Tree Genetics & Genomes

, 5:117

Search for nucleotide diversity patterns of local adaptation in dehydrins and other cold-related candidate genes in Scots pine (Pinus sylvestris L.)

  • Witold Wachowiak
  • Peter A. Balk
  • Outi Savolainen
Original Paper

Abstract

Nucleotide variation at several cold candidate genes including seven members of the dehydrin gene family was surveyed in haplotypes of Scots pine (Pinus sylvestris) sampled in populations showing divergence for cold tolerance in Europe. Patterns of nucleotide diversity, linkage disequilibrium, and frequency spectrum of alleles were compared between north and south populations to search for signs of directional selection potentially underlying adaptation to cold. Significant differentiation between populations in allelic frequency or haplotype structure was detected at dhn1, dhn3, and abaH loci. Allelic dimorphism with no evidence of haplotype clustering by geographical distribution was found at dhn9. An excess of fixed non-synonymous mutations as compared to the outgroup P. pinaster pine species was found at dhn1. Differences in nucleotide polymorphisms were found between the members of the Kn class of dehydrin upregulated during cold acclimation (average πsil = 0.004) as compared to the SKn class (average πsil = 0.024). The multilocus nucleotide diversity at silent sites (θW = 0.009) was moderate compared to other conifer species, but higher than previous estimates for Scots pine. There was an excess of rare and high frequency derived variants as revealed by significantly negative multilocus value of Tajima’s D (D = −0.72, P < 0.01) and negative mean value of Fay and Wu H statistics (H = −0.50). The level of linkage disequilibrium decayed rapidly with an average expected r2 of 0.2 at about 200 bp. Overall, there was a positive correlation between polymorphism and divergence at ten loci when outgroup sequence was available. The discovered polymorphism will be used for further evaluation of the adaptive role of genes through association mapping studies.

Keywords

Plant adaptation Cold tolerance Gene families Nucleotide diversity Linkage disequilibrium SNPs Pinus sylvestris 

Supplementary material

11295_2008_188_MOESM1_ESM.doc (90 kb)
Table S1Summary statistics of nucleotide and haplotype variation, neutrality tests, and recombination rate estimates at cold-related genes in the north and south groups of Scots pine (DOC 89.5 KB).
11295_2008_188_MOESM2_ESM.doc (26 kb)
Table S2Nucleotide variation measured as θW (Watterson 1975) in a total dataset and in P. sylvestris samples divided into four geographical regions. θW = median for silent sites (synonymous and non-coding), CI = credibility intervals (97.5%) (DOC 26.5 KB).
11295_2008_188_MOESM3_ESM.doc (32 kb)
Table S3FST values and heterozygosity estimates at cold candidate loci used for outliers detection using Beaumont and Nichols (1996) approach (DOC 32.0 KB).
11295_2008_188_MOESM4_ESM.doc (40 kb)
Fig. S1Posterior densities of multilocus estimates of nucleotide diversity θw (Watterson 1975) based on silent sites (synonymous and non-coding) for all loci analyzed for P. sylvestris samples from four geographical regions in Europe (see text for details). 95% credibility intervals are given in Supplementary Table S2 (DOC 39.5 KB).
11295_2008_188_MOESM5_ESM.doc (97 kb)
Fig. S2a, b Scatter plot of the squared correlation of allele frequencies (r2) as a function of distance in base pairs between pairs of polymorphic sites in north and south groups for dhn1 locus (a) and five loci combined (excluding dhn1) (b). Decline in linkage disequilibrium is shown by non-linear fitting curve of the mutation-recombination-drift model (see “Material and methods” section for details). Recombination rate parameter c (standard error in parentheses) for dhn1 in north group is c = 0.005 (0.001) and in the south group is c = 0.010 (0.001). Recombination rate parameter c for the remaining loci in north group is c = 0.0036 (0.0005) and in south group is c = 0.0029 (standard error 0.0005) (DOC 97.0 KB).
11295_2008_188_MOESM6_ESM.doc (50 kb)
Fig. S3Distribution of FST values estimated from 14 cold candidate genes in Scots pine plotted against heterozygosity (see Supplementary Table S3). The quantiles plotted are estimated using Beaumont and Nichols (1996) approach and the infinite allele model with expected mean FST = 0.014. The outlier indicates abaH locus (DOC 50.0 KB).
11295_2008_188_MOESM7_ESM.doc (34 kb)
Fig. S4Distribution of FST values estimated from 99 SNPs and Indels of MAF >10% in Scots pine plotted against total diversity (π). The quantiles plotted are estimated using Beaumont and Nichols (1996) approach and the infinite allele model with expected mean FST = 0.012. The outliers include polymorphic sites in dhn1, dhn9, abaH locus (see “Results” section) (DOC 34.0 KB).

