Abstract
Nucleotide polymorphisms in two North American balsam poplars (Populus trichocarpa Torr. & Gray and P. balsamifera L.; section Tacamahaca), and one Eurasian aspen (P. tremula L.; section Populus) were compared using nine loci involved in defense, stress response, photoperiodism, freezing tolerance, and housekeeping. Nucleotide diversity varied among species and was highest for P. tremula (θ w = 0.005, π T = 0.007) as compared to P. balsamifera (θ w = 0.004, π T = 0.005) or P. trichocarpa (θ w = 0.002, π T = 0.003). Across species, the defense and the stress response loci accounted for the majority of the observed level of nucleotide diversity. In general, the studied loci did not deviate from neutral expectation either at the individual locus (non-significant normalized Fay and Wu’s H) or at the multi-locus level (non-significant HKA test). Using molecular clock analysis, section Tacamahaca probably shared a common ancestor with section Populus approximately 4.5 million year ago. Divergence between the two closely related balsam poplars was about 0.8 million years ago, a pattern consistent with an isolation-with-migration (IM) model. As expected, P. tremula showed a five-fold higher substitution rate (2 × 10−8 substitution/site/year) compared to the North American species (0.4 × 10−8 substitution/site/year), probably reflecting its complex demographic history. Linkage disequilibrium (LD) varied among species with a more rapid decay in the North American species (<400 bp) in comparison to P. tremula (≫400 bp). The similarities in nucleotide diversity pattern and LD decay of the two balsam poplar species likely reflects the recent time of their divergence.
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References
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Arunyawat U, Stephan W, Städler T (2007) Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes. Mol Biol Evol 24:2310–2322
Auge GA, Perelman S, Crocco CD et al (2009) Gene expression analysis of light-modulated germination in tomato seeds. New Phytol 183:301–314
Battistuzzi FU, Filipski A, Hedges SB et al (2010) Performance of relaxed clock methods in estimating evolutionary divergence times and their credibility intervals. Mol Biol Evol 27:1289–1300
Battistuzzi FU, Billing-Ross P, Paliwal A et al (2011) Fast and slow implementations of relaxed clock methods show similar patterns of accuracy in estimating divergence times. Mol Biol Evol 28:2439–2442
Becquet C, Przeworski M (2007) A new approach to estimate parameters of speciation models with application to apes. Genome Res 17:1505–1519
Benedict C, Skinner JS, Meng R et al (2006) The CBF1-dependent low temperature signalling pathway, regulon, and increase in freeze tolerance are conserved in Populus spp. Plant, Cell Environ 29:1259–1272
Boffelli D, McAuliffe J, Ovcharenko D et al (2003) Phylogenetic shadowing of primate sequences to find functional regions of the human genome. Science 299:1391–1394
Braatne JH, Rood SB, Heilman PE (1996) Life history, ecology, and conservation of riparian cottonwoods in North America. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, Ottawa, pp 57–85
Brayshaw TC (1965) The status of the black cottonwood (Populus trichocarpa Torrey and Gray). Can Field Nat 79:91–95
Breen AL, Glenn E, Yeager A et al (2009) Nucleotide diversity among natural populations of a North American poplar (Populus balsamifera, Salicaceae). New Phytol 182:763–773
Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56
Cervera MT, Storme V, Soto A et al (2005) Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. Theor Appl Genet 111:1440–1456
Chu Y, Su X, Huang Q et al (2008) Patterns of DNA sequence variation at candidate gene loci in black poplar (Populus nigra L.) as revealed by single nucleotide polymorphisms. Genetica 137:141–150
Comes HP, Kadereit W (1998) The effect of quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438
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. Mol Ecol 19:1638–1650
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Photochem Bull 19:11–15
Drummond AJ, Rambaut A (2007) BEAST. Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221
Eckenwalder JE (1977) North American cottonwoods (Populus, Salicaceae) of sections Abaso and Aigeiros. J Arnold Arbor 58:193–208
Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE et al (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, National Research Council of Canada, Ottawa, pp 7–32
Edwards SV (2009) Is a new and general theory of molecular systematics emerging? Evolution 63:1–19
Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284
Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194
Eyre-Walker A, Keightley PD, Smith NGC et al (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149
Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plant Cell 15:1502–1506
Gelman A, Carlin JB, Stern HS et al (2004) Bayesian data analysis, 2nd edn. Chapman & Hall/CRC Press, Boca Raton
Gilchrist EJ, Haughn GW, Ying CC et al (2006) Use of ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa. Mol Ecol 15:1367–1378
Guillet-Claude C, Birolleau-Touchard C, Manicacci P et al (2004) Nucleotide diversity of the ZmPox3 maize peroxidase gene: relationships between a MITE insertion in exon 2 and variation in forage maize digestibility. BMC Genet 5:19
Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT–TRNF region and nuclear rDNA. Am J Bot 91:1398–1408
Hamzeh M, Perinet P, Dayanandan S (2006) Genetic relationships among species of Populus (Salicaceae) based on nuclear genomic data. J Torrey Bot Soc 133:519–527
Hardison RC (2003) Comparative genomics. PLoS Biol 1(2):e58. doi:10.1371/journal.pbio.0000058
Hasegawa M, Kishino H, Yano T (1985) Dating the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hedges SB, Kumar S (2003) Genomic clocks and evolutionary timescales. Trends Genet 19:200–206
Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913
Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78
Hollick JB, Gordon MP (1993) A poplar tree proteinase inhibitor-like gene promoter is responsive to wounding in transgenic tobacco. Plant Mol Biol 22:561–572
Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159
Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus termula L., Salicaceae). Genetics 169:945–953
Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340
