Molecular evolution and functional divergence of tubulin superfamily in the fungal tree of life

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Zhao, Zhongtao ^a   Liu, Huiquan ^a   Luo, Yongping ^a   Zhou, Shanyue ^b   An, Lin ^a   Wang, Chenfang ^a   Jin, Qiaojun ^a   Zhou, Mingguo ^c   Xu, Jin Rong ^a,b  

^a NORTHWEST A F UNIVERSITY   (China)

^b PURDUE UNIVERSITY   (United States)

^c NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TUBULIN;

FUNGUS; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY;

EVOLUTION, MOLECULAR; FUNGI; GENETIC VARIATION; MULTIGENE FAMILY; PHYLOGENY; TUBULIN;

EID: 84926421870     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06746     Document Type: Article

References (60)

1. McKean, P. G., Vaughan, S. & Gull, K. The extended tubulin superfamily. J. Cell Sci. 114, 2723-2733 (2001).
2. Oakley, B. R. An abundance of tubulins. Trends Cell Biol. 10, 537-542 (2000).
3. Dutcher, S. K. Long-lost relatives reappear: identification of new members of the tubulin superfamily. Curr. Opin. Microbio. 6, 634-640 (2003).
4. Hollomon, D. W., Butters, J. A., Barker, H. & Hall, L. Fungal beta-tubulin, expressed as a fusion protein, binds benzimidazole and phenylcarbamate fungicides. Antimicrob. Agents Ch. 42, 2171-2173 (1998).
5. Ma, Z. H. & Michailides, T. J. Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop. Prot. 24, 853-863, doi: 10.1016/j.cropro.2005.01.011 (2005).
6. Zou, G., Ying, S. H., Shen, Z. C. & Feng, M. G. Multi-sited mutations of betatubulin are involved in benzimidazole resistance and thermotolerance of fungal biocontrol agent Beauveria bassiana. Environ. Microb. 8, 2096-2105, doi:10.1111/j.1462-2920.2006.01086.x (2006).
7. Dutcher, S. K. The tubulin fraternity: alpha to eta. Curr. Opin. Cell Biol. 13, 49-54 (2001).
8. Tuszynski, J. A. et al. The evolution of the structure of tubulin and its potential consequences for the role and function of microtubules in cells and embryos. Int. J. Dev. Biol. 50, 341-358, doi:10.1387/ijdb.052063jt (2006).
9. Doshi, P., Bossie, C. A., Doonan, J. H., May, G. S. & Morris, N. R. Two alphatubulin genes of Aspergillus nidulans encode divergent proteins. Mol. Gen. Genet: MGG 225, 129-141 (1991).
10. Schatz, P. J., Pillus, L., Grisafi, P., Solomon, F. & Botstein, D. Two functional alphatubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. Mol. Cel. Biol. 6, 3711-3721 (1986).
11. Adachi, Y., Toda, T., Niwa, O. & Yanagida, M. Differential expressions of essential and nonessential alpha-tubulin genes in Schizosaccharomyces pombe. Mol. Cel. Biol. 6, 2168-2178 (1986).
12. Chen, C. J. et al. Mutations in a beta-tubulin confer resistance of Gibberella zeae to benzimidazole fungicides. Phytopathology 99, 1403-1411, doi:10.1094/PHYTO-99-12-1403 (2009).
13. Schatz, P. J., Solomon, F. & Botstein, D. Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins. Mol. Cel. Biol. 6, 3722-3733 (1986).
14. Oakley, B. R. Tubulins in Aspergillus nidulans. Fungal Genet. Biol. 41, 420-427, doi:10.1016/j.fgb.2003.11.013 (2004).
15. Liu, S., Duan, Y., Ge, C., Chen, C. & Zhou, M. Functional analysis of the beta2-tubulin gene of Fusarium graminearum and the beta-tubulin gene of Botrytis cinerea by homologous replacement. Pest Manag. Sci. 69, 582-588, doi:10.1002/ps.3474 (2013).
16. Begerow, D., John, B. & Oberwinkler, F. Evolutionary relationships among betatubulin gene sequences of basidiomycetous fungi. Mycol. Res. 108, 1257-1263, doi:Doi 10.1017/S0953756204001066 (2004).