References

  1. Aho ML (1994) Autumn frost hardening of one-year-old Pinus sylvestris (L) seedlings—effect of origin and parent trees. Scand J For Res 9:17–24CrossRefGoogle Scholar
  2. Ahuja MR, Neale DB (2005) Evolution of genome size in conifers. Silvae Genet 54:126–137Google Scholar
  3. Barton NH (1999) Clines in polygenic traits. Genet Res 74:223–236PubMedCrossRefGoogle Scholar
  4. Beaumont MA (2005) Adaptation and speciation: what can F ST tell us. Trends Ecol Evol 20:435–440PubMedCrossRefGoogle Scholar
  5. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond B 263:1619–1626CrossRefGoogle Scholar
  6. Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13:969–980PubMedCrossRefGoogle Scholar
  7. Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446PubMedCrossRefGoogle Scholar
  8. Bouille 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 92:63–73CrossRefGoogle Scholar
  9. Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci U S A 101:15255–15260PubMedCrossRefGoogle Scholar
  10. Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. Plos Genetics 2:379–384CrossRefGoogle Scholar
  11. Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet Res 70:155–174PubMedCrossRefGoogle Scholar
  12. Cheddadi R, Vendramin GG, Litt T, Francois L, Kageyama M, Lorentz S, Laurent JM, de Beaulieu JL, Sadori L, Jost A, Lunt D (2006) Imprints of glacial refugia in the modern genetic diversity of Pinus sylvestris. Global Ecol Biogeogr 15:271–282Google Scholar
  13. Choi DW, Zhu B, Close TJ (1999) The barley (Hordeum vulgare L.) dehydrin multigene family: sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv Dicktoo. Theor Appl Genet 98:1234–1247CrossRefGoogle Scholar
  14. Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plantarum 100:291–296CrossRefGoogle Scholar
  15. Cockerham CC, Weir BS (1993) Estimation of gene flow from F-statistics. Evolution 47:855–863CrossRefGoogle Scholar
  16. Critchfield WB, Little ELJ (1966) Geographic distribution of the pines of the World. Miscellaneous Publication 991 edn. USDA Forest Service, pp 97Google Scholar
  17. Day IS, Reddy VS, Ali GS, Reddy ASN (2002) Analysis of EF-hand-containing proteins in Arabidopsis. Genome Biol 3:research0056.1–research0056.24CrossRefGoogle Scholar
  18. Dvornyk V, Sirvio A, Mikkonen M, Savolainen O (2002) Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol Biol Evol 19:179–188PubMedGoogle Scholar
  19. Eriksson G, Andersson S, Eiche V, Ifver J, Persson A (1980) Severity index and transfer effects on survival and volume production of Pinus sylvestris in Northern Sweden. Stud For Suec 156:1–36Google Scholar
  20. Eveno E, Collada C, Guevara MA, Léger V, Soto A, Díaz L, Léger P, González-Martínez SC, Cervera MT, Plomion C, Garnier-Géré PH (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25(2):417–437PubMedCrossRefGoogle Scholar
  21. Eyre-Walker A, Keightley PD, Smith NG, Gaffney D (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19(12):2142–2149PubMedGoogle Scholar
  22. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413PubMedGoogle Scholar
  23. Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45PubMedGoogle Scholar
  24. García-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol Ecol 12:1195–1206PubMedCrossRefGoogle Scholar
  25. Gaut BS, Wright SI, Rizzon C, Dvorak J, Anderson LK (2007) Opinion—Recombination: an underappreciated factor in the evolution of plant genomes. Nat Rev, Genet 8:77–84CrossRefGoogle Scholar
  26. González-Martínez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006a) DNA sequence variation and selection of tag single-nucleotide polymorphisms at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1915–1926PubMedCrossRefGoogle Scholar
  27. González-Martínez SC, Krutovsky KV, Neale DB (2006b) Forest-tree population genomics and adaptive evolution. New Phytol 170:227–238PubMedCrossRefGoogle Scholar
  28. González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB (2007) Association genetics in Pinus taeda L. I. Wood property traits. Genetics 175:399–409PubMedCrossRefGoogle Scholar
  29. Hall D, Luquez V, Garcia VM, Onge KR, Jansson S, Ingvarsson PK (2007) Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61-12:2849–2860CrossRefGoogle Scholar
  30. Hedrick PW (2007) Balancing selection. Curr Biol 17:R230–R231PubMedCrossRefGoogle Scholar
  31. Heuertz M, De Paoli E, Kallman 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 174:2095–2105PubMedCrossRefGoogle Scholar
  32. Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231CrossRefGoogle Scholar
  33. Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78PubMedCrossRefGoogle Scholar
  34. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438PubMedCrossRefGoogle Scholar
  35. Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unravelling the complexities of cold adaptation in forest trees. Can J Bot—Revue Canadienne De Botanique 81:1247–1266CrossRefGoogle Scholar
