Tree Genetics & Genomes

, Volume 9, Issue 6, pp 1447–1463 | Cite as

Signatures of adaptation and genetic structure among the mainland populations of Pinus radiata (D. Don) inferred from SNP loci

  • Shannon K. Dillon
  • Maureen F. Nolan
  • Philippe Matter
  • Washington J. Gapare
  • Jason G. Bragg
  • Simon G. Southerton
Original Paper


Insights into the relative contributions of locus specific and genome-wide effects on population genetic diversity can be gained through separation of their resulting genetic signals. Here we explore patterns of adaptive and neutral genetic diversity in the disjunct natural populations of Pinus radiata (D. Don) from mainland California. A first-generation common garden of 447 individuals revealed significant differentiation of wood phenotypes among populations (P ST), possibly reflecting local adaptation in response to environment. We subsequently screened all trees for genetic diversity at 149 candidate gene single nucleotide polymorphism (SNP) loci for signatures of adaptation. Ten loci were identified as being possible targets of diversifying selection following F ST outlier tests. Multivariate canonical correlation performed on a data set of 444 individuals identified significant covariance between environment, adaptive phenotypes and outlier SNP diversity, lending support to the case for local adaptation suggested from F ST and P ST tests. Covariation among discrete sets of outlier SNPs and adaptive phenotypes (inferred from multivariate loadings) with environment are supported by existing studies of candidate gene function and genotype–phenotype association. Canonical analyses failed to detect significant correlations between environment and 139 non-outlier SNP loci, which were applied to estimate neutral patterns of genetic differentiation among populations (F ST 4.3 %). Using this data set, significant hierarchical structure was detected, indicating three populations on the mainland. The hierarchical relationships based on neutral SNP markers (and SSR) were in contrast with those inferred from putatively adaptive loci, potentially highlighting the independent action of selection and demography in shaping genetic structure in this species.


Radiata pine SNP Differentiation Local adaptation Population structure 



The authors would like to extend gratitude to the late Dr Ken Eldridge, whose efforts towards conservation of radiata pine genetic resources have underpinned so much of the work achieved in this species. We sincerely thank Ken and Charlie Bell for their insightful discussions; David Neale, Gavin Moran and Colin Matheson for helpful comments on the manuscript and Wei Li for laboratory support. We would also like to thank several anonymous reviewers for constructive suggestions and advice in early versions of the manuscript. The SSR data set of Karhu et al. (2006) was used with permission from the authors. This research was funded by the Commonwealth Scientific and Industrial Research Organisation, ArborGen LLC, Forest and Wood Products Australia and the Southern Tree Breeding Association.

Data Archiving Statement

SNP genotype data, phenotypic traits and environmental parameters on individual trees applied in this study will be made available as supplemental text files which can be downloaded with the manuscript.

Supplementary material

11295_2013_650_MOESM1_ESM.doc (982 kb)
ESM 1 (DOC 982 kb).
11295_2013_650_MOESM2_ESM.doc (360 kb)
ESM 2 (DOC 360 kb).


