Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa.

• Plant population genomics informs evolutionary biology, breeding, conservation and bioenergy feedstock development. For example, the detection of reliable phenotype-genotype associations and molecular signatures of selection requires a detailed knowledge about genome-wide patterns of allele frequency variation, linkage disequilibrium and recombination. • We resequenced 16 genomes of the model tree Populus trichocarpa and genotyped 120 trees from 10 subpopulations using 29,213 single-nucleotide polymorphisms. • Significant geographic differentiation was present at multiple spatial scales, and range-wide latitudinal allele frequency gradients were strikingly common across the genome. The decay of linkage disequilibrium with physical distance was slower than expected from previous studies in Populus, with r(2) dropping below 0.2 within 3-6 kb. Consistent with this, estimates of recent effective population size from linkage disequilibrium (N(e) ≈ 4000-6000) were remarkably low relative to the large census sizes of P. trichocarpa stands. Fine-scale rates of recombination varied widely across the genome, but were largely predictable on the basis of DNA sequence and methylation features. • Our results suggest that genetic drift has played a significant role in the recent evolutionary history of P. trichocarpa. Most importantly, the extensive linkage disequilibrium detected suggests that genome-wide association studies and genomic selection in undomesticated populations may be more feasible in Populus than previously assumed.

[1]  S. Garman,et al.  Gene flow and simulation of transgene dispersal from hybrid poplar plantations. , 2012, The New phytologist.

[2]  N. Young,et al.  Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula , 2011, Proceedings of the National Academy of Sciences.

[3]  Steven J. M. Jones,et al.  SNP discovery in black cottonwood (Populus trichocarpa) by population transcriptome resequencing , 2011, Molecular ecology resources.

[4]  Ryan D. Hernandez,et al.  Classic Selective Sweeps Were Rare in Recent Human Evolution , 2011, Science.

[5]  D. Neale,et al.  Forest tree genomics: growing resources and applications , 2011, Nature Reviews Genetics.

[6]  Mark F. Davis,et al.  Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. , 2010, The New phytologist.

[7]  Alkes L. Price,et al.  New approaches to population stratification in genome-wide association studies , 2010, Nature Reviews Genetics.

[8]  S. Strauss,et al.  Population substructure in continuous and fragmented stands of Populus trichocarpa , 2010, Heredity.

[9]  M. Goddard,et al.  Accurate Prediction of Genetic Values for Complex Traits by Whole-Genome Resequencing , 2010, Genetics.

[10]  P. Tiffin,et al.  Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). , 2010, The New phytologist.

[11]  S. Keller,et al.  Genomic diversity, population structure, and migration following rapid range expansion in the Balsam Poplar, Populus balsamifera , 2010, Molecular ecology.

[12]  Or Zuk,et al.  A Composite of Multiple Signals Distinguishes Causal Variants in Regions of Positive Selection , 2010, Science.

[13]  D. Neale,et al.  Populus Breeding: From the Classical to the Genomic Approach , 2010 .

[14]  G. Slavov,et al.  Salient Biological Features, Systematics, and Genetic Variation of Populus , 2010 .

[15]  A. Groover,et al.  Genetics and genomics of Populus , 2010 .

[16]  M. Metzker Sequencing technologies — the next generation , 2010, Nature Reviews Genetics.

[17]  Robert J. Elshire,et al.  A First-Generation Haplotype Map of Maize , 2009, Science.

[18]  John Novembre,et al.  Spatial patterns of variation due to natural selection in humans , 2009, Nature Reviews Genetics.

[19]  Sanzhen Liu,et al.  Mu Transposon Insertion Sites and Meiotic Recombination Events Co-Localize with Epigenetic Marks for Open Chromatin across the Maize Genome , 2009, PLoS genetics.

[20]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[21]  S. DiFazio,et al.  Extensive pollen flow in two ecologically contrasting populations of Populus trichocarpa , 2009, Molecular ecology.

[22]  Chris P. Tsokos,et al.  Mathematical Statistics with Applications , 2009 .

[23]  R. Durbin,et al.  Mapping Quality Scores Mapping Short Dna Sequencing Reads and Calling Variants Using P

, 2022 .

[24]  John Novembre,et al.  The Population Reference Sample, POPRES: a resource for population, disease, and pharmacological genetics research. , 2008, American journal of human genetics.

[25]  Pär K Ingvarsson,et al.  Multilocus Patterns of Nucleotide Polymorphism and the Demographic History of Populus tremula , 2008, Genetics.

[26]  Edward M. Rubin,et al.  Genomics of cellulosic biofuels , 2008, Nature.

[27]  Noah A Rosenberg,et al.  Mathematical properties of the r2 measure of linkage disequilibrium. , 2008, Theoretical population biology.

[28]  Montgomery Slatkin,et al.  Linkage disequilibrium — understanding the evolutionary past and mapping the medical future , 2008, Nature Reviews Genetics.

[29]  D. Neale,et al.  Population, quantitative and comparative genomics of adaptation in forest trees. , 2008, Current opinion in plant biology.

[30]  Detlef Weigel,et al.  Recombination and linkage disequilibrium in Arabidopsis thaliana , 2007, Nature Genetics.

