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Molecular identification and characterization of the Arabidopsis AtADF1, AtADF5 and AtADF6 genes

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Abstract

Actin depolymerizing factor (ADF) is a key regulator of the organization of the actin cytoskeleton during various cellular activities. We found that ADF genes in Arabidopsis form a large family consisting of at least nine members, four of which were cloned and sequenced in this study. Comparison of genomic and cDNA sequences showed that the AtADF1, AtADF5, and AtADF6 genes all contain two introns at conserved positions. Analysis of transgenic Arabidopsis plants carrying promoter-GUS fusion constructs revealed that AtADF1 and AtADF6 are expressed in the vascular tissues of all organs, whereas expression of AtADF5 is restricted to the root tip meristem. GFP-AtADF1, GFP-AtADF5, and GFP-AtADF6 fusion proteins were found to bind to actin filaments in vivo, and to reorganize the actin cytoskeleton when transiently expressed in plant cells.

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References

  • Agnew, B.J., Minamide, L.S. and Bamburg, JR. 1995. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J. Biol. Chem. 270: 17582–17587.

    Google Scholar 

  • Aizawa, H., Sutoh, K., Tsubuki, S., Kawashima, S., Ishii, A. and Yahara, I. 1995. Identification, characterization, and intracellu-lar distribution of cofilin in Dictyostelium discoideum. J. Biol. Chem. 270: 10923–10932.

    Google Scholar 

  • Aizawa, H., Sutoh, K. and Yahara, I. 1996. Overexpression of cofilin stimulates bundling of actin filaments, membrane ruffling, and cell movement in Dictyostelium. J. Cell Biol. 132: 335–344.

    Google Scholar 

  • Aizawa, H., Fukui, Y. and Yahara, I. 1997. Live dynamics of Dic-tyostelium cofilin suggests a role in remodeling actin latticework into bundles. J. Cell Sci. 110: 2333–2344.

    Google Scholar 

  • Ayscough, K.R 1998. In vivo functions of actin-binding proteins. Curr. Opin. Cell Biol. 10: 102–111.

    Google Scholar 

  • Barnes, S.A., Nishizawa, N.K., Quaggi, R.B., Whitelam, G.C. and Chua, N.-H. 1996. Far-red light blocks greening of Arabidopsis seedling via a phytochrome A-mediated change in plastid change in plastic development. Plant Cell 8: 601–615.

    Google Scholar 

  • Christensen, H.E.M., Ramachandran, S., Tan, C.T., Surana, U., Dong, C.-H. and Chua, N.-H. 1996. Arabidopsis profilins are functionally similar to yeast profilins: identification of vascular bundle-specific profilin and a pollen-specific profilin.Plant J. 10: 269–279.

    Google Scholar 

  • Carlier, M.F., Santolini, J., Lanrent, V., Melki, R., Didry, D., Hong, Y., Xia, G.-X., Chua N.-H. and Pantolni, D. 1997. Actin de-polymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136: 1307–1322.

    Google Scholar 

  • Carlier, M.F. 1998. Control of actin dynamics. Curr. Opin. Cell Biol. 10: 45–51.

    Google Scholar 

  • Eun, S.-O. and Lee Y. 1997. Actin filaments of guard cells are reor-ganized in response to light and abscisic acid. Plant Physiol. 115: 1491–1498.

    Google Scholar 

  • Fedorov, A.A., Lappalainen, P., Fedorov, E.V., Drubin, D.G. and Almo, S.C. 1997. Structure determination of yeast cofilin. Nature Struct. Biol. 4: 366–369.

    Google Scholar 

  • Goode, B.L., Drubin, D.G. and Lappalainen, P. 1998. Regulation of the cortical actin cytoskeleton in budding yeast by Twinfilin, a ubiquitous actin monomer-sequestering protein. J. Cell Biol. 142: 723–733.

    Google Scholar 

  • Gunsalus, K.C., Bonaccorsi, S., Williams, E., Verni, F., Gatti, M. and Goldberg, M.L. 1995. Mutations in twinstar,aDrosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131: 1243–1259..527

    Google Scholar 

  • Hatanaka, H., Ogura, K., Moriyama, M., Ichikawa, S., Yahara, I. and Inagaki, F. 1996. Tertiary structure of destrin and structural similarity between two actin-regulating protein families. Cell 85: 1047–1055.

