Genomes of ashbya fungi isolated from insects reveal four mating-type loci, numerous translocations, lack of transposons, and distinct gene duplications

G3: Genes, Genomes, Genetics

Volumn 3, Issue 8, 2013, Pages 1225-1239

  Dietrich, Fred S ^a,b   Voegeli, Sylvia ^c   Kuo, Sidney ^a,c   Philippsen, Peter ^c  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Duplications; Fungal ecology; Intron evolution; Mating type; Tandem

Indexed keywords

RIBOSOME DNA;

ANIMAL; ARTICLE; ASHBYA GOSSYPII; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ECOLOGICAL NICHE; EREMOTHECIUM; FUNGAL ECOLOGY; FUNGAL GENOME; FUNGAL MATING TYPE GENE; FUNGAL STRAIN; FUNGAL STRUCTURES; FUNGUS ISOLATION; GENE DUPLICATION; GENE LOCUS; GENE ORDER; GENE TRANSLOCATION; GENETICS; GENOME; HETEROPTERA; INSECT; INTRON; INTRON EVOLUTION; ISOLATION AND PURIFICATION; MATING TYPE; MICROBIOLOGY; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENETIC TREE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SIBLING; TANDEM DUPLICATIONS; TRANSPOSON; UNITED STATES;

EREMOTHECIUM; EREMOTHECIUM GOSSYPII; FUNGI; GOSSYPIUM HIRSUTUM; HETEROPTERA; HEXAPODA; SACCHAROMYCES CEREVISIAE;

FUNGAL ECOLOGY; INTRON EVOLUTION; MATING TYPE; TANDEM DUPLICATIONS;

ANIMALS; BASE SEQUENCE; DNA, RIBOSOMAL; EREMOTHECIUM; GENES, MATING TYPE, FUNGAL; GENOME, FUNGAL; HETEROPTERA; INSECTS; INTRONS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84883258237     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.002881     Document Type: Article

References (83)

