Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex

Molecular Ecology

Volumn 21, Issue 2, 2012, Pages 281-299

  Vincenot, Lucie ^a,f   Nara, Kazuhide ^b   Sthultz, Christopher ^a   Labbé, Jessy ^c,d   Dubois, Marie Pierre ^a   Tedersoo, Leho ^e   Martin, Francis ^c   Selosse, Marc André ^a  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITÉ DE LORRAINE   (France)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF TARTU   (Estonia)

^f RESEARCH AND INNOVATION CENTRE   (Italy)

Author keywords

cryptic speciation; ectomycorrhizal fungi; gene flow; inbreeding; isolation by distance; microsatellite markers; phylogeography; population structure

Indexed keywords

BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; FUNGI; LACCARIA; LACCARIA AMETHYSTINA;

EID: 84855433737     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05392.x     Document Type: Article

References (73)

1. Abarenkov K, Nilsson RH, Larsson K-H, et al. (2010) The UNITE database for molecular identification of fungi-recent updates and future perspectives. New Phytologist, 186, 281-285.
2. Amend A, Garbelotto M, Fang Z, Keeley S, (2010) Isolation by landscape in populations of a prized edible mushroom Tricholoma matsutake. Conservation Genetics, 11, 795-802.
3. Bagley SJ, Orlovich DA, (2004) Genet size and distribution of Amanita muscaria in a suburban park, Dunedin, New Zealand. New Zealand Journal of Botany, 42, 939-947. (Pubitemid 40198951)
4. BarrÃs B, Halkett F, Dutech C, Andrieux A, Pinon J, Frey P, (2008) Genetic structure of the poplar rust fungus Melampsora larici-populina: evidence for isolation by distance in Europe and recent founder effects overseas. Infection, Genetics and Evolution, 8, 577-587.
5. Bergemann SE, Miller SL, (2002) Size, distribution, and persistence of genets in local populations of the late-stage ectomycorrhizal basidiomycete, Russula brevipes. New Phytologist, 156, 313-320. (Pubitemid 35255167)
6. Brown JKM, HovmÃller MS, (2002) Epidemiology-aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 297, 537-541. (Pubitemid 34815327)
7. Burchhardt KM, Rivera Y, Baldwin T, Vanearden D, Kretzer AM, (2011) Analysis of genet size and local gene flow in the ectomycorrhizal basidiomycete Suillus spraguei (synonym S. pictus). Mycologia, 103, 722-730.
8. Carriconde F, Gardes M, Jargeat P, Heilmann-Clausen J, Mouhamadou B, Gryta H, (2008) Population evidence of cryptic species and geographical structure in the cosmopolitan ectomycorrhizal fungus, Tricholoma scalpturatum. Microbial Ecology, 56, 513-524.
9. David P, Pujol B, Viard F, Castella V, Goudet J, (2007) Reliable selfing rate estimates from imperfect population genetic data. Molecular Ecology, 16, 2474-2487. (Pubitemid 46897144)
10. Dilmaghani A, Balesdent MH, Didier JP, et al. (2009) The Leptosphaeria maculans-Leptosphaeria biglobosa species complex in the American continent. Plant Pathology, 58, 1044-1058.
11. Donges K, Schlobinski D, Cremer E, Rexer KH, Kost G, (2008) Six newly developed microsatellite markers of Laccaria amethystina, using an improved CSSR approach. Mycological Progress, 7, 285-290.
12. Douhan GW, Huryn KL, Douhan LI, (2007) Significant diversity and potential problems associated with inferring population structure within the Cenococcum geophilum species complex. Mycologia, 99, 812-819. (Pubitemid 351198221)
13. Douhan G, Vincenot L, Gryta H, Selosse MA, (2011) Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biology, 115, 569-597.
