Mating system of the anther smut fungus Microbotryum violaceum: Selfing under heterothallism

Eukaryotic Cell

Volumn 7, Issue 5, 2008, Pages 765-775

  Giraud, Tatiana ^a,b   Yockteng, Roxana ^c   López Villavicencio, Manuela ^c   Refrégier, Guislaine ^a,b   Hood, Michael E ^d  

^a UNIVERSITÉ PARIS SUD   (France)

^b CNRS   (France)

^c MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^d AMHERST COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIDIOMYCETES; CARYOPHYLLACEAE; CELL DIVISION; CHROMOSOME; CLASSIFICATION; CYTOLOGY; FLOWER; FUNGAL GENE; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; SHORT SURVEY;

BASIDIOMYCOTA; CARYOPHYLLACEAE; CELL DIVISION; CHROMOSOMES, FUNGAL; FLOWERS; GENES, MATING TYPE, FUNGAL; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES;

FUNGI; MICROBOTRYUM VIOLACEUM;

EID: 47049093932     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00440-07     Document Type: Short Survey

References (114)

1. Aimi, T., R. Yoshida, M. Ishikawa, D. Bao, and Y. Kitamoto. 2005. Identification and linkage mapping of the genes for the putative homeodomain protein (hox1) and the putative pheromone receptor protein homologue (rcb1) in a bipolar basidiomycete, Pholiota nameko. Curr. Genet. 48:184-194.
2. Alexander, H. M. 1990. Epidemiology of the anther-smut fungus infection of Silene alba caused by Ustilago violacea: patterns of spore deposition and disease incidence. J. Ecol. 78:166-179.
3. Alexander, H. M., and J. Antonovics. 1988. Disease spread and population dynamics of anther-smut fungus of Silene alba caused by the fungus Ustilago violacea. J. Ecol. 76:91-104.
4. Allsop, D. J., and S. A. West. 2003. Changing sex at the same relative body size: similar forces may select for gender switching across taxa in all animals with this facility. Nature 425:783-784.
5. Almaraz, T., C. Roux, S. Maumont, and G. Durrieu. 2002. Phylogenetic relationships among smut fungi parasitizing dicotyledons based on ITS sequence analysis. Mycol. Res. 106:541-548.
6. Ames, L. M. 1934. Hermaphroditism involving self-sterility and cross-fertility in the Ascomycete Pleurage anserine. Mycologia 26:392-414.
7. Antonovics, J., M. Hood, J. Partain, and A. M. Heuhsen. 2002. The ecology and genetics of a host-shift: Microbotryum as a model system. Am. Nat. 160:S40-S53.
8. Antonovics, J., Y. Iwasa, and M. P. Hassel. 1995. A generalized model of parasitoid, venereal, and vector-based transmission processes. Am. Nat. 145:661-675.
9. Antonovics, J., K. O'Keefe, and M. E. Hood. 1998. Theoretical population genetics of mating-type linked haplo-lethal alleles. Int. J. Plant Sci. 159:192-198.
10. Antonovics, J., D. Stratton, P. H. Thrall, and A. Jarosz. 1996. Anther-smut disease (Ustilago violacea) of fire-pink (Silene virginica): its biology and relationship to the anther-smut disease of white campion (Silene alba). Am. Midl. Nat. 135:130-143.
11. Baker, H. G. 1947. Infection of species of Melandrium by Ustilago violacea (Pers.) Fuckel and the transmission of the resultant disease. Ann. Bot. 11:333-348.
12. Bakkeren, G., G. Jiang, R. L. Warren, Y. Butterfield, H. Shin, R. Chiu, R. Linning, J. Schein, N. Lee, and G. Hu. 2006. Mating factor linkage and genome evolution in basidiomycetous pathogens of cereals. Fungal Genet. Biol. 43:655-666.
13. Bakkeren, G., and J. Kronstad. 2007. Bipolar and tetrapolar mating systems in the ustilaginales, p. 389-404. In J. Heitman, J. Kronstad, J. Taylor, and L. Casselton (ed.), Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC.
14. Bakkeren, G., and J. W. Kronstad. 1994. Linkage of mating type loci distinguishes bipolar from tetrapolar mating in basidiomycetous smut fungi. Proc. Natl. Acad. Sci. USA 91:7085-7089.
15. Bakkeren, G., and J. W. Kronstad. 1996. The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143:1601-1613.
16. Banuett, F. 1995. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 29:179-208.
