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Molecular analysis of the myosin gene family in Arabidopsis thaliana

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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.

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References

  1. Benton WD, Davis RW: Screening lambda-gt recombinant clones by hybridization to single plaques in situ. Science 196: 180–182 (1977).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  3. Cheney RE, Mooseker MS: Unconventional myosins. Curr Opin Cell Biol 4: 27–35 (1992).

    Article  PubMed  Google Scholar 

  4. Cheney RE, Riley MA, Mooseker MS: A phylogenetic analysis of the myosin superfamily. Cell Motil Cytoskel 24: 215–223 (1993).

    Google Scholar 

  5. Corpet F: Multiple sequence alignment with hierarchical clustering. Nucl Acids Res 16: 10881–10890 (1988).

    PubMed  Google Scholar 

  6. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programs for the VAX. Nucl Acids Res 12: 387–395 (1984).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  13. Harrington WF, Rodgers ME: Myosin. Annu Rev Biochem 53: 35–73 (1984).

    Article  PubMed  Google Scholar 

  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. Higgins DG, Bleasby AJ, Fuchs R: Clustal V, improved software for multiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).

    PubMed  Google Scholar 

  16. Horowitz JA, Hammer JA: A new Acanthamoeba myosin heavy chain. J Biol Chem 265: 20646–20652 (1990).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  21. Kellerman KA, Miller KG: An unconventional myosin heavy chain gene from Drosophila melanogaster. J Cell Biol 119: 823–834 (1992).

    Article  PubMed  Google Scholar 

  22. Kiehart DP: Molecular genetic dissection of myosin heavy chain function. Cell 60: 347–350 (1990).

    Article  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  24. Knight A, Kendrick-Jones J: A myosin-like protein from a higher plant. J Mol Biol 231: 148–154 (1993).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  26. Kohno T, Chaen S, Shimmen T: Characterization of the translocator associated with pollen tube organelles. Protoplasma 154: 179–183 (1990).

    Google Scholar 

  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. Korn ED, Hammer JA: Myosins of nonmuscle cells. Annu Rev Biophys Biophys Chem 17: 23–45 (1988).

    Article  PubMed  Google Scholar 

  29. Kuroda K: Cytoplasmic streaming in plant cells. Int Rev Cytol 121: 267–307 (1990).

    Google Scholar 

  30. La Claire JW: Actin cytoskeleton in intact and wounded coenocytic green algae. Planta 177: 47–57 (1989).

    Google Scholar 

  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. Lupas A, VanDyke M, Stock J: Predicting coiled coils from protein sequences. Science 252: 1162–1164 (1991).

    PubMed  Google Scholar 

  33. Ma Y, Yen L: Actin and myosin in pea tendrils. Plant Physiol 89: 586–589 (1989).

    Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  40. Mooseker M: A multitude of myosins. Curr Biol 3: 245–248 (1993).

    Article  PubMed  Google Scholar 

  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. Pearson WR, Lipman DJ: Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444–2448 (1988).

    PubMed  Google Scholar 

  43. Pollard T, Doberstein S, Zot H: Myosin-I. Annu Rev Physiol 53: 653–681 (1991).

    Article  PubMed  Google Scholar 

  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. 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. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    PubMed  Google Scholar 

  47. Schiefelbein JW, Somerville C: Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2: 235–243 (1990).

    Article  PubMed  Google Scholar 

  48. Schnepf E: Cellular polarity. Annu Rev Plant Physiol 37: 23–47 (1986).

    Google Scholar 

  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. Staiger CJ, Schliwa M: Actin localization and function in higher plants. Protoplasma 141: 1–12 (1987).

    Google Scholar 

  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. Sweeney FP, Watts FZ, Pocklington MJ, Orr E: The MYO1 gene from Saccharomyces cerevisiae: its complete nucleotide sequence. Nucl Acids Res 18: 7147 (1990).

    PubMed  Google Scholar 

  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).

    PubMed  Google Scholar 

  54. Titus MA, Warrick HM, Spudich JA: Multiple actinbased motor genes in Dictyostelium. Cell Regul 1: 55–63 (1989).

    PubMed  Google Scholar 

  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. Warrick HM, Spudich J: Myosin structure and function in cell motility. Annu Rev Cell Biol 3: 379–421 (1987).

    PubMed  Google Scholar 

  57. Yokota E, Shimmen T: Isolation and characterization of plant myosin from pollen tubes of lily. Protoplasma 177: 153–162 (1994).

    Google Scholar 

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  1. Department of Biology, University of Michigan, 830 North University Avenue, 48 109, Ann Arbor, MI, USA

    Mark Kinkema, Haiyang Wang & John Schiefelbein

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  1. Mark Kinkema
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  2. Haiyang Wang
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  3. John Schiefelbein
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Kinkema, M., Wang, H. & Schiefelbein, J. Molecular analysis of the myosin gene family in Arabidopsis thaliana . Plant Mol Biol 26, 1139–1153 (1994). https://doi.org/10.1007/BF00040695

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