  36. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014PubMedGoogle Scholar
  37. Hudson RR (2001) Two-locus sampling distributions and their application. Genetics 159:1805–1817PubMedGoogle Scholar
  38. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159PubMedGoogle Scholar
  39. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151PubMedGoogle Scholar
  40. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335:167–170PubMedCrossRefGoogle Scholar
  41. Huntley B, Birks HJB (1983) An atlas of past and present pollen map in Europe: 0–13000 years ago. Cambridge University Press, CambridgeGoogle Scholar
  42. Hurme P, Repo T, Savolainen O, Paakkonen T (1997) Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Can J Forest Res—Revue Canadienne De Recherche Forestiere 27:716–723CrossRefGoogle Scholar
  43. Hurme P, Sillanpaa MJ, Arjas E, Repo T, Savolainen O (2000) Genetic basis of climatic adaptation in Scots pine by Bayesian quantitative trait locus analysis. Genetics 156:1309–1322PubMedGoogle Scholar
  44. Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953PubMedCrossRefGoogle Scholar
  45. Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci U S A 96:13566–13570PubMedCrossRefGoogle Scholar
  46. Järvinen P, Lemmetyinen J, Savolainen O, Sopanen T (2003) DNA sequence variation in BpMADS2 gene in two populations of Betula pendula. Mol Ecol 12:369–384PubMedCrossRefGoogle Scholar
  47. Jermstad KD, Bassoni DL, Wheeler NC, Anekonda TS, Aitken SN, Adams WT, Neale DB (2001) Mapping of quantitative trait loci controlling adaptive traits in coastal Douglas-fir. II. Spring and fall cold-hardiness. Theor Appl Genet 102:1152–1158CrossRefGoogle Scholar
  48. Joosen RVL, Lammers M, Balk PA, Bronnum P, Konings MCJM, Perks M, Stattin E, Van Wordragen MF, van der Geest AHM (2006) Correlating gene expression to physiological parameters and environmental conditions during cold acclimation of Pinus sylvestris, identification of molecular markers using cDNA microarrays. Tree Physiol 26:1297–1313PubMedGoogle Scholar
  49. Kado T, Yoshimaru H, Tsumura Y, Tachida H (2003) DNA variation in a conifer, Cryptomeria japonica (Cupressaceae sensu lato). Genetics 164:1547–1559PubMedGoogle Scholar
  50. Kalberer SR, Wisniewski M, Arora R (2006) Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Science 171:3–16CrossRefGoogle Scholar
  51. Karhu A, Hurme P, Karjalainen M, Karvonen P, Karkkainen K, Neale D, Savolainen O (1996) Do molecular markers reflect patterns of differentiation in adaptive traits of conifers. Theor Appl Genet 93:215–221CrossRefGoogle Scholar
  52. Koag MC, Fenton RD, Wilkens S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol 131:309–316PubMedCrossRefGoogle Scholar
  53. Koelewijn HP, Koski V, Savolainen O (1999) Magnitude and timing of inbreeding depression in Scots pine (Pinus sylvestris L.). Evolution 53:758–768CrossRefGoogle Scholar
  54. Kontunen-Soppela S, Taulavuori K, Taulavuori E, Lahdesmaki P, Laine K (2000) Soluble proteins and dehydrins in nitrogen-fertilized Scots pine seedlings during deacclimation and the onset of growth. Physiol Plantarum 109:404–409CrossRefGoogle Scholar
  55. Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041PubMedCrossRefGoogle Scholar
  56. Latta RG (1998) Differentiation of allelic frequencies at quantitative trait loci affecting locally adaptive traits. Am Nat 151:283–292PubMedCrossRefGoogle Scholar
  57. Latta RG (2004) Gene flow, adaptive population divergence and comparative population structure across loci. New Phytol 161:51–58CrossRefGoogle Scholar
  58. Le Corre V, Kremer A (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics 164:1205–1219PubMedGoogle Scholar
  59. Lerceteau E, Szmidt AE, Andersson B (2001) Detection of quantitative trait loci in Pinus sylvestris L. across years. Euphytica 121:117–122CrossRefGoogle Scholar
  60. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394PubMedGoogle Scholar
  61. Ma XF, Szmidt AE, Wang XR (2006) Genetic structure and evolutionary history of a diploid hybrid pine Pinus densata inferred from the nucleotide variation at seven gene loci. Mol Biol Evol 23:807–816PubMedCrossRefGoogle Scholar
  62. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654PubMedCrossRefGoogle Scholar
  63. McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291CrossRefGoogle Scholar
  64. McVean G, Awadalla P, Fearnhead P (2002) A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160:1231–1241PubMedGoogle Scholar
  65. Morgenstern EK (1996) In: Morgenstern EK (ed) Geographic variation in forest trees: genetic basis and application of knowledge in silviculture. UBC, Washington, p 214Google Scholar
  66. Mouillon JM, Gustafsson P, Harryson P (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol 141:638–650PubMedCrossRefGoogle Scholar
