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Interspecific Sex in Grass Smuts and the Genetic Diversity of Their Pheromone-Receptor System


The grass smuts comprise a speciose group of biotrophic plant parasites, so-called Ustilaginaceae, which are specifically adapted to hosts of sweet grasses, the Poaceae family. Mating takes a central role in their life cycle, as it initiates parasitism by a morphological and physiological transition from saprobic yeast cells to pathogenic filaments. As in other fungi, sexual identity is determined by specific genomic regions encoding allelic variants of a pheromone-receptor (PR) system and heterodimerising transcription factors. Both operate in a biphasic mating process that starts with PR–triggered recognition, directed growth of conjugation hyphae, and plasmogamy of compatible mating partners. So far, studies on the PR system of grass smuts revealed diverse interspecific compatibility and mating type determination. However, many questions concerning the specificity and evolutionary origin of the PR system remain unanswered. Combining comparative genetics and biological approaches, we report on the specificity of the PR system and its genetic diversity in 10 species spanning about 100 million years of mating type evolution. We show that three highly syntenic PR alleles are prevalent among members of the Ustilaginaceae, favouring a triallelic determination as the plesiomorphic characteristic of this group. Furthermore, the analysis of PR loci revealed increased genetic diversity of single PR locus genes compared to genes of flanking regions. Performing interspecies sex tests, we detected a high potential for hybridisation that is directly linked to pheromone signalling as known from intraspecies sex. Although the PR system seems to be optimised for intraspecific compatibility, the observed functional plasticity of the PR system increases the potential for interspecific sex, which might allow the hybrid-based genesis of newly combined host specificities.


Vyšlo v časopise: Interspecific Sex in Grass Smuts and the Genetic Diversity of Their Pheromone-Receptor System. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002436
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002436

Souhrn

The grass smuts comprise a speciose group of biotrophic plant parasites, so-called Ustilaginaceae, which are specifically adapted to hosts of sweet grasses, the Poaceae family. Mating takes a central role in their life cycle, as it initiates parasitism by a morphological and physiological transition from saprobic yeast cells to pathogenic filaments. As in other fungi, sexual identity is determined by specific genomic regions encoding allelic variants of a pheromone-receptor (PR) system and heterodimerising transcription factors. Both operate in a biphasic mating process that starts with PR–triggered recognition, directed growth of conjugation hyphae, and plasmogamy of compatible mating partners. So far, studies on the PR system of grass smuts revealed diverse interspecific compatibility and mating type determination. However, many questions concerning the specificity and evolutionary origin of the PR system remain unanswered. Combining comparative genetics and biological approaches, we report on the specificity of the PR system and its genetic diversity in 10 species spanning about 100 million years of mating type evolution. We show that three highly syntenic PR alleles are prevalent among members of the Ustilaginaceae, favouring a triallelic determination as the plesiomorphic characteristic of this group. Furthermore, the analysis of PR loci revealed increased genetic diversity of single PR locus genes compared to genes of flanking regions. Performing interspecies sex tests, we detected a high potential for hybridisation that is directly linked to pheromone signalling as known from intraspecies sex. Although the PR system seems to be optimised for intraspecific compatibility, the observed functional plasticity of the PR system increases the potential for interspecific sex, which might allow the hybrid-based genesis of newly combined host specificities.


Zdroje

1. WeismannA 1886 Zur Frage nach der Vererbung erworbener Eigenschaften. Biologisches Zentralblatt 6 33 48

2. HamiltonWDAxelrodRTaneseR 1990 Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci U S A 87 3566 3573

3. WilhelmDPalmerSKoopmanP 2007 Sex determination and gonadal development in mammals. Physiol Rev 87 1 28

4. JohnsonMTSmithSDRausherMD 2009 Plant sex and the evolution of plant defenses against herbivores. Proc Natl Acad Sci U S A 106 18079 18084

5. LeeSCNiMLiWShertzCHeitmanJ 2010 The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74 298 340

6. SekidoRLovell-BadgeR 2009 Sex determination and SRY: down to a wink and a nudge? Trends Genet 25 19 29

7. BarrettSC 2010 Understanding plant reproductive diversity. Philos Trans R Soc Lond B Biol Sci 365 99 109

8. HarshmanLGZeraAJ 2007 The cost of reproduction: the devil in the details. Trends Ecol Evol 22 80 86

9. GoddardMRGodfrayHCBurtA 2005 Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434 636 640

10. AanenDKHoekstraRF 2007 Why Sex Is Good: On Fungi and Beyond. HeitmanJKronstadJWTaylorDRCasseltonLA Sex in fungi - Molecular Determination and Evolutionary Implications Washington D.C. ASM Press 527 534