  1. Allona I, Quinn M, Shoop E, Swope K, St Cyr S, Carlis J, Riedl J, Retzel E, Campbell MM, Sederoff R, Whetten RW (1998) Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci USA 95(16):9693–9698Google Scholar
  2. Axelrod DI (1980) History of the maritime close-coned pines, Alta and Baja California, vol 120. University of California Publications in Geological Sciences, University of California Press, BerkeleyGoogle Scholar
  3. Axelrod DI (1981) Holocene climatic changes in relation to vegetation disjunction and speciation. Am Nat 117:847–870Google Scholar
  4. Axelrod DI, Hill TG (1988) Pinus × critchfieldii, a late pleistocene hybrid pine from coastal Southern California. Am J Bot 75:558–569Google Scholar
  5. 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(2):643–655PubMedGoogle Scholar
  6. Ballian D, Longauer R, Mikic T, Paule L, Kajba D, Gomory D (2006) Genetic structure of a rare European conifer, Serbian spruce (Picea omorika (Panc.) Purk.). Plant Syst Evol 260(1):53–63Google Scholar
  7. Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23(1):38–44Google Scholar
  8. Battaglia M, Solorzano RM, Hernandez M, Cuellar-Ortiz S, Garcia-Gomez B, Marquez J, Covarrubias AA (2007) Proline-rich cell wall proteins accumulate in growing regions and phloem tissue in response to water deficit in common bean seedlings. Planta 225(5):1121–1133PubMedGoogle Scholar
  9. Beaumont MA, Balding DJ (2004) Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13(4):969–980Google Scholar
  10. Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond 263:1619–1626Google Scholar
  11. Boys J, Cherry M, Dayanandan S (2005) Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa Pinaceae). Am J Bot 92(5):833–841PubMedGoogle Scholar
  12. Brommer JE (2011) Whither P-st? The approximation of Q(st) by P-st in evolutionary and conservation biology. J Evol Biol 24(6):1160–1168PubMedGoogle Scholar
  13. Brou YC, Zeze A, Diouf O, Eyletters M (2007) Water stress induces overexpression of superoxide dismutases that contribute to the protection of cowpea plants against oxidative stress. Afr J Biotechnol 6(17):1982–1986Google Scholar
  14. 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(42):15255–15260PubMedGoogle Scholar
  15. Burdon RD (1992) Genetic survey of Pinus radiata. 9: General discussion and implications for genetic management. N Z J For Sci 22:274–298Google Scholar
  16. Burdon RD, Bannister MH, Low CA (1992) Genetic survey of Pinus radiata. 2: Population comparisons for growth rate, disease resistance, and morphology. N Z J For Sci 22:138–159Google Scholar
  17. Burdon RD, Broekhuizen P, Zabkiewicz JA (1997) Comparison of native-population and New Zealand land-race samples of Pinus radiata using cortical oleoresin monoterpenes. In: Burdon RD, Moore JM (eds) IUFRO ’97 Genetics of Radiata Pine: proceedings of NZFRI–IUFRO Conference, December 1–4, and Workshop December 5 1997, Rotorua, NZ. New Zealand Forest Research Institute, FRI Bull. No. 203, pp 50–56Google Scholar
  18. Burk DH, Liu B, Zhong RQ, Morrison WH, Ye ZH (2001) A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13(4):807–827PubMedGoogle Scholar
  19. Cabin RJ (1996) Genetic comparisons of seed bank and seedling populations of a perennial desert mustard, Lesquerella fendleri. Evolution 50(5):1830–1841. doi: 10.2307/2410740 Google Scholar
  20. Carbone MS, Williams AP, Ambrose AR, Boot CM, Bradley ES, Dawson TE, Schaeffer SM, Schimel JP, Still CJ (2013) Cloud shading and fog drip influence the metabolism of a coastal pine ecosystem. Glob Chang Biol 19:484–497Google Scholar
  21. Caruso A, Morabito D, Delmotte F, Kahlem G, Carpin S (2002) Dehydrin induction during drought and osmotic stress in Populus. Plant Physiol Biochem 40(12):1033–1042Google Scholar
  22. Cellier F, Conejero G, Breitler JC, Casse F (1998) Molecular and physiological responses to water deficit in drought-tolerant and drought-sensitive lines of sunflower—accumulation of dehydrin transcripts correlates with tolerance. Plant Physiol 116(1):319–328PubMedGoogle Scholar
