Plant Molecular Biology

, Volume 26, Issue 4, pp 1139–1153

Molecular analysis of the myosin gene family in Arabidopsis thaliana

  • Mark Kinkema
  • Haiyang Wang
  • John Schiefelbein
Research Article

Abstract

Myosin is believed to act as the molecular motor for many actin-based motility processes in eukaryotes. It is becoming apparent that a single species may possess multiple myosin isoforms, and at least seven distinct classes of myosin have been identified from studies of animals, fungi, and protozoans. The complexity of the myosin heavy-chain gene family in higher plants was investigated by isolating and characterizing myosin genomic and cDNA clones from Arabidopsis thaliana. Six myosin-like genes were identified from three polymerase chain reaction (PCR) products (PCR1, PCR11, PCR43) and three cDNA clones (ATM2, MYA2, MYA3). Sequence comparisons of the deduced head domains suggest that these myosins are members of two major classes. Analysis of the overall structure of the ATM2 and MYA2 myosins shows that they are similar to the previously-identified ATM1 and MYA1 myosins, respectively. The MYA3 appears to possess a novel tail domain, with five IQ repeats, a six-member imperfect repeat, and a segment of unique sequence. Northern blot analyses indicate that some of the Arabidopsis myosin genes are preferentially expressed in different plant organs. Combined with previous studies, these results show that the Arabidopsis genome contains at least eight myosin-like genes representing two distinct classes.

Key words

Arabidopsis thaliana actin-binding protein cytoplasmic streaming intracellular motility IQ motif molecular motor myosin genes 