17. James, T. Y. et al. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818-822, doi:Doi 10.1038/Nature05110 (2006).
18. Keeling, P. J., Luker, M. A. & Palmer, J. D. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23-31 (2000).
19. Loppnau, P. A. & Breuil, C. Species level identification of conifer associated Ceratocystis sapstain fungi by PCR-RFLP on a beta-tubulin gene fragment. Fems. Microbiol Lett. 222, 143-147, doi:Doi 10.1016/S0378-1097(03)00256-8 (2003).
20. Msiska, Z. & Morton, J. B. The beta-tubulin gene as a means to discriminate species of arbuscular mycorrhizal fungi. Phytopathology 95, S157-S157 (2005).
21. Gogendeau, D. et al. Sas-4 proteins are required during basal body duplication in Paramecium. Mol. Biol. Cell 22, 1035-1044, doi:10.1091/mbc.E10-11-0901 (2011).
22. Ross, I., Clarissa, C., Giddings, T. H., Jr. & Winey, M. epsilon-tubulin is essential in Tetrahymena thermophila for the assembly and stability of basal bodies. J. Cell Sci. 126, 3441-3451, doi:10.1242/jcs.128694 (2013).
23. James, T. Y. et al. A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98, 860-871 (2006).
24. Liu, Y. J., Hodson, M. C. & Hall, B. D. Loss of the flagellumhappened only once in the fungal lineage: phylogenetic structure of kingdom Fungi inferred from RNA polymerase II subunit genes. BMC Evol. Biol. 6, 74, doi:10.1186/1471-2148-6-74 (2006).
25. Ma, L. J. et al. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS genetics 5, e1000549, doi:10.1371/journal.pgen.1000549 (2009).
26. Spang, A., Geissler, S., Grein, K. & Schiebel, E. gamma-Tubulin-like Tub4p of Saccharomyces cerevisiae is associated with the spindle pole body substructures that organize microtubules and is required for mitotic spindle formation. J. Cell Biol. 134, 429-441 (1996).
27. Gurvitz, A., Hartig, A., Ruis, H., Hamilton, B. & de Couet, H. G. Preliminary characterisation of DML1, an essential Saccharomyces cerevisiae gene related to misato of Drosophila melanogaster. FEMS Yeast Res. 2, 123-135 (2002).
28. Miklos, G. L., Yamamoto, M., Burns, R. G. & Maleszka, R. An essential cell division gene of Drosophila, absent from Saccharomycetes, encodes an unusual protein with tubulin-like and myosin-like peptide motifs. P. Natl. Acad. Sci. USA 94, 5189-5194 (1997).
29. Mottier-Pavie, V., Cenci, G., Verni, F., Gatti, M. & Bonaccorsi, S. Phenotypic analysis of misato function reveals roles of noncentrosomal microtubules in Drosophila spindle formation. J. Cell Sci. 124, 706-717, doi:10.1242/jcs.072348 (2011).
30. Bielawski, J. P. & Yang, Z. H. A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J. Mol. Evol. 59, 121-132, doi:DOI 10.1007/s00239-004-2597-8 (2004).
31. Luduena, R. F. Are Tubulin Isotypes Functionally Significant. Mol. Biol. Cell 4, 445-457 (1993).
32. Libusova, L. & Draber, P. Multiple tubulin forms in ciliated protozoan Tetrahymena and Paramecium species. Protoplasma 227, 65-76, doi:10.1007/s00709-005-0152-0 (2006).
33. Hou, Y. et al. Molecular evidence for beta-tubulin neofunctionalization in Retaria (Foraminifera and radiolarians). Mol. Biol. Evol. 30, 2487-2493, doi:10.1093/molbev/mst150 (2013).
34. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591, doi:10.1093/molbev/msm088 (2007).
35. Gu, X. Functional divergence in protein (family) sequence evolution. Genetica 118, 133-141, doi:Doi 10.1023/A,1024197424306 (2003).
36. Gu, X. et al. AnUpdate of DIVERGE Software for Functional Divergence Analysis of Protein Family. Mol. Biol. Evol. 30, 1713-1719, doi:DOI 10.1093/molbev/mst069 (2013).
37. Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391, 199-203, doi:10.1038/34465 (1998).