1. Altmann-Jöhl, R., and P. Philippsen, 1996 AgTHR4, a new selection marker for transformation of the filamentous fungus Ashbya gossypii, maps in a four-gene cluster that is conserved between A. gossypii and Saccharomyces cerevisiae. Mol. Gen. Genet. 250: 69-80.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang et al., 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Ashby, S. F., 1916 Annual Report of the Microbiologist, 1915-1916. Annual report of the Department of Agriculture, Jamaica, pp. 29-31.
4. Ashby, S. F., and W. Nowell, 1926 The fungi of Stigmatomycosis. Ann. Bot. (Lond.) 40: 69-83.
5. Astrom, S. U., A. Kegel, J. O. Sjostrand, and J. Rine, 2000 Kluyveromyces lactis Sir2p regulates cation sensitivity and maintains a specialized chromatin structure at the cryptic alpha-locus. Genetics 156: 81-91.
6. Bacher, A., S. Eberhardt, M. Fischer, K. Kis, and G. Richter, 2000 Biosynthesis of vitamin B2 (riboflavin). Annu. Rev. Nutr. 20: 153-167.
7. Batra, L. R., 1973 Nematosporaceae (Hemiascomycetidae): Taxonomy, Pathogenicity, Distribution, and Vector Relations [Nematospora, Ashbya gossypii, Economic Crops]. USDA Technical Bulletin 1469. U.S. Department of Agriculture, Washington, DC.
8. Bentley, D. R., 2006 Whole-genome re-sequencing. Curr. Opin. Genet. Dev. 16: 545-552.
9. Bieganowski, P., K. Shilinski, P. N. Tsichlis, and C. Brenner, 2004 Cdc123 and checkpoint forkhead associated with RING proteins control the cell cycle by controlling eIF2gamma abundance. J. Biol. Chem. 279: 44656-44666.
10. Brachat, S., F. S. Dietrich, S. Voegeli, Z. Zhang, L. Stuart et al., 2003 Reinvestigation of the Saccharomyces cerevisiae genome annotation by comparison to the genome of a related fungus: Ashbya gossypii. Genome Biol. 4: R45.
11. Brudno, M., C. B. Do, G. M. Cooper, M. F. Kim, E. Davydov et al., 2003 LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res. 13: 721-731.
12. Burgess, L., and H. H. Weegar, 1986 A method for rearing Nysius ericae (Hemiptera: Lygaeidae), the false chinch bug. Can. Entomol. 118: 1059-1061.
13. Burgess, L., and D. L. McKenzie, 1991 Role of the insect Nysius niger, and flixweed, Descurainia sophia, infection of Saskatchewan mustard crop with a yeast, Nematospora sinecauda. Can. Plant Dis. Surv. 71: 37-41.
14. Burgess, L., J. Dueck, and D. L. McKenzie, 1983 Insect vectors of the yeast Nematospora coryli in mustard, Brassica juncea, crops in southern Saskatchewan. Can. Entomol. 115: 25-30.
15. Cashman, J. R., B. Y. Perotti, C. E. Berkman, and J. Lin, 1996 Pharmacokinetics and molecular detoxication. Environ. Health Perspect. 104(Suppl 1): 23-40.
16. Clarke, R. G., and G. E. Wilde, 1970 Association of the green stink bug and the yeast-spot disease organism of soybeans. II. Frequency of transmission to soybeans, transmission from insect to insect, isolation from field population. [Acrosternum Hilare, Nematospora Coryli, Insect Vectors, Plant Disease Transmission]. J. Econ. Entomol. 63: 355-357.
17. Crooks, G. E., G. Hon, J. M. Chandonia, and S. E. Brenner, 2004 WebLogo: a sequence logo generator. Genome Res. 14: 1188-1190.
18. DeMay, B. S., R. A. Meseroll, P. Occhipinti, and A. S. Gladfelter, 2009 Regulation of distinct septin rings in a single cell by Elm1p and Gin4p kinases. Mol. Biol. Cell 20: 2311-2326.
19. Dietrich, F. S., S. Voegeli, S. Brachat, A. Lerch, K. Gates et al., 2004 The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304: 304-307.
20. Dujon, B., D. Sherman, G. Fischer, P. Durrens, S. Casaregola et al., 2004 Genome evolution in yeasts. Nature 430: 35-44.
21. Everist, S. L., 1981 Poisonous Plants of Australia, Ed. 2. Angus and Robertson, London.
22. Farries, E. H. M., and A. F. Bell, 1930 On the Metabolism of Nematospora gossypii and related fungi, with special reference to the source of nitrogen. Ann. Bot. (Lond.) 44: 423-455.
23. Fink, G. R., 1987 Pseudogenes in yeast? Cell 49: 5-6.
24. Finlayson, M. R., A. K. Helfer-Hungerbuhler, and P. Philippsen, 2011 Regulation of exit from mitosis in multinucleate Ashbya gossypii cells relies on a minimal network of genes. Mol. Biol. Cell 22: 3081-3093.
25. Fisk, D. G., C. A. Ball, K. Dolinski, S. R. Engel, E. L. Hong et al., 2006 Saccharomyces cerevisiae S288C genome annotation: a working hypothesis. Yeast 23: 857-865.
26. Foster, J. E., and D. M. Daugherty, 1969 Isolation of the organism causing yeast-spot disease from the salivary system of the green stink bug. J. Econ. Entomol. 62: 424-427.
27. Frazer, H. L., 1944 Observations on the method of transmission of internal boll disease of cotton by the stainer-bug. Ann. Appl. Biol. 31: 271-290.
