Interspecific sex in grass smuts and the genetic diversity of their pheromone-receptor system

PLoS Genetics

Volumn 7, Issue 12, 2011, Pages

  Kellner, Ronny ^a   Vollmeister, Evelyn ^b   Feldbrügge, Michael ^b   Begerow, Dominik ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHEROMONE RECEPTOR; FUNGAL PROTEIN; PHEROMONE; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA FLANKING REGION; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; GRASS; HOST RANGE; INTERSPECIFIC HYBRIDIZATION; MATING TYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; PLESIOMORPHY; SEX DETERMINATION PROCESS; SMUT (PLANT DISEASE); SYNTENY; UNINDEXED SEQUENCE; USTILAGINALES; ALLELE; AMINO ACID SEQUENCE; EVOLUTION; FUNGAL GENE; FUNGAL GENOME; FUNGUS HYPHAE; GENETICS; HYBRIDIZATION; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; REPRODUCTION;

FUNGI; POACEAE; USTILAGINACEAE;

ALLELES; AMINO ACID SEQUENCE; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; GENOME, FUNGAL; HYBRIDIZATION, GENETIC; HYPHAE; MOLECULAR SEQUENCE DATA; PHEROMONES; PHYLOGENY; RECEPTORS, PHEROMONE; REPRODUCTION; TRANSCRIPTION FACTORS; USTILAGINALES;

EID: 84855286458     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002436     Document Type: Article

References (115)