38. Bielawski, J. P. & Yang, Z. Maximum likelihood methods for detecting adaptive evolution after gene duplication. J. Struct. Funct. Genom. 3, 201-212 (2003).
39. Tassan, J. P. & Le Goff, X. An overview of the KIN1/PAR-1/MARK kinase family. Biol. Cell 96, 193-199, doi:10.1016/j.biolcel.2003.10.009 (2004).
40. Luo, Y. P. et al. The FgKin1 kinase localizes to the septal pore and differentially regulates the localization of two beta-tubulins in Fusarium. New Phytol. In Press (2014).
41. Yan, K. Y. & Dickman, M. B. Isolation of a beta-tubulin gene from Fusarium moniliforme that confers cold-sensitive benomyl resistance. Appl. Environ. Microb. 62, 3053-3056 (1996).
42. Chen, Z., Gao, T., Zhou, M. & Chen, C. Molecular mechanism of resistance of Fusarium fujikuroi to benzimidazole fungicides. Fems. Microbiol. Lett. doi:10.1111/1574-6968.12504 (2014).
43. Gold, S. E., Casale, W. L. & Keen, N. T. Characterization of two beta-tubulin genes from Geotrichum candidum. Mol. Gen Genet. 230, 104-112 (1991).
44. Goldman, G.H. et al. A nucleotide substitution in one of the beta-tubulin genes of Trichoderma viride confers resistance to the antimitotic drug methyl benzimidazole-2-yl-carbamate. Mol. Gen Genet. 240, 73-80 (1993).
45. Eddy, S. R. A new generation of homology search tools based on probabilistic inference. Genome Inf. 23, 205-211, doi:9781848165632-0019 [pii] (2009).
46. Punta, M. et al. The Pfam protein families database. Nucleic Acids Res. 40, D290-301, doi:10.1093/nar/gkr1065 (2012).
47. Di Tommaso, P. et al. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13-17, doi:10.1093/nar/gkr245 (2011).
48. Capella-Gutierrez, S., Silla-Martinez, J. M. & Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973, doi:10.1093/bioinformatics/btp348 (2009).
49. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol 59, 307-321, doi:10.1093/sysbio/syq010 (2010).
50. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164-1165, doi:10.1093/bioinformatics/btr088 (2011).
51. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61, 539-542, doi:10.1093/sysbio/sys029 (2012).
52. Sennblad, B., Schreil, E., Sonnhammer, A. C. B., Lagergren, J. & Arvestad, L. primetv: a viewer for reconciled trees. BMC Bioinformatics 8, doi: 10.1186/1471-2105-8-148 (2007).
53. Wang, H., Xu, Z., Gao, L. & Hao, B. L. A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol Biol 9, doi: 10.1186/1471-2148-9-195 (2009).
54. Ebersberger, I. et al. A Consistent Phylogenetic Backbone for the Fungi. Mol. Biol. Evol. 29, 1319-1334, doi:DOI 10.1093/molbev/msr285 (2012).
55. Zhang, J., Nielsen, R. & Yang, Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472-2479, doi:10.1093/molbev/msi237 (2005).
56. Ayaz, P., Ye, X., Huddleston, P., Brautigam, C. A. & Rice, L. M. A TOG:Alphabeta-tubulin complex structure reveals conformation-based mechanisms for a microtubule polymerase. Science 337, 857-860, doi:10.1126/science.1221698 (2012).
57. Yang, Z. et al. UCSF Chimera, MODELLER, and IMP: an integrated modeling system. J. Struct. Biol. 179, 269-278, doi:10.1016/j.jsb.2011.09.006 (2012).
58. Soding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucl. Acids Res. 33, W244-248, doi:10.1093/nar/gki408 (2005).
59. Hou, Z. M. et al. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol. Plant Microbe In. 15, 1119-1127, doi:Doi 10.1094/Mpmi.2002.15.11.1119 (2002).
60. Wang, C. F. et al. Functional Analysis of the Kinome of the Wheat Scab Fungus Fusarium graminearum. PloS Pathog. 7, doi:DOI 10.1371/journal.ppat.1002460 (2011).