11. CasseltonLA 2002 Mate recognition in fungi. Heredity 88 142 147

12. HeitmanJKronstadJWTaylorDRCasseltonLA 2007 Sex in fungi - Molecular Determination and Evolutionary Implications Washington ASM Press 572

13. KniepH 1928 Die Sexualität der niederen Pflanzen Jena Fisher 544

14. RaperJ 1966 Genetics of Sexuality in Higher Fungi New York The Ronald Press Co 283

15. CasseltonLAOlesnickyNS 1998 Molecular genetics of mating recognition in basidiomycete fungi. Microbiol Mol Biol Rev 62 55 70

16. KüesU 2000 Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64 316 353

17. KotheEGolaSWendlandJ 2003 Evolution of multispecific mating-type alleles for pheromone perception in the homobasidiomycete fungi. Curr Genet 42 268 275

18. RaudaskoskiMKotheE 2010 Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9 847 859

19. HuGKampALinningRNaikSBakkerenG 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. FowlerTJDeSimoneSMMittonMFKurjanJRaperCA 1999 Multiple sex pheromones and receptors of a mushroom-producing fungus elicit mating in yeast. Mol Biol Cell 10 2559 2572

21. BakkerenGKronstadJW 1996 The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143 1601 1613

22. MayGShawFBadraneHVekemansX 1999 The signature of balancing selection: fungal mating compatibility gene evolution. Proc Natl Acad Sci U S A 96 9172 9177

23. DevierBAguiletaGHoodMEGiraudT 2008 Ancient Trans-specific Polymorphism at Pheromone Receptor Genes in Basidiomycetes. Genetics 181 209 223

24. CasseltonLAKüesU 2007 The Origin of Multiple Mating Types in the Model Mushrooms Coprinopsis cinerea and Schizophyllum commune. HeitmanJKronstadJWTaylorDRCasseltonLA Sex in fungi - Molecular Determination and Evolutionary Implications Washington D.C. ASM Press 283 300

25. FraserJADiezmannSSubaranRLAllenALengelerKB 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. JamesTYSrivilaiPKüesUVilgalysR 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. CoelhoMASampaioJPGoncalvesP 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. SpelligTBölkerMLottspeichFFrankRWKahmannR 1994 Pheromones trigger filamentous growth in Ustilago maydis. EMBO J 13 1620 1627

29. XueCHsuehYPHeitmanJ 2008 Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32 1010 1032

30. FeldbrüggeMBölkerMSteinbergGKämperJKahmannR 2006 Regulatory and structural networks orchestrating mating, dimorphism, cell shape, and pathogenesis in Ustilago maydis. KüesUFisherR The Mycota I: growth, differentiation and sexuality Heidelberg Springer-Verlag 375 391

31. FowlerTJMittonMFVaillancourtLJRaperCA 2001 Changes in mate recognition through alterations of pheromones and receptors in the multisexual mushroom fungus Schizophyllum commune. Genetics 158 1491 1503

32. OlesnickyNSBrownAJHondaYDyosSLDowellSJ 2000 Self-compatible B mutants in Coprinus with altered pheromone-receptor specificities. Genetics 156 1025 1033

33. GolaSKotheE 2003 The little difference: in vivo analysis of pheromone discrimination in Schizophyllum commune. Curr Genet 42 276 283

34. SzaboZTönnisMKesslerHFeldbrüggeM 2002 Structure-function analysis of lipopeptide pheromones from the plant pathogen Ustilago maydis. Mol Genet Genomics 268 362 370

35. KostedPJGerhardtSAAndersonCMStierleASherwoodJE 2000 Structural requirements for activity of the pheromones of Ustilago hordei. Fungal Genet Biol 29 107 117

36. FisherGWHoltonCS 1957 Biology and Control of the Smut Fungi New York The Ronald Press Company 622

37. StollMBegerowDOberwinklerF 2005 Molecular phylogeny of Ustilago, Sporisorium, and related taxa based on combined analyses of rDNA sequences. Mycol Res 109 342 356

