Isolation and characterization of the single β-tubulin gene in Phytophthora cinnamomi

LITERATURE CITED

• Amos, L. A., and W. B. Amos. 1991. Molecules of the cytoskeleton. Guilford Press, New York. 253 pp.
   Google Scholar
• Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith and K. Struhl. 1993. Current protocols in molecular biology. Current Protocols, New York.
   Google Scholar
• Barahona, I., H. Soares, L. Cyrne, D. Penque, P. Denoulet and C. Rodrigues-Pousada. 1988. Sequence of one α-and two β-tubulin genes of Tetrahymena pyriformis. J. Molec. Biol. 202: 365–382.
   PubMed Web of Science ®Google Scholar
• Barr, D. J. S. 1981. The phylogenetic and taxonomic implications of flagellar rootlet morphology among zoosporic fungi. BioSystems 14: 359–370.
   PubMed Web of Science ®Google Scholar
• Barr, D. J. S., and P. M. E. Allan. 1985. A comparison of the flagellar apparatus in Phytophthora, Saprolegnia, Thraustochytrium and Rhizidiomyces. Canad. J. Bot. 63: 138–154.
   Google Scholar
• Barr, D. J. S., and P. M. E. Allan, and N. L. Désaulniers. 1990. The flagellar apparatus in the Phytophthora infestans zoospore. Canad. J. Bot. 68: 2112–2118.
   Google Scholar
• Bartnicki-Garcia, S. 1970. Cell wall composition and other biochemical markers in fungal phylogeny. Pp. 81–103. In: Phytochemical phylogeny. Ed., J. B. Harborne. Academic Press, London.
   Google Scholar
• Bartnicki-Garcia, S.. 1996. The hypha: unifying thread of the fungal kingdom. Pp. 105–133. In: A century of mycology. Ed., B. C. Sutton. Cambridge University Press, Cambridge.
   Google Scholar
• Bhattacharya, D., and L. D. Druehl. 1988. Phylogenetic comparison of the small-subunit ribosomal DNA sequence of Costaria costata (Phaeophyta) with those of other algae, vascular plants and Oomycetes. J. Phycol. 24: 539–543.
   Web of Science ®Google Scholar
• Bhattacharya, D., and L. D. Druehl, and S. K. Stickel. 1994. Sequence analysis of duplicated actin genes in Lagenidium giganteum and Pythium irregulare (Oomycota). J. Molec. Evol. 39: 56–61.
   PubMed Web of Science ®Google Scholar
• Bhattacharya, D., and L. D. Druehl, and S. K. Stickel, and M. L. Sogin. 1991. Molecular phylogenetic analysis of actin genie regions from Achlya bisexualis (Oomycota) and Costaria costata (Chromophyta). J. Molec. Evol. 33: 525–536.
   PubMed Web of Science ®Google Scholar
• Bond, J. F., J. L. Fridovich-Keil, L. Pillus, R. C. Mulligan, and F. Solomon. 1986. A chicken-yeast chimeric β-tubulin protein is incorporated into mouse microtubules in vivo. Cell (Cambridge) 44: 461–468.
   PubMed Web of Science ®Google Scholar
• Buhr, T. L., and M. B. Dickman. 1994. Isolation, characterization, and expression of a second β-tubulin gene from Colletotrichum gloeosporioides f. sp. aeschynomene. Appl. Environm. Microbiol. 60: 4155–4159.
   PubMed Web of Science ®Google Scholar
• Bu'Lock, J. D., and A. U. Osagie. 1976. Sterol biosynthesis via cycloartenol in Saprolegnia. Phytochemistry 15: 1249–1251.
   Web of Science ®Google Scholar
• Cameron, L. E., J.-A. Hutsul, L. Thorlacius and H. B. LéJohn. 1990. Cloning and analysis of β-tubulin gene from a protoctist. J. Biol. Chem. 265: 15245–15252.
   PubMed Web of Science ®Google Scholar
• Cavalier-Smith, T. 1981. Eukaryote kingdoms: seven or nine? BioSystems 14: 461–481.
