Lessons learned from microsatellite development for nonmodel organisms using 454 pyrosequencing

Journal of Evolutionary Biology

Volumn 26, Issue 3, 2013, Pages 600-611

  Schoebel, C N ^a   Brodbeck, S ^a   Buehler, D ^a   Cornejo, C ^a   Gajurel, J ^b   Hartikainen, H ^c   Keller, D ^a   Leys, M ^d   Říčanová, Š ^e   Segelbacher, G ^f   Werth, S ^a,g   Csencsics, D ^a  

^a SWISS FEDERAL RESEARCH INSTITUTE WSL   (Switzerland)

^b TRIBHUVAN UNIVERSITY   (Nepal)

^c DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^d SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^e INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^f UNIVERSITY OF FREIBURG   (Germany)

^g UNIVERSITY OF ICELAND   (Iceland)

Author keywords

Comparative studies; Conservation genetics; Massively parallel sequencing; Next generation sequencing technology; Population genetics; Shotgun sequencing

Indexed keywords

FUNGAL DNA; MICROSATELLITE DNA; PLANT DNA; PRIMER DNA;

BIRD; CONSERVATION GENETICS; DATA SET; EVOLUTIONARY BIOLOGY; FUNGUS; GENETIC ANALYSIS; GENETIC MARKER; GENOME; GENOMICS; INVERTEBRATE; LEARNING; MAMMAL; PLANT; POLYMORPHISM; POPULATION GENETICS;

ANGIOSPERM; ANIMAL; ARTICLE; BIRD; DNA SEQUENCE; GENE LOCUS; GENETICS; GENOME SIZE; INVERTEBRATE; METHODOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE MOTIF; PHYTOPHTHORA;

ANGIOSPERMS; ANIMALS; BIRDS; DNA PRIMERS; DNA, FUNGAL; DNA, PLANT; EVOLUTION, MOLECULAR; GENETIC LOCI; GENOME SIZE; INVERTEBRATES; MICROSATELLITE REPEATS; NUCLEOTIDE MOTIFS; PHYTOPHTHORA; SEQUENCE ANALYSIS, DNA;

AVES; FUNGI; INVERTEBRATA; MAMMALIA;

EID: 84873720080     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12077     Document Type: Article

References (66)

