Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce

Abstract

Conifers are characterized by a large genome size and a rapid decay of linkage disequilibrium, most often within gene limits. Genome scans based on noncoding markers are less likely to detect molecular adaptation linked to genes in these species. In this study, we assessed the effectiveness of a genome‐wide single nucleotide polymorphism (SNP) scan focused on expressed genes in detecting local adaptation in a conifer species. Samples were collected from six natural populations of white spruce ( Picea glauca ) moderately differentiated for several quantitative characters. A total of 534 SNPs representing 345 expressed genes were analysed. Genes potentially under natural selection were identified by estimating the differentiation in SNP frequencies among populations ( F ST ) and identifying outliers, and by estimating local differentiation using a Bayesian approach. Both average expected heterozygosity and population differentiation estimates ( H E = 0.270 and F ST = 0.006) were comparable to those obtained with other genetic markers. Of all genes, 5.5% were identified as outliers with F ST at the 95% confidence level, while 14% were identified as candidates for local adaptation with the Bayesian method. There was some overlap between the two gene sets. More than half of the candidate genes for local adaptation were specific to the warmest population, about 20% to the most arid population, and 15% to the coldest and most humid higher altitude population. These adaptive trends were consistent with the genes’ putative functions and the divergence in quantitative traits noted among the populations. The results suggest that an approach separating the locus and population effects is useful to identify genes potentially under selection. These candidates are worth exploring in more details at the physiological and ecological levels.

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References 92

1. 1.

   Acheré V, Favre JM, Besnard G, Jeandroz S. Genomic organization of molecular differentiation in Norway spruce (Picea abies. Molecular Ecology. 2005;14:3191-3201.

   Not in our library10.1111/j.1365-294x.2005.02646.x

2. 2.

   Akey JM, Zhang G, Zhang K, Jin L, Shriver MD. Interrogating a high-density SNP map for signatures of natural selection. Genome Research. 2002;12:1805-1814.

   Not in our library10.1101/gr.631202

3. 3.

   Altshuler D, Pollara VJ, Cowles CR, et al. An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature. 2000;407:513-516.

   Not in our library10.1038/35035083

4. 4.

   Andalo C, Beaulieu J, Bousquet J. The impact of climate change on growth of local white spruce populations in Québec, Canada. Forest Ecology and Management. 2005;205:169-182.

   Not in our library

5. 5.

   Beaty TH, Fallin MD, Hetmanski JB, et al. Haplotype diversity in 11 candidate genes across four populations. Genetics. 2005;171:259-267.

   Not in our library10.1534/genetics.105.043075

6. 6.

   Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology. 2004;13:969-980.

   Not in our library10.1111/j.1365-294x.2004.02125.x

7. 7.

   Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Scoiety B: Biological Sciences. 1996;263:1619-1626.

   Not in our library

8. 8.

   Bedon F, Grima-Pettenati J, Mackay J. Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca. BMC Plant Biology. 2007;7:17.

   Not in our library10.1186/1471-2229-7-17

9. 9.

   Bonin A, Taberlet P, Miaud C, Pompanon F. Explorative genome scan to detect candidate loci for adaptation along a gradient in the common frog (Rana temporaria. Molecular Biology and Evolution. 2006;23:773-783.

   Not in our library10.1093/molbev/msj087

10. 10.

    Bouck A, Vision T. The molecular ecologist's guide to expressed sequence tag. Molecular Ecology. 2007;16:909-924.

    Not in our library10.1111/j.1365-294x.2006.03195.x

11. 11.

    Bousquet J, Isabel N, Pelgas B, Kole C, et al. Spruce. Forest Trees. 2007;Vol. 7:93-114.

    Not in our library

12. 12.

    Bradshaw HDJ, Schemske DW. Allele substitution at a flower colour locus produces a pollinator shift in monkey flowers. Nature. 2003;426:176-178.

    Not in our library10.1038/nature02106

13. 13.

    Brem RB, Yvert G, Clinton R, Kruglyak L. Genetic dissection of transcriptional regulation in budding yeast. Science. 2002;296:752-755.

    Not in our library10.1126/science.1069516

14. 14.

    Broderick P, Carvajal-Carmona L, Webb E, et al. A genome–wide association study shows that common alleles of SMAD7 influence colorectal cancer risk. Nature Genetics. 2007;39:1315-1317.