   PubMed Web of Science ®Google Scholar
• Cleveland, D. W., and N. G. Theodorakis. 1994. Regulation of tubulin synthesis. Pp. 47–58. In: Microtubules. Eds., J. Hyams and C. W. Lloyd. Wiley-Liss, Inc., New York.
   Google Scholar
• Conner, T. W., M. D. Thompson, and C. D. Silflow. 1989. Structure for the three β-tubulin-encoding genes of the unicellular alga, Polytomella agilis. Gene 84: 345–358.
   PubMed Web of Science ®Google Scholar
• Conzelmann, K. K., and E. Helftenbein. 1987. Nucleotide sequences and expression of two β-tubulin genes in Stylonychia lemnae. J. Molec. Biol. 198: 643–653.
   PubMed Web of Science ®Google Scholar
• Cupples, C. G. and R. E. Pearlman. 1986. Isolation and characterization of the actin gene from Tetrahymena thermophila. Proc. Natl. Acad. Sci. U. S. A. 83: 5160–5164.
   PubMed Web of Science ®Google Scholar
• Delves, C. J., R. G. Ridley, M. Goman, S. P. Holloway, J. E. Hyde, and J. G. Scaife. 1989. Cloning of a β-tubulin gene from Plasmodium falciparum. Molec. Microbiol. 3: 1511–1519.
   PubMed Web of Science ®Google Scholar
• Dibb, N. J. and A. J. Newman. 1989. Evidence that introns arose at proto-splice sites. E. M. B. O. J. 8: 2015–2021.
   PubMed Web of Science ®Google Scholar
• Dudler, R. 1990. The single-copy actin gene of Phytophthora megasperma encodes a protein considerably diverged from any other known actin. Pl. Molec. Biol. 14: 415–422.
   PubMed Web of Science ®Google Scholar
• Farr, G. W., and H. Sternlicht. 1992. Site-directed mutagenesis of the GTP-binding domain of β-tubulin. J. Molec. Biol. 227: 307–321.
   PubMed Web of Science ®Google Scholar
• Felsenstein, J. 1989. PHYLIP-phylogeny inference package (Version 3. 2). Cladistics 5: 164–166.
   Google Scholar
• Fong, D., and B. Lee. 1988. Beta tubulin gene of the parasitic protozoan Leishmania mexicana. Molec. Biochem. Parasitol. 31: 97–106.
   PubMed Web of Science ®Google Scholar
• Förster, H., M. D. Coffey, H. Elwood and M. L. Sogin. 1990. Sequence analysis of the small subunit ribosomal RNAs of three zoosporic fungi and implications for fungal evolution. Mycologia 82: 306–312.
   Web of Science ®Google Scholar
• Fulton, C., and P. A. Simpson. 1976. Selective synthesis and utilization of flagellar tubulin. The multi-tubulin hypothesis. Pp. 987–1005. In: Cell motility. Eds., R. Goldman, T. Pollard and J. Rosenbaum. Cold Spring Harbor, New York.
   Google Scholar
• Gaertig, J., T. H. Thatcher, K. E. McGrath, R. C. Callahan and M. A. Gorovsky. 1993. Perspectives on tubulin isotype function and evolution based on the observation that Tetrahymena thermophila microtubules contain a single α- and β-tubulin. Cell Motil. Cytoskel. 25: 243–253.
   PubMed Web of Science ®Google Scholar
• Gunderson, J. H., H. Elwood, A. Ingold, K. Kindle and M. L. Sogin. 1987. Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc. Natl. Acad. Sci. U. S. A. 84: 5823–5827.
   PubMed Web of Science ®Google Scholar
• Hardham, A. R. 1987. Microtubules and the flagellar apparatus in zoospores and cysts of the fungus Phytophthora cinnamomi. Protoplasma 137: 109–124.
   Web of Science ®Google Scholar
• Hardham, A. R., F. Gubler, J. Duniec, and J. Elliott. 1991. A review of methods for the production and use of monoclonal antibodies to study zoosporic plant pathogens. J. Microscopy 162: 305–318.