17. Bennett, R. J., and A. D. Johnson. 2005. Mating in Candida albicans and the search for a sexual cycle. Annu. Rev. Microbiol. 59:233-255.
18. Bucheli, E., B. Gautschi, and J. A. Shykoff. 2000. Host specific differentiation in the anther smut fungus Microbotryum violaceum as revealed by microsatellites. J. Evol. Biol. 13:188-198.
19. Bucheli, E., and J. A. Shykoff. 1999. The influence of plant spacing on density-dependent versus frequency-dependent spore transmission of the anther smut fungus Microbotryum violaceum. Oecologia 119:55-62.
20. Casselton, L. A. 2002. Mate recognition in fungi. Heredity 88:142-147.
21. Charlesworth, D., B. Charlesworth, and G. Marais. 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118-128.
22. Coppin, E., R. Debuchy, S. Arnaise, and M. Picard. 1997. Mating types and sexual development in filamentous ascomycetes. Microbiol. Mol. Biol. Rev. 61:411-.
23. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
24. Czárán, T. L., and R. F. Hoekstra. 2004. Evolution of sexual asymmetry. BMC Evol. Biol. 4:34.
25. Darlington, L. C., and R. L. Kiesling. 1975. A compatibility-linked, haplolethal factor in race 1, Ustilago nigra (Tapke). North Dakota Acad. Sci. 27:116-119.
26. Delmotte, F., E. Bucheli, and J. A. Shykoff. 1999. Host and parasite population structure in a natural plant-pathogen system. Heredity 82:300-308.
27. Deml, G., and F. Oberwinkler. 1982. Studies in Heterobasidiomycetes. Part 24. On Ustilago violacea (Pers.) Rouss. from Saponaria officinalis L. Phytopathol. Z. 104:345-356.
28. Denchev, C. M. 2007. Microbotryum lagerheimii sp. nov. (Microbotryaceae). Mycologica Balcanica 4:61-67.
29. Denchev, C. M. 2007. Microbotryum savilei sp. nov. (Microbotryaceae). Mycologica Balcanica 4:69-73.
30. Dodge, B. O. 1936. Facultative and obligate heterothallism in Ascomycetes. Mycologia 28:399-409.
31. Feldbrugge, M., J. Kamper, G. Steinberg, and R. Kahmann. 2004. Regulation of mating and pathogenic development in Ustilago maydis. Curr. Opin. Microbiol. 7:666-672.
32. Fischer, G. 1940. Two cases of haplo-lethal deficiency in Ustilago bullata operative against saprophytism. Mycologia 32:275-289.
33. Fishman, L., and R. Wyatt. 1999. Pollinator-mediated competition, reproductive character displacement, and the evolution of selfing in Arenaria uniflora (Caryophyllaceae). Evolution 53:1723-1733.
34. Fraser, J., and J. Heitman. 2005. Chromosomal sex-determining regions in animals, plants and fungi. Curr. Opin. Genet. Dev. 15:645-651.
35. Fraser, J. A., S. Diezmann, R. L. Subaran, A. Allen, K. B. Lengeler, F. S. Dietrich, and J. Heitman. 2004. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biol. 2:2243-2255.
36. Fraser, J. A., and J. Heitman. 2004. Evolution of fungal sex chromosomes. Mol. Microbiol. 51:299-306.
37. Freeman, A. B., K. Kellye, T.-L. Shi, C. F. Hughes, and M. H. Perlin. 2002. Isolates of Microbotryum violaceum from North American host species are phylogenetically distinct from their European host-derived counterparts. Mol. Phylogenet. Evol. 23:158-170.
38. Gallegos, A., D. J. Jacobson, N. B. Raju, M. P. Skupski, and D. O. Natvig. 2000. Suppressed recombination and a pairing anomaly on the mating-type chromosome of Neurospora tetrasperma. Genetics 154:623-633.
39. Garber, E. D., and M. Ruddat. 2002. Transmission genetics of Microbotryum violaceum (Ustilago violacea): a case study. Adv. Appl. Microbiol. 51:107-127.
40. Giraud, T. 2004. Patterns of within population dispersion and mating of the fungus Microbotryum violaceum parasitising the plant Silene latifolia. Heredity 93:559-565.
41. Giraud, T., O. Jonot, and J. Shykoff. 2006. Common sex-linked deleterious alelles in a parasitic fungus alter infection success but show no pleiotropic advantage. J. Evol. Biol. 19:970-980.
42. Giraud, T., O. Jonot, and J. A. Shykoff. 2005. Selfing propensity under choice conditions in a parasitic fungus, Microbotryum violaceum, and parameters influencing infection success in artificial inoculations. Int. J. Plant Sci. 166:649-657.