1. Abdelkrim, J., Robertson, B.C., Stanton, J.-A.L. & Gemmell, N.J. 2009. Fast, cost-effective development of species-specific microsatellite markers by genomic sequencing. Biotechniques 46: 185-192.
2. Ansell, S.W., Grundmann, M., Russell, S.J., Schneider, H. & Vogel, J.C. 2008. Genetic discontinuity, breeding-system change and population history of Arabis alpina in the Italian Peninsula and adjacent Alps. Mol. Ecol. 17: 2245-2257.
3. Armaleo, D. & May, S. 2009. Sizing the fungal and algal genomes of the lichen Cladonia grayi through quantitative PCR. Symbiosis 49: 43-51.
4. van Asch, B., Pinheiro, R., Pereira, R., Alves, C., Pereira, V., Pereira, F. et al. 2010. A framework for the development of STR genotyping in domestic animal species: characterization and population study of 12 canine X-chromosome loci. Electrophoresis 31: 303-308.
5. Barbara, T., Palma-Silva, C., Paggi, G.M., Bered, F., Fay, M.F. & Lexer, C. 2007. Cross-species transfer of nuclear microsatellite markers: potential and limitations. Mol. Ecol. 16: 3759-3767.
6. Bertolino, S., Amori, G., Henttonen, H., Zagorodnyuk, I., Zima, J., Juškatis, R. et al. 2008. 'Eliomys quercinus'. IUCN Red list of Threatened Species. Version 3.1. Available at: www.iucnredlist.org.
7. Buehler, D., Graf, R., Holderegger, R. & Gugerli, F. 2011. Using the 454 pyrosequencing-based technique in the development of nuclear microsatellite loci in the alpine plant Arabis alpina (Brassicaceae). Am. J. Bot. 98(5): e103-e105.
8. Casalegno, S., Amatulli, G., Camia, A., Nelson, A. & Pekkarinen, A. 2010. Vulnerability of Pinus cembra L. in the Alps and the Carpathian mountains under present and future climates. Forest Ecol. Manag. 259: 750-761.
9. Castoe, T.A., Poole, A.W., Gu, W., de Koning, J., Daza, J.M., Smith, E.N. et al. 2010. Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Mol. Ecol. Resour. 10: 341-347.
10. Csencsics, D., Brodbeck, S. & Holderegger, R. 2010. Cost-effective, species-specific microsatellite development for the endangered dwarf bulrush (Typha minima) using next-generation sequencing technology. J. Hered. 101: 789-793.
11. Doležel, J., Bartoš, J., Voglmayr, H. & Greilhuber, J. 2003. Nuclear DNA content and genome size of trout and human. Cytometry 51A: 127-128.
12. Dolgener, N., Schroeder, C., Schneeweiss, N. & Tiedemann, R. 2012. Genetic population structure of the Fire-bellied toad Bombina bombina in an area of high population density: implications for conservation. Hydrobiologia 689: 111-120.
13. Dutech, C., Enjalbert, J., Fourneier, E., Delmotte, F., Barrès, B., Carlier, J. et al. 2007. Challenges of microsatellite isolation in fungi. Fungal Genet. Biol. 44: 933-949.
14. Erwin, D.C. & Ribeiro, O.K. 1996. Phytophthora Diseases Worldwide. APS Press, St. Paul, MN.
15. Faircloth, B.C. 2008. MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol. Ecol. Resour. 8: 92-94.
16. Farjon, A. 1998. World Checklist and Bibliography of Conifers. Royal Botanic Gardens, Kew.
17. Gallagher, R.V., Leishman, M.R., Miller, J.T., Hui, C., Richardson, D.M., Suda, J. et al. 2011. Invasiveness in introduced Australian acacias: the role of species traits and genome size. Divers. Distr. 17: 884-897.
18. Gardner, M.G., Fitch, A.J., Bertozzi, T. & Lowe, A.J. 2011. Rise of the machines - recommendations for ecologists when using next generation sequencing for microsatellite development. Mol. Ecol. Resour. 11: 1093-1101.
19. Garner, W.J. 2002. Genome size and microsatellites: the effect of nuclear size on amplification potential. Genome 45: 212-215.
20. Goldstein, D.B. & Schlötterer, C. 1999. Microsatellites: evolution and applications. Oxford University Press, Oxford.
21. Greilhuber, J. 1986. Severely distorted Feulgen-DNA amounts in Pinus (Coniferophytina) after nonadditive fixations as a result of meristematic self-tanning with vacuole contents. Can. J. Genet. Cytol. 28: 409-415.
22. Greilhuber, J., Borsch, T., Müller, K., Worberg, A., Porembski, S. & Barthlott, W. 2006. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biol. 8: 770-777.