38. BegerowDStollMBauerR 2006 A phylogenetic hypothesis of Ustilaginomycotina based on multiple gene analyses and morphological data. Mycologia 98 906 916

39. UrbanMKahmannRBölkerM 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. SnetselaarKMBölkerMKahmannR 1996 Ustilago maydis Mating Hyphae Orient Their Growth toward Pheromone Sources. Fungal Genet Biol 20 299 312

41. BakkerenGJiangGWarrenRLButterfieldYShinH 2006 Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet Biol 43 655 666

42. SchirawskiJHeinzeBWagenknechtMKahmannR 2005 Mating type loci of Sporisorium reilianum: novel pattern with three a and multiple b specificities. Eukaryot Cell 4 1317 1327

43. KämperJKahmannRBölkerMMaLJBrefortT 2006 Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444 97 101

44. BrefortTDoehlemannGMendoza-MendozaAReissmannSDjameiA 2009 Ustilago maydis as a Pathogen. Annu Rev Phytopathol 47 423 445

45. VollmeisterESchipperKBaumannSHaagCPohlmannT 2011 Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev DOI:10.1111/j.1574-6976.2011.00296.x

46. KaffarnikFMüllerPLeibundgutMKahmannRFeldbrüggeM 2003 PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22 5817 5826

47. ZarnackKEichhornHKahmannRFeldbrüggeM 2008 Pheromone-regulated target genes respond differentially to MAPK phosphorylation of transcription factor Prf1. Mol Microbiol 69 1041 1053

48. KahmannRKämperJ 2004 Ustilago maydis: how its biology relates to pathogenic development. New Phytologist 164 31 42

49. RowellJBDeVayJE 1954 Genetics of Ustilago zeae in relation to basic problems of its pathogenicity. Phytopathology 44 356 362

50. FedlerMLuhKSStelterKNieto-JacoboFBasseCW 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. AltschulSFMaddenTLSchäfferAAZhangJZhangZ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402

52. WebbCOAckerlyDDKembelSW 2008 Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24 2098 2100

53. BannaiHTamadaYMaruyamaONakaiKMiyanoS 2002 Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18 298 305

54. BortfeldMAuffarthKKahmannRBasseCW 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. StankeMDiekhansMBaertschRHausslerD 2008 Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24 637 644

56. SchultzJMilpetzFBorkPPontingCP 1998 SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95 5857 5864

57. LetunicIDoerksTBorkP 2009 SMART 6: recent updates and new developments. Nucleic Acids Res 37 D229 32

58. RomeisTBrachmannAKahmannRKämperJ 2000 Identification of a target gene for the bE-bW homeodomain protein complex in Ustilago maydis. Mol Microbiol 37 54 66

59. BrachmannAWeinzierlGKämperJKahmannR 2001 Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42 1047 1063

60. PrasadVStrombergCAAlimohammadianHSahniA 2005 Dinosaur coprolites and the early evolution of grasses and grazers. Science 310 1177 1180

61. CasseltonLAFeldbrüggeM 2010 Mating and sexual morphogenesis in basidiomycete fungi. BorkovichKEbboleD Cellular and Molecular Biology of Filamentous Fungi Washington D.C. ASM Press 536 551

62. LiWMetinBWhiteTCHeitmanJ 2010 Organization and evolutionary trajectory of the mating type (MAT) locus in dermatophyte and dimorphic fungal pathogens. Eukaryot Cell 9 46 58

63. OhmRAde JongJFLugonesLGAertsAKotheE 2010 Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28 957 963

64. HsuehYPFraserJAHeitmanJ 2008 Transitions in sexuality: recapitulation of an ancestral tri- and tetrapolar mating system in Cryptococcus neoformans. Eukaryot Cell 7 1847 1855

65. XuJSaundersCWHuPGrantRABoekhoutT 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. MetinBFindleyKHeitmanJ 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. SwansonWJVacquierVD 2002 The rapid evolution of reproductive proteins. Nat Rev Genet 3 137 144

68. ClarkNLAagaardJESwansonWJ 2006 Evolution of reproductive proteins from animals and plants. Reproduction 131 11 22

69. WikLKarlssonMJohannessonH 2008 The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8 109

70. MüllerPWeinzierlGBrachmannAFeldbrüggeMKahmannR 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. HakesLLovellSCOliverSGRobertsonDL 2007 Specificity in protein interactions and its relationship with sequence diversity and coevolution. Proc Natl Acad Sci U S A 104 7999 8004