1. Weismann A, (1886) Zur Frage nach der Vererbung erworbener Eigenschaften. Biologisches Zentralblatt 6: 33-48.
2. Hamilton WD, Axelrod R, Tanese R, (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci U S A 87: 3566-3573.
3. Wilhelm D, Palmer S, Koopman P, (2007) Sex determination and gonadal development in mammals. Physiol Rev 87: 1-28.
4. Johnson MT, Smith SD, Rausher MD, (2009) Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci U S A 106: 18079-18084.
5. Lee SC, Ni M, Li W, Shertz C, Heitman J, (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74: 298-340.
6. Sekido R, Lovell-Badge R, (2009) Sex determination and SRY: down to a wink and a nudge? Trends Genet 25: 19-29.
7. Barrett SC, (2010) Understanding plant reproductive diversity. Philos Trans R Soc Lond B Biol Sci 365: 99-109.
8. Harshman LG, Zera AJ, (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22: 80-86.
9. Goddard MR, Godfray HC, Burt A, (2005) Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434: 636-640.
10. Aanen DK, Hoekstra RF, (2007) Why Sex Is Good: On Fungi and Beyond. In: Heitman J, Kronstad JW, Taylor DR, Casselton LA, editors. Sex in fungi- Molecular Determination and Evolutionary Implications Washington D.C. ASM Press pp. 527-534.
11. Casselton LA, (2002) Mate recognition in fungi. Heredity 88: 142-147.
12. Heitman J, Kronstad JW, Taylor DR, Casselton LA, (2007) Sex in fungi- Molecular Determination and Evolutionary Implications Washington ASM Press.
13. Kniep H, (1928) Die Sexualität der niederen Pflanzen Jena Fisher.
14. Raper J, (1966) Genetics of Sexuality in Higher Fungi New York The Ronald Press Co.
15. Casselton LA, Olesnicky NS, (1998) Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62: 55-70.
16. Kües U, (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64: 316-353.
17. Kothe E, Gola S, Wendland J, (2003) Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi. Curr Genet 42: 268-275.
18. Raudaskoski M, Kothe E, (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9: 847-859.
19. Hu G, Kamp A, Linning R, Naik S, Bakkeren G, (2007) Complementation of Ustilago maydis MAPK mutants by a wheat leaf rust, Puccinia triticina homolog: potential for functional analyses of rust genes. Mol Plant Microbe Interact 20: 637-647.
20. Fowler TJ, DeSimone SM, Mitton MF, Kurjan J, Raper CA, (1999) Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol Biol Cell 10: 2559-2572.
21. Bakkeren G, Kronstad JW, (1996) The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143: 1601-1613.
22. May G, Shaw F, Badrane H, Vekemans X, (1999) The signature of balancing selection: fungal mating compatibility gene evolution. Proc Natl Acad Sci U S A 96: 9172-9177.
23. Devier B, Aguileta G, Hood ME, Giraud T, (2008) Ancient Trans-specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes. Genetics 181: 209-223.
24. Casselton LA, Kües U, (2007) The Origin of Multiple Mating Types in the Model Mushrooms Coprinopsis cinerea and Schizophyllum commune. In: Heitman J, Kronstad JW, Taylor DR, Casselton LA, editors. Sex in fungi- Molecular Determination and Evolutionary Implications Washington D.C. ASM Press pp. 283-300.
25. Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, et al. (2004) Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol 2: e384 doi:10.1371/journal.pbio.0020384.
26. James TY, Srivilai P, Kües U, Vilgalys R, (2006) Evolution of the bipolar mating system of the mushroom Coprinellus disseminatus from its tetrapolar ancestors involves loss of mating-type-specific pheromone receptor function. Genetics 172: 1877-1891.
27. Coelho MA, Sampaio JP, Goncalves P, (2010) A deviation from the bipolar-tetrapolar mating paradigm in an early diverged basidiomycete. PLoS Genet 6: e1001052 doi:10.1371/journal.pgen.1001052.
28. Spellig T, Bölker M, Lottspeich F, Frank RW, Kahmann R, (1994) Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13: 1620-1627.
29. Xue C, Hsueh YP, Heitman J, (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32: 1010-1032.
30. Feldbrügge M, Bölker M, Steinberg G, Kämper J, Kahmann R, (2006) Regulatory and structural networks orchestrating mating, dimorphism, cell shape, and pathogenesis in Ustilago maydis. In: Kües U, Fisher R, editors. The Mycota I: growth, differentiation and sexuality Heidelberg Springer-Verlag pp. 375-391.
31. Fowler TJ, Mitton MF, Vaillancourt LJ, Raper CA, (2001) Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics 158: 1491-1503.
32. Olesnicky NS, Brown AJ, Honda Y, Dyos SL, Dowell SJ, et al. (2000) Self-compatible B mutants in Coprinus with altered pheromone-receptor specificities. Genetics 156: 1025-1033.
33. Gola S, Kothe E, (2003) The little difference: in vivo analysis of pheromone discrimination in Schizophyllum commune. Curr Genet 42: 276-283.
34. Szabo Z, Tönnis M, Kessler H, Feldbrügge M, (2002) Structure-function analysis of lipopeptide pheromones from the plant pathogen Ustilago maydis. Mol Genet Genomics 268: 362-370.
35. Kosted PJ, Gerhardt SA, Anderson CM, Stierle A, Sherwood JE, (2000) Structural requirements for activity of the pheromones of Ustilago hordei. Fungal Genet Biol 29: 107-117.
