High-resolution mapping reveals hotspots and sex-biased recombination in Populus trichocarpa

Fine-scale meiotic recombination is fundamental to the outcome of natural and artificial selection. Here, dense genetic mapping and haplotype reconstruction were used to estimate recombination for a full factorial Populus trichocarpa cross of seven males and seven females. Genomes of the resulting 49 full-sib families (N=829 offspring) were re-sequenced, and high-fidelity biallelic SNP/INDELs and pedigree information were used to ascertain allelic phase and impute progeny genotypes to recover gametic haplotypes. The fourteen parental genetic maps contained 1820 SNP/INDELs on average that covered 376.7 Mb of physical length across 19 chromosomes. Comparison of parental and progeny haplotypes allowed fine-scale demarcation of cross-over (CO) regions, where 38,846 CO events in 1,658 gametes were observed. CO events were positively associated with gene density and negatively associated with GC content and long terminal repeats. One of the most striking findings was higher rates of COs in males in 8 out of 19 chromosomes. Regions with elevated male CO rates had lower gene density and GC content than windows showing no sex bias. High-resolution analysis identified 67 candidate CO hotspots spread throughout the genome. DNA sequence motifs enriched in these regions showed striking similarity to those of maize, Arabidopsis and wheat. These findings, and recombination estimates, will be useful for ongoing efforts to accelerate domestication of this and other biomass feedstocks, as well as future studies investigating broader questions related to evolutionary history, perennial development, phenology, wood formation, vegetative propagation, and dioecy that cannot be studied using annual plant model systems.

[1]  Qichao Lian,et al.  The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis , 2021, Proceedings of the National Academy of Sciences.

[2]  M. J. Neale,et al.  Meiosis and beyond – understanding the mechanistic and evolutionary processes shaping the germline genome , 2021, Biological reviews of the Cambridge Philosophical Society.

[3]  B. Kersten,et al.  The genetic basis of sex determination in Populus provides molecular markers across the genus and indicates convergent evolution , 2021, Silvae Genetica.

[4]  J. Schmutz,et al.  Sequencing and Analysis of the Sex Determination Region of Populus trichocarpa , 2020, Genes.

[5]  Joshua V. Peñalba,et al.  From molecules to populations: appreciating and estimating recombination rate variation , 2020, Nature Reviews Genetics.

[6]  Q. Cronk,et al.  Gene expression trajectories during male and female reproductive development in balsam poplar (Populus balsamifera L.) , 2020, Scientific Reports.

[7]  Mark F. Davis,et al.  Accurate determination of genotypic variance of cell wall characteristics of a Populus trichocarpa pedigree using high-throughput pyrolysis-molecular beam mass spectrometry , 2020, Biotechnology for Biofuels.

[8]  K. Edwards,et al.  Examining the Effects of Temperature on Recombination in Wheat , 2020, Frontiers in Plant Science.

[9]  I. Henderson,et al.  Interacting Genomic Landscapes of REC8-Cohesin, Chromatin, and Meiotic Recombination in Arabidopsis[CC-BY] , 2020, Plant Cell.

[10]  Jason M. Sardell,et al.  Sex Differences in the Recombination Landscape* , 2020, The American Naturalist.

[11]  Robert J. Schmitz,et al.  A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa , 2019, bioRxiv.

[12]  N. Street,et al.  Inferring the Genomic Landscape of Recombination Rate Variation in European Aspen (Populus tremula) , 2019, G3: Genes, Genomes, Genetics.

[13]  S. DiFazio,et al.  Phylogenomics of the genus Populus reveals extensive interspecific gene flow and balancing selection. , 2019, The New phytologist.

[14]  I. Henderson,et al.  An Ultra High-Density Arabidopsis thaliana Crossover Map That Refines the Influences of Structural Variation and Epigenetic Features , 2019, Genetics.

[15]  Minghui Wang,et al.  Diversity and Determinants of Meiotic Recombination Landscapes. , 2019, Trends in genetics : TIG.

[16]  Ajaya K. Biswal,et al.  Multitrait genome-wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits. , 2019, The New phytologist.

[17]  Qinghua Zhang,et al.  Single gametophyte sequencing reveals that crossover events differ between sexes in maize , 2019, Nature Communications.

