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PLOS ONE  2013 

Mating Type Locus of Chinese Black Truffles Reveals Heterothallism and the Presence of Cryptic Species within the T. indicum Species Complex

DOI: 10.1371/journal.pone.0082353

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Abstract:

Tuber spp. are filamentous ascomycetes which establish symbiosis with the roots of trees and shrub species. By virtue of this symbiosis they produce hypogeous ascocarps, known as truffles. Filamentous ascomycetes can reproduce by homothallism or heterothallism depending on the structure and organization of their mating type locus. The first mating type locus in a truffle species has been recently characterized in Tuber melanosporum and it has been shown that this fungus, endemic in Europe, is heterothallic. The availability of sequence information for T. melanosporum mating type genes is seminal to cloning their orthologs from other Tuber species and assessing their reproductive mode. Here we report on the organization of the mating type region in T. indicum, the black truffle species present in Asia, which is the closest relative to T. melanosporum and is characterized by an high level of morphological and genetic variability. The present study shows that T. indicum is also heterothallic. Examination of Asiatic black truffles belonging to different genetic classes, sorted according to the sequence polymorphism of the internal transcribed spacer rDNA region, has revealed sequence variations and rearrangements in both coding and non-coding regions of the mating type locus, to suggest the existence of cryptic species within the T. indicum complex. The presence of transposable elements within or linked to the mating type region suggests a role of these elements in generating the genotypic diversity present among T. indicum strains. Overall, comparative analyses of the mating type locus have thus allowed us to tackle taxonomical and phylogenetic issues within black truffles and make inferences about the evolution of T. melanosporum-T. indicum lineage. Our results are not only of fundamental but also of applied relevance as T. indicum produces edible fruit bodies that are imported also into Europe and thus may represent a biological threat for T. melanosporum.