    Not in our library10.1038/ng.2007.18

15. 15.

    Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale D. Nucleotide diversity and linkage disequilibrium in loblolly pine. Proceedings of the National Academy of Sciences, USA. 2004;101:15255-15260.

    Not in our library10.1073/pnas.0404231101

16. 16.

    Brumfield RT, Beerli P, Nickerson DA, Edwards SV. The utility of single nucleotide polymorphisms in inferences of population history. Trends in Ecology and Evolution. 2003;18:249-256.

    Not in our library

17. 17.

    Campbell D, Bernatchez L. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Molecular Biology and Evolution. 2004;21:945-956.

    Not in our library10.1093/molbev/msh101

18. 18.

    Carmel L, Wolf YI, Rogozin IB, Koonin EV. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Research. 2007;17:1034-1044.

    Not in our library10.1101/gr.6438607

19. 19.

    Chamary JV, Hurst LD. Similar rates but different modes of sequence evolution in introns and at exonic silent sites in rodents: evidence for selectively driven codon usage. Molecular Biology and Evolution. 2004;21:1014-1023.

    Not in our library10.1093/molbev/msh087

20. 20.

    Ching A, Caldwell K, Jung M, et al. SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genetics. 2002;3:19.

    Not in our library10.1186/1471-2156-3-19

21. 21.

    Corcuera L, Camarero JJ, Gil-Pelegrín E. Effects of a severe drought on growth and wood anatomical properties of Quercus Faginea. IAWA Journal. 2004;25:185-204.

    Not in our library

22. 22.

    Cork JM, Purugganan MD. High-diversity genes in the Arabidopsis genome. Genetics. 2005;170:1897-1911.

    Not in our library10.1534/genetics.104.036152

23. 23.

    Drake JA, Bird C, Nemesh J, et al. Conserved noncoding sequences are selectively constrained and not mutation cold spots. Nature Genetics. 2005;38:223-227.

    Not in our library10.1038/ng1710

24. 24.

    Erickson DL, Fenster CB, Stenoien HK, Price D. Quantitative trait locus analyses and the study of evolutionary process. Molecular Ecology. 2004;13:2505-2522.

    Not in our library10.1111/j.1365-294x.2004.02254.x

25. 25.

    Fan JB, Oliphant A, Shen R, et al. Highly parallel SNP genotyping. Cold Spring Harbor Symposia on Quantitative Biology. 2003;69-78.

    Not in our library10.1101/sqb.2003.68.69

26. 26.

    Ford MJ. Applications of selective neutrality tests to molecular ecology. Molecular Ecology. 2002;11:1245-1262.

    Not in our library10.1046/j.1365-294x.2002.01536.x

27. 27.

    Frank AC, Lobry JR. Asymmetric substitution patterns: a review of possible underlying mutational or selective mechanisms. Gene. 1999;238:65-77.

    Not in our library10.1016/s0378-1119(99)00297-8

28. 28.

    Frewen BE, Chen THH, Howe GT, et al. Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics. 2000;154:837-845.

    Not in our library10.1093/genetics/154.2.837

29. 29.

    Gazave E, Marqués-Bonet T, Fernando O, Charlesworth B, Navarro A. Patterns and rates of intron divergence between humans and chimpanzees. Genome Biology. 2007;8:R21.

    Not in our library10.1186/gb-2007-8-2-r21

30. 30.

    Glazier AM, Nadeau JH, Aitman TJ. Finding genes that underlie complex traits. Science. 2002;298:2345-2349.

    Not in our library10.1126/science.1076641

31. 31.

    Godt MJW, Hamrick MA, Edwards-Burke MA, Williams JH. Comparisons of genetic diversity in white spruce (Picea glauca) and jack pine (Pinus banksiana) seed orchards with natural populations. Canadian Journal of Forest Research. 2001;31:943-949.

    Not in our library

32. 32.
    Nucleotide diversity of the <it>ZmPox3 </it>maize peroxidase gene: Relationships between a MITE insertion in exon 2 and variation in forage maize digestibility · 2004

    Not checked
33. 33.

    Hassett DJ, Cohen MS. Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. The Federation of American Societies for Experimental Biology. 1989;3:2574-2582.

    Not in our library10.1096/fasebj.3.14.2556311

34. 34.

    Hedrick PW. Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution. 1999;53:313-318.