[18]  A. Lloyd,et al.  Modelling Sex-Specific Crossover Patterning in Arabidopsis , 2018, Genetics.

[19]  T. Yin,et al.  High-density genetic map of Populus deltoides constructed by using specific length amplified fragment sequencing , 2018, Tree Genetics & Genomes.

[20]  J. Mudge,et al.  High-resolution crossover mapping reveals similarities and differences of male and female recombination in maize , 2018, Nature Communications.

[21]  Quiterie Haenel,et al.  Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics , 2018, Molecular ecology.

[22]  G. Copenhaver,et al.  Meiotic Recombination: Mixing It Up in Plants. , 2018, Annual review of plant biology.

[23]  Thomas J. Hardcastle,et al.  Nucleosomes and DNA methylation shape meiotic DSB frequency in Arabidopsis thaliana transposons and gene regulatory regions , 2018, Genome research.

[24]  P. Rastas,et al.  A High-Resolution Genetic Map for the Laboratory Rat , 2018, G3: Genes, Genomes, Genetics.

[25]  R. Camerini-Otero,et al.  Extensive sex differences at the initiation of genetic recombination , 2017, Nature.

[26]  B. Payseur,et al.  Connecting theory and data to understand recombination rate evolution , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  J. Uzunović,et al.  Coevolution between transposable elements and recombination , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  Peter J. Bradbury,et al.  Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize , 2017, Proceedings of the National Academy of Sciences.

[29]  B. Servin,et al.  High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism , 2017, Genetics.

[30]  Adam Auton,et al.  Refined genetic maps reveal sexual dimorphism in human meiotic recombination at multiple scales , 2017, Nature Communications.

[31]  S. Berlin,et al.  Allelic incompatibility can explain female biased sex ratios in dioecious plants , 2017, BMC Genomics.

[32]  F. C. H. Franklin,et al.  Understanding and Manipulating Meiotic Recombination in Plants[OPEN] , 2017, Plant Physiology.

[33]  M. Bink,et al.  A high-density, multi-parental SNP genetic map on apple validates a new mapping approach for outcrossing species , 2016, Horticulture Research.

[34]  Julian Lange,et al.  The Landscape of Mouse Meiotic Double-Strand Break Formation, Processing, and Repair , 2016, Cell.

[35]  R. Vaillancourt,et al.  Genome-wide variation in recombination rate in Eucalyptus , 2016, BMC Genomics.

[36]  R. Vaillancourt,et al.  Genome-wide variation in recombination rate in Eucalyptus , 2016, BMC Genomics.

[37]  Daniel L. Vera,et al.  Open chromatin reveals the functional maize genome , 2016, Proceedings of the National Academy of Sciences.

[38]  Douglas G. Scofield,et al.  Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species , 2015, Genetics.

[39]  O. Martin,et al.  Recombination patterns in maize reveal limits to crossover homeostasis , 2015, Proceedings of the National Academy of Sciences.

[40]  D. Grattapaglia,et al.  Genome-wide patterns of recombination, linkage disequilibrium and nucleotide diversity from pooled resequencing and single nucleotide polymorphism genotyping unlock the evolutionary history of Eucalyptus grandis. , 2015, The New phytologist.

[41]  Candida Nibau,et al.  The effect of temperature on the male and female recombination landscape of barley. , 2015, The New phytologist.

[42]  Gordon J Burleigh,et al.  The relationship of recombination rate, genome structure, and patterns of molecular evolution across angiosperms , 2015, BMC Evolutionary Biology.

[43]  N. Barkai,et al.  DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis[OPEN] , 2015, Plant Cell.

[44]  I. Henderson,et al.  Meiotic recombination hotspots - a comparative view. , 2015, The Plant journal : for cell and molecular biology.

[45]  C. Hefer,et al.  Recent Y chromosome divergence despite ancient origin of dioecy in poplars (Populus). , 2015, Molecular ecology.

[46]  Y. El-Kassaby,et al.  Using Populus as a lignocellulosic feedstock for bioethanol , 2015, Biotechnology journal.