14. Dunham SM, Kretzer A, Pfrender ME, (2003) Characterization of Pacific golden chanterelle (Cantharellus formosus) genet size using co-dominant microsatellite markers. Molecular Ecology, 12, 1607-1618. (Pubitemid 36708465)
15. Edman M, Gustafsson M, Stenlid J, Ericson L, (2004) Abundance and viability of fungal spores along a forestry gradient-responses to habitat loss and fragmentation? Oikos, 104, 35-42. (Pubitemid 38143318)
16. Engh IB, Carlsen T, SÃtre GP, Högberg N, Doi S, Kauserud H, (2010) Two invasive populations of the dry rot fungus Serpula lacrymans show divergent population genetic structures. Molecular Ecology, 19, 706-715.
17. Excoffier L, Lischer HEL, (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
18. Fiore-Donno AM, Martin F, (2001) Populations of ectomycorrhizal Laccaria amethystina and Xerocomus spp. show contrasting colonization patterns in a mixed forest. New Phytologist, 152, 533-542. (Pubitemid 34000004)
19. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhiza and rusts. Molecular Ecology, 2, 113-118.
20. Geml J, Laursen GA, O'Neill K, Nusbaum HC, Taylor DL, (2006) Beringian origins and cryptic speciation events in the fly agaric Amanita muscaria. Molecular Ecology, 15, 225-239.
21. Geml J, Laursen GA, Timling I, et al. (2009) Molecular phylogenetic biodiversity assessment of arctic and boreal ectomycorrhizal Lactarius Pers. (Russulales; Basidiomycota) in Alaska, based on soil and sporocarp DNA. Molecular Ecology, 18, 2213-2227.
22. Gherbi H, Delaruelle C, Selosse MA, Martin F, (1999) High genetic diversity in a population of the ectomycorrhizal basidiomycete Laccaria amethystina in a 150-year-old beech forest. Molecular Ecology, 12, 2003-2013. (Pubitemid 30079110)
23. Guillot G, Santos F, Estoup A, (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics, 24, 1406-1407. (Pubitemid 351737151)
24. Guindon S, Gascuel O, (2003) A simple, fast and accurate method to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704. (Pubitemid 37365050)
25. Halling RE, Osmundson TW, Neves MA, (2008) Pacific boletes: implications for biogeographic relationships. Mycological Research, 112, 437-447.
26. Hibbett DS, (2001) Shiitake mushrooms and molecular clocks: historical biogeography of Lentinula. Journal of Biogeography, 28, 231-241. (Pubitemid 32608164)
27. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978. (Pubitemid 43013915)
28. Hosaka K, Castellano MA, Spatafora JW, (2008) Biogeography of Hysterangiales (Phallomycetidae, Basidiomycota). Mycological Research, 112, 448-462.
29. Hughes KW, Petersen RH, Lickey EB, (2007) Megacollybia (Agaricales). Reports of the Tottori Mycological Institute, 45, 1-57.
30. Hughes KW, Petersen RH, Lickey EB, (2009) Using heterozygosity to estimate a percentage DNA sequence similarity for environmental species' delimitation across basidiomycete fungi. New Phytologist, 182, 795-798.
31. Irwin DE, (2009) Incipient ring speciation revealed by a migratory divide. Molecular Ecology, 18, 2923-2925.
32. Ishida TA, Nara K, Tanaka M, Kinoshita A, Hogetsu T, (2008) Germination and infectivity of ectomycorrhizal fungal spores in relation to their ecological traits during primary succession. New Phytologist, 180, 491-500.
33. James TY, Porter D, Hamrick JL, Vilgalys R, (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune. Evolution, 53, 1665-1677. (Pubitemid 30044802)
34. Jany JL, Garbaye J, Martin F, (2002) Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytologist, 154, 651-659. (Pubitemid 34548633)