43. Giraud, T., G. Refrégier, D. M. de Vienne, M. Le Gac, and M. E. Hood. Speciation in fungi. Fungal Genet. Biol., in press.
44. Glemin, S., T. Bataillon, J. Ronfort, A. Mignot, and I. Olivieri. 2001. Inbreeding depression in small populations of self-incompatible plants. Genetics 159:1217-1229.
45. Gouyon, P.-H. 1999. Sex: a pluralist approach includes species selection. (One step beyond and it's good). J. Evol. Biol. 12:1029-1030.
46. Granberg, A., U. Carlsson-Graner, P. Arnqvist, and B. Giles. 2008. Variation in breeding system traits within and among populations of Microbotryum violaceum on Silene dioica. Int. J. Plant Sci. 169:293-303.
47. Grasso, V. 1955. A haplo-lethal deficiency in Ustilago kolleri. Phytopathology 45:521-522.
48. Hagen, D. C., G. McCaffrey, and G. F. Sprague. 1986. Evidence the yeast Ste3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc. Natl. Acad. Sci. USA 83:1418-1422.
49. Halsall, J., M. Milner, and L. Casselton. 2000. Three subfamilies of pheromone and receptor genes generate multiple B mating specificities in the mushroom Coprinus cinereus. Genetics 154:1115-1123.
50. Handley, L. L., H. Ceplitis, and H. Ellegren. 2004. Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167:367-376.
51. Hedrick, P. 1987. Population genetics of intragametophytic selfing. Evolution 41:137-144.
52. Hood, M. E. 2002. Dimorphic mating-type chromosomes in the fungus Microbotryum violaceum. Genetics 160:457-461.
53. Hood, M. E. 2003. Dynamics of multiple infection and within-host competition by the anther-smut pathogen. Am. Nat. 162:122-133.
54. Hood, M. E. 2005. Repetitive DNA in the automictic fungus Microbotryum violaceum. Genetica 124:1-10.
55. Hood, M. E., and J. Antonovics. 1998. Two-celled promycelia and matingtype segregation in Ustilago violacea (Microbotryum violaceum). Int. J. Plant Sci. 159:199-205.
56. Hood, M. E., and J. Antonovics. 2000. Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea). Heredity 85:231-241.
57. Hood, M. E., J. Antonovics, and B. Koskella. 2004. Shared forces of sex chromosome evolution in haploids and diploids. Genetics 168:141-146.
58. Hood, M. E., and J. A. Antonovics. 2004. Mating within the meiotic tetrad and the maintenance of genomic heterozygosity. Genetics 166:1751-1759.
59. Hood, M. E., M. Katawezik, and T. Giraud. 2005. Repeat-induced point mutation and the population structure of transposable elements in Microbotryum violaceum. Genetics 170:1081-1089.
60. Iwasa, Y., and A. Sasaki. 1987. Evolution of the number of sexes. Evolution 41:49-65.
61. James, T., P. Srivilai, U. Kues, and R. Vilgalys. 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.
62. Janzen, F. J., and G. L. Paukstis. 1991. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66:149-179.
63. Johnson, L. J., J. Antonovics, and M. E. Hood. 2005. The evolution of intratetrad mating rate. Evolution 59:2525-2532.
64. Kaltz, O., S. Gandon, Y. Michalakis, and J. Shykoff. 1999. Local maladaptation of the plant pathogen Microbotryum violaceum to its host Silene latifolia: evidence from a cross-inoculation experiment. Evolution 53:395-407.
65. Kaltz, O., and J. A. Shykoff. 1997. Sporidial mating-type ratios of teliospores from natural populations of the anther smut fungus Microbotryum (=Ustilago) violaceum. Int. J. Plant Sci. 158:575-584.
66. Kaltz, O., and J. A. Shykoff. 1999. Selfing propensity of the fungal pathogen Microbotryum violaceum varies across Silene latifolia host plants. J. Evol. Biol. 12:340-349.
67. Kemler, M., M. Goker, F. Oberwinkler, and D. Begerow. 2006. Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evol. Biol. 6:35.
68. Kirby, G. C. 1984. Breeding systems and heterozygosity in populations of tetrad forming fungi. Heredity 52:35-41.
69. Kniep, H. 1919. Untersuchungen uber den Antherenbrand (Ustilago violacea Pers.). Ein Beitrag zum sexualitatproblem. Z. Botanike 11:257-284.