  23. Chang S, Puryear JD, Dias MA, Funkhouser EA, Newton RJ, Cairney J (1996) Gene expression under water deficit in loblolly pine (Pinus taeda): isolation and characterization of cDNA clones. Physiol Plant 97(1):139–148Google Scholar
  24. Chang-Quan W, Rui-Chang L (2008) Enhancement of superoxide dismutase activity in the leaves of white clover (Trifolium repens L.) in response to polyethylene glycol-induced water stress. Acta Physiol Plant 30(6):841–847Google Scholar
  25. Chen ZZ, Hong XH, Zhang HR, Wang YQ, Li X, Zhu JK, Gong ZZ (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43(2):273–283PubMedGoogle Scholar
  26. Chen KM, Abbott RJ, Milne RI, Tian XM, Liu JQ (2008) Phylogeography of Pinus tabulaeformis Carr. (Pinaceae), a dominant species of coniferous forest in northern China. Mol Ecol 17(19):4276–4288PubMedGoogle Scholar
  27. Cochard H, Froux F, Mayr FFS, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134(1):401–408PubMedGoogle Scholar
  28. Dalla-Salda G, Martinez-Meier A, Cochard H, Rozenberg P (2009) Variation of wood density and hydraulic properties of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) clones related to a heat and drought wave in France. For Ecol Manag 257(1):182–189Google Scholar
  29. Darley CP, Forrester AM, McQueen-Mason SJ (2001) The molecular basis of plant cell wall extension. Plant Mol Biol 47(1–2):179–195PubMedGoogle Scholar
  30. Dawson TE (1998) Fog in the California redwood forest: ecosystem inputs and use by plants. Oecologia 117:476–485Google Scholar
  31. De Mita S, Thuillet AC, Gay L, Ahmadi N, Manel S, Ronfort J, Vigouroux Y (2013) Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol 22(5):1383–1399PubMedGoogle Scholar
  32. Delmer DP, Pear JR, Andrawis A, Stalker DM (1995) Genes encoding small GTP-binding proteins analogous to mammalian Rac are preferentially expressed in developing cotton fibers. Mol Gen Genet 248(1):43–51PubMedGoogle Scholar
  33. Diad M, Padmanabhan V, Sen. S., Magallanesl J, Cairney J, Newtonl RJ (1995) Isolation and characterization of water deficit stress inducible cDNAs and their genomic counterparts from Pinus taeda (loblollypine), unpublishedGoogle Scholar
  34. DiGiovanni F, Kevan PG, Arnold J (1996) Lower planetary boundary layer profiles of atmospheric conifer pollen above a seed orchard in northern Ontario, Canada. For Ecol Manag 83(1–2):87–97Google Scholar
  35. Dillon SK, Nolan M, Li W, Bell C, Wu HX, Southerton SG (2010) Allelic variation in cell wall candidate genes affecting solid wood properties in natural populations and land races of Pinus radiata. Genetics 185(4):1477–1487PubMedGoogle Scholar
  36. Doblin MS, Kurek I, Jacob-Wilk D, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43(12):1407–1420PubMedGoogle Scholar
  37. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  38. 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(2):179–188PubMedGoogle Scholar
  39. Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, Clair JBS, Neale DB (2009a) Association genetics of coastal Douglas fir (Pseudotsuga menziesu var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182(4):1289–1302PubMedGoogle Scholar
  40. Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009b) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold hardiness in coastal Douglas fir (Pseudotsuga menziesii var. menziesii). Genetics 183(1):289–298PubMedGoogle Scholar
  41. Eckert AJ, Bower AD, Gonzalez-Martinez SC, Wegrzyn JL, Coop G, Neale DB (2010a) Back to nature: ecological genomics of loblolly pine (Pinus taeda, Pinaceae). Mol Ecol 19(17):3789–3805PubMedGoogle Scholar
  42. Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonza’lez-Martı’nez SC, Neale DB (2010b) Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982PubMedGoogle Scholar
  43. Edjolo A, Laffray D, Guerrier G (2001) The ascorbate–glutathione cycle in the cytosolic and chloroplastic fractions of drought-tolerant and drought-sensitive poplars. J Plant Physiol 158(12):1511–1517Google Scholar
