Abstract
Gravitropism, the directed plant growth with respect to the gravity vector, is regulated by auxin and its polar transport system, several secondary messengers, and by the cytoskeleton. Recently we have shown that the actin cytoskeleton in the root transition zone of Arabidopsis thaliana (L.) Heynh was rearranged after gravistimulation (rotation by 90°): the fraction of axially aligned microfilaments decreased and the fraction of oblique and transversally-oriented microfilaments increased. In the present research we have studied the effect of ethylene and inhibitors of its synthesis on actin cytoskeleton rearrangement during the gravitropic response. Application of the ethylene releasing substance ethephon to A. thaliana seedlings led to the disassembly of actin microfilaments as well as their broad angle distribution in cells of the root transition zone. This actin rearrangement was escaped by treatment with the ethylene synthesis inhibitor aminoethoxyvinylglycine (AVG). Another negative regulator of ethylene, salicylic acid, was shown to disturb actin microfilament rearrangement as well. We conclude that ethylene is essential for the process of actin cytoskeleton rearrangement in root cortex cells during the gravitropic bending response.
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Abbreviations
- AVG:
-
L-a-(2-Aminoethoxyvinyl)glycine
- ACC:
-
1-aminocyclopropane-1-carboxylic acid
- fABD2:
-
second actinbinding domain of fimbrin 1
- GFP:
-
green fluorescent protein
References
Sato, E.M., Hijazi, H., M.J. Bennett, M.J., Vissenberg, K. and Swarup, R., New insights into the dynamics of root gravitropic signalling, J. Exp. Bot., 2015, vol. 66, p. 2155–2165.
Medvedev, S.S., Mechanisms and physiological role of polarity in plants, Russ. J. Plant Physiol., 2012, vol. 59, pp. 502–514.
Neljubow, D., Über die horizontale Nutation der Stengel von Pisum sativum und einiger anderer Pflanzen, Beih. Bot. Centralbl., 1901, vol. 10, pp. 128–138.
Morita, M.T., Directional gravity sensing in gravitropism, Annu. Rev. Plant Biol., 2010, vol. 61, pp. 705–720.
Blancaflor, E.B., Regulation of plant gravity sensing and signaling by the actin cytoskeleton, Am. J. Bot., 2013, vol. 100, pp. 143–152.
Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mähönen, A., Prasad, K., Blilou, I., Geldner, N., Xu, J., Uemura, T., Chory, J., Ueda, T., Nakano, A., Scheres, B., and Friml, J., Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions, Nature, 2008, vol. 456, pp. 962–966.
Rahman, A., Takahashi, M., Shibasaki, K., Wu, S., Inaba, T., Tsurumi, S., and Baskin, T.I., Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells, Plant Cell, 2010, vol. 22, pp. 1762–1776.
Pozhvanov, G.A., Suslov, D.V., and Medvedev, S.S., Actin cytoskeleton rearrangements during the gravitropic response of Arabidopsis roots, Tsitologiya, 2013, vol. 55, pp. 28–35.
Nick, P. Han, M.-J., and An, G., Auxin stimulates its own transport by shaping actin filaments, Plant Physiol., 2009, vol. 151, pp. 155–167.
Zhao, Y., Zhao, S., Mao, T., Qu, X., Cao, W., Zhang, L., Zhang, W., He, L., Li, S., Ren, S., Zhao, J., Zhu, G., Huang, S., Ye, K., Ming, Y.M., et al., The plant-specific actin binding protein SCAB1 stabilizes actin filaments and regulates stomatal movement in Arabidopsis, Plant Cell, 2011, vol. 23, pp. 2314–2330.
Sheahan, M.B., Staiger, C.J., Rose, R.J., and McCurdy, D.W., A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells, Plant Physiol., 2004, vol. 136, pp. 3968–3978.
Jacques, E., Buytaert, J., Wells, D.M., Lewandowski, M., Bennett, M.J., Dirckx, J., Verbelen, J.P., and Vissenberg, K., MicroFilament Analyzer, an image analysis tool for quantifying fibrillar orientation, reveals changes in microtubule organization during gravitropism, Plant J., 2013, vol. 74, pp. 1045–1058.
Baluška, F., Barlow, P.W., Baskin, T.I., Chen, R., Feldman, L., Forde, B.G., Geisler, M., Jernstedt, J., Menzel, D., Muday, G.K., and Murphy, A., What is apical and what is basal in plant root development? Trends Plant Sci., 2005, vol. 10, pp. 409–411.
Wheeler, R.M. and Salisbury, F.B., Gravitropism in higher plant shoots. I. A role for ethylene, Plant Physiol., 1981, vol. 67, pp. 686–690.
Kramer, S., Piotrowski, M., Èhnemann, F.K., and Edelmann, H.G., Physiological and biochemical characterization of ethylene-generated gravicompetence in primary shoots of coleoptile-less gravi-incompetent rye seedlings, J. Exp. Bot., 2003, vol. 54, pp. 2723–2732.