    Google Scholar 

  • Hussey, P.J., Yuan, M., Calder, G., Khan, S. and Lioyd, C.W. 1998. Microinjection of pollen-specific actin-depolymerizing factor, ZmADF1, reorients F-actin strands in Tradescantia stamen hair cells. Plant J. 14: 353–357.

    Google Scholar 

  • Huang, S., McDowell, J.M., Weise, M.J. and Meagher, R.B. 1996. The Arabidopsis profilin gene family: evidence for an ancient split between constitutive and pollen-specific profilin genes. Plant Physiol. 111: 115–126.

    Google Scholar 

  • Iida, K., Moriyama, K., Matsumoto, S., Kawasaki, H., Nishida, E. and Yahara, I. 1993. Isolation of a yeast essential gene, COF1, that encodes a homologue of mammalian cofilin, a low-Mr actin-binding and depolymerizing protein. Gene 124: 115–120.

    Google Scholar 

  • Jefferson, R.A. 1987. Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387–405.

    Google Scholar 

  • Johnston, G., Prendergast, J. and Singer, R. 1991. The Saccha-romyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. I. Cell Biol. 113: 539–551.

    Google Scholar 

  • Kim, S.-R., Kim, Y. and An, G. 1993. Molecular cloning and characterization of anther-preferential cDNA encoding a putative actin-depolymerizing factor. Plant Mol. Biol. 21: 39–45.

    Google Scholar 

  • Klahre, U., Friederich, E., Kost, B., Louvard, D. and Chua, N.-H. 1999. The actin binding protein VILLIN is expressed ubiquitously in Arabidopsis. Plant Physiol. 122: 35–47.

    Google Scholar 

  • Kopczak, S.D., Haas, N.A., Hussey, P.J., Silflow, C.D. and Snustad, D.P. 1992. The small genome of Arabidopsis contains at least six expressed alpha-tubulin genes. Plant Cell 4: 539–547.

    Google Scholar 

  • Kost, B., Spielhofer, P. and Chua, N.-H. 1998. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J. 16: 393–401.

    Google Scholar 

  • Kost, B., Mathur, J. and Chua, N.-H. 1999. Cytoskeleton in plant development. Curr. Opin. Plant Biol. 2: 462–470.

    Google Scholar 

  • Kost, B., Spielholfer, P., Mathur, J., Dong, C.-H. and Chua, N.-H. 2000. Non-invasive F-actin visualization in living plant cells using a GFP-mouse talin fusion protein. In: C.J. Staiger, F. Baluska, D. Volkmann and P. Barlow (Eds.) Actin: A Dynamic Framework For Multiple Plant Cell Functions, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 637–659.

    Google Scholar 

  • Lappalainen, P. and Drubin, D.G. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature 388: 78–82.

    Google Scholar 

  • Leonard, S., Gittis, A., Petrella, E., Pollard, T. and Lattman, E. 1997. Crystal structure of the actin-binding protein actophorin from Acanthamoeba. Nature Struct. Biol. 4: 369–373.

    Google Scholar 

  • Lopez, I., Anthony, R.G., Maciver, S.K., Jiang, C.-J., Khan, S,, Weeds, A.G. and Hussey, P.J.1996. Pollen specific expression of maize genes encoding actin depolymerizing factor-like proteins. Proc. Natl. Acad. Sci. USA 93: 7415–7420.

    Google Scholar 

  • Mabuchi, 1.1983. An actin-depolymerizing protein (depactin) from starfish oocytes: properties and interaction with actin. J. Cell Biol. 97: 1612–1621.

    Google Scholar 

  • Maciver, S.K., Pope, B.J., Whytock, S. and Weeds, A.G. 1998. The effect of two actin depolymerizing factors (ADF/cofilins) on actin filament turnover: pH sensitivity of F-actin binding by hu-man ADF, but not of Acanthamoeba actophorin. Eur. J. Biochem. 256: 388–397.

    Google Scholar 

  • Marthur, J., Spielhofer, P., Kost, B. and Chua, N.-H. 1999. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126: 5559–5568.

    Google Scholar 

  • Meagher, R.B., McKinney, E.C. and Kandasmy, M.K. 1999. Iso-variant dynamics expand and buffer the responses of complex systems: the diverse plant actin gene family. Plant Cell 11: 995–1005.