  44. Eldridge KG (1978) Refreshing the genetic resources of radiata pine plantations. Division of Forrest Research: Genetics Section Report Number 7 CSIROGoogle Scholar
  45. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620PubMedGoogle Scholar
  46. Eveno E, Collada C, Guevara MA, Leger V, Soto A, Diaz L, Leger P, Gonzalez-Martinez SC, Cervera MT, Plomion C, Garnier-Gere 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):417–437PubMedGoogle Scholar
  47. Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298Google Scholar
  48. Ficetola GF, Bonin A (2011) Conserving adaptive genetic diversity in dynamic landscapes. Mol Ecol 20(8):1569–1571PubMedGoogle Scholar
  49. Forde MB (1964) Variation in natural populations of Pinus radiata in California. Part 2. Needle characters. N Z J Bot 2:237–257Google Scholar
  50. Forde MB (1966) Pinus radiata in California. N Z J For Sci 11:20–42Google Scholar
  51. Gapare WJ, Aitken SN (2005) Strong spatial genetic structure in peripheral but not core populations of Sitka spruce [Picea sitchensis (Bong.) Carr.]. Mol Ecol 14(9):2659–2667PubMedGoogle Scholar
  52. Gapare W, Ivkovich M, Dutkowski W, Spencer DJ, Buxton P, Wu H (2012a) Genetic parameters and provenance variation of Pinus radiata D. Don. ‘Eldridge collection’ in Australia 1: growth and form traits. Tree Genetics and Genomes 8(2):391–407Google Scholar
  53. Gapare W, Ivkovich M, Dillon S, Chen F, Evans R, Wu H (2012b) Genetic parameters and provenance variation of Pinus radiata D. Don. ‘Eldridge collection’ in Australia 2: wood properties. Tree Genetics and Genomes 8(2):391–407Google Scholar
  54. Garcia-Gil MR, Francois O, Kamruzzahan S, Waldmann P (2009) Joint analysis of spatial genetic structure and inbreeding in a managed population of Scots pine. Heredity 103(1):90–96PubMedGoogle Scholar
  55. Gonzalez-Martinez SC, Krutovsky KV, Neale DB (2006) Forest-tree population genomics and adaptive evolution. New Phytol 170(2):227–238PubMedGoogle Scholar
  56. Gonzalez-Martinez SC, Huber D, Ersoz E, Davis JM, Neale DB (2008) Association genetics in Pinus taeda L. II. Carbon isotope discrimination. Heredity 101(1):19–26PubMedGoogle Scholar
  57. Gough L, Shaver GR, Carroll J, Royer DL, Laundre JA (2000) Vascular plant species richness in Alaskan arctic tundra: the importance of soil pH. J Ecol 88(1):54–66Google Scholar
  58. Gram WK, Sork VL (2001) Association between environmental and genetic heterogeneity in forest tree populations. Ecology 82(7):2012–2021Google Scholar
  59. Grieser J, Gommes R, Bernardi M (2006) New LocClim—the local climate estimator of FAO. Geophysical Research Abstracts, vol 8. European Geosciences Union, SRef-ID: 1607-7962/gra/EGU06-A-08305Google Scholar
  60. Griffin AR (1980) Isolation of a radiata pine seed orchard from external pollen. Aust For Res 10(1):83–94Google Scholar
  61. Hamrick JL, Godt MJW (1989) Allozyme diversity in plant species. In: Brown ADH, Clegg MT, Kahler AL, Weir BS (eds) Plant population genetics, breeding and genetic resources. Sinauer, Sunderland, pp 43–63Google Scholar
  62. Hamrick JL, Mitton JB, Linhart YB (1981) Levels of genetic variation in trees: influences of life history characteristics. In: Conkle MT (ed) Proceedings of the Symposium on Isozymes of North American Forest Trees and Forest Insects. U.S. Forest Service General Technical Report, PSW-48, pp 35–41Google Scholar
  63. Harrak H, Chamberland H, Plante M, Bellemare C, Lafontaine JG, Tabaeizadeh Z (1999) A proline-, threonine-, and glycine-rich protein down-regulated by drought is localized in the cell wall of xylem elements. Plant Physiol 121(2):557–564PubMedGoogle Scholar
  64. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, SunderlandGoogle Scholar
  65. He CY, Zhang JS, Chen SY (2002) A soybean gene encoding a proline-rich protein is regulated by salicylic acid, an endogenous circadian rhythm and by various stresses. Theor Appl Genet 104(6–7):1125–1131PubMedGoogle Scholar