72. CosmidesLMToobyJ 1981 Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89 83 129

73. BirkyCW 1995 Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A 92 11331 11338

74. PartridgeLHurstLD 1998 Sex and conflict. Science 281 2003 2008

75. XuJ 2005 The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48 951 958

76. BasseCW 2010 Mitochondrial inheritance in fungi. Current Opinion in Microbiology 13 712 719

77. BaackEJRiesebergLH 2007 A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17 513 518

78. BurkeJMArnoldML 2001 Genetics and the fitness of hybrids. Annu Rev Genet 35 31 52

79. MalletJ 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. GiraudTRefregierGLe GacMde VienneDMHoodME 2008 Speciation in fungi. Fungal Genet Biol 45 791 802

81. QvarnströmABaileyRI 2008 Speciation through evolution of sex-linked genes. Heredity 102 4 15

82. MalletJ 2005 Hybridization as an invasion of the genome. Trends Ecol Evol 20 229 237

83. MalletJ 2007 Hybrid speciation. Nature 446 279 283

84. BegerowDGökerMLutzMStollM 2004 On the evolution of smut fungi on their hosts. AgererRPiepenbringMBlanzP Frontiers in basidiomycote mycology Eching IHW Verlag 81 98

85. MunkacsiABStoxenSMayG 2007 Domestication of maize, sorghum, and sugarcane did not drive the divergence of their smut pathogens. Evolution 61 388 403

86. NewcombeGStirlingBBradshawHD 2001 Abundant Pathogenic Variation in the New Hybrid Rust Melampsora xcolumbiana on Hybrid Poplar. Phytopathology 91 981 985

87. BensonDAKarsch-MizrachiILipmanDJOstellJSayersEW 2011 GenBank. Nucleic Acids Res 39 D32 7

88. BanuettFHerskowitzI 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. BrachmannAKönigJJuliusCFeldbrüggeM 2004 A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272 216 226

90. HoffmanCSWinstonF 1987 A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57 267 272

91. WhiteTJBrunsTDLeeSTaylorDR 1990 Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. InnisMAGelfandDHSninskyJWhiteTJ PCR Protocols: a Guide to Methods and Amplification San Diego Academic Press 315 322

92. GargasATaylorJW 1992 Polymerase chain reaction (PCR) primers for amplifying and sequencing nuclear 18S rDNA from lichenized fungi. Mycologia 84 589 592

93. MoncalvoJMWangHHseuRS 1995 Phylogenetic relationships in Ganoderma inferred from the internal transcribed spacers and 25S ribosomal DNA sequences. Mycologia 87 223 238

94. VigalysRHesterM 1990 Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172 4238 4246

95. RehnerSABuckleyE 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. KibbeWA 2007 OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35 W43 46 doi:10.1093/nar/gkm234

98. KatohKAsimenosGTohH 2009 Multiple alignment of DNA sequences with MAFFT. Methods Mol Biol 537 39 64

99. HallTA 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. ThompsonJDHigginsDGGibsonTJ 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. FelsensteinJ 1981 Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17 368 376

102. StamatakisALudwigTMeierH 2005 RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21 456 463

103. StamatakisAHooverPRougemontJ 2008 A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57 758 771

104. RonquistFHuelsenbeckJP 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. HofmannKStoffelW 1993 TMbase - A database of membrane spanning proteins segments. Biol Chem 374 166

108. NugentTJonesDT 2009 Transmembrane protein topology prediction using support vector machines. BMC Bioinformatics 10 159

109. BuchanDWWardSMLobleyAENugentTCBrysonK 2010 Protein annotation and modelling servers at University College London. Nucleic Acids Res 38 W563 8

110. LibradoPRozasJ 2009 DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 1451 1452

111. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556

112. YangZ 2007 PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol 24 1586 1591

113. YangZWongWSNielsenR 2005 Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22 1107 1118

114. KorberB 2000 Computational Analysis of HIV Molecular Sequences. RodrigoAGLearnGH HIV Signature and Sequence Variation Analysis Netherlands Kluwer Academic Publishers 55 72

115. McDowellEMTrumpBF 1976 Histologic fixatives suitable for diagnostic light and electron microscopy. Arch Pathol Lab Med 100 405 414

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