Parallel and lineage-specific molecular adaptation to climate in boreal black spruce

Molecular Ecology

Volumn 21, Issue 17, 2012, Pages 4270-4286

  Prunier, Julien ^a   GÉrardi, Sébastien ^a   Laroche, Jérôme ^a   Beaulieu, Jean ^a,b   Bousquet, Jean ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b NATURAL RESOURCES CANADA   (Canada)

Author keywords

adaptation; gene SNP; genetic lineages; natural selection; phylogeography; Picea mariana

Indexed keywords

PLANT DNA; RAIN;

ACCLIMATIZATION; ARTICLE; CELL NUCLEUS; CLIMATE; DNA SEQUENCE; GENE FREQUENCY; GENETIC VARIABILITY; GENETICS; GENOTYPING TECHNIQUE; MOLECULAR EVOLUTION; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; SPRUCE; TEMPERATURE;

ACCLIMATIZATION; CELL NUCLEUS; CLIMATE; DNA, PLANT; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENETIC VARIATION; GENETICS, POPULATION; GENOTYPING TECHNIQUES; PICEA; POLYMORPHISM, SINGLE NUCLEOTIDE; RAIN; SEQUENCE ANALYSIS, DNA; TEMPERATURE;

PICEA MARIANA;

EID: 84865515150     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05691.x     Document Type: Article

References (99)