References

[1]  Kronstad JW, Staben C (1997) Mating types in filamentous fungi. Annu Rev Genet 31: 245–76.
[2]  Debuchy R, Berteaux-Lecellier V, Silar P (2010) Mating systems and sexual morphogenesis in Ascomycetes. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular Biology of Filamentous Fungi. Washington DC: ASM Press. 501–536.
[3]  Casselton LA, Feldbrügge M (2010) Mating and sexual morphogenesis in basidiomycete fungi. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular Biology of Filamentous Fungi. Washington DC: ASM Press. 536–555.
[4]  Yoder OC, Valent B, Chumley F (1986) Genetic nomenclature and practice for plant pathogenic fungi. Phytopathology 76: 383–385.
[5]  Turgeon BG, Yoder OC (2000) Proposed nomenclature for mating type genes of filamentous Ascomycetes. Fungal Genet Biol 31: 1–5.
[6]  Billiard S, López-Villavicencio M, Hood ME, Giraud T (2012) Sex, outcrossing and mating types: unsolved questions in fungi and beyond. J Evolution Biol 25: 1020–1038.
[7]  Metzenberg RL, Glass NL (1990) Mating type and mating strategies in Neurospora. Bioessays 12: 53–59.
[8]  Butler G (2007) The evolution of MAT: The ascomycetes. In: Heitman J, Kronstad JW, Taylor JW, Casselton L, editors. Sex in Fungi. Molecular determination and evolutionary implications. Washington DC: ASM press. 3–18.
[9]  Rubini A, Riccioni C, Arcioni S, Paolocci F (2007) Troubles with truffles: unveiling more of their biology. New Phytol 174: 256–259.
[10]  Bertault G, Raymond M, Berthomieu A, Callot G, Fernandez D (1998) Trifling variation in truffles. Nature 394: 734.
[11]  Rubini A, Paolocci F, Riccioni C, Vendramin GG, Arcioni S (2005) Genetic and phylogeographic structures of the symbiotic fungus Tuber magnatum. Appl Environ Microbiol 71: 6584–6589.
[12]  Paolocci F, Rubini A, Riccioni C, Arcioni S (2006) Reevaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72: 2390–2393.
[13]  Riccioni C, Belfiori B, Rubini A, Passeri V, Arcioni S, et al. (2008) Tuber melanosporum outcrosses: analysis of the genetic diversity within and among its natural populations under this new scenario. New Phytol 180: 466–478.
[14]  Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, et al. (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033–1038.
[15]  Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, et al. (2011) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189: 710–722.
[16]  Martin F, Murat C, Paolocci F, Rubini A, Riccioni C, et al.. (2012) Molecular method for the identification of mating type genes of truffles species. European Patent Application EP2426215.
[17]  Fourré G, Riousset LJ, Riousset G (1996) Ces “Truffes de l’Inde” qui nous arrivent …. de Chine! Bull Féd Assoc Mycol Médit 9: 3–21.
[18]  Janex-Favre MC, Parguey-Leduc A, Sejalon-Delmas N, Dargent R, Kulifaj M (1996) Etude préliminaire de l'ascocarpe de Tuber indicum, truffe chinoise récemment introduite en France. CR Acad Sci III-Vie 319: 517–521.
[19]  Comandini O, Pacioni G (1997) Mycorrhizae of Asian black truffles, Tuber himalayense and T. indicum. Mycotaxon 63: 77–86.
[20]  Geng LY, Wang XH, Yu FQ, Deng XJ, Tian XF, et al. (2009) Mycorrhizal synthesis of Tuber indicum with two indigenous hosts, Castanea mollissima and Pinus armandii.. Mycorrhiza 19: 461–467.
[21]  Zhang BC, Minter DW (1988) Tuber himalayense sp. nov. with notes on Himalayan truffles. Trans Br Mycol Soc 91: 593–597.
[22]  Tao K, Liu B (1989) A new species of the genus Tuber from China. J Shanxi Univ 12: 215–218.
[23]  Moreno G, Manjón JL, Díez J, Di Massimo G, García-Montero LG (1997) Tuber pseudohimalayense sp. nov. an Asiatic species commercialized, in Spain similar to the ‘‘Perigord’’ truffle. Mycotaxon 63: 217–224.
[24]  Wang Y, Moreno G, Riousset L, Manjón JL, Riousset G, et al. (1998) Tuber pseudoexcavatum sp. nov. A new species from China commercialized in Spain, France and Italy with additional comments on Chinese truffles. Cryptogam Mycol 19: 113–120.
[25]  Hu HT (1992) Tuber formosanum sp. nov. and its mycorrhizal associations. Q J Exp Forest Natl Taiwan Univ 6: 79–86.
[26]  Chen J, Guo S, Liu PG (2011) Species recognition and cryptic species in the Tuber indicum complex. PLoS One 6: e14625.