28. Gibeaux, R., A. Z. Politi, F. Nedelec, C. Antony, and M. Knop, 2013 Spindle pole body-anchored Kar3 drives the nucleus along microtubules from another nucleus in preparation for nuclear fusion during yeast karyogamy. Genes Dev. 27: 335-349.
29. Gladfelter, A. S., A. K. Hungerbuehler, and P. Philippsen, 2006 Asynchronous nuclear division cycles in multinucleated cells. J. Cell Biol. 172: 347-362.
30. Gordon, J. L., K. P. Byrne, and K. H. Wolfe, 2009 Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet. 5: e1000485.
31. Grava, S., and P. Philippsen, 2010 Dynamics of multiple nuclei in Ashbya gossypii hyphae depend on the control of cytoplasmic microtubules length by Bik1, Kip2, Kip3, and not on a capture/shrinkage mechanism. Mol. Biol. Cell 21: 3680-3692.
32. Grunler, A., A. Walther, J. Lammel, and J. Wendland, 2010 Analysis of flocculins in Ashbya gossypii reveals FIG2 regulation by TEC1. Fungal Genet. Biol. 47: 619-628.
33. Guilliermond, A. 1928 Recherches sur quelques Ascomycetes Inferieurs. Rev. générale Botanique 40: 328-342; 397-414; 474-485; 555-574; 606-624; 690-704.
34. Hull, C. M., and A. D. Johnson, 1999 Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 285: 1271-1275.
35. Jiao, X., S. Xiang, C. Oh, C. E. Martin, L. Tong et al., 2010 Identification of a quality-control mechanism for mRNA 5'-end capping. Nature 467: 608-611.
36. Jorde, S., A. Walther, and J. Wendland, 2011 The Ashbya gossypii fimbrin SAC6 is required for fast polarized hyphal tip growth and endocytosis. Microbiol. Res. 166: 137-145.
37. Kato, T., and E. Y. Park, 2012 Riboflavin production by Ashbya gossypii. Biotechnol. Lett. 34: 611-618.
38. Kaufmann, A., and P. Philippsen, 2009 Of bars and rings: Hof1-dependent cytokinesis in multiseptated hyphae of Ashbya gossypii. Mol. Cell. Biol. 29: 771-783.
39. Kitagaki, H., H. Wu, H. Shimoi, and K. Ito, 2002 Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins re-quired for cell wall biogenesis in Saccharomyces cerevisiae. Mol. Microbiol. 46: 1011-1022.
40. Knechtle, P., J. Wendland, and P. Philippsen, 2006 The SH3/PH domain protein AgBoi1/2 collaborates with the Rho-type GTPase AgRho3 to prevent nonpolar growth at hyphal tips of Ashbya gossypii. Eukaryot. Cell 5: 1635-1647.
41. Koehli, M., S. Buck, and H.-P. Schmitz, 2008a The function of two closely related Rho proteins is determined by an atypical switch I region. J. Cell Sci. 121: 1065-1075.
42. Koehli, M., V. Galati, K. Boudier, R. W. Roberson, and P. Philippsen, 2008b Growth-speed-correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. J. Cell Sci. 121: 3878-3889.
43. Lai, C. Y., and P. Baumann, 1992 Genetic analysis of an aphid endosymbiont DNA fragment homologous to the rnpA-rpmH-dnaA-dnaN-gyrB region of eubacteria. Gene 113: 175-181.
44. Lang, C., S. Grava, M. Finlayson, R. Trimble, P. Philippsen et al., 2010 Structural mutants of the spindle pole body cause distinct alteration of cytoplasmic microtubules and nuclear dynamics in multinucleated hyphae. Mol. Biol. Cell 21: 753-766.
45. Langel, D., and D. Ober, 2011 Evolutionary recruitment of a flavindependent monooxygenase for stabilization of sequestered pyrrolizidine alkaloids in arctiids. Phytochemistry 72(13): 1576-1584.
46. Lewis, W. H., and M. P. H. Elvin-Lewis, 1986 Medic Botany: Plants Affecting Human Health. John Wiley & Sons, Hoboken, NJ.
47. Li, H., and R. Durbin, 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
48. Li, H., J. Ruan, and R. Durbin, 2008 Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18: 1851-1858.
49. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
50. Lipman, D. J., and W. R. Pearson, 1985 Rapid and sensitive protein similarity searches. Science 227: 1435-1441.
51. Liti, G., D. B. Barton, and E. J. Louis, 2006 Sequence diversity, reproductive isolation and species concepts in Saccharomyces. Genetics 174: 839-850.
52. Maruyama, R., M. Nishizawa, Y. Itoi, S. Ito, and M. Inoue, 2002 The enzymes with benzil reductase activity conserved from bacteria to mammals. J. Biotechnol. 94: 157-169.
53. Miranda, C. L., W. Chung, R. E. Reed, X. Zhao, M. C. Henderson et al., 1991 Flavin-containing monooxygenase: a major detoxifying enzyme for the pyrrolizidine alkaloid senecionine in guinea pig tissues. Biochem. Biophys. Res. Commun. 178: 546-552.
54. Nair, D. R., C. A. D'Ausilio, P. Occhipinti, M. E. Borsuk, and A. S. Gladfelter, 2010 A conserved G regulatory circuit promotes asynchronous behavior of nuclei sharing a common cytoplasm. Cell Cycle 9: 3771-3779.