1. Abbott RJ, Smith LC, Milne RI, et al. (2000) Molecular analysis of plant migration and refugia in the Arctic. Science, 289, 1343-1346. (Pubitemid 30656049)
2. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD, (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Research, 12, 1805-1814. (Pubitemid 35469929)
3. Anderson LL, Hu FS, DM Nelson, Petit RJ, Paige KN, (2006) Ice-age endurance: DNA evidence of a white spruce refugium in Alaska. Proceedings of the National Academy of Sciences, USA, 103, 12447-12450. (Pubitemid 44267279)
4. Arendt J, Reznick D, (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology & Evolution, 23, 26-32.
5. Aubry KB, Statham MJ, Sacks BN, Perrine JD, Wisely SM, (2009) Phylogeography of the North American red fox: vicariance in Pleistocene forest refugia. Molecular Ecology, 18, 2668-2686.
6. Barrett RD, Hoekstra HE, (2011) Molecular spandrels: tests of adaptation at the genetic level. Nature Genetics, 12, 767-780.
7. Beaulieu J, Perron M, Bousquet J, (2004) Multivariate patterns of adaptive genetic variation and seed source transfer in Picea mariana. Canadian Journal of Forest Research, 34, 531-545. (Pubitemid 38784053)
8. Beaulieu J, Doerksen T, Boyle B, et al. (2011) Association genetics of wood physical traits in the conifer white spruce and relationships with gene expression. Genetics, 188, 197-214.
9. Beaumont MA, Nichols RA, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London B, 263, 1619-1626. (Pubitemid 27055553)
10. Bedon F, Grima-Pettenati J, Mackay J, (2007) Conifer R2R3-MYB transcription factors: sequence analyses and gene expression in wood-forming tissues of white spruce (Picea glauca). BMC Plant Biology, 7, 17.
11. Bedon F, Bomal C, Caron S, et al. (2010) Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented responses. Journal of Experimental Botany, 61, 3847-3864.
12. Bierne N, Welch J, Loire E, Bonhomme F, David P, (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044-2072.
13. Bigras F, Colombo SJ, (2001) Conifer Cold Hardiness. Kluwer Academic Publishers, Dordrecht, The Netherlands.
14. Blödner C, Skroppa T, Johnsen O, Polle A, (2005) Freezing tolerance in two Norway spruce (Picea abies [L.] Karst) progenies is physiologically correlated with drought tolerance. Journal of Plant Physiology, 162, 549-558. (Pubitemid 40588932)
15. Bonin A, Taberlet P, Miaud C, Pompanon F, (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Molecular Biology and Evolution, 23, 773-783.
16. Bouillé M, Bousquet J, (2005) Trans-species shared polymorphisms at orthologous nuclear gene loci among distant species in the conifer Picea (Pinaceae): implications for the long-term maintenance of genetic diversity in trees. American Journal of Botany, 92, 63-73. (Pubitemid 40113108)
17. Bousquet J, Isabel N, Pelgas B, Cottrell J, Rungis D, Ritland K, (2007) Spruce. In: Genome Mapping and Molecular Breeding in Plants (ed., Kole C,), pp. 93-114. Springer-Verlag, Berlin, Germany.
18. Campbell D, Bernatchez L, (2004) Genomic scan using AFLP markers as a mean to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Molecular Biology and Evolution, 21, 945-956. (Pubitemid 38529736)
19. Cockerham CC, Weir BS, (1993) Estimation of gene flow from F-statistics. Evolution, 47, 855-863.
20. Condit R, Hubbell SP, Foster RB, (1995) Mortality-rates of 205 neotropical tree and shrub species and the impact of a severe drought. Ecological Monographs, 65, 419-439. (Pubitemid 3004411)
21. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411-1423.
22. Corander J, Sirén J, Arjas E, (2008) Bayesian spatial modeling of genetic population structure. Computational Statistics, 23, 111-129.
23. Davis MB, Shaw RG, (2001) Range shifts and adaptive responses to Quaternary climate change. Science, 292, 673-679. (Pubitemid 32385531)
24. De Carvalho D, Ingvarsson PK, Joseph J, et al. (2010) Admixture facilitates adaptation from standing variation in the European aspen (Populus tremula L.), a widespread forest tree. Molecular Ecology, 19, 1638-1650.
25. De Young BJ, Bickle KL, Muskett P, Patel K, Clark SE, (2006) The CLAVATA1-related BAM1,BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. The Plant Journal, 45, 1-16. (Pubitemid 43373728)
26. Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK, (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proceedings of the National Academy of Sciences, USA, 103, 8281-8286. (Pubitemid 43801089)
27. Eckert AJ, Bower AD, Wegrzyn JL, et al. (2009) Association genetics of coastal Douglas-fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics, 182, 1289-1302.
28. El Kayal W, Allen CCG, Ju CJ-T, et al. (2011) Molecular events of apical bud formation in white spruce, Picea glauca. Plant, Cell & Environment, 34, 480-500.
29. Elmer KR, Meyer A, (2011) Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends in Ecology & Evolution, 26, 298-306.
30. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620. (Pubitemid 40886055)
31. Eveno E, Collada C, Guevara MA, et al. (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Molecular Biology and Evolution, 25, 417-437. (Pubitemid 351231615)
32. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity, 103, 285-298.
33. Farrar JL, (1995) Trees in Canada. Fitzhenry and Whitesite Ltd, Markham, Ontario, Canada.