    Not in our library10.1111/j.1558-5646.1999.tb03767.x

35. 35.

    Heidelberger P, Welch P. Spectral method for confidence interval generation and run length control in simulations. Communications of the ACM. 1981;24:233-245.

    Not in our library

36. 36.

    Howe GT, Aitken SN, Neale DB, et al. From genotype to phenotype: unravelling the complexities of cold adaptation in forest trees. Canadian Journal of Botany. 2003;81:1247-1266.

    Not in our library

37. 37.

    Hurme P, Sillanpaa MJ, Arjas E, Repo T, Savolainen O. Genetic basis of climatic adaptation in Scots pine by Bayesian quantitative trait locus analysis. Genetics. 2000;156:1309-1322.

    Not in our library10.1093/genetics/156.3.1309

38. 38.
    Accuracy and quality of massively parallel DNA pyrosequencing · 2007

    No notice
39. 39.

    Isabel N, Beaulieu J, Bousquet J. Complete congruence between gene diversity estimates derived from genotypic data at enzyme and RAPD loci in black spruce. Proceedings of the National Academy of Sciences, USA. 1995;92:6369-6373.

    Not in our library10.1073/pnas.92.14.6369

40. 40.

    Isabel N, Beaulieu J, Theriault P, Bousquet J. Direct evidence for biased gene diversity estimates from dominant random amplified polymorphic DNA (RAPD) fingerprints. Molecular Ecology. 1999;8:477-483.

    Not in our library

41. 41.

    Jaramillo-Correa JP, Beaulieu J, Bousquet J. Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Molecular Ecology. 2001;10:2729-2740.

    Not in our library10.1046/j.0962-1083.2001.01386.x

42. 42.

    Kaplan NL, Hudson RR, Langley CH. The ‘hitchhiking effect′ revisited. Genetics. 1989;123:887-899.

    Not in our library10.1093/genetics/123.4.887

43. 43.

    Kayser M, Brauer S, Stoneking M. A genome scan to detect candidate regions influenced by local natural selection in human populations. Molecular Biology and Evolution. 2003;20:893-900.

    Not in our library10.1093/molbev/msg092

44. 44.

    Keightley PD, Gaffney DJ. Functional constraints and frequency of deleterious mutations in noncoding DNA of rodents. Proceedings of the National Academy of Sciences, USA. 2003;100:13402-13406.

    Not in our library10.1073/pnas.2233252100

45. 45.

    Kelley JL, Madeoy J, Calhoun JC, Swanson W, Akey JM. Genomic signatures of positive selection in humans and the limits of outlier approaches. Genome Research. 2006;16:980-989.

    Not in our library10.1101/gr.5157306

46. 46.
    A Practical Genome Scan for Population-Specific Strong Selective Sweeps That Have Reached Fixation · 2007

    No notice
47. 47.

    Kirst M, Johnson AF, Baucom C, et al. Apparent homology of expressed genes from wood-forming tissues of loblolly pine (Pinus taeda L.) with Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA. 2003;100:7383-7388.

    Not in our library10.1073/pnas.1132171100

48. 48.

    Krutovsky KV, Neale DB. Nucleotide diversity and linkage disequilibrium in cold-hardiness and wood quality-related candidate genes in Douglas fir. Genetics. 2005;171:2029-2041.

    Not in our library10.1534/genetics.105.044420

49. 49.

    Li P, Beaulieu J, Corriveau A, Bousquet J. Genetic variation in juvenile growth and phenology in a white spruce provenance-progeny test. Silvae Genetica. 1993;42:52-59.

    Not in our library

50. 50.

    Li P, Beaulieu J, Bousquet J. Genetic structure and patterns of genetic variation among populations in eastern white spruce (Picea glauca. Canadian Journal of Forest Research. 1997;27:189-198.

    Not in our library

51. 51.

    Li L, Brunk BP, Kissinger JC, et al. Gene discovery in the Apicomplexa as revealed by EST sequencing and assembly of a comparative gene database. Genome Research. 2003;13:443-454.

    Not in our library10.1101/gr.693203

52. 52.

    Luikart G, England P, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nature Reviews of Genetics. 2003;4:981-994.

    Not in our library10.1038/nrg1226

53. 53.

    Lynch M. The origins of eukaryotic gene structure. Molecular Biology and Evolution. 2006;23:450-468.