[27]  Paolocci F, Rubini A, Granetti B, Arcioni S (1997) Typing Tuber melanosporum and Chinese black truffle species by molecular markers. FEMS Microbiol Lett 153: 255–260.
[28]  Zhang L, Yang ZL, Song DS (2005) A phylogenetic study of commercial Chinese truffles and their allies: taxonomic implications. FEMS Microbiol Lett 245: 85–92.
[29]  Wang Y, Tan ZM, Zhang DC, Murat C, Jeandroz S, et al. (2006) Phylogenetic relationships between Tuber pseudoexcavatum, a Chinese truffle, and other Tuber species based on parsimony and distance analysis of four different gene sequences FEMS Microbiol Lett. 259: 269–281.
[30]  Huang J, Hu H, Shen W (2009) Phylogenetic study of two truffles, Tuber formosanum and Tuber furfuraceum, identified from Taiwan. FEMS Microbiol Lett 294: 157–171.
[31]  Wang Y, Tan ZM, Zhang DC, Murat C, Jeandroz S, et al. (2006) Phylogenetic and populational study of the Tuber indicum complex. Mycol Res 110: 1034–1045.
[32]  Roux C, Séjalon-Delmas N, Martins M, Parguey-Leduc A, Dargent R, et al. (1999) Phylogenetic relationships between European and Chinese truffles based on parsimony and distance analysis of ITS sequences. FEMS Microbiol Lett 180: 147–155.
[33]  Paolocci F, Rubini A, Riccioni C, Granetti B, Arcioni S (2000) Cloning and characterization of two repeated sequences in the symbiotic fungus Tuber melanosporum Vitt. FEMS Microbiol Ecol 34: 139–146.
[34]  Jeandroz S, Murat C, Wang Y, Bonfante P, Le Tacon F (2008) Molecular phylogeny and historical biogeography of the genus Tuber, the ‘true truffles’. J Biogeogr 35: 815–829.
[35]  Yun SH, Berbee ML, Yoder OC, Turgeon BG (1999) Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc Natl Acad Sci U S A 96: 5592–5597.
[36]  Nygren K, Strandberg R, Wallberg A, Nabholz B, Gustaffson T, et al. (2011) A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol Phylogenet Evol 59: 649–663.
[37]  Dyer PS, O'Gorman CM (2011) Sexual development and cryptic sexuality in fungi: insights from Aspergillus species FEMS Microbiol Rev. 36: 165–192.
[38]  Turgeon BG (1998) Application of mating type gene technology to problems in fungal biology. Annu Rev Phytopathol 36: 115–137.
[39]  Wang X (2012) Truffle cultivation in China. In: Zambonelli A, Bonito G, editors. Edible Mycorrhizal Mushrooms. Soil Biology series 34. Berlin, Heidelberg: Springer Verlag. 227–240.
[40]  Rubini A, Paolocci F, Granetti B, Arcioni S (1998) Single step molecular characterization of morphologically similar black truffle species. FEMS Microbiol Lett 164: 7–12.
[41]  Murat C, Martin F (2008) Sex and truffles: first evidence of Perigord black truffle outcrosses. New Phytol 180: 260–263.
[42]  White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand MA, Sninski DH, White TJ, editors. PCR protocols. A Guide to Methods and Applications. San Diego, CA: Academic Press. 315–322.
[43]  Marshall OJ (2004) PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20: 2471–2472.
[44]  Robertson HM (2002) Evolution of DNA transposons in eukaryotes. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II. Washington, DC: ASM Press. 1093–1110.
[45]  Sarkar A, Sim C, Hong YS, Hogan JR, Fraser MJ, et al. (2003) Molecular evolutionary analysis of the widespread PiggyBac transposon family and related “domesticated” sequences. Mol Genet Genomics 270: 173–180.
[46]  Kempken F, Kück U (1998) Transposon in filamentous fungi – facts and perspectives. BioEssays 20: 652–659.
[47]  Yuan YW, Wessler SR (2011) The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc Natl Acad Sci U S A 108: 7884–7889.
[48]  Bonito G, Trappe JM, Donovan S, Vilgalys R (2011) The Asian black truffle Tuber indicum can form ectomycorrhizas with North American host plants and complete its life cycle in non-native soils. Fungal Ecol 4: 83–93.
[49]  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.
[50]  Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET (2011) Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Mol Biol Evol 28: 1987–2003.
[51]  Zaffarano PL, Duò A, Grünig CR (2010) Characterization of the mating type (MAT) locus in the Phialocephala fortinii s.l. – Acephala applanata species complex. Fungal Genet Biol 47: 761–772.
[52]  P?ggeler S, O’Gorman CM, Hoff B, Kuck U (2011) Molecular organization of the mating type loci in the homothallic ascomycetes Eupenicillium crustaceum. Fungal Biol 115: 615–624.