  66. Hohn M, Gugerli F, Abran P, Bisztray G, Buonamici A, Cseke K, Hufnagel L, Quintela-Sabaris C, Sebastiani F, Vendramin GG (2009) Variation in the chloroplast DNA of Swiss stone pine (Pinus cembra L.) reflects contrasting post-glacial history of populations from the Carpathians and the Alps. J Biogeogr 36(9):1798–1806Google Scholar
  67. 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 Phytol 188(2):501–514PubMedGoogle Scholar
  68. Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European Aspen (Populus tremula L., Salicaceae). Genetics 169(2):945–953PubMedGoogle Scholar
  69. Ingvarsson PK, Garcia MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172(3):1845–1853PubMedGoogle Scholar
  70. Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178(4):2217–2226PubMedGoogle Scholar
  71. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806Google Scholar
  72. Jayawichrama KJS, Balocchi C (1993) Growth and form of provenances of Pinus radiata in Chile. Aust For 56:172–178Google Scholar
  73. Johnson IG, Ades PK, Eldridge KG (1997) Growth of natural Californian provenances of Pinus radiata in New South Wales. Australia N Z J For Sci 27:23–38Google Scholar
  74. Johnstone JA, Dawson TE (2010) Climatic context and ecological implications of summer fog decline in the coast redwood region. Proc Natl Acad Sci USA 107:4533–4538Google Scholar
  75. Joshi CP, Mansfield SD (2007) The cellulose paradox—simple molecule, complex biosynthesis. Curr Opin Plant Biol 10(3):220–226PubMedGoogle Scholar
  76. Kaldenhoff R, Fischer M (2006) Aquaporins in plants. Acta Physiologica 187(1–2):169–176PubMedGoogle Scholar
  77. Karhu A, Vogl C, Moran GF, Bell JC, Savolainen O (2006) Analysis of microsatellite variation in Pinus radiata reveals effects of genetic drift but no recent bottlenecks. J Evol Biol 19(1):167–175PubMedGoogle Scholar
  78. Kawaoka A, Nanto K, Sugita K, Endo S, Yamada-Watanabe K, Matsunaga E, Ebinuma H (2001) Transcriptional regulation of lignin biosynthesis by tobacco LIM protein in transgenic woody plants. In: Molecular breeding of woody plants, proceedings. Prog Biotechnol 18, pp 205–210Google Scholar
  79. Kawaoka A, Nanto K, Ishii K, Ebinuma H (2006) Reduction of lignin content by suppression of expression of the LIM domain transcription factor in Eucalyptus camaldulensis. Silvae Genet 55(6):269–277Google Scholar
  80. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7(12):1225–1241Google Scholar
  81. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, Futschik A, Kosiol C, Schlotterer C (2011) PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. Plos One 6 (1). doi: e1592510.1371/journal.pone.0015925
  82. Ledig FT, Vargas-Hernandez JJ, Johnsen KH (1998) Conservation of forest genetic resources: case histories from Canada, Mexico, and the United States. J For 96:32–41Google Scholar
  83. Lian HL, Yu X, Ye Q, Ding XS, Kitagawa Y, Kwak SS, Su WA, Tang ZC (2004) The role of aquaporin RWC3 in drought avoidance in rice. Plant Cell Physiol 45(4):481–489PubMedGoogle Scholar
  84. Lindsay AD (1932) Monterey pine (Pinus radiata D. Don) in its native habitat. Commonwealth Forestry Bureau Report, Bulletin No. 10. Commonwealth Forestry Bureau Canberra, AustraliaGoogle Scholar
  85. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4(12):981–994PubMedGoogle Scholar
  86. Lynch M (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci USA 104:8597–8604Google Scholar
  87. Martinez-Meier A, Sanchez L, Dalla-Salda G, Gallo L, Pastorino M, Rozenberg P (2009) Ring density record of phenotypic plasticity and adaptation to drought in Douglas-fir. For Ecol Manag 258(5):860–867Google Scholar
  88. Matheson C, Spencer D, Bush D, Porada H (2007) A strategy to develop a low rainfall breed of Pinus radiata. Joint Venture Agroforestry Program, RIRDC, Land & Water Australia and FWPRDC, CanberraGoogle Scholar
  89. McDonald JB (1959) An ecological study of Monterey pine in Monterey County. University of California, BerkeleyGoogle Scholar