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References

  1. 1.
    Benton WD, Davis RW: Screening lambda-gt recombinant clones by hybridization to single plaques in situ. Science 196: 180–182 (1977).PubMedGoogle Scholar
  2. 2.
    Chapman ER, Au D, Alexander KA, Nicholson TA, Storm DR: Characterization of the calmodulin binding domain of neuromodulin. J Biol Chem 266: 207–213 (1991).PubMedGoogle Scholar
  3. 3.
    Cheney RE, Mooseker MS: Unconventional myosins. Curr Opin Cell Biol 4: 27–35 (1992).CrossRefPubMedGoogle Scholar
  4. 4.
    Cheney RE, Riley MA, Mooseker MS: A phylogenetic analysis of the myosin superfamily. Cell Motil Cytoskel 24: 215–223 (1993).Google Scholar
  5. 5.
    Corpet F: Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16: 10881–10890 (1988).PubMedGoogle Scholar
  6. 6.
    Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).PubMedGoogle Scholar
  7. 7.
    Espreafico EM, Cheney RE, Matteoli M, Nascimento AAC, De Camilli PV, Larson RE, Mooseker MS: Primary structure and cellular localization of chicken brain myosin V (p190), an unconventional myosin with calmodulin light chains. J Cell Biol 119: 1541–1557 (1992).CrossRefPubMedGoogle Scholar
  8. 8.
    Garcia AE, Coudrier E, Carboni J, Anderson J, Vandekerckhove MS: Partial deduced sequence of the 110-kDa calmodulin complex of the avian intestinal microvillus shows that this mechanoenzyme is a member of the myosin-I family. J Cell Biol 109: 2895–2903 (1989).CrossRefPubMedGoogle Scholar
  9. 9.
    George EL, Ober MB, Emerson CP: Functional domains of the Drosophila melanogaster muscle myosin heavy-chain gene are encoded by alternatively spliced exons. Mol Cell Biol 9: 2957–2974 (1989).PubMedGoogle Scholar
  10. 10.
    Grolig F, Williamson RE, Parke J, Miller C, Anderton BH: Myosin and Ca2+-sensitive streaming in the alga Chara: detection of two polypeptides reacting with a monoclonal anti-myosin and their localization in the streaming endoplasm. Eur J Cell Biol 47: 22–31 (1988).PubMedGoogle Scholar
  11. 11.
    Haarer BK, Petzold A, Lillie SH, Brown SS: Identification of MYO4, a second class V myosin gene in yeast. J Cell Sci 107: 1055–1064 (1994).PubMedGoogle Scholar
  12. 12.
    Halsall DJ, Hammer JA: A second isoform of chicken brush border myosin I contains a 29 residue inserted sequence that binds to calmodulin. FEBS Lett 267: 126–130 (1990).CrossRefPubMedGoogle Scholar
  13. 13.
    Harrington WF, Rodgers ME: Myosin. Annu Rev Biochem 53: 35–73 (1984).CrossRefPubMedGoogle Scholar
  14. 14.
    Heslop-Harrison J, Heslop-Harrison Y: Myosin associated with the surface of organelles, vegetative nuclei and generative cells in angiosperm pollen grains and tubes. J Cell Sci 94: 319–325 (1989).Google Scholar
  15. 15.
    Higgins DG, Bleasby AJ, Fuchs R: Clustal V, improved software for multiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).PubMedGoogle Scholar
  16. 16.
    Horowitz JA, Hammer JA: A new Acanthamoeba myosin heavy chain. J Biol Chem 265: 20646–20652 (1990).PubMedGoogle Scholar
  17. 17.
    Huang WM, Reed-Fourquet L, Wu E, Wu JY: Molecular cloning and amino acid sequence of brain I-glutamate decarboxylase. Proc Natl Acad Sci USA 87: 8491–8495 (1990).PubMedGoogle Scholar
  18. 18.
    Johnston GC, Prendergast JA, Singer RA: The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J Cell Biol 113: 539–551 (1991).CrossRefPubMedGoogle Scholar
  19. 19.
    Jung G, Saxe CL, Kimmel AR, Hammer JA: Dictyostelium discoideum contains a gene encoding a myosin-I heavy chain. Proc Natl Acad Sci USA 86: 6186–6190 (1989).PubMedGoogle Scholar
  20. 20.
    Kachar B, Reese TS: The mechanism of cytoplasmic streaming in characean algal cells: sliding of endoplasmic reticulum along actin filaments. J Cell Biol 106: 1545–1552 (1988).CrossRefPubMedGoogle Scholar
  21. 21.
    Kellerman KA, Miller KG: An unconventional myosin heavy chain gene from Drosophila melanogaster. J Cell Biol 119: 823–834 (1992).CrossRefPubMedGoogle Scholar
  22. 22.
    Kiehart DP: Molecular genetic dissection of myosin heavy chain function. Cell 60: 347–350 (1990).CrossRefPubMedGoogle Scholar
  23. 23.
    Kinkema M, Schiefelbein J: A myosin from a higher plant has structural similarities to class V myosins. J Mol Biol 239: 591–597 (1994).PubMedGoogle Scholar
  24. 24.
    Knight A, Kendrick-Jones J: A myosin-like protein from a higher plant. J Mol Biol 231: 148–154 (1993).PubMedGoogle Scholar
  25. 25.
    Kohno T, Shimmen T: Accelerated sliding of pollen tube organelles along Characean actin bundles regulated by Ca2+. J Cell Biol 106: 1539–1543 (1988).PubMedGoogle Scholar
  26. 26.
    Kohno T, Chaen S, Shimmen T: Characterization of the translocator associated with pollen tube organelles. Protoplasma 154: 179–183 (1990).Google Scholar
  27. 27.
    Kohno T, Okagaki T, Kohama K, Shimmen T: Pollen tube extract supports the movement of actin filaments in vitro. Protoplasma 161: 75–77 (1991).Google Scholar
  28. 28.