  67. Muona O, Harju A (1989) Effective population sizes, genetic variability, and mating system in natural stands and seed orchards of Pinus sylvestris. Silvae Genet 38:221–228Google Scholar
  68. Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330PubMedCrossRefGoogle Scholar
  69. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  70. Nylander M, Svensson J, Palva ET, Welin BV (2001) Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:263–279PubMedCrossRefGoogle Scholar
  71. Pot D, McMillan L, Echt C, Le Provost G, Garnier-Gere P, Cato S, Plomion C (2005) Nucleotide variation in genes involved in wood formation in two pine species. New Phytol 167:101–112PubMedCrossRefGoogle Scholar
  72. Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753PubMedCrossRefGoogle Scholar
  73. Pyhäjärvi T, García-Gil MR, Knürr T, Mikkonen M, Wachowiak W, Savolainen O (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics 177:1713–1724PubMedCrossRefGoogle Scholar
  74. Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genom 4:247–254CrossRefGoogle Scholar
  75. Ramos-Onsins S, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedGoogle Scholar
  76. Rorat T (2006) Plant dehydrins—tissue location, structure and function. Cell Mol Biol Lett 11:536–556PubMedCrossRefGoogle Scholar
  77. Roselius K, Stephan W, Stadler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763PubMedCrossRefGoogle Scholar
  78. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  79. Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, Gabriel SB, Platko JV, Patterson NJ, McDonald GJ, Ackerman HC, Campbell SJ, Altshuler D, Cooper R, Kwiatkowski D, Ward R, Lander ES (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–837PubMedCrossRefGoogle Scholar
  80. Savolainen O, Pyhäjärvi T, Knürr T (2007) Gene flow and local adaptation in trees. Ann Rev Ecol 38:595–619CrossRefGoogle Scholar
  81. Savolainen O, Pyhäjärvi T (2007) Genomic diversity in forest trees. Curr Opin Plant Biol 10:1–6CrossRefGoogle Scholar
  82. Seppänen MM, Cardi T, Hyökki MB, Pehu E (2000) Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Science 153:125–133PubMedCrossRefGoogle Scholar
  83. Soranzo N, Alia R, Provan J, Powell W (2000) Patterns of variation at a mitochondrial sequence-tagged-site locus provides new insights into the postglacial history of European Pinus sylvestris populations. Mol Ecol 9:1205–1211PubMedCrossRefGoogle Scholar
  84. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  85. Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225PubMedCrossRefGoogle Scholar
  86. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  87. Tiffin P, Gaut BS (2001) Sequence diversity in the tetraploid Zea perennis and the closely related diploid Z. diploperennis: insights from four nuclear loci. Genetics 158:401–412PubMedGoogle Scholar
  88. Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276PubMedCrossRefGoogle Scholar
  89. Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plantarum 127:167–181CrossRefGoogle Scholar
  90. Welling A, Rinne P, Vihera-Aarnio A, Kontunen-Soppela S, Heino P, Palva ET (2004) Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.). J Exp Bot 55:507–516PubMedCrossRefGoogle Scholar
  91. Wisniewski ME, Bassett CL, Renaut J, Farrell R, Tworkoskii T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26:575–584PubMedGoogle Scholar
  92. Wright SI, Charlesworth B (2004) The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168:1071–1076PubMedCrossRefGoogle Scholar
  93. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22(3):506–519PubMedCrossRefGoogle Scholar
  94. Wright SI, Lauga B, Charlesworth D (2003) Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol 12:1247–1263PubMedCrossRefGoogle Scholar
  95. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Ann Rev Plant Biol 57:781–803CrossRefGoogle Scholar
  96. Yang TW, Zhang LJ, Zhang TG, Zhang H, Xu SJ, An LZ (2005) Transcriptional regulation network of cold-responsive genes in higher plants. Plant Science 169:987–995CrossRefGoogle Scholar
  97. Yazdani R, Nilsson JE, Plomion C, Mathur G (2003) Marker trait association for autumn cold acclimation and growth rhythm in Pinus sylvestris. Scand J For Res 18:29–38CrossRefGoogle Scholar
  98. Yin ZM, Rorat T, Szabala BM, Ziolkowska A, Malepszy S (2006) Expression of a Solanum sogarandinum SK3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170:1164–1172CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Witold Wachowiak
    • 1
    • 2
  • Peter A. Balk
    • 3
  • Outi Savolainen
    • 1
  1. 1.Department of BiologyUniversity of OuluOuluFinland
  2. 2.Institute of DendrologyPolish Academy of SciencesKórnikPoland
  3. 3.NSure bvWageningenThe Netherlands

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