23. Grover, A., Aishwarya, V. & Sharma, P.C. 2012. Searching microsatellites in DNA sequences: approaches used and tools developed. Physiol. Mol. Biol. Plants 18: 11-19.
24. Guichoux, E., Lagache, L., Wagner, S., Chaumeil, P., Leger, P., Lepais, O. et al. 2011. Current trends in microsatellite genotyping. Mol. Ecol. Resour. 11: 591-611.
25. Hallingbäck, T. & Martinsson, P.O. 1987. The retreat of two lichens, Lobaria pulmonaria and L. scrobiculata in the district of Gäsene (SW Sweden). Windahlia 17: 27-32.
26. Hancock, J.M. 2002. Genome size and the accumulation of simple sequence repeats: implications of new data from genome sequencing projects. Genetica 115: 93-103.
27. Hartikainen, H. & Jokela, J. 2012. Characterisation of polymorphic microsatellite loci in the freshwater bryozoan Fredericella sultana. Conserv. Genet. Resour. 4: 475-477.
28. Horáček, I. 1986. Fossil records and chorological status of dormice in Czechoslovakia, Part I: Glis glis, Eliomys quercinus. Folia Musei Rerum Naturalium Bohemiae Occidentalis, Plzen, Zoologica 24: 49-59.
29. Humpesch, U.H. 1979. Life-cycles and growth-rates of Baetis spp (Ephemeroptera, Baetidae) in the laboratory and in 2 stony streams in Austria. Freshwater Biol. 9: 467-479.
30. Hurtado, L.A., Santamaria, C.A. & Fitzgerald, L.A. 2012. Conservation genetics of the critically endangered Saint Croix ground lizard (Ameiva polops Cope 1863). Conserv. Genet. 13: 665-679.
31. Jennings, T.N., Knaus, B.J., Mullins, T.D., Haig, S.M. & Cronn, R.C. 2011. Multiplexed microsatellite recovery using massively parallel sequencing. Mol. Ecol. Resour. 11: 1060-1067.
32. Jung, T. & Burgess, T.I. 2009. Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia 22: 95-110.
33. Keller, D., Jung, E. & Holderegger, R. 2012. Development of microsatellite markers for the wetland grasshopper Stethophyma grossum. Conserv. Genet. Resour. 4: 507-509.
34. Kopatz, A., Geir Eiken, H., Hagen, S.B., Ruokonen, M., Esparza-Salas, R., Schregel, J. et al. 2012. Connectivity and population subdivision at the fringe of a large brown bear (Ursus arctos) population in North Western Europe. Conserv. Genet. 13: 681-692.
35. Kroon, L.P.N.M., Brouwer, H., de Cock, A.W.A.M. & Govers, F. 2011. The Genus Phytophthora Anno 2012. Phytopathology. 102: 348-364.
36. Leitch, I.J., Hanson, L., Winfield, M., Parker, J. & Bennett, M.D. 2001. Nuclear DNA C-values complete familial representation in gymnosperms. Ann. Bot. 88: 843-849.
37. Lepais, O. & Bacles, C.F.E. 2011. Comparison of random and microsatellite-enriched shotgun pyrosequencing for microsatellite discovery and single multiplex PCR optimization in Acacia harpophylla F. Muell. Ex Benth. Mol. Ecol. Resour. 11: 711-724.
38. Malausa, T., Gilles, A., Meglécz, E., Blanquart, H., Duthoy, S., Costedoat, C. et al. 2011. High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Mol. Ecol. Resour. 11: 638-644.
39. Manel, S., Poncet, B.N., Legendre, P., Gugerli, F. & Holderegger, R. 2010. Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Mol. Ecol. 19: 3824-3835.
40. Manoel, R.O., Alves, P.F., Dourado, C.L., Gaino, A.P.S.C., Freitas, M.L.M., Moraes, M.L.T. et al. 2012. Contemporary pollen flow, mating patterns and effective population size inferred from paternity analysis in a small fragmented population of the Neotropical tree Copaifera langsdorffii Desf. (Leguminosae-Caesalpinioideae). Conserv. Genet. 13: 613-623.
41. Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader, J.S., Bemben, L.A. et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
42. Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Kryštufek, B., Reijnders, P.J.H., Spitzenberger, F. et al. 1999. The atlas of European mammals. Academic Press, London.
43. Monnerat, C., Thorens, P., Walter, T. & Gonseth, Y. 2007. Rote Liste der gefährdeten Arten der Schweiz: Heuschrecken. BAFU, Bern, Switzerland.
44. Müller, N. 1991. Verbreitung, Vergesellschaftung und Rückgang des Zwergrohrkolbens (Typha minima Hoppe). Hoppea 50: 19.
45. Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. & Wahli, T. 2011. Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshwater Biol. 56: 735-753.
46. Oxford, E. 1996. The great famine - when a blight struck the Irish potato crop in the 1840s, it precipitated a famine that caused more than a million deaths and the exodus of that many more to America. Am. Hist. 31: 52-61.
47. Parchman, T., Geist, K., Grahnen, J., Benkman, C. & Buerkle, C.A. 2010. Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 11: 180.
48. Prunier, P., Garraud, L., Köhler, C., Lambelet-Haueter, C., Selvaggi, A. & Werner, P. 2010. Distribution et régression de la petite massette (Typha minima) dans les Alpes. Bot. Helv. 120: 43-52.
49. Reid, K., Hoareau, T. B. & Bloomer, P. 2012. High-throughput microsatellite marker development in two sparid species and verification of their transferability in the family Sparidae. Mol. Ecol. Resour. 12: 740-752.
50. Rolshausen, G., Segelbacher, G., Hobson, K.A & Schaefer, H.M. 2009. Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Curr. Biol. 19: 2097-101.
51. Rozen, S. & Skaletsky, H.J. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics Methods and Protocols: Methods in Molecular Biology (S. Krawetz & S. Misener, eds), pp. 365-386. Humana Press, Totowa.
52. Rushforth, K.D. 1987. Conifers. Helm, London.
53. Santana, Q.C., Coetzee, M.P.A., Steenkamp, E.T., Mlonyeni, O.X., Hammond, G.N.A., Wingfield, M.J. et al. 2009. Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 46: 217-223.
54. Sartori, M. & Landolt, P. 1999. Atlas de distribution des éphémères de Suisse (Insecta, Ephemeroptera). Centre Suisse de Cartographie de la Faune, Neuchâtel, Switzerland.
55. Schopf, T.J.M. 1983. A genomic library and the genome size for the cheilostome bryozoan Watersipora. In: Bryozoa: Ordovician to recent (C. Nielsen & G.P. Larwood, eds), pp. 285-292. Olsen & Olsen, Fredensborg.
56. Schultze-Motel, W. 1986. Arabis alpina. In: Illustrierte Flora von Mitteleuropa, Band 4 Teil 1 (H.J. Conert, U. Hamann, W. Schultze-Motel & G. Wagenitz, eds), pp. 248-251. Parey, Berlin.
57. Selkoe, K.A. & Toonen, R.J. 2006. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol. Lett. 9: 615-629.
58. Takayama, K., Lopez, P., Konig, C., Kohl, G., Novak, J. & Stuessy, T.F. 2011. A simple and cost-effective approach for microsatellite isolation in non-model plant species using small-scale 454 pyrosequencing. Taxon 60: 144: 2-1449.
59. Tóth, G., Gaspari, Z. & Jurka, J. 2000. Microsatellites in different eukaryotic genomes: Survey and analysis. Genome Res. 10: 967-981.
60. Tyler, B., Tripathy, S., Grunwald, N., Lamour, K., Ivors, K., Garbelotto, M. et al. 2006. Genome sequence of Phytophthora ramorum: implications for management. In: Proceedings of the sudden oak death second science symposium: the state of our knowledge (S.J. Frankel, P.J. Shea & M.I. Haverty, tech. coords, eds), pp. 157-158. Gen. Tech. Rep. PSW-GTR-196. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA.
61. Van De Vliet, M.S., Diekmann, O.E., Serrao, E.A. & Beja, P. 2009. Isolation of highly polymorphic microsatellite loci for a species with a large genome size: sharp-ribbed salamander (Pleurodeles waltl). Mol. Ecol. Resour. 9: 425-428.
62. Vance, S. 1996. Morphological and behavioural sex reversal in mermithid-infected mayflies. Proc. R. Soc. B 263: 907-912.
63. Wang, R., Farrona, S., Vincent, C., Joecker, A., Schoof, H., Turck, F. et al. 2009. PEP1 regulates perennial flowering in Arabis alpina. Nature 42: 3-428.
64. Werth, S., Cornejo, C. & Scheidegger, C. In press. Characterization of microsatellite loci in the lichen fungus Lobaria pulmonaria (Lobariaceae). APPS.
65. Wood, T. S. & Backus, B. T. 1992. Differentiation of North American and European forms of Fredericella sultana (Blumenbach) (Ectoprocta: Phylactolaemata). Hydrobiologia 237: 185-193.
66. Zalapa, J.E., Cuevas, H., Zhu, H., Steffan, S., Senalik, D., Zeldin, E. et al. 2012. Using next-generation sequencing approaches to isolate simple sequence repeat (microsatellite) loci in the plant sciences. Am. J. Bot. 99: 193-208.