   Web of Science ®Google Scholar
• Harper, J. D. I., D. W. McCurdy, M. A. Sanders, J. L. Salisbury, and P. C. L. John. 1992. Actin dynamics during the cell cycle in Chlamydomonas reinhardtii. Cell Motil. Cytoskel. 22: 117–126.
   PubMed Web of Science ®Google Scholar
• Hemmes, D. E. 1983. Cytology of Phytophthora. Pp. 9–40. In: Phytophthora. Its biology, taxonomy, ecology, and pathology. Eds., D. C. Erwin, S. Bartnicki-Garcia, and P. H. Tsao. American Phytopathological Society, St. Paul, Minnesota.
   Google Scholar
• Herman, I. M. 1993. Actin isoforms. Curr. Opin. Cell Biol. 5: 48–55.
   PubMed Web of Science ®Google Scholar
• Hirono, M., H. Endoh, N. Okada, O. Numata and Y. Watanabe. 1987. Cloning and sequencing of the Tetrahymena actin gene and identification of its gene product. J. Molec. Biol. 194: 181–192.
   PubMed Web of Science ®Google Scholar
• Huang, S. R., Y. Q. An, J. M. McDowell, E. C. McKinney and R. B. Meagher. 1996. The Arabidopsis thaliana ACT4/ACT12 actin gene subclass is strongly expressed throughout pollen development. Pl. J. 10: 189–202.
   PubMed Web of Science ®Google Scholar
• Hussey, P. J., D. P. Snustad, and C. D. Silflow. 1991. Tubulin gene expression in higher plants. Pp. 15–27. In: The cytoskeletal basis of plant growth and form. Ed., C. W. Lloyd. Academic Press, London.
   Google Scholar
• Hyde, G. J., and A. R. Hardham. 1992. Confocal microscopy of microtubule arrays in cryosectioned sporangia of Phytophthora cinnamomi. Exp. Mycol. 16: 207–218.
   Google Scholar
• Hyde, G. J., and A. R. Hardham. 1993. Microtubules regulate the generation of polarity in zoospores of Phytophthora cinnamomi. Eur. J. Cell Biol. 62: 75–85.
   PubMed Web of Science ®Google Scholar
• Judelson, H. S., and R. W. Michelmore. 1989. Structure and expression of a gene encoding heat-shock protein Hsp70 from the Oomycete fungus Bremia lactucae. Gene 79: 207–217.
   PubMed Web of Science ®Google Scholar
• Kalshoven, H. W., J. Brederoo, A. M. C. Emons, A. Musgrave, F. Schuring, B. Welk, and H. van den Ende. 1994. Actin in mating structures of Chlamydomonas eugametos gametes. Physiol. Pl. 91: 657–664.
   Web of Science ®Google Scholar
• Kamoun, S., K. M. Klucher, M. D. Coffey and B. M. Tyler. 1993. A gene encoding a host-specific elicitor protein of Phytophthora parasitica. Molec. Pl.-Microbe Interact. 6: 573–581.
   PubMed Web of Science ®Google Scholar
• Kopczak, S. D., N. A. Haas, P. J. Hussey, C. D. Silflow and D. P. Snustad. 1992. The small genome of Arabidopsis contains at least six expressed a-tubulin genes. Pl. Cell 4: 539–547.
   PubMed Web of Science ®Google Scholar
• LéJohn, H. B. 1989. Structure and expression of fungal calmodulin gene. J. Biol. Chem. 264: 19366–19372.
   PubMed Web of Science ®Google Scholar
• LéJohn, H. B., L. E. Cameron, B. Yang, G. MacBeath, D. S. Barker and S. A. Williams. 1994. Cloning and analysis of a constitutive heat shock (cognate) protein 70 gene inducible by L-glutamine. J. Biol. Chem. 269: 4513–4522.
   PubMed Web of Science ®Google Scholar
• Liang, A., and K. Heckmann. 1993. The macronuclear β-tubulin-encoding gene of Euplotes odocarinatus contains two introns and an in-frame TGA. Gene 136: 319–322.