55. Nowell, W. 1915 The internal disease of cotton bolls. Agric. News (Barbados) 14: 222, 234, 238-239.
56. Nowell, W. 1916 The internal disease of cotton bolls. Agric. News (Barbados) 15: 126-127, 182-183, 214-215.
57. Pearson, E. O., 1934 Preliminary observations on cotton stainers and internal boll disease of cotton in South Africa. Bull. Entomol. Res. 25: 383-414.
58. Philippsen, P., A. Kaufmann, and H. P. Schmitz, 2005 Homologues of yeast polarity genes control the development of multinucleated hyphae in Ashbya gossypii. Curr. Opin. Microbiol. 8: 370-377.
59. Rice, P., I. Longden, and A. Bleasby, 2000 EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16: 276-277.
60. Robbins, W. J., and M. B. Schmidt, 1939 Preliminary experiments on Biotin. Bull. Torrey Bot. Club 66: 139-150.
61. Rusche, L. N., A. L. Kirchmaier, and J. Rine, 2003 The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu. Rev. Biochem. 72: 481-516.
62. Scannell, D. R., A. C. Frank, G. C. Conant, K. P. Byrne, M. Woolfit et al., 2007 Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proc. Natl. Acad. Sci. USA 104: 8397-8402.
63. Schmitz, H. P., and P. Philippsen, 2011 Evolution of multinucleated Ashbya gossypii hyphae from a budding yeast-like ancestor. Fungal Biol 115: 557-568.
64. Schmitz, H. P., A. Kaufmann, M. Kohli, P. P. Laissue, and P. Philippsen, 2006 From function to shape: a novel role of a formin in morphogenesis of the fungus Ashbya gossypii. Mol. Biol. Cell 17: 130-145.
65. Sehlmeyer, S., L. Wang, D. Langel, D. G. Heckel, H. Mohagheghi et al., 2010 Flavin-dependent monooxygenases as a detoxification mechanism in insects: new insights from the arctiids (lepidoptera). PLoS ONE 5: e10435.
66. Seret, M. L., J. F. Diffels, A. Goffeau, and P. V. Baret, 2009 Combined phylogeny and neighborhood analysis of the evolution of the ABC transporters conferring multiple drug resistance in hemiascomycete yeasts. BMC Genomics 10: 459.
67. Sherman, F., G. R. Fink, and J. B. Hicks, 1987 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
68. Slater, J. A., 1982, Hemiptera, pp. 417-447 in Synopsis and Classification of Living Organisms, edited by S. P. Parker. McGraw-Hill, New York.
69. Souciet, J. L., B. Dujon, C. Gaillardin, M. Johnston, P. V. Baret et al., 2009 Comparative genomics of protoploid Saccharomycetaceae. Genome Res. 19: 1696-1709.
70. Stahmann, K. P., J. L. Revuelta, and H. Seulberger, 2000 Three biotechnical processes using Ashbya gossypii, Candida famata, or Bacillus subtilis compete with chemical riboflavin production. Appl. Microbiol. Biotechnol. 53: 509-516.
71. Stajich, J. E., and F. S. Dietrich, 2006 Evidence of mRNA-mediated intron loss in the human-pathogenic fungus Cryptococcus neoformans. Eukaryot. Cell 5: 789-793.
72. Stajich, J. E., D. Block, K. Boulez, S. E. Brenner, S. A. Chervitz et al., 2002 The Bioperl toolkit: Perl modules for the life sciences. Genome Res. 12: 1611-1618.
73. Steiner, S., J. Wendland, M. C. Wright, and P. Philippsen, 1995 Homologous recombination as the main mechanism for DNA integration and cause of rearrangements in the filamentous ascomycete Ashbya gossypii. Genetics 140: 973-987.
74. 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. Nucleic Acids Res. 22: 4673-4680.
75. van Hoof, A., R. R. Staples, R. E. Baker, and R. Parker, 2000 Function of the ski4p (Csl4p) and Ski7p proteins in 39-to-59 degradation of mRNA. Mol. Cell. Biol. 20: 8230-8243.
76. Verstrepen, K. J., A. Jansen, F. Lewitter, and G. R. Fink, 2005 Intragenic tandem repeats generate functional variability. Nat. Genet. 37: 986-990.
77. Wendland, J., 2003 Analysis of the landmark protein Bud3 of Ashbya gossypii reveals a novel role in septum construction. EMBO Rep. 4: 200-204.
78. Wendland, J., and P. Philippsen, 2001 Cell polarity and hyphal morphogenesis are controlled by multiple rho-protein modules in the filamentous ascomycete Ashbya gossypii. Genetics 157: 601-610.
79. Wendland, J., and A. Walther, 2005 Ashbya gossypii: a model for fungal developmental biology. Nat. Rev. Microbiol. 3: 421-429.
80. Wendland, J., and A. Walther, 2011 Genome evolution in the eremothecium clade of the Saccharomyces complex revealed by comparative genomics. G3 (Bethesda) 1: 539-548.
81. Williams, C. B., 1934 The cotton stainer problem. Empire Cotton Growing Rev. 11: 99-110.
82. Wong, S., M. A. Fares, W. Zimmermann, G. Butler, and K. H. Wolfe, 2003 Evidence from comparative genomics for a complete sexual cycle in the 'asexual' pathogenic yeast Candida glabrata. Genome Biol. 4: R10.
83. Zerbino, D. R., and E. Birney, 2008 Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821-829.