Microsatellite size homoplasies and null alleles do not affect species diagnosis and population genetic analysis in a fungal species complex

Molecular Ecology Resources

Volumn 10, Issue 2, 2010, Pages 348-367

  Queloz, V ^a   Duo A ^a   Sieber, T N ^a   Grunig C R ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Assignment tests; Cross species amplification; Dark septate endophytes; Microsatellite; Null alleles; Phialocephala fortinii; Size homoplasy; Species complex

Indexed keywords

ACEPHALA APPLANATA; PHIALOCEPHALA FORTINII;

EID: 77949336703     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/j.1755-0998.2009.02757.x     Document Type: Article

References (84)

1. Ablett G, Hill H, Henry RJ. Sequence polymorphism discovery in wheat microsatellite flanking regions using pyrophosphate sequencing. Molecular Breeding 2006, 17:281-289.
2. Addy HD, Hambleton S, Currah RS. Distribution and molecular characterization of the root endophyte Phialocephala fortinii along an environmental gradient in the boreal forest of Alberta. Mycological Research 2000, 104:1213-1221.
3. Angers B, Estoup A, Jarne P. Microsatellite size homoplasy, SSCP, and population structure: a case study in the freshwater snail Bulinus truncatus. Molecular Biology and Evolution 2000, 17:1926-1932.
4. Batley J, Mogg R, Edwards D, O'Sullivan H, Edwards KJ. A high-throughput SNuPE assay for genotyping SNPs in the flanking regions of Zea mays sequence tagged simple sequence repeats. Molecular Breeding 2003, 11:111-120.
5. Brenn N, Menkis A, Grünig CR, Sieber TN, Holdenrieder O. Community structure of Phialocephala fortinii s. lat. in European tree nurseries, and assessment of the potential of the seedlings as dissemination vehicles. Mycological Research 2008, 112:650-662.
6. Callen DF, Thompson AD, Shen Y. Incidence and origin of null alleles in the (AC)n microsatellite markers. American Journal of Human Genetics 1993, 52:922-927.
7. Carbone I, Kohn LM. Inferring process from pattern in fungal population genetics. Applied Mycology & Biotechnology: Fungal Genomics 2004, 1-30. Arora DK, Khachatourians GG. In, eds, pp, Elsevier Science, Amsterdam
8. Chapuis MP, Estoup A. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 2007, 24:621-631.
9. Crawford AM, Kappes SM, Paterson KA. Microsatellite evolution: testing the ascertainment bias hypothesis. Journal of Molecular Evolution 1998, 46:256-260.
10. Crous PW, Groenewald JZ. Hosts, species and genotypes: opinions versus data. Australasian Plant Pathology 2005, 34:463-470.
11. Crow JF, Kimura M. An introduction to population genetics 1970, Harper and Row, New York
12. Dakin EE, Avise JC. Microsatellite null alleles in parentage analysis. Heredity 2004, 93:504-509.
13. Dettman JR, Taylor JW. Mutation and evolution of microsatellite loci in Neurospora. Genetics 2004, 168:1231-1248.
14. Dutech C, Enjalbert J, Fournier E. Challenges of microsatellite isolation in fungi. Fungal Genetics and Biology 2007, 44:933-949.
15. Ellegren H. Microsatellites: simple sequences with complex evolution. Nature Reviews Genetics 2004, 5:435-445.
16. Ellegren H, Primmer CR, Sheldon BC. Microsatellite evolution-directionality or bias. Nature Genetics 1995, 11:360-362.
17. Elnifro EM, Ashshi AM, Cooper RJ, Klapper PE. Multiplex PCR: optimization and application in diagnostic virology. Clinical Microbiology Reviews 2000, 13:559-570.
18. Estoup A, Angers B. Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. Advances in Molecular Ecology 1998, 306:55-86.
19. Estoup A, Jarne P, Cornuet JM. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology 2002, 11:1591-1604.
20. Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 2005, 1:47-50.
21. Fisher MC, Koenig G, White TJ, Taylor JW. A test for concordance between the multilocus genealogies of genes and microsatellites in the pathogenic fungus Coccidioides immitis. Molecular Biology and Evolution 2000, 17:1164-1174.
22. Fisher MC, Rannala B, Chaturvedi V, Taylor JW. Disease surveillance in recombining pathogens: multilocus genotypes identify sources of human Coccidioides infections. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:9067-9071.
23. Fournier E, Giraud T. Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. Journal of Evolutionary Biology 2008, 21:122-132.
24. Froufe E, Knizhin I, Koskinen MT, Primmer CR, Weiss S. Identification of reproductively isolated lineages of Amur grayling (Thymallus grubii Dybowski 1869): concordance between phenotypic and genetic variation. Molecular Ecology 2003, 12:2345-2355.
25. Goldstein DB, Pollock DD. Launching microsatellites: a review of mutation processes and methods of phylogenetic inference. Journal of Heredity 1997, 88:335-342.