[47]  Peter J. Bradbury,et al.  Recombination in diverse maize is stable, predictable, and associated with genetic load , 2015, Proceedings of the National Academy of Sciences.

[48]  C. Bastien,et al.  Potential for marker-assisted selection for forest tree breeding: lessons from 20 years of MAS in crops , 2014, Tree Genetics & Genomes.

[49]  Christophe Plomion,et al.  LPmerge: an R package for merging genetic maps by linear programming , 2014, Bioinform..

[50]  M. Stephens,et al.  fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets , 2014, Genetics.

[51]  Byung-Kwan Cho Genome Resequencing을 이용한 세균 적응진화연구 , 2014 .

[52]  F. Isik Genomic selection in forest tree breeding: the concept and an outlook to the future , 2014, New Forests.

[53]  O. Martin,et al.  Intraspecific variation of recombination rate in maize , 2013, Genome Biology.

[54]  Wendy S. Schackwitz,et al.  Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. , 2012, The New phytologist.

[55]  Krystyna A. Kelly,et al.  Epigenetic Remodeling of Meiotic Crossover Frequency in Arabidopsis thaliana DNA Methyltransferase Mutants , 2012, PLoS genetics.

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

[57]  Henry D. Priest,et al.  Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression , 2012, BMC Genomics.

[58]  Ruth Heller,et al.  False discovery rate controlling procedures for discrete tests , 2011, 1112.4627.

[59]  O. Martin,et al.  Genome-Wide Crossover Distribution in Arabidopsis thaliana Meiosis Reveals Sex-Specific Patterns along Chromosomes , 2011, PLoS genetics.

[60]  M. Noor,et al.  Recombination rate variation in closely related species , 2011, Heredity.

[61]  Kevin Brick,et al.  Genome-wide analysis reveals novel molecular features of mouse recombination hotspots , 2011, Nature.

[62]  C. Saintenac,et al.  Variation in crossover rates across a 3-Mb contig of bread wheat (Triticum aestivum) reveals the presence of a meiotic recombination hotspot , 2011, Chromosoma.

[63]  D. Grattapaglia,et al.  Genomic selection in forest tree breeding , 2011, Tree Genetics & Genomes.

[64]  G. Coop,et al.  Scrambling Eggs: Meiotic Drive and the Evolution of Female Recombination Rates , 2011, Genetics.

[65]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[66]  Xuan Zhu,et al.  A Hierarchical Combination of Factors Shapes the Genome-wide Topography of Yeast Meiotic Recombination Initiation , 2011, Cell.

[67]  Carl Kingsford,et al.  A fast, lock-free approach for efficient parallel counting of occurrences of k-mers , 2011, Bioinform..

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

[69]  A. Gylfason,et al.  Fine-scale recombination rate differences between sexes, populations and individuals , 2010, Nature.

[70]  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.

[71]  A. Ragauskas,et al.  Poplar as a feedstock for biofuels: A review of compositional characteristics , 2010 .

[72]  G. Coop,et al.  PRDM9 Is a Major Determinant of Meiotic Recombination Hotspots in Humans and Mice , 2010, Science.

[73]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[74]  Mikael Bodén,et al.  MEME Suite: tools for motif discovery and searching , 2009, Nucleic Acids Res..

[75]  E. Segal,et al.  Poly(da:dt) Tracts: Major Determinants of Nucleosome Organization This Review Comes from a Themed Issue on Protein-nucleic Acid Interactions Edited , 2022 .

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

[77]  Max Kuhn,et al.  Building Predictive Models in R Using the caret Package , 2008 .

[78]  Karl W Broman,et al.  Crossover interference underlies sex differences in recombination rates. , 2007, Trends in genetics : TIG.

[79]  A. Auton,et al.  Recombination rate estimation in the presence of hotspots. , 2007, Genome research.

[80]  Anete P. Souza,et al.  OneMap: software for genetic mapping in outcrossing species. , 2007, Hereditas.

[81]  O. Martin,et al.  Sex-Specific Crossover Distributions and Variations in Interference Level along Arabidopsis thaliana Chromosome 4 , 2007, PLoS genetics.

[82]  G. Mugnozza,et al.  Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait , 2007, Tree Genetics & Genomes.

