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

Volumn 70, Issue 4, 2010, Pages 371-386

  Namroud, Marie Claire ^a   Guillet Claude, Carine ^a   MacKay, John ^a   Isabel, Nathalie ^a,b   Bousquet, Jean ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAURENTIAN FORESTRY CENTRE   (Canada)

Author keywords

Bottleneck; HD Zip III; knox I; Linkage disequilibrium; Picea; Population expansion; Selection signatures

Indexed keywords

HOMEODOMAIN PROTEIN; KNOX1 PROTEIN, PLANT; NUCLEOTIDE; VEGETABLE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BIOLOGY; DNA SEQUENCE; GENE LINKAGE DISEQUILIBRIUM; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; HAPLOTYPE; INDEL MUTATION; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENE; PLANT SEED; SPECIES DIFFERENCE; SPRUCE;

AMINO ACID SUBSTITUTION; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENES, PLANT; HAPLOTYPES; HOMEODOMAIN PROTEINS; INDEL MUTATION; LINKAGE DISEQUILIBRIUM; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; PICEA; PLANT PROTEINS; POLYMORPHISM, GENETIC; SEEDS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

PICEA;

EID: 77954460187     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-010-9335-1     Document Type: Article

References (93)

1. Acheré V, Favre JM, Besnard G, Jeandroz S (2005) Genomic organisation of molecular differentiation in Norway spruce (Picea abies). Mol Ecol 14:3191-3201
2. Anderson PM, Lozhkin VA (2001) The Stage 3 interstadial complex (Karginskii/middle Wisconsinan interval) of Beringia: variations in paleoenvironments and implications for paleoclimatic interpretations. Quat Sci Rev 20:93-125
3. Anderson LL, Hu FS, Nelson DM, Petit RJ, Paige KN (2006) Ice-age endurance: DNA evidence of a white spruce refugium in Alaska. Proc Natl Acad Sci USA 103:12447-12450
4. Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G (2001) The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126:643-655
5. Barrier M, Bustamante CD, Yu J, Purugganan MD (2003) Selection on rapidly evolving proteins in the Arabidopsis genome. Genetics 163:723-733
6. Beaulieu J (1996) Breeding program and strategy for white spruce in Québec Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Québec, QC, Canada, Information Report LAU-X-117E
7. Beaulieu J, Corriveau A, Daoust G (1989) Phenotypic stability and delineation of black spruce breeding zones in Québec. Canadian Forestry Service, Laurentian Forest Research Centre, Québec, Canada, Information Report LAU-X-85E
8. 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 Biol 7:17
9. 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. Am J Bot 92:63-73
10. Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci USA 101:15255-15260
11. BrubakerLB,AndersonPM,Edwards ME, LozhkinAV(2005)Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. J Biogeogr 32:833-848
12. Charlesworth J, Eyre-Walker A (2008) The McDonald-Kreitman test and slightly deleterious mutations. Mol Biol Evol 25:1007-1101
13. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303
14. Charlesworth B, Charlesworth D, Barton NH (2003) The effects of genetic and geographic structure on neutral variation. Annu Rev Ecol Syst 34:99-125
15. Chen J, Källman Gyllenstrand N, Lascoux M (2010) New insights on the speciation history and nucleotide diversity of three boreal spruce species and a tertiary relict. Heredity 104:3-14
16. Collignon A-M, Van de Sype H, Favre J-M (2002) Geographical variation in random amplified polymorphic DNA and quantitative traits in Norway spruce. Can J For Res 32:266-282
17. Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19-31
18. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinf 9:539
19. Corriveau A, Beaulieu J, Daoust G (1988) Phenotypic stability and productivity of central European Norway spruce provenances in Québec, Canada. Proceedings meeting of the IUFRO working party S-202-211, Tjörnarp, Sweden
20. Davis M, Shaw R (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673-679
21. Depaulis F, Veuille M (1998) Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol 15:1788-1790
22. Depaulis F, Mousset S, Veuille M (2001) Haplotype tests using coalescent simulations conditional on the number of segregating sites. Mol Biol Evol 18:1136-1138
23. Depaulis F, Mousset S, Veuille M (2005) Detecting selective sweeps with haplotype tests. In: Nurminsky D (ed) Hitchhiking and haplotype tests. Springer, New York, pp 34-54
24. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker N, Izhaki A, Baum S, Bowman J (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768-1774
25. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413
26. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925
27. Gamache I, Jaramillo-Correa JP, Payette S, Bousquet J (2003) Diverging patterns of mitochondrial and nuclear DNA diversity in subarctic black spruce: imprint of a founder effect associated with postglacial colonization. Mol Ecol 12:891-901
28. Garcia-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195-1206
29. Goncharenko GG, Zadeika IV, Birgelis JJ (1994) Genetic structure diversity and differentiation of Norway spruce (Picea abies (L.) Karst) in natural populations of Latvia. Forest Ecol Manag 72:31-38
30. González-Mart́inez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006) DNA sequence variation and selection of tag single-nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1-12
31. Green KA, Prigge MJ, Katzman RB, Clark SE (2005) CORONA, a member of the Class III Homeodomain Leucine Zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell 17:691-704
32. 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. Mol Biol Evol 21:2232-2245
33. Haddrill PR, Thornton KR, Charlesworth B, Andolfatto P (2005) Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations. Genome Res 15:790-799
34. Hake S, Smith HM, Holtan H, Magnani E, Mele G, Ramirez J (2004) The role of knox genes in plant development. Annu Rev Cell Dev Bi 20:125-151
35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
36. Heuertz M, De Paoli E, Källman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway Spruce [Picea abies (L) Karst]. Genetics 174:2095-2105
37. Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226-231
38. Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibrium in finite populations. Theor Popul Biol 33:54-78
39. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805-1817