36. Fisher GW, Holton CS, (1957) Biology and Control of the Smut Fungi New York The Ronald Press Company.
37. Stoll M, Begerow D, Oberwinkler F, (2005) Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109: 342-356.
38. Begerow D, Stoll M, Bauer R, (2006) A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98: 906-916.
39. Urban M, Kahmann R, Bölker M, (1996) The biallelic a mating type locus of Ustilago maydis: remnants of an additional pheromone gene indicate evolution from a multiallelic ancestor. Mol Gen Genet 250: 414-420.
40. Snetselaar KM, Bölker M, Kahmann R, (1996) Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources. Fungal Genet Biol 20: 299-312.
41. Bakkeren G, Jiang G, Warren RL, Butterfield Y, Shin H, et al. (2006) Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet Biol 43: 655-666.
42. Schirawski J, Heinze B, Wagenknecht M, Kahmann R, (2005) Mating type loci of Sporisorium reilianum: novel pattern with three a and multiple b specificities. Eukaryot Cell 4: 1317-1327.
43. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, et al. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
44. Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, et al. (2009) Ustilago maydis as a Pathogen. Annu Rev Phytopathol 47: 423-445.
45. Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T, et al. (2011) Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev DOI:10.1111/j.1574-6976.2011.00296.x.
46. Kaffarnik F, Müller P, Leibundgut M, Kahmann R, Feldbrügge M, (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22: 5817-5826.
47. Zarnack K, Eichhorn H, Kahmann R, Feldbrügge M, (2008) Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol 69: 1041-1053.
48. Kahmann R, Kämper J, (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytologist 164: 31-42.
49. Rowell JB, DeVay JE, (1954) Genetics of Ustilago zeae in relation to basic problems of its pathogenicity. Phytopathology 44: 356-362.
50. Fedler M, Luh KS, Stelter K, Nieto-Jacobo F, Basse CW, (2008) The a2 Mating-type Locus Genes lga2 and rga2 Direct Uniparental mtDNA Inheritance and Constrain Mitochondrial DNA Recombination During Sexual Development of Ustilago maydis. Genetics 181: 847-860.
51. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
52. Webb CO, Ackerly DD, Kembel SW, (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24: 2098-2100.
53. Bannai H, Tamada Y, Maruyama O, Nakai K, Miyano S, (2002) Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18: 298-305.
54. Bortfeld M, Auffarth K, Kahmann R, Basse CW, (2004) The Ustilago maydis a2 mating-type locus genes lga2 and rga2 compromise pathogenicity in the absence of the mitochondrial p32 family protein Mrb1. Plant Cell 16: 2233-2248.
55. Stanke M, Diekhans M, Baertsch R, Haussler D, (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637-644.
56. Schultz J, Milpetz F, Bork P, Ponting CP, (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95: 5857-5864.
57. Letunic I, Doerks T, Bork P, (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37: D229-32.
58. Romeis T, Brachmann A, Kahmann R, Kämper J, (2000) Identification of a target gene for the bE-bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37: 54-66.
59. Brachmann A, Weinzierl G, Kämper J, Kahmann R, (2001) Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42: 1047-1063.
60. Prasad V, Stromberg CA, Alimohammadian H, Sahni A, (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310: 1177-1180.
61. Casselton LA, Feldbrügge M, (2010) Mating and sexual morphogenesis in basidiomycete fungi. In: Borkovich K, Ebbole D, editors. Cellular and Molecular Biology of Filamentous Fungi Washington D.C. ASM Press pp. 536-551.
62. Li W, Metin B, White TC, Heitman J, (2010) Organization and evolutionary trajectory of the mating type (MAT) locus in dermatophyte and dimorphic fungal pathogens. Eukaryot Cell 9: 46-58.
63. Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, et al. (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28: 957-963.
64. Hsueh YP, Fraser JA, Heitman J, (2008) Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans. Eukaryot Cell 7: 1847-1855.
65. Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, et al. (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci U S A 104: 18730-18735.
66. Metin B, Findley K, Heitman J, (2010) The mating type locus (MAT) and sexual reproduction of Cryptococcus heveanensis: insights into the evolution of sex-determining chromosomal regions in fungi. PLoS Genet 6: e1000961 doi:10.1371/journal.pgen.1000961.
67. Swanson WJ, Vacquier VD, (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137-144.
68. Clark NL, Aagaard JE, Swanson WJ, (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131: 11-22.
69. Wik L, Karlsson M, Johannesson H, (2008) The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8: 109.
70. Müller P, Weinzierl G, Brachmann A, Feldbrügge M, Kahmann R, (2003) Mating and pathogenic development of the Smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot Cell 2: 1187-1199.