Edelmann, H.G. and Roth, U., Gravitropic plant growth regulation and ethylene: an unsought cardinal coordinate for a disused model, Protoplasma, 2006, vol. 229, pp. 183–191.
Harrison, M.A. and Pickard, B.G., Evaluation of ethylene as a mediator of gravitropism by tomato hypocotyls, Plant Physiol., 1986, vol. 80, pp. 592–595.
Leslie, C.A. and Romani, R.J., Inhibition of ethylene biosynthesis by salicylic acid, Plant Physiol., 1988, vol. 88, pp. 833–837.
Medvedev, S.S. and Markova, I.V., Participation of salicylic acid in plant gravitropism, Dokl. Akad. Nauk SSSR, 1991, vol. 316, pp. 1014–1016.
Lee, J.H., Jin, E.S., and Kim, W.T., Inhibition of auxin-induced ethylene production by salicylic acid in mung bean hypocotyls, J. Plant Biol., 1999, vol. 42, pp. 1–7.
Matoušková, J., Janda, M., Fišer, R., Šašek, V., Kocourková, D., Burketová, L., Dušková, J., Martinec, J., and Valentová, O., Changes in actin dynamics are involved in salicylic acid signaling pathway, Plant Sci., 2014, vol. 223, pp. 36–44.
Vicente, M.R. and Plasencia, J., Salicylic acid beyond defence: its role in plant growth and development, J. Exp. Bot., 2011, vol. 62, pp. 3321–3338.
Durango, D., Pulgarin, N., Echeverri, F., Escobar, G., and Quiñones, W., Effect of salicylic acid and structurally related compounds in the accumulation of phytoalexins in cotyledons of common bean (Phaseolus vulgaris L.) cultivars, Molecules, 2013, vol. 9, pp. 10609–10628.
Madlung, A., Behringer, F.J., and Lomax, T.L., Ethylene plays multiple nonprimary roles in modulating the gravitropic response in tomato, Plant Physiol., 1999, vol. 120, pp. 897–906.
Gupta, A., Singh, M., Jones, A.M., and Laxmi, A., Hypocotyl directional growth in Arabidopsis: a complex trait, Plant Physiol., 2012, vol. 159, pp. 1463–1476.
Yu, Y.B. and Yang, S.F., Auxin-induced ethylene production and its inhibition by aminoethoxyvinyiglycine and cobaltion, Plant Physiol., 1979, vol. 64, pp. 1074–1077.
Chang, S.C., Kim, Y.S.K., Lee, J.Y., Kaufman, P.B., Kirakosyan, A., Yun, H.S., Kim, T.W., Kim, S.Y., Cho, M.H., Lee, J.S., and Kim, S.K., Brassinolide interacts with auxin and ethylene in the root gravitropic response of maize (Zea mays), Physiol. Plant., 2004, vol. 121, pp. 666–673.
Muday, G.K., Brady, S.R., Argueso, C., Deruère, J., Kieber, J.J., and DeLong, A., RCN1-regulated phosphatase activity and EIN2 modulate hypocotyl gravitropism by a mechanism that does not require ethylene signaling, Plant Physiol., 2006, vol. 141, pp. 1617–1629.
Huang, S.J., Chang, C.L., Wang, P.H., Tsai, M.C., Hsu, P.H., and Chang, F., A type III ACC synthase, ACS7, is involved in root gravitropism in Arabidopsis thaliana, J. Exp. Bot., 2013, vol. 64, pp. 4343–4360.
Verbelen, J.P., Cnodder, T.D., Le, J., Vissenberg, K., and Baluška, F., The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone, Plant Signal. Behav., 2006, vol. 1, pp. 296–304.
Baluška, F., Mancuso, S., Volkmann, D., and Barlow, P.W., Root apex transition zone: a signallingresponse nexus in the root, Trends Plant Sci., 2010, vol. 15, pp. 402–408.
Friml, J., Wiśniewska, J., Benková, E., Mendgen, K., and Palme, K., Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis, Nature, 2002, vol. 415, pp. 806–809.
De Cnodder, T., Vissenberg, K., van der Straeten, D., and Verbelen, J.P., Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor 1-aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions, New Phytol., 2005, vol. 168, pp. 541–550.
Kandasamy, M.K., Deal, R.B., McKinney, E.C., and Meagher, R.B., Plant actin-related proteins, Trends Plant Sci., 2004, vol. 9, pp. 196–202.
Baluška, F., Volkmann, D., and Barlow, B.W., A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications, J. Plant Growth Regul., 2001, vol. 20, pp. 170–181.
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Published in Russian in Fiziologiya Rastenii, 2016, Vol. 63, No. 5, pp. 624–635.
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Pozhvanov, G.A., Gobova, A.E., Bankin, M.P. et al. Ethylene is involved in the actin cytoskeleton rearrangement during the root gravitropic response of Arabidopsis thaliana . Russ J Plant Physiol 63, 587–596 (2016). https://doi.org/10.1134/S1021443716050095
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DOI: https://doi.org/10.1134/S1021443716050095