34. Ffrench-Constant RH, Anthony N, Aronstein K, Rocheleau T, Stilwell G, (2000) Cyclodiene insecticide resistance: from molecular to population genetics. Annual Review of Entomology, 45, 449-466. (Pubitemid 30187869)
35. Gamache I, Jaramillo-Correa JP, Payette S, Bousquet J, (2003) Diverging patterns of mitochondrial and nuclear DNA diversity in subartic black spruce: imprint of a founder effect associated with postglacial colonization. Molecular Ecology, 12, 891-901. (Pubitemid 36524284)
36. Gasteiger E, Gattiker A, Hoogland C, et al. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research, 31, 3784-3788. (Pubitemid 37442246)
37. Gérardi S, Jaramillo-Correa JP, Beaulieu J, Bousquet J, (2010) From glacial refugia to modern populations: new assemblages of organelle genomes generated by differential cytoplasmic gene flow in transcontinental black spruce. Molecular Ecology, 19, 5265-5280.
38. Grivet D, Sebastiani F, Alia R, et al. (2011) Molecular footprints of local adaptation in two mediterranean conifers. Molecular Biology and Evolution, 28, 101-116.
39. Guillet-Claude C, Isabel N, Pelgas B, Bousquet J, (2004) The evolutionary implications of knox-I gene duplications in conifers: correlated evidence from phylogeny, gene mapping, and analysis of functional divergence. Molecular Biology and Evolution, 21, 2232-2245. (Pubitemid 39488894)
40. Hancock AM, Witonsky DB, Gordon AS, et al. (2008) Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genetics, 4, e32.
41. Hancock AM, Witonsky DB, Ehler E, et al. (2010) Human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proceedings of the National Academy of Sciences, USA, 107, 8924-8930.
42. Hancock AM, Brachi B, Faure N, et al. (2011) Adaptation to climate across the Arabidopsis thaliana genome. Science, 334, 83-86.
43. Hewitt GM, (1999) Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68, 87-112. (Pubitemid 29485515)
44. Hoekstra HE, Nachman MW, (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Molecular Ecology, 12, 1185-1194. (Pubitemid 36573120)
45. Holliday JA, Ritland K, Aitken SN, (2010) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytologist, 188, 501-514.
46. Howe GT, Aitken SN, Neale DB, et al. (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Canadian Journal of Botany, 81, 1247-1266. (Pubitemid 38390482)
47. Ingram J, Bartels D, (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 377-403.
48. Isabel N, Beaulieu J, Bousquet J, (1995) Complete congruence between gene diversity estimates derived from genotypic data at enzyme and random amplified polymorphic DNA loci in black spruce. Proceedings of the National Academy of Sciences, USA, 92, 6369-6373.
49. Jaramillo-Correa JP, Bousquet J, (2003) New evidence from mitochondrial DNA of a progenitor-derivative species relationship between black spruce and red spruce (Pinaceae). American Journal of Botany, 90, 1801-1806. (Pubitemid 38092690)
50. Jaramillo-Correa JP, Beaulieu J, Bousquet J, (2004) Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Molecular Ecology, 13, 2735-2747. (Pubitemid 39151630)
51. Jaramillo-Correa JP, Beaulieu J, Khasa DP, Bousquet J, (2009) Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Canadian Journal of Forest Research, 39, 286-307.
52. Joost S, Bonin A, Bruford MW, et al. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969. (Pubitemid 47397327)
53. Joost S, Kalbermatten M, Bonin A, (2008) Spatial analysis method (SAM): a software tool combining molecular and environmental data to identify candidate loci for selection. Molecular Ecology Resources, 8, 957-960.
54. Jump AS, Hunt JM, Penuelas J, (2006) Rapid climate change-related growth decline at the southern range edge of Fagus sylvatica. Global Change Biology, 12, 2163-2174. (Pubitemid 44560726)
55. Jump AS, Penuelas J, Rico L, et al. (2008) Simulated climate change provokes rapid genetic change in the Mediterranean shrub Fumana thymifolia. Global Change Biology, 14, 637-643. (Pubitemid 351228533)
56. Kalinowski ST, (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Molecular Ecology Notes, 5, 187-189. (Pubitemid 40350919)
57. Kimchi-Sarfaty C, Oh JM, Kim I-W, et al. (2007) A 'silent' polymorphism in the MDR1 gene changes substrate specificity. Science, 315, 525-528. (Pubitemid 46175758)
58. Ladd AN, Cooper TA, (2002) Finding signals that regulate alternative splicing in the post genomic era. Genome Biology 3, reviews0008.I-008.I6.
59. Laval G, Excoffier L, (2004) SIMCOAL 2.0: a program to simulate genomic diversity over large recombining regions in a subdivided population with a complex history. Bioinformatics, 20, 2485-2487. (Pubitemid 39429927)
60. Legendre P, Legendre L, (1998) Numerical Ecology, 2nd edn. Elsevier, Amsterdam and New York.
61. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P, (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics, 4, 981-994. (Pubitemid 37474645)
62. Lynch M, Force A, (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics, 154, 459-473. (Pubitemid 30045935)
63. McKenney JL, Cripps MG, Price WJ, Hinz HL, Schwarzlander M, (2007) No difference in competitive ability between invasive North American and native European Lepidium draba populations. Plant Ecology, 193, 293-303. (Pubitemid 47624469)
64. Mechta-Grigoriou F, Gerald D, Yaniv M, (2001) The mammalian Jun proteins: redundancy and specificity. Oncogene, 20, 2378-2389. (Pubitemid 32531296)