[31]  Nicholas H. Putnam,et al.  A physical map of the highly heterozygous Populus genome: integration with the genome sequence and genetic map and analysis of haplotype variation. , 2007, The Plant journal : for cell and molecular biology.

[32]  Peter M Visscher,et al.  Recent human effective population size estimated from linkage disequilibrium. , 2007, Genome research.

[33]  T. Pyhäjärvi,et al.  Genomic diversity in forest trees. , 2007, Current opinion in plant biology.

[34]  D. Reich,et al.  Population Structure and Eigenanalysis , 2006, PLoS genetics.

[35]  M. Morgante,et al.  Multilocus Patterns of Nucleotide Diversity, Linkage Disequilibrium and Demographic History of Norway Spruce [Picea abies (L.) Karst] , 2006, Genetics.

[36]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[37]  D. Stram,et al.  An utter refutation of the ‘Fundamental Theorem of the HapMap’ by Terwilliger and Hiekkalinna , 2006, European Journal of Human Genetics.

[38]  A. Vasemägi The Adaptive Hypothesis of Clinal Variation Revisited: Single-Locus Clines as a Result of Spatially Restricted Gene Flow , 2006, Genetics.

[39]  D. Reich,et al.  Principal components analysis corrects for stratification in genome-wide association studies , 2006, Nature Genetics.

[40]  B. Potts,et al.  A framework for community and ecosystem genetics: from genes to ecosystems , 2006, Nature Reviews Genetics.

[41]  D. Neale,et al.  Forest-tree population genomics and adaptive evolution. , 2006, The New phytologist.

[42]  J. Terwilliger,et al.  An utter refutation of the ‘Fundamental Theorem of the HapMap’ , 2006, European Journal of Human Genetics.

[43]  S. Otto,et al.  Use of Ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa , 2006, Molecular ecology.

[44]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[45]  Garth R. Brown,et al.  DNA Sequence Variation and Selection of Tag Single-Nucleotide Polymorphisms at Candidate Genes for Drought-Stress Response in Pinus taeda L. , 2006, Genetics.

[46]  Zhaohui S. Qin,et al.  A comparison of phasing algorithms for trios and unrelated individuals. , 2006, American journal of human genetics.

[47]  Hadi Quesneville,et al.  Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination "hot spots". , 2005, Genome research.

[48]  D. Neale,et al.  Nucleotide Diversity and Linkage Disequilibrium in Cold-Hardiness- and Wood Quality-Related Candidate Genes in Douglas Fir , 2005, Genetics.

[49]  P. Donnelly,et al.  A Fine-Scale Map of Recombination Rates and Hotspots Across the Human Genome , 2005, Science.

[50]  M. Stephens,et al.  Accounting for Decay of Linkage Disequilibrium in Haplotype Inference and Missing-data Imputation , 2022 .

[51]  Dana C Crawford,et al.  Evidence for substantial fine-scale variation in recombination rates across the human genome , 2004, Nature Genetics.

[52]  P. Donnelly,et al.  The Fine-Scale Structure of Recombination Rate Variation in the Human Genome , 2004, Science.

[53]  Matthew A. Gitzendanner,et al.  Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America , 1997, Plant Systematics and Evolution.

[54]  J. Hamrick,et al.  Factors influencing levels of genetic diversity in woody plant species , 1992, New Forests.

[55]  M. Stephens,et al.  Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. , 2003, Genetics.

[56]  L. Lehmann,et al.  The population genetics of clonal and partially clonal diploids. , 2003, Genetics.

[57]  R. Petit,et al.  Glacial Refugia: Hotspots But Not Melting Pots of Genetic Diversity , 2003, Science.

[58]  P. Donnelly,et al.  A new statistical method for haplotype reconstruction from population data. , 2001, American journal of human genetics.

[59]  M. Nordborg,et al.  The effect of gene conversion on intralocus associations. , 1998, Genetics.

[60]  P. Green,et al.  Consed: a graphical tool for sequence finishing. , 1998, Genome research.

[61]  R. Stettler,et al.  Genetic variation and productivity of , 1998 .

[62]  D. Nickerson,et al.  PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. , 1997, Nucleic acids research.

[63]  F. Rousset Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. , 1997, Genetics.

[64]  M. Nei,et al.  A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. , 1990, Genetics.

[65]  B S Weir,et al.  Variances and covariances of squared linkage disequilibria in finite populations. , 1988, Theoretical population biology.

[66]  P. Heilman,et al.  Genetic variation and productivity of Populustrichocarpa and its hybrids. I. Morphology and phenology of 50 native clones , 1985 .

[67]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[68]  W. Reese,et al.  Atlas of United States Trees. Volume 1. Conifers and Important Hardwoods , 1972 .

[69]  E. L. Little Atlas of United States trees. , 1971 .

[70]  O. Correspondent Chloroplast DNA , 1967, Nature.

[71]  S. Wright THE INTERPRETATION OF POPULATION STRUCTURE BY F‐STATISTICS WITH SPECIAL REGARD TO SYSTEMS OF MATING , 1965 .

[72]  G. A. Leng ON POPULATION. , 1963, Singapore medical journal.