    Not in our library10.1093/molbev/msj050

54. 54.

    Majewski J, Ott J. Distribution and characterization of regulatory elements in the human genome. Genome Research. 2002;12:1827-1836.

    Not in our library10.1101/gr.606402

55. 55.

    Mariette S, Le Corre V, Austerlitz F, Kremer A. Sampling within the genome for measuring within-population diversity: trade-offs between markers. Molecular Ecology. 2002;11:1145-1156.

    Not in our library10.1046/j.1365-294x.2002.01519.x

56. 56.

    Maynard Smith J, Haigh J. The hitch-hiking effect of a favorable gene. Genetic Research. 1974;23:23-35.

    Not in our library

57. 57.

    Miller WG, Englen MD, Kathariou S, et al. Single nucleotide polymorphism and linkage disequilibrium within the TCR α/δ. Human Molecular Genetics. 2000;9:1011-1019.

    Not in our library10.1093/hmg/9.7.1011

58. 58.

    Moffatt MF, Traherne JA, Abecasis JR, Cookson WOCM. Single nucleotide polymorphism and linkage disequilibrium within the TCR α/δ locus. Human Molecular Genetics. 2000;9:1011-1019.

    Not in our library10.1093/hmg/9.7.1011

59. 59.

    Morin PA, Luikart G, Wayne RK, the SNP workshop Group. SNPs in ecology, evolution and conservation. Trends in Ecology and Evolution. 2004;19:208-216.

    Not in our library

60. 60.

    Murray BG. Nuclear DNA amounts in gymnosperms. Annals of Botany. 1998;82:3-15.

    Not in our library

61. 61.

    Neale DB, Savolainen O. Association genetics of complex traits in conifers. Trends in Plant Science. 2004;9:325-330.

    Not in our library10.1016/j.tplants.2004.05.006

62. 62.

    Nei M. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 1978;89:583-590.

    Not in our library10.1093/genetics/89.3.583

63. 63.

    Nybom H. Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology. 2004;13:1143-1155.

    Not in our library10.1111/j.1365-294x.2004.02141.x

64. 64.

    Oetjen K, Reusch TBH. Identification and characterization of 14 polymorphic EST-derived microsatellites in eelgrass (Zostera marina. Molecular Ecology Notes. 2007;7:777-780.

    Not in our library

65. 65.

    Ostrowski M-F, David J, Santoni S, et al. Evidence for a large-scale population structure among accessions of Arabidopsis thaliana: possible causes and consequences for the distribution of linkage disequilibrium. Molecular Ecology. 2006;15:1507-1517.

    Not in our library10.1111/j.1365-294x.2006.02865.x

66. 66.
    Generation, annotation, analysis and database integration of 16,500 white spruce EST clusters · 2005

    Not checked
67. 67.
    Automated SNP detection from a large collection of white spruce expressed sequences: contributing factors and approaches for the categorization of SNPs · 2006

    Not checked
68. 68.

    Pavy N, Pelgas B, Beauseigle S, et al. Enhancing genetic mapping of complex genomes through the design of highly-multiplexed SNP arrays: application to the large and unsequenced genomes of white spruce and black spruce. BMC Genomics. 2008;9:21.

    Not in our library10.1186/1471-2164-9-21

69. 69.

    Pelgas B, Beauseigle S, Acheré V, et al. Comparative genome mapping among Picea glauca, P. abies and P. mariana X rubens, and correspondance with other Pinaceae. Theoretical and Applied Genetics. 2006;113:1371-1393.

    Not in our library10.1007/s00122-006-0354-7

70. 70.

    Perry DJ, Bousquet J. Genetic diversity and mating system of post-fire and post-harvest black spruce: an investigation using codominant sequence-tagged site (STS) markers. Canadian Journal of Forest Research. 2001;31:32-40.

    Not in our library

71. 71.

    Przeworski M. The signature of positive selection at randomly chosen loci. Genetics. 2002;160:1179-1189.

    Not in our library10.1093/genetics/160.3.1179

72. 72.

    Quesada V, Dean C, Simpson GG. Regulating RNA processing in the control of Arabidospsis flowering. International Journal of Developmental Biology. 2005;49:773-780.

    Not in our library10.1387/ijdb.051995vq

73. 73.