26. Goldstein DB, Schlötterer C. Microsatellites: Evolution and Applications 1999, Oxford University Press, New York
27. Goldstein DB, Linares AR, Cavallisforza LL, Feldman MW. Genetic absolute dating based on microsatellites and the origin of modern humans. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:6723-6727.
28. Grünig CR, Sieber TN. Molecular and phenotypic description of the widespread root symbiont Acephala applanata gen. et sp nov., formerly known as dark-septate endophyte Type 1. Mycologia 2005, 97:628-640.
29. Grünig CR, Sieber TN, Rogers SO, Holdenrieder O. Spatial distribution of dark septate endophytes in a confined forest plot. Mycological Research 2002, 106:832-840.
30. Grünig CR, Linde CC, Sieber TN, Rogers SO. Development of single-copy RFLP markers for population genetic studies of Phialocephala fortinii and closely related taxa. Mycological Research 2003, 107:1332-1341.
31. Grünig CR, McDonald BA, Sieber TN, Rogers SO, Holdenrieder O. Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fungal Genetics and Biology 2004, 41:676-687.
32. Grünig CR, Duò A, Sieber TN. Population genetic analysis of Phialocephala fortinii s.l. and Acephala applanata in two undisturbed forests in Switzerland and evidence for new cryptic species. Fungal Genetics and Biology 2006, 43:410-421.
33. Grünig CR, Brunner PC, Duò A, Sieber TN. Suitability of methods for species recognition in the Phialocephala fortinii-Acephala applanata species complex using DNA analysis. Fungal Genetics and Biology 2007, 44:773-788.
34. Grünig CR, Duò A, Sieber TN, Holdenrieder O. Assignment of species rank to six reproductively isolated cryptic species of the Phialocephala fortinii s.l.-Acephala applanata species complex. Mycologia 2008a, 100:47-67.
35. Grünig CR, Queloz V, Sieber Thomas N, Holdenrieder O. Dark septate endophytes (DSE) of the Phialocephala fortinii s.l-Acephala applanata species complex in tree roots-classification, population biology and ecology. Botany 2008b, 86:1355-1369.
36. Hayden HL, Wilson LM, Cozijnsen AJ, Howlett BJ. Characterization and cross-species amplification of microsatellite loci in the plant pathogenic fungus Leptosphaeria maculans. Molecular Ecology Notes 2004, 4:480-481.
37. Henegariu O, Heerema NA, Dlouhy SR, Vance GH, Vogt PH. Multiplex PCR: critical parameters and step-by-step protocol. BioTechniques 1997, 23:504-511.
38. Hey J. The structure of genealogies and the distribution of fixed differences between DNA-sequence samples from natural-populations. Genetics 1991, 128:831-840.
39. Kimura M, Crow JF. The number of alleles that can be maintained in a finite population. Genetics 1964, 49:725-738.
40. Koedprang W, Na-Nakorn U, Nakajima M, Taniguchi N. Evaluation of genetic diversity of eight grouper species Epinephelus spp. based on microsatellite variations. Fisheries Science 2007, 73:227-236.
41. Langella O. Populations 1.2.30. Population genetic software (individuals or populations distances, phylogenetic trees) 1999, http://bioinformatics.org/~tryphon/populations/, Available from CNRS
42. Lehmann T, Hawley WA, Collins FH. An evaluation of evolutionary constraints on microsatellite loci using null alleles. Genetics 1996, 144:1155-1163.
43. Li G, Hubert S, Bucklin K, Ribes V, Hedgecock D. Characterization of 79 microsatellite DNA markers in the Pacific oyster Crassostrea gigas. Molecular Ecology Notes 2003, 3:228-232.
44. Markoulatos P, Siafakas N, Moncany M. Multiplex polymerase chain reaction: a practical approach. Journal of Clinical Laboratory Analysis 2002, 16:47-51.
45. Matute DR, McEwen JG, Montes BA. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Molecular Biology and Evolution 2006a, 23:65-73.
46. Matute DR, Sepulveda VE, Quesada LM. Microsatellite analysis of three phylogenetic species of Paracoccidioides brasiliensis. Journal of Clinical Microbiology 2006b, 44:2153-2157.
47. McDonald BA. The population genetics of fungi: tools and techniques. Phytopathology 1997, 87:448-453.
48. McGill BJ, Etienne RS, Gray JS. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecology Letters 2007, 10:995-1015.
49. Menkis A, Vasiliauskas R, Taylor AFS, Stenlid J, Finlay R. Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation. Mycorrhiza 2005, 16:33-41.
50. Nei M. Molecular Evolutionary Genetics 1987, Columbia University Press, New York
51. Nei M, Tajima F, Tateno Y. Accuracy of estimated phylogenetic trees from molecula data. Journal of Molecular Evolution 1983, 19:153-170.
52. Ohta T, Kimura M. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetical Research 1973, 22:201-204.
53. Orti G, Pearse DE, Avise JC. Phylogenetic assessment of length variation at a microsatellite locus. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:10745-10749.