35. Jargeat P, Martos F, Carriconde F, Gryta H, Moreau P-A, Gardes M, (2010) Phylogenetic species delimitation in ectomycorrhizal fungi and implications for barcoding: the case of the Tricholoma scalpturatum complex (Basidiomycota). Molecular Ecology, 19, 5216-5230.
36. Kauserud H, SvegÃ¥rden IB, SÃ∥tre GP, et al. (2007) Asian origin and rapid global spread of the destructive dry rot fungus Serpula lacrymans. Molecular Ecology, 16, 3350-3360. (Pubitemid 47221131)
37. Kretzer AM, Dunham S, Molina R, Spatafora JW, (2005) Patterns of vegetative growth and gene flow in Rhizopogon vinicolor and R. vesiculosus (Boletales, Basidiomycota). Molecular Ecology, 14, 2259-2268. (Pubitemid 40886029)
38. de La Bastide PY, Kropp BR, Piché R, (1995) Vegetative interactions among mycelia of Laccaria bicolor in pure culture and in symbiosis with Pinus banksiana. Canadian Journal of Botany, 73, 1768-1779. (Pubitemid 3002047)
39. Labbé J, Zhang X, Yin T, et al. (2008) A genetic linkage map for the ectomycorrhizal fungus Laccaria bicolor and its alignment to the whole-genome sequence assemblies. New Phytologist, 180, 316-328.
40. Li DW, (2005) Release and dispersal of basidiospores from Amanita muscaria var. alba and their infiltration into a residence. Mycological Research, 109, 1235-1242.
41. Martin F, Selosse M-A, Le Tacon F, (1999) The nuclear ribosomal DNA intergenic spacers of the ectomycorrhizal basidiomycete Laccaria bicolor: structural analysis and intraspecific polymorphisms. Microbiology, 145, 1605-1611. (Pubitemid 29352004)
42. Martin F, Diez J, Dell B, Delaruelle C, (2002) Phylogeography of the ectomycorrhizal Pisolithus species as inferred from nuclear ribosomal DNA ITS sequences. New Phytologist, 153, 345-357. (Pubitemid 34140149)
43. Martin F, Aerts A, Ahrén D, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature, 452, 88-93.
44. Moncalvo JM, Buchanan PK, (2008) Molecular evidence for long distance dispersal across the Southern Hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycological Research, 112, 425-436.
45. Mueller GM, Schmit JP, Leacock PR, et al. (2007) Global diversity and distribution of macrofungi. Biodiversity and Conservation, 16, 37-48.
46. Murat C, Diez J, Luis P, et al. (2004) Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytologist, 164, 401-411. (Pubitemid 39384752)
47. Nara K, (2005) Ectomycorrhizal networks and seedling establishment during early primary succession. New Phytologist, 169, 169-178.
48. Nara K, Nakaya H, Wu B, Zhou Z, Hogetsu T, (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytologist, 159, 743-746.
49. Niculita-Hirzel H, Labbé J, Kohler A, et al. (2008) Gene organization of the mating type regions in the ectomycorrhizal fungus Laccaria bicolor reveals distinct evolution between the two mating type loci. New Phytologist, 180, 329-342.
50. Nielsen R, Wakeley JW, (2001) Distinguishing migration from isolation: an MCMC approach. Genetics, 158, 885-896. (Pubitemid 32552323)
51. Nylander JAA, (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
52. O'Malley MA, (2007) The nineteenth century roots of 'everything is everywhere'. Nature Reviews Microbiology, 5, 647-651. (Pubitemid 47078772)
53. Parrent JL, Garbelotto M, Gilbert GS, (2004) Population genetic structure of the polypore Datronia caperata in fragmented mangrove forests. Mycological Research, 108, 403-410. (Pubitemid 38681844)
54. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. (Pubitemid 30397141)
55. Prospero JM, Blades E, Mathison G, Naidu R, (2005) Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia, 21, 1-19. (Pubitemid 41038420)