Ingvarsson PK (2010) Nucleotide polymorphism, linkage disequilibrium and complex trait Dissection in Populus. In: Jansson S, Bhaleroa R, Groover A (eds) Genetics and Genomics of Populus. Springer, New York, pp 91–112
Ingvarsson PK, Garcia MV, Hall D et al (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 172:845–1853
Ismail, M (2010) Molecular genetic diversity among natural population of Populus. PhD thesis, Faculty of Forestry, University of British Columbia
Jackson S, Rounsley S, Purugganan M (2006) Comparative sequencing of plant genomes: choices to make. Plant Cell 18:1100–1104
Jianxin Ma, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. PNAS 101:12404–12410
Joseph JA, Lexer C (2008) A set of novel DNA polymorphisms within candidate genes potentially involved in ecological divergence between Populus alba and P. tremula, two hybridising European forest trees. Mol Ecol Notes 8:188–192
Keller SR, Olson MS, Silim S et al (2010) Genomic diversity, population structure, and migration following rapid range expansion in the Balsam Poplar, Populus balsamifera. Mol Ecol 19:1212–1226
Keller SR, Soolanayakanahally RY, Guy RD et al (2011) Climate-driven local adaptation of ecophysiology and phenology in balsam poplar (Populus balsamifera L., Salicaceae). Am J Bot 98:99–108
Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:14831498
Kowalski SP, Lan TH, Feldmann KA et al (1994) Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization. Genetics 138:499–510
Lexer C, Fay MF, Joseph JA et al (2005) Barrier to gene flow between two ecologically divergent Populus species, P. alba (White Poplar) and P. tremula (European Aspen): the role of ecology and life history in gene introgression. Mol Ecol 14:1045–1057
Lexer C, Buerkle CA, Joseph JA et al (2007) Admixture in European Populus hybrid zones makes feasible the mapping of loci that contribute to reproductive isolation and trait differences. Heredity 98:74–84
Li N, Stephens M (2003) Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165:2213–2233
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Liu AZ, Burke JM (2006) Patterns of nucleotide diversity in wild and cultivated sunflower. Genetics 173:321–330
Liu L, Pearl DK (2007) Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. Syst Biol 56:504–514
Luquez V, Hall D, Albrectsen BR et al (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genet Genomes 4:279–292
Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394
Major IT, Constabel CP (2008) Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiol 146:888–903
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Olson MS, Robertson AL, Takebayashi N et al (2010) Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). New Phytol 186:526–536
Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583
Petit JR, Aguinagalde I, de Beaulieu J-L et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
Plummer M, Best N, Cowles K, et al. (2006) CODA: output analysis and diagnostics for MCMC. R package version 0.13-5
Rambaut A, Drummond AJ (2007a) BEAUti version 1.4.2. http://beast.bio.ed.ac.uk/BEAUti
Rambaut A, Drummond AJ (2007b) Tracer version 1.5. http://tree.bio.ed.ac.uk/software/tracer/
Ramos-Onsins SE, Stranger BE, Mitchell-Olds T et al (2004) Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373–388
Rand DM, Kann LM (1996) Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol 13:735–748
Reid N, John R, Demboski JR, Sullivan J (2012) Phylogeny estimation of the radiation of western North American chipmunks (Tamias) in the face of introgression using reproductive protein genes. Syst Biol 61:44–62
Remington DL, Thornsberry JM, Matsuoka Y et al (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. PNAS 98:11479–11484
Rose LE, Bittner-Eddy P, Langley CH et al (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517–1527
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386
Sanderson M (1997) Nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1231
Slavov GT, Zhelev P (2010) Salient biological features, systematics, and genetic variation of Populus. In: Jansson S, Bhalerao R, Groover AT (eds) Genetics and genomics of Populus. Springer, New York, pp 15–38
Soolanayakanahally RY, Guy RD, Silim SN et al (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant, Cell Environ 32:1821–1832
Städler T, Haubold B, Merino C, et al (2009) The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics 182:205–216
Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Am J Hum Genet 76:449–462
Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Strand AE, Leebens-Mack J, Milligan GB (1997) Nuclear-DNA-based markers for plant evolutionary biology. Mol Ecol 6:113–118
Sweigart AL, Willis JH (2003) Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evol Int J Org Evol 57:2490–2506
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tang JT, Vosman B, Voorrips RE et al (2006) QualitySNP: a pipeline for detecting single nucleotide polymorphisms and insertions/deletions in EST data from diploid and polyploid species. BMC Bioinformatics 7:438–453
Thorne JL, Kishino H (2005) Estimation of divergence times from molecular sequence data. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, New York, pp 233–256
Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Weir BS (1990) Genetic data analysis II. Sinauer Associates, Inc., Sunderland
Wood DA, Vandergast AG, Lemos-Espinal JA et al (2011) Refugial isolation and divergence in the narrowheaded Gartersnake species complex (Thamnophis rufipunctatus) as revealed by multilocus DNA sequence data. Mol Ecol 20:3856–3878
Wright S, Lauga B, Charlesworth D (2003) Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol 19:1407–1420
Xie CY, Ying CC, Yanchuk AD et al (2009) Ecotypic mode of regional differentiation caused by restricted gene migration: a case in black cottonwood (Populus trichocarpa) along the Pacific Northwest coast. Can J For Res 39:519–526
Zeng K, Fu Y-X, Shi S, Wu C-I (2006) Statistical tests for detecting positive selection by utilizing high-frequency variants. Genetics 174:1431–1439
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Ismail, M., Soolanayakanahally, R.Y., Ingvarsson, P.K. et al. Comparative Nucleotide Diversity Across North American and European Populus Species. J Mol Evol 74, 257–272 (2012). https://doi.org/10.1007/s00239-012-9504-5
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DOI: https://doi.org/10.1007/s00239-012-9504-5