SNP Design from 454 Sequencing of Podosphaera plantaginis Transcriptome Reveals a Genetically Diverse Pathogen Metapopulation with High Levels of Mixed-Genotype Infection

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Tollenaere, Charlotte ^a   Susi, Hanna ^a   Nokso Koivisto, Jussi ^a   Koskinen, Patrik ^a,b   Tack, Ayco ^a   Auvinen, Petri ^b   Paulin, Lars ^b   Frilander, Mikko J ^b   Lehtonen, Rainer ^a   Laine, Anna Liisa ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; TRANSCRIPTOME;

ALLELE; ARTICLE; FINLAND; FUNGAL PLANT DISEASE; FUNGUS; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC VARIABILITY; METAPOPULATION; NONHUMAN; PLANT LEAF; PODOSPHAERA PLANTAGINIS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; VALIDATION PROCESS;

ASCOMYCOTA; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENETIC MARKERS; GENOTYPE; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE ANNOTATION; MYCOSES; PLANTAGO; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; RNA, FUNGAL; SEQUENCE ANALYSIS, RNA;

ERYSIPHALES; PLANTAGO LANCEOLATA; PODOSPHAERA PLANTAGINIS;

EID: 84871650682     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052492     Document Type: Article

References (61)

1. Archie EA, Luikart G, Ezenwa VO, (2009) Infecting epidemiology with genetics: a new frontier in disease ecology. Trends in Ecology & Evolution 24: 21-30.
2. Criscione CD, Poulin R, Blouin MS, (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14: 2247-2257.
3. Giraud T, Enjalbert J, Fournier E, Delmote F, Dutech C, (2008) Population genetics of fungal diseases of plants. Parasite 15: 449-454.
4. Laine AL, Hanski I, (2006) Large-scale spatial dynamics of a specialist plant pathogen in a fragmented landscape. Journal of Ecology 94: 217-226.
5. Soubeyrand S, Laine AL, Hanski I, Penttinen A, (2009) Spatiotemporal structure of host-pathogen interactions in a metapopulation. Am Nat 174: 308-320.
6. Ovaskainen O, Laine AL, (2006) Inferring evolutionary signals from ecological data in a plant-pathogen metapopulation. Ecology 87: 880-891.
7. Salvaudon L, Giraud T, Shykoff JA, (2008) Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Current Opinion in Plant Biology 11: 135-143.
8. Laine AL, (2005) Spatial scale of local adaptation in a plant-pathogen metapopulation. J Evol Biol 18: 930-938.
9. Laine AL, (2006) Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc Biol Sci 273: 267-273.
10. Laine AL, (2008) Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecol Lett 11: 327-337.
11. van Baalen M, Sabelis MW (1995) The scope for virulence management: a comment on Ewald's view on the evolution of virulence. Trends Microbiol 3: 414-416; discussion 416-417.
12. Mideo N, (2009) Parasite adaptations to within-host competition. Trends Parasitol 25: 261-268.
13. Frank SA, (1996) Models of parasite virulence. Q Rev Biol 71: 37-78.
14. Chao L, Hanley KA, Burch CL, Dahlberg C, Turner PE, (2000) Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q Rev Biol 75: 261-275.
15. Alizon S, Hurford A, Mideo N, Van Baalen M, (2009) Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol 22: 245-259.
16. Read AF, Taylor LH, (2001) The ecology of genetically diverse infections. Science 292: 1099-1102.
17. Mideo N, Alizon S, Day T, (2008) Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23: 511-517.
18. Agrios GN (2005) Plant pathology, 5th edition. California: Academic Press.
19. Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, et al. (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13: 414-430.
20. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, et al. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543-1546.
21. Godfrey D, Bohlenius H, Pedersen C, Zhang ZG, Emmersen J, et al. (2010) Powdery mildew fungal effector candidates share N-terminal Y/F/WxC-motif. Bmc Genomics 11.
22. Webling R, Schmidt SM, Micali CO, Knaust F, Reinhardt R, et al. (2012) Transcriptome analysis of enriched Golovinomyces orontii haustoria by deep 454 pyrosequencing. Fungal Genetics and Biology.
23. Frenkel O, Portillo I, Brewer MT, Peros JP, Cadle-Davidson L, et al. (2012) Development of microsatellite markers from the transcriptome of Erysiphe necator for analysing population structure in North America and Europe. Plant Pathology 61: 106-119.
24. Mori Y, Sato Y, Takamatsu S, (2000) Evolutionary analysis of the powdery mildew fungi using nucleotide sequences of the nuclear ribosomal DNA. Mycologia 92: 74-93.
25. Glawe DA, (2008) The powdery mildews: A review of the world's most familiar (yet poorly known) plant pathogens. Annual Review of Phytopathology 46: 27-51.
26. Takamatsu S, Matsuda S, (2004) Estimation of molecular clocks for ITS and 28S rDNA in Erysiphales. Mycoscience 45: 340-344.
27. Morin PA, Luikart G, Wayne RK, Grp SW, (2004) SNPs in ecology, evolution and conservation. Trends in Ecology & Evolution 19: 208-216.
28. Garvin MR, Saitoh K, Gharrett AJ, (2010) Application of single nucleotide polymorphisms to non-model species: a technical review. Molecular Ecology Resources 10: 915-934.