[53]  Sedgwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24: 311–316.
[54]  Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, et al. (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973–982.
[55]  Fraser MJ, Ciszczon T, Elick T, Bauser C (1996) Precise excision of TTAA-specific lepidopteran transposons piggyBac (IFP2) and tagalong (TFP3) from the baculovirus genome in cell lines from two species of Lepidoptera. Insect Mol Biol 5: 141–151.
[56]  Lengeler KB, Fox DS, Fraser JA, Allen A, Forrester K, et al. (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell 1: 704–718.
[57]  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.
[58]  Brewer MT, Cadle-Davidson L, Cortesi P, Spanu PD, Milgroom MG (2011) Identification and structure of the mating-type locus and development of PCR based markers for mating type in powdery mildew fungi. Fungal Genet Biol 48: 704–713.
[59]  Idnurm A (2011) Sex and speciation: the paradox that non-recombining DNA promotes recombination. Fungal Biol Rev 25: 121–127.
[60]  Gross A, Zaffarano PL, Duo A, Grünig CR (2012) Reproductive mode and life cycle of the ash dieback pathogen Hymenoscyphus pseudoalbidus. Fungal Genet Biol 49: 977–986.
[61]  Fraser JA, Heitman J (2005) Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev 15: 645–651.
[62]  Gioti A, Mushegian AA, Strandberg R, Stajich JE, Johannesson H (2012) Unidirectional evolutionary transitions in fungal mating systems and the role of transposable elements. Mol Biol Evol 29: 3215–3226.
[63]  Gryganskyi AP, Lee SC, Litvintseva AP, Smith ME, Bonito G, et al. (2010) Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS ONE 12: e15273.
[64]  Bonito G, Smith ME, Nowak M, Healy RA, Guevara G, et al. (2013) Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS ONE 8: e52765.
[65]  Murat C, Zampieri E, Vizzini A, Bonfante P (2008) Is the Perigord black truffle threatened by an invasive species? We dreaded it and it has happened. New Phytol 178: 699–702.
[66]  Chase TE, Ullrich RC (1990) Genetic basis of biological species in Heterobasidion annosum: Mendelian determinants. Mycologia 82: 67–72.
[67]  Gonthier P, Nicolotti G, Linzer R, Guglielmo F, Garbellotto M (2007) Invasion of European pine stands by a North American forest pathogen and its hybridization with a native interfertile taxon. Mol Ecol 16: 1389–1400.
[68]  Brasier CM, Kirk SA, Pipe ND, Buck KW (1998) Rare interspecific hybrids in natural populations of the Dutch elm disease pathogens Ophiostoma ulmi and O. novo-ulmi. Mycol Res 102: 45–57.
[69]  Newcombe G, Stirling B, McDonald S, Bradshaw HD (2000) Melampsora × columbiana, a natural hybrid of M. medusae and M. occidentalis. Mycol Res 104: 261–274.
[70]  Gladieux P, Vercken E, Fontaine MC, Hood ME, Jonot O, et al. (2011) Maintenance of fungal pathogen species that are specialized to different hosts: allopatric divergence and introgression through secondary contact. Mol Biol Evol 28: 459–471.
[71]  Swanson WJ, Vacquier VD (2002) Reproductive protein evolution. Annu Rev Ecol Syst 33: 161–179.
[72]  Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animal and plants. Reproduction 131: 11–22.
[73]  Palumbi SR (2008) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity 102: 66–76.
[74]  Turgeon BG (1998) Application of mating type gene technology to problems in fungal biology. Annu Rev Phytopathol 36: 115–137.
[75]  Brown AJ, Casselton LA (2001) Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet 17: 393–400.
[76]  Mayrhofer S, P?ggeler S (2005) Functional characterization of an α-factor-like Sordaria macrospora peptide pheromone and analysis of its cognate receptor in Saccharomyces cerevisiae. Eukaryot Cell 4: 661–672.
[77]  Rubini A, Belfiori B, Riccioni C, Arcioni S, Martin F, et al. (2011) Tuber melanosporum: mating type distribution in a natural plantation and dynamics of strains of different mating types on the roots of nursery-inoculated host plants. New Phytol 189: 723–735.
[78]  Murat C, Rubini A, Riccioni C, De la Varga H, Akroume E, et al. (2013) Fine scale spatial genetic structure of the black truffle (Tuber melanosporum) investigated with neutral microsatellites and functional mating type genes. New Phytol 199: 176–187.

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