    Régnière J. A generalized approach to landscape-wide seasonal forecasting with temperature-driven simulation models. Environmental Entomology. 1996;25:869-881.

    Not in our library

74. 74.

    Schieble WR, Morcuende R, Czechowski T, et al. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to Nitrogen. Plant Physiology. 2004;136:2483-2499.

    Not in our library10.1104/pp.104.047019

75. 75.

    Schlötterer C. Hitchhiking mapping — functional genomics from the population genetics perspective. Trends in Genetics. 2003;19:32-38.

    Not in our library10.1016/s0168-9525(02)00012-4

76. 76.

    Scotti-Saintagne C, Mariette S, Porth I, et al. Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. & Quercus petraea (Matt.) Liebl.]. Genetics. 2004;168:1615-1626.

    Not in our library10.1534/genetics.104.026849

77. 77.

    Shen R, Fan JB, Campbell D, et al. High-throughput SNP genotyping on universal bead arrays. Mutation Research. 2005;573:70-82.

    Not in our library10.1016/j.mrfmmm.2004.07.022

78. 78.

    Stephan W, Wiehe THE, Lenz MW. The effect of strongly selected substitutions on neutral polymorphism: analytical results based on diffusion theory. Theoretical Population Biology. 1992;41:237-254.

    Not in our library

79. 79.

    Storz JF. Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology. 2005;14:671-688.

    Not in our library10.1111/j.1365-294x.2005.02437.x

80. 80.

    Storz JF, Payseur BA, Nachman MW. Genome scans of DNA variability in humans reveal evidence for selective sweeps outside of Africa. Molecular Biology and Evolution. 2004;21:1800-1811.

    Not in our library10.1093/molbev/msh192

81. 81.

    Thumma BR, Nolan MF, Evans R, Moran GF. Polymorphisms in Cinnamoyl CoA Redustase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics. 2005;171:1257-1265.

    Not in our library10.1534/genetics.105.042028

82. 82.

    Tsumura Y, Kado T, Takahashi T, et al. Genome scan to detect genetic structure and adaptive genes of natural populations of Cryptomeria japonica. Genetics. 2007;176:2393-2403.

    Not in our library10.1534/genetics.107.072652

83. 83.

    Vasemägi A, Primmer CR. Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Molecular Ecology. 2005;14:3623-3642.

    Not in our library10.1111/j.1365-294x.2005.02690.x

84. 84.

    Vasemägi A, Nilsson J, Primmer CR. Expressed sequence tag-linked microsatellites as a source of gene-associated polymorphisms for detecting signatures of divergent selection in Atlantic Salmon (Salmo salar L.). Molecular Biology and Evolution. 2005;22:1067-1076.

    Not in our library10.1093/molbev/msi093

85. 85.

    Wakamiya I, Newton RJ, Johnston JS, Price HJ. Genome size and environmental factors in the genus Pinus. American Journal of Botany. 1993;80:1235-1241.

    Not in our library

86. 86.

    Wang KS, Liu M, Paterson A. Evaluating outlier loci and their effect on the identification of pedigree errors. BMC Genetics. 2005;6:S155.

    Not in our library10.1186/1471-2156-6-s1-s155

87. 87.

    Weir BC, Cockerham CC. Estimating F-statistics for the analysis of population structure. Evolution. 1984;38:1358-1137.

    Not in our library10.1111/j.1558-5646.1984.tb05657.x

88. 88.

    Williams EJ, Hurst LD. The proteins of linked genes evolve at similar rates. Nature. 2000;407:900-903.

    Not in our library10.1038/35038066

89. 89.

    Wright SI, Gaut BS. Molecular population genetics and the search for adaptive evolution in plants. Molecular Biology and Evolution. 2005;22:506-519.

    Not in our library10.1093/molbev/msi035

90. 90.

    Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF. The effects of artificial selection on the maize genome. Science. 2005;308:1310-1314.

    Not in our library10.1126/science.1107891

91. 91.

    Zayed A, Whitfield CW. A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proceedings of the National Academy of Sciences, USA. 2008;105:3421-3426.

    Not in our library10.1073/pnas.0800107105

92. 92.

    Zhu YL, Song QJ, Hyten DL, et al. Single-nucleotide polymorphisms in soybean. Genetics. 2003;163:1123-1134.

    Not in our library10.1093/genetics/163.3.1123

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