29. Seeb JE, Carvalho G, Hauser L, Naish K, Roberts S, et al. (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Molecular Ecology Resources 11: 1-8.
30. Helyar SJ, Hemmer-Hansen J, Bekkevold D, Taylor MI, Ogden R, et al. (2011) Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Molecular Ecology Resources 11: 123-136.
31. Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, et al. (2010) Adaptation genomics: the next generation. Trends in Ecology & Evolution 25: 705-712.
32. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
33. Ekblom R, Galindo J, (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107: 1-15.
34. Wheat CW, (2010) Rapidly developing functional genomics in ecological model systems via 454 transcriptome sequencing. Genetica 138: 433-451.
35. Slate J, Gratten J, Beraldi D, Stapley J, Hale M, et al. (2009) Gene mapping in the wild with SNPs: guidelines and future directions. Genetica 136: 97-107.
36. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, et al. (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Molecular Ecology 17: 1636-1647.
37. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, et al. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. Bmc Genomics 10.
38. Novaes E, Drost DR, Farmerie WG, Pappas GJ, Grattapaglia D, et al. (2008) High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. Bmc Genomics 9.
39. Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Muller WEG, et al. (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research 14: 1147-1159.
40. Panstruga R, Dodds PN, (2009) Terrific Protein Traffic: The Mystery of Effector Protein Delivery by Filamentous Plant Pathogens. Science 324: 748-750.
41. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods 8: 785-786.
42. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL, (2001) Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. Journal of Molecular Biology 305: 567-580.
43. Ridout CJ, Skamnioti P, Porritt O, Sacristan S, Jones JDG, et al. (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18: 2402-2414.
44. Sacristan S, Vigouroux M, Pedersen C, Skamnioti P, Thordal-Christensen H, et al. (2009) Coevolution between a Family of Parasite Virulence Effectors and a Class of LINE-1 Retrotransposons. Plos One 4.
45. Brewer MT, Lance CDB, Paolo CC, 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 Genetics and Biology 48: 704-713.
46. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CIA, et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proceedings of the National Academy of Sciences of the United States of America 103: 8888-8893.
47. Sanchez CC, Smith TPL, Wiedmann RT, Vallejo RL, Salem M, et al. (2009) Single nucleotide polymorphism discovery in rainbow trout by deep sequencing of a reduced representation library. Bmc Genomics 10.
48. Barbazuk WB, Emrich SJ, Chen HD, Li L, Schnable PS, (2007) SNP discovery via 454 transcriptome sequencing. Plant Journal 51: 910-918.
49. Whitlock MC, (1992) Temporal Fluctuations in Demographic Parameters and the Genetic Variance among Populations. Evolution 46: 608-615.
50. Shama LNS, Kubow KB, Jokela J, Robinson CT (2011) Bottlenecks drive temporal and spatial genetic changes in alpine caddisfly metapopulations. Bmc Evolutionary Biology 11.
51. Hahn DA, Ragland GJ, Shoemaker DD, Denlinger DL (2009) Gene discovery using massively parallel pyrosequencing to develop ESTs for the flesh fly Sarcophaga crassipalpis. Bmc Genomics 10.
52. Rieux A, Halkett F, de Bellaire LD, Zapater MF, Rousset F, et al. (2011) Inferences on pathogenic fungus population structures from microsatellite data: new insights from spatial genetics approaches. Molecular Ecology 20: 1661-1674.
53. 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. Molecular Biology and Evolution 28: 459-471.
54. Tokarska M, Marshall T, Kowalczyk R, Wojcik JM, Pertoldi C, et al. (2009) Effectiveness of microsatellite and SNP markers for parentage and identity analysis in species with low genetic diversity: the case of European bison. Heredity 103: 326-332.
55. Blows MW, Hoffmann AA, (2005) A reassessment of genetic limits to evolutionary change. Ecology 86: 1371-1384.
56. Lopez-Villavicencio M, Jonot O, Coantic A, Hood ME, Enjalbert J, et al. (2007) Multiple infections by the anther smut pathogen are frequent and involve related strains. PLoS Pathog 3: e176.
57. Linde CC, Zhan J, McDonald BA, (2002) Population Structure of Mycosphaerella graminicola: From Lesions to Continents. Phytopathology 92: 946-955.
58. Perez G, Slippers B, Wingfield BD, Hunter GC, Wingfield MJ, (2010) Micro- and macrospatial scale analyses illustrates mixed mating strategies and extensive geneflow in populations of an invasive haploid pathogen. Mol Ecol 19: 1801-1813.
59. Lopez-Villavicencio M, Courjol F, Gibson AK, Hood ME, Jonot O, et al. (2011) Competition, cooperation among kin, and virulence in multiple infections. Evolution 65: 1357-1366.
60. May RM, Nowak MA, (1994) Superinfection, Metapopulation Dynamics, and the Evolution of Diversity. Journal of Theoretical Biology 170: 95-114.
61. Alizon S, van Baalen M, (2008) Multiple infections, immune dynamics, and the evolution of virulence. American Naturalist 172: E150-E168.