65. Moellering ER, Muthan B, Benning C, (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science, 330, 226-228.
66. Murray BG, (1998) Nuclear DNA amounts in gymnosperms. Annals of Botany, 82, 3-15. (Pubitemid 29014736)
67. Namroud M-C, Beaulieu J, Juge N, Laroche J, Bousquet J, (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology, 17, 3599-3613.
68. Namroud M-C, Guillet-Claude C, Mackay J, Isabel N, Bousquet J, (2010) Molecular evolution of regulatory genes in spruces from different species and continents: heterogeneous patterns of linkage disequilibrium and selection but correlated recent demographic changes. Journal of Molecular Evolution, 70, 371-386.
69. Namroud M-C, Bousquet J, Doerksen T, Beaulieu J, (2012) Scanning SNPs from large set of expressed genes to assess the impact of artificial selection on the undomesticated genetic diversity of white spruce. Evolutionary Applications, doi:10.1111/j.1752-4571.2012.00242.x.
70. Nielsen R, (2005) Molecular signatures of natural selection. Annual Review of Genetics, 39, 197-218. (Pubitemid 43011113)
71. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375-402.
72. Novembre J, Di Rienzo A, (2009) Spatial patterns of variation due to natural selection in humans. Nature Reviews Genetics, 10, 745-755.
73. Pavy N, Pelgas B, Beauseigle S, et al. (2008) 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, 9, 21.
74. Pavy N, Namroud M-C, Gagnon F, Isabel N, Bousquet J, (2012) The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers. Heredity, 108, 273-284.
75. Pelgas B, Isabel N, Bousquet J, (2004) Efficient screening for expressed sequence tag polymorphisms (ESTPs) by DNA pool sequencing and denaturing gradient gel electrophoresis (DGGE) in spruces. Molecular Breeding, 13, 263-279. (Pubitemid 39001302)
76. Pelgas B, Bousquet J, Meirmans PG, Ritland K, Isabel N, (2011) QTL mapping in white spruce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genomics, 12, 145.
77. Perron M, Bousquet J, (1997) Natural hybridization between black spruce and red spruce. Molecular Ecology, 6, 725-734. (Pubitemid 27324718)
78. Perry DJ, Bousquet J, (2001) 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, 31, 32-40. (Pubitemid 32185337)
79. Petit RJ, Excoffier L, (2009) Gene flow and species delimitation. Trends in Ecology & Evolution, 24, 386-393.
80. Petit RJ, Duminil J, Fineschi S, et al. (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology, 14, 689-701. (Pubitemid 40346461)
81. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959. (Pubitemid 30397141)
82. Prunier J, Laroche J, Beaulieu J, Bousquet J, (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Molecular Ecology, 20, 1702-1716.
83. Régnière J, (1996) Generalized approach to landscape-wide seasonal forecasting with temperature-driven simulation models. Environmental Entomology, 25, 869-881.
84. Renaut S, Nolte AW, Bernatchez L, (2010) Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae). Molecular Ecology, 19, 115-131.
85. Richter-Boix A, Quintela M, Segelbacher G, Laurila A, (2011) Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis. Molecular Ecology, 20, 1582-1600.
86. Rigault P, Boyle B, Lepage P, et al. (2011) A white spruce gene catalog for conifer genome analyses. Plant Physiology, 157, 14-28.
87. Root TL, Price JT, Hall KR, et al. (2003) Fingerprints of global warming on wild animals and plants. Nature, 421, 57-60. (Pubitemid 36077083)
88. Shafer ABA, Cullingham CI, Cote SD, Coltman DW, (2010) Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Molecular Ecology, 19, 4589-4621.
89. Storey JM, Storey KB, (2004) Cold hardiness and freeze tolerance. In: Functional Metabolism: Regulation and Adaptation (ed., Strorey KB,), pp. 473-503. John Wiley and Sons, Hoboken, New Jersey.
90. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences, USA, 100, 9440-9445. (Pubitemid 37033947)
91. Storz JF, (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology, 14, 671-688. (Pubitemid 40346460)
92. Sullivan JA, Deng XW, (2003) From seed to seed: the role of photoreceptors in Arabidopsis development. Developmental Biology, 260, 289-297. (Pubitemid 36960079)
93. Sun WN, Van Montagu M, Verbruggen N, (2002) Small heat shock proteins and stress tolerance in plants. Biochimica Et Biophysica Acta, 1577, 1-9. (Pubitemid 34876598)
94. Thornton KR, Jensen JD, Becquet C, Andolfatto P, (2007) Progress and prospects in mapping recent selection in the genome. Heredity, 98, 340-348. (Pubitemid 46801773)
95. Vasemägi A, Primmer CR, (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Molecular Ecology, 14, 3623-3642.
96. Viereck LA, Johnston WF, (1990) Picea mariana (Mill.) B.S.P. Black spruce. In: Silvics of North America: 1. Conifers (ed., Burns RM, &, Honkala BH,), pp. 227-237. United States Department of Agriculture (USDA), Forest Service, Agriculture Handbook 654, Washington DC, USA.
97. Wright SI, Gaut BS, (2005) Molecular population genetics and the search for adaptive evolution in plants. Molecular Biology and Evolution, 22, 506-519. (Pubitemid 40299500)
98. Wright S, (1951) The genetic structure of populations. Annual Eugenics, 15, 323-354.
99. Yamaguchi-Shinozaki K, Shinozaki K, (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology, 57, 781-803. (Pubitemid 44061045)