  90. McKeon JJ (1966) Canonical analysis: some relations between canonical correlation, factor analysis, discriminant function analysis, and scaling theory. Psychometric monographs, vol 13. Psychometric Society, RichmondGoogle Scholar
  91. McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111(4):1177–1181PubMedGoogle Scholar
  92. Millar C (1997) Quaternary evolution of Pinus radiata. FRI Bulletin 203:22–25Google Scholar
  93. Millar CI (1999) Evolution and biogeography of Pinus radiata, with a proposed revision of its quaternary history. N Z J For Sci 29(3):335–365Google Scholar
  94. Mimura M, Aitken SN (2007) Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis. Heredity 99(2):224–232PubMedGoogle Scholar
  95. Moen T, Hayes B, Nilsen F, Delghandi M, Fjalestad KT, Fevolden SE, Berg PR, Lien S (2008) Identification and characterisation of novel SNP markers in Atlantic cod: evidence for directional selection. BMC Genet 9Google Scholar
  96. Moffatt BA, Weretilnyk EA (2001) Sustaining S-adenosyl-l-methionine-dependent methyltransferase activity in plant cells. Physiol Plant 113(4):435–442Google Scholar
  97. Moran GF, Bell JC, Eldridge KG (1988) The genetic-structure and the conservation of the 5 natural-populations of Pinus-radiata. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 18(5):506–514Google Scholar
  98. Nairn CJ, Haselkorn T (2005) Three loblolly pine CesA genes expressed in developing xylem are orthologous to secondary cell wall CesA genes of angiosperms. New Phytol 166(3):907–915PubMedGoogle Scholar
  99. 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(16):3599–3613PubMedGoogle Scholar
  100. Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9(7):325–330PubMedGoogle Scholar
  101. Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233PubMedGoogle Scholar
  102. Neigel JE (2002) Is F-ST obsolete? Conserv Genet 3(2):167–173Google Scholar
  103. Nielsen R (2005) Molecular signatures of natural selection. In: Annual review of genetics, vol 39. Annual Review of Genetics, pp 197–218Google Scholar
  104. Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18(15):3128–3150PubMedGoogle Scholar
  105. O’Connell LM, Mosseler A, Rajora OP (2007) Extensive long-distance pollen dispersal in a fragmented landscape maintains genetic diversity in white spruce. J Hered 98(7):640–645PubMedGoogle Scholar
  106. Olafsdottir GA, Snorrason SS (2009) Parallels, nonparallels, and plasticity in population differentiation of threespine stickleback within a lake. Biol J Linn Soc 98(4):803–813Google Scholar
  107. Oleksyk TK, Smith MW, O'Brien SJ (2010) Genome-wide scans for footprints of natural selection. Philosophical Transactions of the Royal Society B—Biological Sciences 365(1537):185–205Google Scholar
  108. Owens D, Adams D (1999) Overview of pitch canker in California. In: Devey M, Matheson C, Gordon T (eds) IMACT Monterey Workshop : Current and Potential Impacts of Pitch Canker in Radiata Pine, Monterey, California. Commonwealth Scientific and Industrial Research Organization, CanberraGoogle Scholar
  109. Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36(6):743–754PubMedGoogle Scholar
  110. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295Google Scholar
  111. Peter G, Neale D (2004) Molecular basis for the evolution of xylem lignification. Curr Opin Plant Biol 7(6):737–742PubMedGoogle Scholar
  112. Petit JR, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214Google Scholar
  113. Plessas ME, Strauss SH (1986) Allozyme differentiation among populations, stands, and cohorts in Monterey pine. Canadian Journal of Forest Research—Revue Canadienne De Recherche Forestiere 16(6):1155–1164Google Scholar
  114. Porcel R, Aroca R, Azcon R, Ruiz-Lozano JM (2006) PIP aquaporin gene expression in arbuscular mycorrhizal Glycine max and Lactuca sativa plants in relation to drought stress tolerance. Plant Mol Biol 60(3):389–404PubMedGoogle Scholar