71. Hakes L, Lovell SC, Oliver SG, Robertson DL, (2007) Specificity in protein interactions and its relationship with sequence diversity and coevolution. Proc Natl Acad Sci U S A 104: 7999-8004.
72. Cosmides LM, Tooby J, (1981) Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89: 83-129.
73. Birky CW, (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A 92: 11331-11338.
74. Partridge L, Hurst LD, (1998) Sex and conflict. Science 281: 2003-2008.
75. Xu J, (2005) The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48: 951-958.
76. Basse CW, (2010) Mitochondrial inheritance in fungi. Current Opinion in Microbiology 13: 712-719.
77. Baack EJ, Rieseberg LH, (2007) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17: 513-518.
78. Burke JM, Arnold ML, (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35: 31-52.
79. Mallet J, (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc Lond B Biol Sci 363: 2971-2986.
80. Giraud T, Refregier G, Le Gac M, de Vienne DM, Hood ME, (2008) Speciation in fungi. Fungal Genet Biol 45: 791-802.
81. Qvarnström A, Bailey RI, (2008) Speciation through evolution of sex-linked genes. Heredity 102: 4-15.
82. Mallet J, (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229-237.
83. Mallet J, (2007) Hybrid speciation. Nature 446: 279-283.
84. Begerow D, Göker M, Lutz M, Stoll M, (2004) On the evolution of smut fungi on their hosts. In: Agerer R, Piepenbring M, Blanz P, editors. Frontiers in basidiomycote mycology Eching IHW Verlag pp. 81-98.
85. Munkacsi AB, Stoxen S, May G, (2007) Domestication of maize, sorghum, and sugarcane did not drive the divergence of their smut pathogens. Evolution 61: 388-403.
86. Newcombe G, Stirling B, Bradshaw HD, (2001) Abundant Pathogenic Variation in the New Hybrid Rust Melampsora xcolumbiana on Hybrid Poplar. Phytopathology 91: 981-985.
87. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW, (2011) GenBank. Nucleic Acids Res 39: D32-7.
88. Banuett F, Herskowitz I, (1989) Different a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci U S A 86: 5878-5882.
89. Brachmann A, König J, Julius C, Feldbrügge M, (2004) A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272: 216-226.
90. Hoffman CS, Winston F, (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
91. White TJ, Bruns TD, Lee S, Taylor DR, (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky J, White TJ, editors. PCR Protocols: a Guide to Methods and Amplification San Diego Academic Press pp. 315-322.
92. Gargas A, Taylor JW, (1992) Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84: 589-592.
93. Moncalvo JM, Wang H, Hseu RS, (1995) Phylogenetic relationships in Ganoderma inferred from the internal transcribed spacers and 25S ribosomal DNA sequences. Mycologia 87: 223-238.
94. Vigalys R, Hester M, (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238-4246.
95. Rehner SA, Buckley E, (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-alpha sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97: 84-98.
96. Oligo-Calc: Oliginucleotide Properties Calculator. Available: http://basic.northwestern.edu/biotools/OligoCalc.html via the Internet.
97. Kibbe WA, (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35: W43-46 doi:10.1093/nar/gkm234.
98. Katoh K, Asimenos G, Toh H, (2009) Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537: 39-64.
99. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
100. Thompson JD, Higgins DG, Gibson TJ, (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.
101. Felsenstein J, (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368-376.
102. Stamatakis A, Ludwig T, Meier H, (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456-463.
103. Stamatakis A, Hoover P, Rougemont J, (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57: 758-771.
104. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
105. MUMDB MIPS Ustilago Maydis DataBase. Available: http://mips.helmholtz-muenchen.de/genre/proj/ustilago via the Internet.
106. MSRDB MIPS Sporisorium Reilianum DataBase. Available: http://mips.helmholtz-muenchen.de/genre/proj/sporisorium/ via the Internet.
107. Hofmann K, Stoffel W, (1993) TMbase- A database of membrane spanning proteins segments. Biol Chem 374: 166.
108. Nugent T, Jones DT, (2009) Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 10: 159.
109. Buchan DW, Ward SM, Lobley AE, Nugent TC, Bryson K, et al. (2010) Protein annotation and modelling servers at University College London. Nucleic Acids Res 38: W563-8.
110. Librado P, Rozas J, (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
111. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
112. Yang Z, (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol 24: 1586-1591.
113. Yang Z, Wong WS, Nielsen R, (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107-1118.
114. Korber B, (2000) Computational Analysis of HIV Molecular Sequences. In: Rodrigo AG, Learn GH, editors. HIV Signature and Sequence Variation Analysis Netherlands Kluwer Academic Publishers pp. 55-72.
115. McDowell EM, Trump BF, (1976) Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100: 405-414.