54. Paetkau D, Strobeck C. The molecular basis and evolutionary history of a microsatellite null allele in bears. Molecular Ecology 1995, 4:519-520.
55. Peay KG, Kennedy PG, Bruns TD. Fungal community ecology: a hybrid beast with a molecular master. BioScience 2008, 58:799-810.
56. Piry S, Alapetite A, Cornuet JM. geneclass2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 2004, 95:536-539.
57. Posada D, Crandall KA. modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
58. Prospero S, Lung-Escarmant B, Dutech C. Genetic structure of an expanding Armillaria root rot fungus (Armillaria ostoyae) population in a managed pine forest in southwestern France. Molecular Ecology 2008, 17:3366-3378.
59. Queloz V. La face cachée du Creux du Van: présence des endophytes racinaires Phialocephala fortinii s.l. et Acephala applanata sur le pergélisol du Creux du Van. Actes de la Société Jurassienne d'émulation 2008, 2007:47-68.
60. Queloz V, Duò A, Grünig CR. Isolation and characterization of microsatellite markers for the tree-root endophytes Phialocephala subalpina and Phialocephala fortinii s.s. Molecular Ecology Notes 2008, 8:1322-1325.
61. r: A language and environment for statistical computing 2008, http://www.R-project.org, R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0. Available from
62. Rannala B, Mountain JL. Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:9197-9201.
63. Rhode C, Slabbert R, Roodt-Wilding R. Microsatellite flanking regions: a SNP mine in South African abalone (Haliotis midae). Animal Genetics 2008, 39.
64. Roques S, Duchesne P, Bernatchez L. Potential of microsatellites for individual assignment: the North Atlantic redfish (genus Sebastes) species complex as a case study. Molecular Ecology 1999, 8:1703-1717.
65. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
66. Sekino M, Hara M. Individual assignment tests proved genetic boundaries in a species complex of Pacific abalone (genus Haliotis). Conservation Genetics 2007, 8:823-841.
67. Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 1999, 16:1114-1116.
68. Slippers B, Burgess T, Wingfield BD. Development of simple sequence repeat markers for Botryosphaeria spp. with Fusicoccum anamorphs. Molecular Ecology Notes 2004, 4:675-677.
69. Stoyke G, Egger KN, Currah RS. Characterization of sterile endophytic fungi from the mycorrhizae of subalpine plants. Canadian Journal of Botany 1992, 70:2009-2016.
70. Stukenbrock EH, Banke S, McDonald BA. Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Molecular Ecology 2006, 15:2895-2904.
71. Sunnucks P. Efficient genetic markers for population biology. Tree 2000, 15:199-203.
72. Swofford DL. paup-a computer-program for phylogenetic inference using maximum parsimony. Journal of General Physiology 1993, 102:A9.
73. Takezaki N, Nei M. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 1996, 144:389-399.
74. Takezaki N, Nei M. Empirical tests of the reliability of phylogenetic trees constructed with microsatellite DNA. Genetics 2008, 178:385-392.
75. Taylor JW, Jacobson DJ, Kroken S. Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology 2000, 31:21-32.
76. Thelma B, Palma-Silva C, Paggi GM. Cross-species transfer of nuclear microsatellite markers: potential and limitations. Molecular Ecology 2007, 16:3759-3767.
77. Vallone PM, Butler JM. AutoDimer: a screening tool for primer-dimer and hairpin structures. BioTechniques 2004, 37:226-231.
78. Viard F, Franck P, Dubois MP, Estoup A, Jarne P. Variation of microsatellite size homoplasy across electromorphs, loci, and populations in three invertebrate species. Journal of Molecular Evolution 1998, 47:42-51.
79. Wadud MA, Lian CL, Nara K, Ishida TA, Hogetsu T. Development of microsatellite markers from an ectomycorrhizal fungus, Laccaria amethystina, by a dual-suppression-PCR technique. Molecular Ecology Notes 2006, 6:130-132.
80. Walser JC, Sperisen C, Soliva M, Scheidegger C. Fungus-specific microsatellite primers of lichens: application for the assessment of genetic variation on different spatial scales in Lobaria pulmonaria. Fungal Genetics and Biology 2003, 40:72-82.
81. Weir BS, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
82. Werle E, Schneider C, Renner M, Volker M, Fiehn W. Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Research 1994, 22:4354-4355.
83. Woodcock S, Curtis TP, Head IM, Lunn M, Sloan WT. Taxa-area relationships for microbes: the unsampled and the unseen. Ecology Letters 2006, 9:805-812.
84. Zheng Y, Zhang G, Lin F. Development of microsatellite markers and construction of genetic map in rice blast pathogen Magnaporthe grisea. Fungal Genetics and Biology 2008, 45:1340-1347.