[83]  R. Petit,et al.  Some Evolutionary Consequences of Being a Tree , 2006 .

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

[85]  C. Mézard,et al.  Meiotic recombination hotspots in plants. , 2006, Biochemical Society transactions.

[86]  Richard G. F. Visser,et al.  RECORD: a novel method for ordering loci on a genetic linkage map , 2005, Theoretical and Applied Genetics.

[87]  B. Charlesworth,et al.  Steps in the evolution of heteromorphic sex chromosomes , 2005, Heredity.

[88]  J. Dutheil,et al.  Recombination Difference between Sexes: A Role for Haploid Selection , 2005, PLoS biology.

[89]  S. Keeney,et al.  Where the crossovers are: recombination distributions in mammals , 2004, Nature Reviews Genetics.

[90]  Jody Hey,et al.  What's So Hot about Recombination Hotspots? , 2004, PLoS biology.

[91]  G. Tuskan,et al.  Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map , 2004, Theoretical and Applied Genetics.

[92]  Jinliang Wang,et al.  Sibship reconstruction from genetic data with typing errors. , 2004, Genetics.

[93]  R. Dawe,et al.  Four loci on abnormal chromosome 10 contribute to meiotic drive in maize. , 2003, Genetics.

[94]  T. Lenormand The evolution of sex dimorphism in recombination. , 2003, Genetics.

[95]  P. Hunt,et al.  Sex Matters in Meiosis , 2002, Science.

[96]  Rongling Wu,et al.  Molecular linkage maps of the Populus genome. , 2002, Genome.

[97]  R. Olmstead,et al.  The Importance of Emerging Model Systems in Plant Biology , 2000, Journal of Plant Growth Regulation.

[98]  Reinhart Ceulemans,et al.  Emerging Model Systems in Plant Biology: Poplar (Populus) as A Model Forest Tree , 2000, Journal of Plant Growth Regulation.

[99]  R. F. Stettler,et al.  Developmental quantitative genetics of growth in Populus , 1998, Theoretical and Applied Genetics.

[100]  R. Sederoff,et al.  Genetic mapping of quantitative trait loci controlling growth and wood quality traits in Eucalyptus grandis using a maternal half-sib family and RAPD markers. , 1996, Genetics.

[101]  C. Plomion,et al.  Recombination rate differences for pollen parents and seed parents in Pinus pinaster , 1996, Heredity.

[102]  B. Charlesworth,et al.  Recombination load associated with selection for increased recombination. , 1996, Genetical research.

[103]  A. Groover,et al.  Sex-Related Differences in Meiotic Recombination Frequency in Pinus taeda , 1995 .

[104]  M. Villar,et al.  Molecular genetics of growth and development in Populus. III. A genetic linkage map of a hybrid poplar composed of RFLP, STS, and RAPD markers , 1994, Theoretical and Applied Genetics.

[105]  G. Bell,et al.  Sex differences in recombination , 1991 .

[106]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[107]  John S. Campbell,et al.  Natural poplar hybrids from southern Alberta. I. Continuous variation for foliar characteristics , 1986 .

[108]  J. Felsenstein The evolutionary advantage of recombination. , 1974, Genetics.

[109]  W. G. Hill,et al.  The effect of linkage on limits to artificial selection. , 1966, Genetical research.

[110]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[111]  Michael P. Fay,et al.  Two-sided Exact Tests and Matching Confidence Intervals for Discrete Data , 2010, R J..

[112]  J. Dvorak,et al.  Recombination: an underappreciated factor in the evolution of plant genomes , 2007, Nature Reviews Genetics.

[113]  G. Coop,et al.  Sequencing and Analysis of , 2006 .

[114]  R. H.J.MULLE THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE , 2002 .

[115]  P. VanRaden,et al.  Designs of reference families for the construction of genetic linkage maps. , 1998, Animal biotechnology.

[116]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[117]  A. Hilliker,et al.  Greater meiotic recombination in male vs. female gametes in Pinus radiata , 1983 .

[118]  R. Khesin,et al.  Molecular Genetics , 1968, Springer Berlin Heidelberg.

[119]  I. Bogdanov [Synaptonemal complex]. , 1971, Tsitologiia.