  115. Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119(3):849–858PubMedGoogle Scholar
  116. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedGoogle Scholar
  117. Provan J, Soranzo N, Wilson NJ, Goldstein DB, Powell W (1999) A low mutation rate for chloroplast microsatellites. Genetics 153(2):943–947PubMedGoogle Scholar
  118. 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. Mol Ecol 20(8):1702–1716PubMedGoogle Scholar
  119. Pujol B, Wilson AJ, Ross RIC, Pannell JR (2008) Are Q(ST)-F-ST comparisons for natural populations meaningful? Mol Ecol 17(22):4782–4785PubMedGoogle Scholar
  120. Rahman SML, Mackay WA, Nawata E, Sakuratani T (2004) Superoxide dismutase and stress tolerance of four tomato cultivars. Hortscience 39(5):983–986Google Scholar
  121. Raymond CA, Henson M (2009) Genetic variation amongst and within the native provenances of Pinus radiata D. Don in south-eastern Australia. 1. Growth and form to age 26 years. Silvae Genet 58(5–6):242–252Google Scholar
  122. 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. Mol Ecol 20(8):1582–1600PubMedGoogle Scholar
  123. Rogers DL (2002) In situ genetic conservation of Monterey pine (Pinus radiata D. Don): information and recommendations. Division of Agriculture and Natural resources, Genetic Resources Conservation program, University of California, DavisGoogle Scholar
  124. Rogers DL (2004) In situ genetic conservation of a naturally restricted and commercially widespread species, Pinus radiata. For Ecol Manag 197(1–3):311–322Google Scholar
  125. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138Google Scholar
  126. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GHH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17(6):1749–1763PubMedGoogle Scholar
  127. Scalfi M, Piotti A, Rossi M, Piovani P (2009) Genetic variability of Italian southern Scots pine (Pinus sylvestris L.) populations: the rear edge of the range. Eur J For Res 128(4):377–386Google Scholar
  128. Sgro CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evolutionary Applications 4(2):326–337Google Scholar
  129. Shen R, Fan JB, Campbell D, Chang WH, Chen J, Doucet D, Yeakley J, Bibikova M, Garcia EW, McBride C, Steemers F, Garcia F, Kermani BG, Gunderson K, Oliphant A (2005) High-throughput SNP genotyping on universal bead arrays. Mutat Res 573(1–2):70–82PubMedGoogle Scholar
  130. Smart CC, Amrhein N (1985) The influence of lignification on the development of vascular tissue in Vigna-radiata L. Protoplasma 124(1–2):87–95Google Scholar
  131. Sörensen TA (1948) Method of establishing groups of equal amplitude in plant sociology based on similarity of species content. Biol krifter Bd 4:1–34Google Scholar
  132. Sork VL, Davis FW, Westfall R, Flint A, Ikegami M, Wang HF, Grivet D (2010) Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Nee) in the face of climate change. Mol Ecol 19(17):3806–3823PubMedGoogle Scholar
  133. Spitze K (1993) Population-structure in Daphnia-obtusa—quantitative genetic and allozymic variation. Genetics 135(2):367–374PubMedGoogle Scholar
  134. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences USA 100(16):9440–9445Google Scholar
  135. Szyjanowicz PMJ, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37(5):730–740PubMedGoogle Scholar
  136. Tang D, Ide Y (1998) Detection of genetic variation among seed and seedlings of Chamaecyparis obtusa using allozyme markers. J For Res 3:35–38Google Scholar
  137. Terrab A, Paun O, Talavera S, Tremetsberger K, Arista M, Stuessy TF (2006) Genetic diversity and population structure in natural populations of Moroccan atlas cedar (Cedrus atlantica; Pinaceae) determined with cpSSR markers. Am J Bot 93(9):1274–1280PubMedGoogle Scholar
  138. Thuillet AC, Bru D, David J, Roumet P, Santomi S, Sourdille P, Bataillon T (2002) Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum desf. Mol Biol Evol 19(1):122–125PubMedGoogle Scholar