70. Knop, M. 2006. Evolution of the hemiascomyclete yeasts: on life styles and the importance of inbreeding. Bioessays 28:696-708.
71. Kohn, L. M. 2005. Mechanisms of fungal speciation. Annu. Rev. Phytopathol. 43:279-308.
72. Korpelainen, H. 1998. Labile sex expression in plants. Biol. Rev. 73:157-180.
73. Lahn, B. T., and D. C. Page. 1999. Four evolutionary strata on the human X chromosome. Science 286:964-967.
74. Le Gac, M., M. E. Hood, E. Fournier, and T. Giraud. 2007. Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61:15-26.
75. Le Gac, M., M. E. Hood, and T. Giraud. 2007. Evolution of reproductive isolation within a parasitic fungal complex. Evolution 61:1781-1787.
76. Lewis, K. R., and B. John. 1963. Chromosome marker. Little and Brown, Boston, MA.
77. Lin, X., and J. Heitman. 2007. Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism, p. 35-57. In J. Heitman, J. Kronstad, J. Taylor, and L. Casselton (ed.), Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC.
78. Lin, X. R., C. M. Hull, and J. Heitman. 2005. Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434:1017-1021.
79. Lopez-Villavicencio, M., J. Enjalbert, M. E. Hood, J. A. Shykoff, C. Raquin, and T. Giraud. 2005. The anther smut disease on Gypsophila repens: a case of parasite sub-optimal performance following a recent host shift? J. Evol. Biol. 18:1293-1303.
80. Lopez-Villavicencio, M., O. Jonot, A. Coantic, M. Hood, J. Enjalbert, and T. Giraud. 2007. Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathogens 3:e176.
81. Lutz, M., M. Goker, M. Piatek, M. Kemler, D. Begerow, and F. Oberwinkler. 2005. Anther smuts of Caryophyllaceae: molecular characters indicate host-dependent species delimitation. Mycol. Prog. 4:225-238.
82. Magnin, A. 1888. Sur l'hermaphrodisme parasitaire et le polymorphisme floral du Lychnis dioica. C. R. Acad. Paris 107:663-665.
83. May, G., F. Shaw, H. Badrane, and X. Vekemans. 1999. The signature of balancing selection: fungal mating compatibility gene evolution. Proc. Natl. Acad. Sci. USA 96:9172-9177.
84. Merino, S. T., M. A. Nelson, D. J. Jacobson, and D. O. Natvig. 1996. Pseudohomothallism and evolution of the mating-type chromosome in Neurospora tetrasperma. Genetics 143:789-799.
85. Nauta, M. J., and R. F. Hoekstra. 1992. Evolution of reproductive systems in filamentous ascomycetes. I. Evolution of mating types. Heredity 68:405-410.
86. Nauta, M. J., and R. F. Hoekstra. 1992. Evolution of reproductive systems in filamentous ascomycetes. II. Evolution of hermaphroditism and other reproductive strategies. Heredity 68:537-546.
87. Nicolas, M., G. Marais, V. Hykelova, B. Janousek, V. Laporte, B. Vyskot, D. Mouchiroud, I. Negrutiu, D. Charlesworth, and F. Monéger. 2005. A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol. 3:e4.
88. Nielson, J. 1968. Isolation and culture of monokaryotic haplonts of Ustilago nuda, the role of proline in their metabolism, and the inoculation of barley with resynthesized dikaryons. Can. J. Bot. 46:1193-1200.
89. Ohno, S. 1967. Sex chromosomes and sex-linked genes. Springer-Verlag, New York, NY.
90. Oudemans, P. V., H. M. Alexander, J. Antonovics, S. Altizer, P. H. Thrall, and L. Rose. 1998. The distribution of mating-type bias in natural populations of the anther-smut Ustilago violacea on Silene alba in Virginia. Mycologia 90:372-381.
91. Pardo, E. H., S. F. O'Shea, and L. A. Casselton. 1996. Multiple versions of the A mating type locus of Coprinus cinereus are generated by three paralogous pairs of multiallelic homeobox genes. Genetics 144:87-94.
92. Perlin, M. H. 1996. Pathovars or formae speciales of Microbotryum violaceum differ in electrophoretic karyotype. Int. J. Plant Sci. 157:447-452.
93. Porcher, E., and E. Lande. 2005. Loss of gametophytic self-incompatibility with evolution of inbreeding depression. Evolution 59:46-60.
94. Raper, J. 1966. Genetics of sexuality in higher fungi. Ronald Press, New York, NY.