    Google Scholar 

  • Mckinney, E.C. and Meagher, R.B. 1998. Members of the Ara-bidopsis actin gene family are widely dispersed in the genome. Genetics 149: 663–675.

    Google Scholar 

  • McGough, A., Pope, B., Chiu, W. and Weeds, A. 1997. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 13: 771–781.

    Google Scholar 

  • Miller, D.D., Ruijter, N.C.A., Bisseling, T. and Emons, A.M.C. 1998. The role of actin in root hair morphogenesis: studies with lipochito-oligosaccharide as a growth stimulator and cytocha-lasin as an actin perturbing drug. Plant J. 17: 141–154.

    Google Scholar 

  • Moon, A., Janmey, P.A., Loui, K.A. and Drubin, D.G. 1993. Cofilin is an important component of the yeast cortical cytoskeleton. J. Cell Biol. 120: 421–435.

    Google Scholar 

  • Moriyama, K. and Yahara, I. 1999. Two activities of cofilin, severing and accelerating directional depolymerization of actin filaments, are affected differentially by mutations around the actin-binding helix. EMBO J. 18: 6752–6761.

    Google Scholar 

  • Moriyama, K., Iida, K. and Yahara, I. 1996. Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1: 73–86.

    Google Scholar 

  • Nagaoka, R., Abe, H., Kusano, K. and Obinata, T. 1995a. Concentration of cofilin, a small actin-binding protein, at the cleavage furrow during cytokinesis. Cell Motil. Cytoskel. 30: 1–7.

    Google Scholar 

  • Nagaoka, R., Kusano, K.I., Abe, H. and Obinata, T. 1995b. Effects of cofilin on actin filamentous structures in cultured muscle cells. J. Cell Sci. 108: 581–593.

    Google Scholar 

  • Rosenblatt, J., Agnew, B.J., Abe, H., Bamburg, J.R. and Mitchison, T.J. 1997. Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J. Cell Biol. 136: 1323–1332.

    Google Scholar 

  • Rozycka, M., Khan, S., Lopez, I., Greenland, A.J. and Hussey, P.J. 1995. A Zea mays pollen cDNA encoding a putative actin-depolymerizing factor. Plant Physiol. 107: 1011–1012.

    Google Scholar 

  • Sambrook, D.N., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd. ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Smertenko, A.P., Jiang, C.-J., Simmons, N.J., Weeds, A.G., Davies, D.R. and Hussey, P.J. 1998. Ser6 in the maize actin-depolymerizing factor, ZmADF3, is phosphorylated by calcium-stimulated protein kinase and is essential for the control of functional activity. Plant J. 14: 187–193.

    Google Scholar 

  • Staiger, C.J., Gibbon, B.C., Kovar, D.R. and Zonia, L.E. 1997. Profilin and actin-depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci. 2(7): 275–281.

    Google Scholar 

  • Snustad, D.P., Haas, N.A., Kopczak, S.D. and Silflow, C.D. 1992. The small genome of Arabidopsis contains at least nine expressed beta-tubulin genes. Plant Cell 4: 549–556.

    Google Scholar 

  • Szymanski, D.B., Marks, M.D., and Wick, S.M. 1999. Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11: 2331–2347.

    Google Scholar 

  • Valvekens, D., Van Montagu, M. and Lijsebettens, M. 1988. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants using kanamycin selection. Proc. Natl. Acad. Sci. USA 85: 5536–5540.

    Google Scholar 

  • Wang, H., Lockwood, S.K., Hoeltzel, M.F. and Schiefelbein. J.W. 1997. The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Genes Dev. 11: 799–811.

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Plant Cell Biology, Institute of Molecular Agrobiology, National University of Singapore, Singapore , 117604

    Chun-Hai Dong, Benedikt Kost & Guixian Xia

  2. Laboratory of Plant Molecular Biology, Rockefeller University, New York, NY , 10021, USA

    Nam-Hai Chua

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  1. Chun-Hai Dong
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  2. Benedikt Kost
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Dong, CH., Kost, B., Xia, G. et al. Molecular identification and characterization of the Arabidopsis AtADF1, AtADF5 and AtADF6 genes. Plant Mol Biol 45, 517–527 (2001). https://doi.org/10.1023/A:1010687911374

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