   PubMed Web of Science ®Google Scholar
• Linder, S., M. Schliwa, and E. Kube-Granderath. 1997. Sequence analysis and immunofluorescence study of α- and β-tubulin in reticulomyxa filosa: Implications of the high degree of β2-tubulin divergence. Cell Motil. Cytoskel. 36: 164–178.
   PubMed Web of Science ®Google Scholar
• Linse, K., and E.-M. Mandelkow. 1988. The GTP-binding peptide of β-tubulin: localization by direct photoaffinity labeling and comparison with nucleotide-binding proteins. J. Biol. Chem. 263: 15205–15210.
   PubMed Web of Science ®Google Scholar
• Litde, M. 1985. An evaluation of tubulin as a molecular clock. BioSystems 18: 241–247.
   PubMed Web of Science ®Google Scholar
• Litde, M., and T. Seehaus. 1988. Comparative analysis of tubulin sequences. Comp. Biochem. Physiol. 90B: 655–670.
   Google Scholar
• Lloyd, C. W. 1988. Actin in plants. J. Cell Sci. 90: 185–188.
   Web of Science ®Google Scholar
• Ludueña, R. F. 1993. Are tubulin isotypes functionally significant. Molec. Cell. Biol. 4: 445–457.
   Web of Science ®Google Scholar
• Ludueña, R. F., A. Banerjee, and I. A. Khan. 1992. Tubulin structure and biochemistry. Curr. Opin. Cell Biol. 4: 53–57.
   PubMedGoogle Scholar
• Mao, Y., and B. M. Tyler. 1991. Genome organization of Phytophthora megasperma f. sp. glycinea. Exp. Mycol. 15: 283–291.
   Google Scholar
• Margulis, L., and K. V. Schwartz. 1988. Five kingdoms. 2nd ed. W. H. Freeman and Company, New York. 376 pp.
   Google Scholar
• May, G. S. 1989. The highly divergent β-tubulins of Aspergillus nidulans are functionally interchangable. J. Cell Biol. 109: 2267–2274.
   PubMed Web of Science ®Google Scholar
• McCurdy, D. W., M. Sammut, and B. E. S. Gunning. 1988. Immunofluorescent visualization of arrays of transverse cortical actin microfilaments in wheat root-tip cells. Protoplasma 147: 204–206.
   Web of Science ®Google Scholar
• Meagher, R. B. 1991. Divergence and differential expression of actin gene families in higher plants. Int. Rev. Cytol. 125: 139–163.
   PubMedGoogle Scholar
• Meyerowitz, E. M., and R. E. Pruitt. 1985. Arabidopsis thaliana and plant molecular genetics. Science 229: 1214–1218.
   PubMed Web of Science ®Google Scholar
• Oakley, B. R. 1994. Gamma-tubulin. Pp. 33–45. In: Microtubules. Eds., J. S. Hyams and C. W. Lloyd. Wiley-Liss, New York.
   Google Scholar
• Panabières, F., A. Marais, J.-Y. Le Berre, I. Penot, D. Fournier, and P. Ricci. 1995. Characterization of a gene cluster of Phytophthora cryptogea which codes for elicitins, proteins inducing a hypersensitive-like response in tobacco. Molec. Pl.-Microbe Interact. 8: 996–1003.
   PubMed Web of Science ®Google Scholar
• Pieterse, C. M. J., E. P. Risseeuw, and L. C. Davidse. 1991. An in planta induced gene of Phytophthora infestans codes for ubiquitin. Pl. Molec. Biol. 17: 799–811.
   PubMed Web of Science ®Google Scholar
• Pieterse, C. M. J., E. P. Risseeuw, and L. C. Davidse, H. M. Verbakel, J. H. Spaans, L. C. Davidse and F. Govers. 1993. Increased expression of the calmodulin gene of the late blight fungus Phytophthora infestans during pathogenesis on potato. Molec. Pl.-Microbe Interact. 6: 164–172.
   PubMed Web of Science ®Google Scholar
• Raff, E. C. 1984. Genetics of microtubule systems. J. Cell Biol. 99: 1–10.