95. Rice, W. R. 1987. The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 4:911-914.
96. Richman, A. 2000. Evolution of balanced genetic polymorphism. Mol. Ecol. 9:1953-1963.
97. Roche, B. M., H. H. Alexander, and A. D. Maltby. 1995. Dispersal and disease gradients of anther-smut infection of Silene alba at different life stages. Ecology 76:1863-1871.
98. Shykoff, J. A., and E. Bucheli. 1995. Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal disease plant. J. Ecol. 83:189-198.
99. Shykoff, J. A., A. Meyhöfer, and E. Bucheli. 1999. Genetic isolation among host races of the anther smut fungus Microbotryum violaceum on three host plant species. Int. J. Plant Sci. 160:907-916.
100. Soumalainen, E., A. Saura, and J. Lokki. 1976. Evolution of parthenogenetic insects. Evol. Biol. 9:209-257.
101. Tellier, A., L. Villaréal, and T. Giraud. 2005. Maintenance of sex-linked deleterious alleles by selfing and group selection in metapopulations of the phytopathogenic fungus Microbotryum violaceum. Am. Nat. 165:577-589.
102. Tellier, A., L. Villaréal, and T. Giraud. 2007. Antagonistic pleiotropy may help population-level selection in maintaining genetic polymorphism for transmission rate in a model phytopathogenic fungus. Heredity 98:45-52.
103. Thomas, A., J. Shykoff, O. Jonot, and T. Giraud. 2003. Mating-type ratio bias in populations of the phytopathogenic fungus Microbotryum violaceum from several host species. Int. J. Plant Sci. 164:641-647.
104. Thomas, Y., M. T. Bethenod, L. Pelozuelo, B. Frerot, and D. Bourguet. 2003. Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hubner. I. Sex pheromone, moth emergence timing, and parasitism. Evolution 57:261-273.
105. Thrall, P. H., and J. Antonovics. 1995. Theoretical and empirical studies of metapopulations: population and genetic dynamics of the Silene-Ustilago system. Can. J. Bot. 73:S1249-S1258.
106. Thrall, P. H., A. Biere, and J. Antonovics. 1993. Plant-life history and disease susceptibility: the occurrence of Ustilago violacea on different species within the Caryophyllaceae. J. Ecol. 81:489-498.
107. Vanky, K. 1998. The genus Microbotryum (smut fungi). Mycotaxon 67:33-60.
108. Van Putten, W. F., A. Biere, and J. M. M. Van Damme. 2003. Intraspecific competition and mating between fungal strains of the anther smut Microbotryum violaceum from the host plants Silene latifolia and S. dioica. Evolution 57:766-776.
109. van Putten, W. F., A. Biere, and J. M. M. Van Damme. 2005. Host related genetic differentiation in the anther smut fungus Microbotryum violaceum in sympatric, parapatric and allopatric populations of two host species Silene latifolia and S. dioica. J. Evol. Biol. 18:203-212.
110. van Putten, W. F., J. A. Elzinga, and A. Biere. 2007. Host fidelity of the pollinator guilds of Silene dioica and Silene latifolia: possible consequences for sympatric host race differentiation of a vectored plant disease. Int. J. Plant Sci. 168:421-434.
111. Xu, J., C. W. Saunders, P. Hu, R. A. Grant, T. Boekhout, E. E. Kuramae, J. W. Kronstad, Y. M. DeAngelis, N. L. Reeder, K. R. Johnstone, M. Leland, A. M. Fieno, W. M. Begley, Y. Sun, M. P. Lacey, T. Chaudhary, T. Keough, L. Chu, R. Sears, B. Yuan, and T. L. Dawson, Jr. 2007. Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc. Natl. Acad. Sci. USA 104:18730-18735.
112. Yockteng, R., S. Marthey, H. Chiapello, M. Hood, F. Rodolphe, B. Devier, P. Wincker, C. Dossat, and T. Giraud. 2007. Expressed sequence tags of the anther smut fungus, Microbotryum violaceum, identify mating and pathogenicity genes. BMC Genomics 8:272.
113. Zakharov, I. 1986. Some principles of the gene localization in eukaryotic chromosomes: formation of the problem and analysis of nonrandom localization of the mating-type loci in some fungi. Genetika 22:2620-2624.
114. Zakharov, I. A. 2005. Intratetrad mating and its genetic and evolutionary consequences. Russ. J. Genet. 41:508-519.