40. Hudson RR (2002) Generating samples under a Wright-Fisher neutral of genetic variation. Bioinformatics 18:337-338
41. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164
42. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159
43. 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. Proc Natl Acad Sci USA 92:6369-6373
44. Ito M, Sato Y, Matsuoka M (2002) Involvement of homeobox genes in early body plan of monocot. Int Rev Cytol 218:1-35
45. Jaramillo-Correa JP, Beaulieu J, Bousquet J (2001) Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Mol Ecol 10:2729-2740
46. 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. Mol Ecol 13:2735-2747
47. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111-120
48. Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness and wood quality-related candidate genes in Douglas fir. Genetics 171:2029-2041
49. Lagercrantz U, Ryman N (1990) Genetic structure of Norway spruce (Picea abies): concordance of morphological and allozymic variation. Evolution 44:38-53
50. Latalowa M, van der Knaap WO (2006) Late Quaternary expansion of Norway spruce Picea abies (L) Karst in Europe according to pollen data. Quat Sci Rev 25:2780-2805
51. Lindbladh M, Jacobson GL, Schauffler M (2003) The postglacial history of three Picea species in New England, USA. Quat Res 59:61-69
52. Lindbladh M, Oswald WW, Foster DR, Faison EK, Hou J, Huang Y (2007) A late-glacial transition from Picea glauca to Picea mariana in southern New England. Quat Res 3:502-508
53. Luikart G, England PR, Tallmon D, Jordan S, Tabarlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981-994
54. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654
55. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231-1241
56. Messaoud Y, Bergeron Y, Asselin H (2007) Reproductive potential of balsam fir (Abies balsamea), white spruce (Picea glauca), and black spruce (P. mariana) at the ecotone between mixedwood and coniferous forests in the boreal zone of western Quebec. Am J Bot 94:746-754
57. Murray BG (1998) Nuclear DNA amounts in gymnosperms. Ann Bot 82:3-15
58. Namroud MC, 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. Mol Ecol 17:3599-3613
59. Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325-330
60. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197-218
61. Palmé AE, Wright M, Savolainen O (2008) Patterns of divergence among conifer ESTs and polymorphism in Pinus sylvestris identify putative selective sweeps. Mol Biol Evol 25:2567-2577
62. Pavy N, Pelgas B, Beauseigle S, Blais S, Gagnon F, Gosselin I, Lamothe M, Isabel N, Bousquet J (2008) Enhancing genetic mapping of complex genomes through the design of highly-multiplexed SNP arrays: application to the large and unse-quenced genomes of white spruce and black spruce. BMC Genomics 9:21
63. 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. Can J For Res 31:32-40
64. Pisaric M, Holt C, Szeicz JM, Karst T, Smol JP (2003) Holocene treeline dynamics in the mountains of northeastern British Columbia, Canada, inferred from fossil pollen and stomata. Holocene 13:161-173
65. Pot D, McMillan L, Echt C, Le Provost G, Garnier-Géré P, Cato S, Plomion C (2005) Nucleotide variation in genes involved in wood formation in two pine species. New Phytol 167:101-112
66. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III Homeodomain-Leucine Zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:61-76
67. Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160:1179-1189
68. Pyhäjärvi T, Garcia-Gil MR, Knutt T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177:1713-1724
69. Rafalski A, Morgante M (2004) Corn and humans: recombination and linkage disequilibrium in two genomes of similar size. Trends Genet 20:103-111
70. Ran J-H, Wei X-X, Wang X-Q (2006) Molecular phylogeny and biogeography of Picea (Pinaceae): Implications for phylogeo-graphical studies using cytoplasmic haplotypes. Mol Phylogenet Evol 41:405-419
71. Ravazzi C (2002) Late Quaternary history of spruce in southern Europe. Rev Palaeobot Palyno 120:131-177
72. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497
73. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425
74. Sakuma S, Pourkheirandish M, Matsumoto T, Koba T, Komatsuda T (2009) Duplication of a well-conserved homeodomain-leucine zipper transcription factor gene in barley generates a copy with more specific functions. Funct Integr Genomics. doi: 10.1007/s10142-009-0134-y
75. Sato Y, Fukuda Y, Hirano HY (2001) Mutations that cause amino acid substitutions at the invariant positions in homeodomain of OSH3 KNOX protein suggest artificial selection during rice domestication. Genes Genet Syst 76:381-392
76. Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8,-9 and-14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609-622
77. Siljak-Yakovlev S, Cerbah M, Coulaud J, Stoian V, Brown SC, Zoldos V, Jelenic S, Papes D (2002) Nuclear DNA content, base composition, heterochromatin and rDNA in Picea omorika and Picea abies. Theor Appl Genet 104:505-512
78. Sokal RR, RohlfFJ(1995) Biometry, 3rd edn.WHFreeman, New York
79. Stinchcombe JR, Hoekstra HE (2008) Combining population genom-ics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158-170
80. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671-688
81. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460
82. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595
83. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599
84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882
85. Van de Peer Y, Taylor JS, Braasch I, Meyer A (2001) The ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes. J Mol Evol 53:436-446
86. Vollbrecht E, Veit B, Sinha N, Hake S (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350:241-243
87. Wakamiya I, Newton R, Johnston JS, Price HJ (1993) Genome size and environmental factors in the genus Pinus. Am J Bot 80:1235-1241
88. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256-276
89. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506-519
90. Wu J, Saupe SJ, Glass NL (1998) Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci USA 95:12398-12403
91. Yang Z, Bielawski JP (2000) Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15:496-503
92. Zhong R, Ye ZH (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11:2139-2152
93. Zhong R, Ye ZH (2004) Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45:369-385