56. Queloz V, Sieber TN, Holdenrieder O, McDonald BA, Grünig CR, (2011) No biogeographical pattern for a root-associated fungal species complex. Global Ecology and Biogeography, 20, 160-169.
57. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572-1574. (Pubitemid 37038874)
58. Rousset F, (2008) GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8, 103-106. (Pubitemid 350231212)
59. Roy M, Dubois MP, Proffit M, Vincenot L, Desmarais E, Selosse MA, (2008) Evidence from population genetics that the ectomycorrhizal basidiomycete Laccaria amethystina is an actual multihost symbiont. Molecular Ecology, 17, 2825-2838. (Pubitemid 351793528)
60. Rubini A, Paolocci F, Riccioni C, Vendramin GG, Arcioni S, (2005) Genetic and phylogeographic structures of the symbiotic fungus Tuber magnatum. Applied and Environmental Microbiology, 71, 6584-6589. (Pubitemid 43194140)
61. Selosse MA, Martin F, Bouchard D, Le Tacon F, (1997) Temporal persistence and spatial distribution of an American inoculant strain of the ectomycorrhizal basidiomycete Laccaria bicolor in French plantations. Molecular Ecology, 7, 561-574.
62. Selosse MA, Jacquot D, Bouchard D, Martin F, Le Tacon F, (1998) Survival of an introduced ectomycorrhizal Laccaria bicolor strain in a European forest plantation monitored by mitochondrial ribosomal DNA analysis. New Phytologist, 140, 753-761. (Pubitemid 29064548)
63. Swofford DL, (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.10 b. Sinauer, Sunderland, Massachusetts, USA.
64. Taylor JW, Jacobson DJ, Kroken S, et al. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology, 31, 21-32. (Pubitemid 32066164)
65. Taylor AFS, Hills AE, Simonini G, Both EE, Eberhardt U, (2006) Detection of species within the Xerocomus subtomentosus complex in Europe using rDNA-ITS sequences. Mycological Research, 110, 276-287. (Pubitemid 44061644)
66. Vainio EJ, Korhonena K, Hantulaa J, (1998) Genetic variation in Phlebiopsis gigantea as detected with random amplified microsatellite (RAMS) markers. Mycological Research, 102, 187-192.
67. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538. (Pubitemid 39147523)
68. Wadud MA, (2007) Reproduction ecology of pioneer ectomycorrhizal fungi, Laccaria amethystina and L. laccata, in the volcanic desert on Mount Fuji. PhD Thesis, The University of Tokyo, Tokyo, Japan.
69. Wadud MA, Lian CL, Nara K, Ishida TA, Hogetsu T, (2006a) Development of microsatellite markers from an ectomycorrhizal fungus, Laccaria amethystina, by a dual-suppression-PCR technique. Molecular Ecology Notes, 6, 130-132. (Pubitemid 43373778)
70. Wadud MA, Lian CL, Nara K, Hogetsu T, (2006b) Isolation and characterization of five microsatellite loci in an ectomycorrhizal fungus Laccaria laccata. Molecular Ecology Notes, 6, 700-702. (Pubitemid 44252581)
71. White TJ, Bruns T, Lee S, Taylor J, (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols. A Guide to Methods and Applications (eds., Innis MA, Gelfand DH, Sninsky JJ, White JJ,), pp. 315-322. Academic Press, San Diego, California.
72. Wu QX, Mueller GM, Lutzoni FM, Huang YQ, Guo SY, (2000) Phylogenetic and biogeographic relationships of Eastern Asian and Eastern North American disjunct Suillus species (Fungi) as inferred from nuclear ribosomal RNA ITS sequences. Molecular Phylogenetics and Evolution, 17, 37-47.
73. Xu J, Sha T, Li YC, Zhao ZW, Yang ZL, (2008) Recombination and genetic differentiation among natural populations of the ectomycorrhizal mushroom Tricholoma matsutake from southwestern China. Molecular Ecology, 17, 1238-1247. (Pubitemid 351294606)