  139. Tsumura Y, Kado T, Takahashi T, Tani N, Ujino-Ihara T, Iwata H (2007) Genome scan to detect genetic structure and adaptive genes of natural populations of Cryptomeria japonica. Genetics 176:2393–2403PubMedGoogle Scholar
  140. Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9(5):689–701PubMedGoogle Scholar
  141. Udupa SM, Baum M (2001) High mutation rate and mutational bias at (TAA)(n) microsatellite loci in chickpea (Cicer arietinum L.). Mol Genet Genomics 265(6):1097–1103PubMedGoogle Scholar
  142. Vander Mijnsbrugge K, Beeckman H, De Rycke R, Van Montagu M, Engler G, Boerjan W (2000a) Phenylcoumaran benzylic ether reductase, a prominent poplar xylem protein, is strongly associated with phenylpropanoid biosynthesis in lignifying cells. Planta 211(4):502–509PubMedGoogle Scholar
  143. Vander Mijnsbrugge K, Meyermans H, Van Montagu M, Bauw G, Boerjan W (2000b) Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210(4):589–598PubMedGoogle Scholar
  144. Verbelen JP, Vissenberg K, Kerstens S, Le J (2001) Cell expansion in the epidermis: microtubules, cellulose orientation and wall loosening enzymes. J Plant Physiol 158(5):537–543Google Scholar
  145. Vigouroux Y, Jaqueth JS, Matsuoka Y, Smith OS, Beavis WF, Smith JSC, Doebley J (2002) Rate and pattern of mutation at microsatellite loci in maize. Mol Biol Evol 19(8):1251–1260PubMedGoogle Scholar
  146. Volaire F (2002) Drought survival, summer dormancy and dehydrin accumulation in contrasting cultivars of Dactylis glomerata. Physiol Plant 116(1):42–51PubMedGoogle Scholar
  147. Vonlanthen CM, Kammer PM, Eugster W, Buhler A, Veit H (2006) Alpine vascular plant species richness: the importance of daily maximum temperature and pH. Plant Ecol 184(1):13–25Google Scholar
  148. Wachowiak W, Balk PA, Savolainen O (2009) Search for nucleotide diversity patterns of local adaptation in dehydrins and other cold-related candidate genes in Scots pine (Pinus sylvestris L.). Tree Genetics & Genomes 5(1):117–132Google Scholar
  149. Wang HW, Ge S (2006) Phylogeography of the endangered Cathaya argyrophylla (Pinaceae) inferred from sequence variation of mitochondrial and nuclear DNA. Mol Ecol 15(13):4109–4122PubMedGoogle Scholar
  150. Wasteneys GO, Galway ME (2003) Remodelling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54:691–722PubMedGoogle Scholar
  151. White TA, Stamford J, Hoelzel AR (2010) Local selection and population structure in a deep-sea fish, the roundnose grenadier (Coryphaenoides rupestris). Mol Ecol 19(2):216–226PubMedGoogle Scholar
  152. Wightman R, Turner SR (2008) The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 54(5):794–805PubMedGoogle Scholar
  153. Williams MC, Wardle GM (2007) Pinus radiata invasion in Australia: identifying key knowledge gaps and research directions. Austral Ecol 32(7):721–739Google Scholar
  154. Wolfe KH, Sharp PM, Li WH (1989) Rates of synonymous substitution in plant nuclear genes. J Mol Evol 29:208–211Google Scholar
  155. Wu JY, Krutovskii KV, Strauss SH (1998) Abundant mitochondrial genome diversity, population differentiation and convergent evolution in pines. Genetics 150(4):1605–1614PubMedGoogle Scholar
  156. Yu Q, Li B, Nelson CD, McKeand SE, Batista VB, Mullin TJ (2006) Association of the cad-n1 allele with increased stem growth and wood density in full-sib families of loblolly pine. Tree Genetics & Genomes 2(2):98–108Google Scholar
  157. Zhang Y, Sederoff RR, Allona I (2000) Differential expression of genes encoding cell wall proteins in vascular tissues from vertical and bent loblolly pine trees. Tree Physiol 20(7):457–466PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Shannon K. Dillon
    • 1
  • Maureen F. Nolan
    • 1
  • Philippe Matter
    • 1
  • Washington J. Gapare
    • 1
  • Jason G. Bragg
    • 1
    • 2
  • Simon G. Southerton
    • 1
  1. 1.CSIRO Plant IndustryKingstonAustralia
  2. 2.Research School of Biology and Centre for Biodiversity AnalysisThe Australian National UniversityCanberraAustralia

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