficit, J. Exp. Bot., 2011, vol. 62, pp. 1731–1741.

    Article  CAS  PubMed  Google Scholar 

  24. Zhao, L.N., Shen, L.K., Zhang, W.Z., Zhang, W., Wang, Y., and Wu, W.H., Ca2+-dependent protein kinase 11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tube, Plant Cell, 2013, vol. 25, pp. 649–661.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Wilkins, K.A., Bosch, M., Haque, T., Teng, N., Poulter, N.S., and Franklin-Tong, V.E., Self-incompatibility- induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol, Plant Physiol., 2015, vol. 167, pp. 766–779.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ross, J.J., Weston, D.E., Davidson, S.E., and Reid, J.B., Plant hormone interactions: how complex are they? Physiol. Plant., 2011, vol. 141, pp. 299–309.

    Article  CAS  PubMed  Google Scholar 

  27. Mou, W., Li, D., Bu, J., Jiang, Y., Khan, Z.U., Luo, Z., Mao, L., and Ying, T., Comprehensive analysis of ABA effects on ethylene biosynthesis and signaling during tomato fruit ripening, PLoS One, 2016, vol. 11, no. 4, p. e0154072. doi 10.1371/journal.pone.0154072

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wang, N.N., Shin, M.C., and Li, N., The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtAC7 induced by hormones and stresses, J. Exp. Bot., 2005, vol. 56, pp. 909–920.

    Article  CAS  PubMed  Google Scholar 

  29. Van de Poel, B. and van der Straeten, D., 1-aminocyclopropane- 1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front. Plant Sci., 2014, vol. 5, p. 640. doi 2014.00640 doi 10.3389/pls

    PubMed  PubMed Central  Google Scholar 

  30. Himschoot, E., Beeckman, T., Friml, J., and Vanneste, S., Calcium is an organizer of cell polarity in plants, Biochem. Biophys. Acta, 2015, vol. 1853, no. 9, pp. 2168–2172. doi 10.1016/j.bbamcr.2015.02.017

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Moscow, 127276, Russia

    L. V. Kovaleva, A. S. Voronkov, G. V. Timofeeva & I. M. Andreev

  2. Russian State Agrarian University–Moscow Timiryazev Agricultural Academy, Moscow, 127550, Russia

    E. V. Zakharova

Authors
  1. L. V. Kovaleva
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  2. E. V. Zakharova
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  3. A. S. Voronkov
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  4. G. V. Timofeeva
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  5. I. M. Andreev
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Correspondence to L. V. Kovaleva.

Additional information

Original Russian Text © L.V. Kovaleva, E.V. Zakharova, A.S. Voronkov, G.V. Timofeeva, I.M. Andreev, 2017, published in Fiziologiya Rastenii, 2017, Vol. 64, No. 5, pp. 389–400.

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Kovaleva, L.V., Zakharova, E.V., Voronkov, A.S. et al. Role of abscisic acid and ethylene in the control of water transport-driving forces in germinating petunia male gametophyte. Russ J Plant Physiol 64, 782–793 (2017). https://doi.org/10.1134/S1021443717040070

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  • DOI: https://doi.org/10.1134/S1021443717040070

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