    Korn ED, Hammer JA: Myosins of nonmuscle cells. Annu Rev Biophys Biophys Chem 17: 23–45 (1988).CrossRefPubMedGoogle Scholar
  29. 29.
    Kuroda K: Cytoplasmic streaming in plant cells. Int Rev Cytol 121: 267–307 (1990).Google Scholar
  30. 30.
    La Claire JW: Actin cytoskeleton in intact and wounded coenocytic green algae. Planta 177: 47–57 (1989).Google Scholar
  31. 31.
    Lloyd CW, Pearce KJ, Ridge RW, Rawlins DJ, Shaw PJ: Microtubules are involved in the coupled migration of the nucleus with the tip of legume root hairs, but F-actin is necessary for basipetal migration. Cell Motil Cytoskel 8: 27–36 (1987).Google Scholar
  32. 32.
    Lupas A, VanDyke M, Stock J: Predicting coiled coils from protein sequences. Science 252: 1162–1164 (1991).PubMedGoogle Scholar
  33. 33.
    Ma Y, Yen L: Actin and myosin in pea tendrils. Plant Physiol 89: 586–589 (1989).Google Scholar
  34. 34.
    Menzel D, Schliwa M: Motility in the siphonous green alga Bryopsis II. Chloroplast movement requires organized arrays of both microtubules and actin filaments. Eur J Cell Biol 40: 286–295 (1986).PubMedGoogle Scholar
  35. 35.
    Mercer JA, Seperack PK, Strobel MC, Copeland NG, Jenkins NA: Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349: 709–713 (1991).CrossRefPubMedGoogle Scholar
  36. 36.
    Moepps B, Conrad S, Schraudolf H: PCR-dependent amplification and sequence characterization of partial cDNAs encoding myosin-like proteins in Anemia phyllitidis (L.) Sw. and Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21: 1077–1083 (1993).CrossRefPubMedGoogle Scholar
  37. 37.
    Molina MI, Kropp KE, Gulick J, Robbins J: The sequence of an embryonic myosin heavy chain gene and isolation of its corresponding cDNA. J Biol Chem 262: 6478–6488 (1987).PubMedGoogle Scholar
  38. 38.
    Mollenhauer HH, Moore DJ: Cytochalasin B, but not colchicine, inhibits migration of secretory vesicles in root tips of maize. Protoplasma 87: 39–48 (1976).PubMedGoogle Scholar
  39. 39.
    Montell C, Rubin G: The Drosophila ninaC locus encodes two photoreceptor cell specific proteins with domains homologous to protein kinases and the myosin heavy chain head. Cell 52: 757–762 (1988).CrossRefPubMedGoogle Scholar
  40. 40.
    Mooseker M: A multitude of myosins. Curr Biol 3: 245–248 (1993).CrossRefPubMedGoogle Scholar
  41. 41.
    Parke J, Miller C, Anderton BH: Higher plant myosin heavy-chain identified using a monoclonal antibody. Eur J Cell Biol 41: 9–13 (1986).Google Scholar
  42. 42.
    Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444–2448 (1988).PubMedGoogle Scholar
  43. 43.
    Pollard T, Doberstein S, Zot H: Myosin-I. Annu Rev Physiol 53: 653–681 (1991).CrossRefPubMedGoogle Scholar
  44. 44.
    Qiao L, Grolig F, Jablonsky PP, Williamson RE: Myosin heavy chains: detection by immunoblotting in higher plants and localization by immunofluorescence in the alga Chara. Cell Biol Int Rep 13, 107–117 (1989).Google Scholar
  45. 45.
    Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).Google Scholar
  46. 46.
    Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).PubMedGoogle Scholar
  47. 47.
    Schiefelbein JW, Somerville C: Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243 (1990).CrossRefPubMedGoogle Scholar
  48. 48.
    Schnepf E: Cellular polarity. Annu Rev Plant Physiol 37: 23–47 (1986).Google Scholar
  49. 49.
    Seagull RW, Heath IB: The differential effects of cytochalasin B on microfilament populations and cytoplasmic streaming. Protoplasma 103: 231–240 (1980).Google Scholar
  50. 50.
    Staiger CJ, Schliwa M: Actin localization and function in higher plants. Protoplasma 141: 1–12 (1987).Google Scholar
  51. 51.
    Steer MW: Role of actin in tip growth. In: Heath IB (ed) Tip Growth in Plant and Fungal Cells, pp. 119–145. Academic Press, San Diego (1991).Google Scholar
  52. 52.
    Sweeney FP, Watts FZ, Pocklington MJ, Orr E: The MYO1 gene from Saccharomyces cerevisiae: its complete nucleotide sequence. Nucl Acids Res 18: 7147 (1990).PubMedGoogle Scholar
  53. 53.
    Tang X, Hepler PK, Scordilis SP: Immunochemical and immunocytochemical identification of a myosin chain polypeptide in Nicotiana pollen tubes. J Cell Sci 92: 569–574 (1989).PubMedGoogle Scholar
  54. 54.
    Titus MA, Warrick HM, Spudich JA: Multiple actinbased motor genes in Dictyostelium. Cell Regul 1: 55–63 (1989).PubMedGoogle Scholar
  55. 55.
    Vahey M, Titus M, Trautwein R, Scordilis S: Tomato actin and myosin: contractile proteins from a higher land plant. Cell Motil 2: 131–148 (1982).Google Scholar
  56. 56.
    Warrick HM, Spudich J: Myosin structure and function in cell motility. Annu Rev Cell Biol 3: 379–421 (1987).PubMedGoogle Scholar
  57. 57.
    Yokota E, Shimmen T: Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma 177: 153–162 (1994).Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Mark Kinkema
    • 1
  • Haiyang Wang
    • 1
  • John Schiefelbein
    • 1
  1. 1.Department of BiologyUniversity of MichiganAnn ArborUSA

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