   PubMed Web of Science ®Google Scholar
• Raff, E. C.. 1994. The role of multiple tubulin isoforms in cellular microtubule function. Pp. 85–109. In: Microtubules. Eds., J. S. Hyams and C. W. Lloyd. Wiley-Liss, New York.
   Google Scholar
• Sachay, D. J., D. S. S. Hudspeth, S. A. Nadler and M. E. S. Hudspeth. 1993. Oomycete mtDNA: Phytophthora genes for cytochrome c oxidase use an unmodified genetic code and encode proteins most similar to those of plants. Exp. Mycol. 17: 7–23.
   Google Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning, a laboratory manual. 2. Cold Spring Harbor Laboratory Press, New York.
   Google Scholar
• Schatz, P. J., F. Solomon, and D. Botstein. 1986. Genetically essential and nonessential α-tubulin genes specify functionally interchangable proteins. Molec. Cell Biol. 6: 3722–3733.
   PubMed Web of Science ®Google Scholar
• Silflow, C. D. 1991. Why do tubulin gene families lack diversity in flagellate/ciliate protists? Protoplasma 164: 9–11.
   Web of Science ®Google Scholar
• Snustad, D. P., N. A. Haas, S. D. Kopczak, and C. D. Silflow. 1992. The small genome of Arabidopsis contains at least nine expressed β-tubulin genes. Pl. Cell 4: 549–556.
   PubMed Web of Science ®Google Scholar
• Sugase, Y., M. Hirono, K. L. Kindle, and R. Kamiya. 1996. Cloning and characterization of the actin-encoding gene of Chlamydomonas reinhardtii. Gene 168: 117–121.
   PubMed Web of Science ®Google Scholar
• Sullivan, K. F., and D. W. Cleveland. 1986. Identification of conserved isotype-defining variable region sequences for four vertebrate β-tubulin polypeptide classes. Proc. Natl. Acad. Sd. U. S. A. 83: 4327–4331.
   PubMed Web of Science ®Google Scholar
• Temperli, E., U.-P. Roos and H. R. Hohl. 1990. Actin and tubulin cytoskeleton in germlings of the oomycete fungus Phytophthora infestans. Eur. J. Cell Biol. 53: 75–88.
   PubMed Web of Science ®Google Scholar
• Temperli, E., U.-P. Roos and H. R. Hohl. 1991. Germ tube growth and the microtubule cytoskeleton in Phytophthora infestans: effects of antagonists of hyphal growth, microtubule inhibitors, and ionophores. Mycol. Res. 95: 611–617.
   Web of Science ®Google Scholar
• Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.
   PubMed Web of Science ®Google Scholar
• Tooley, P. W, and C. D. Therrien. 1987. Cytophotometric determination of the nuclear DNA content of 23 Mexican and 18 non-Mexican isolates of Phytophthora infestans. Exp. Mycol. 11: 19–26.
   Google Scholar
• Unkles, S. E., R. P. Moon, A. R. Hawkins, J. M. Duncan, and J. R. Kinghorn. 1991. Actin in the oomycetous fungus Phytophthora infestans is the product of several genes. Gene 100: 105–112.
   PubMed Web of Science ®Google Scholar
• Vogel, H. J. 1965. Lysine biosynthesis and evolution. Pp. 25–40. In: Evolving genes and proteins. Eds., V. Bryson and H. J. Vogel. Academic Press, New York.
   Google Scholar
• Walker, W. F., and W. F. Doolittle. 1982. Nucleotide sequences of 5S ribosomal RNA from four oomycete and chytrid water molds. Nucl. Acids Res. 10: 5717–5721.
   PubMed Web of Science ®Google Scholar
• Youngblom, J., J. A. Schloss, and C. D. Silflow. 1984. The two β-tubulin genes of Chlamydomonas reinhardtii code for identical proteins. Molec. Cell Biol. 4: 2686–2696.
   PubMed Web of Science ®Google Scholar
• Zentmyer, G. A. 1980. Phytophthora cinnamomi and the diseases it causes. The American Phytopathological Society, St. Paul, Minnesota. 96 pp.
   Google Scholar