Population genomics of the eastern cottonwood ( Populus deltoides )
Abstract
Abstract Despite its economic importance as a bioenergy crop and key role in riparian ecosystems, little is known about genetic diversity and adaptation of the eastern cottonwood ( Populus deltoides ). Here, we report the first population genomics study for this species, conducted on a sample of 425 unrelated individuals collected in 13 states of the southeastern United States. The trees were genotyped by targeted resequencing of 18,153 genes and 23,835 intergenic regions, followed by the identification of single nucleotide polymorphisms ( SNP s). This natural P. deltoides population showed low levels of subpopulation differentiation ( F ST = 0.022–0.106), high genetic diversity (θ W = 0.00100, π = 0.00170), a large effective population size ( N e ≈ 32,900), and low to moderate levels of linkage disequilibrium. Additionally, genomewide scans for selection (Tajima's D ), subpopulation differentiation ( X T X ), and environmental association analyses with eleven climate variables carried out with two different methods ( LFMM and BAYENV 2) identified genes putatively involved in local adaptation. Interestingly, many of these genes were also identified as adaptation candidates in another poplar species, Populus trichocarpa , indicating possible convergent evolution. This study constitutes the first assessment of genetic diversity and local adaptation inmore »
- Authors:
-
- School of Forest Resources and Conservation University of Florida Gainesville FL USA, Plant Molecular and Cellular Biology Graduate Program University of Florida Gainesville FL USA
- Horticultural Sciences Department University of Florida Gainesville FL USA
- School of Forest Resources and Conservation University of Florida Gainesville FL USA
- Biology Department University of Florida Gainesville FL USA
- Biology Department University of Florida Gainesville FL USA, University of Florida Genetics Institute University of Florida Gainesville FL USA
- School of Forest Resources and Conservation University of Florida Gainesville FL USA, University of Florida Genetics Institute University of Florida Gainesville FL USA
- Publication Date:
- Research Org.:
- Univ. of Florida, Gainesville, FL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1398844
- Alternate Identifier(s):
- OSTI ID: 1398845; OSTI ID: 1508795
- Grant/Contract Number:
- FG02-05ER64114; SC0003893
- Resource Type:
- Published Article
- Journal Name:
- Ecology and Evolution
- Additional Journal Information:
- Journal Name: Ecology and Evolution Journal Volume: 7 Journal Issue: 22; Journal ID: ISSN 2045-7758
- Publisher:
- Wiley Blackwell (John Wiley & Sons)
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; eastern cottonwood; exome capture; genetic diversity; local adaptation; population structure; Populus deltoides
Citation Formats
Fahrenkrog, Annette M., Neves, Leandro G., Resende, Jr, Márcio F. R., Dervinis, Christopher, Davenport, Ruth, Barbazuk, W. Brad, and Kirst, Matias. Population genomics of the eastern cottonwood ( Populus deltoides ). United Kingdom: N. p., 2017.
Web. doi:10.1002/ece3.3466.
Fahrenkrog, Annette M., Neves, Leandro G., Resende, Jr, Márcio F. R., Dervinis, Christopher, Davenport, Ruth, Barbazuk, W. Brad, & Kirst, Matias. Population genomics of the eastern cottonwood ( Populus deltoides ). United Kingdom. https://doi.org/10.1002/ece3.3466
Fahrenkrog, Annette M., Neves, Leandro G., Resende, Jr, Márcio F. R., Dervinis, Christopher, Davenport, Ruth, Barbazuk, W. Brad, and Kirst, Matias. Tue .
"Population genomics of the eastern cottonwood ( Populus deltoides )". United Kingdom. https://doi.org/10.1002/ece3.3466.
@article{osti_1398844,
title = {Population genomics of the eastern cottonwood ( Populus deltoides )},
author = {Fahrenkrog, Annette M. and Neves, Leandro G. and Resende, Jr, Márcio F. R. and Dervinis, Christopher and Davenport, Ruth and Barbazuk, W. Brad and Kirst, Matias},
abstractNote = {Abstract Despite its economic importance as a bioenergy crop and key role in riparian ecosystems, little is known about genetic diversity and adaptation of the eastern cottonwood ( Populus deltoides ). Here, we report the first population genomics study for this species, conducted on a sample of 425 unrelated individuals collected in 13 states of the southeastern United States. The trees were genotyped by targeted resequencing of 18,153 genes and 23,835 intergenic regions, followed by the identification of single nucleotide polymorphisms ( SNP s). This natural P. deltoides population showed low levels of subpopulation differentiation ( F ST = 0.022–0.106), high genetic diversity (θ W = 0.00100, π = 0.00170), a large effective population size ( N e ≈ 32,900), and low to moderate levels of linkage disequilibrium. Additionally, genomewide scans for selection (Tajima's D ), subpopulation differentiation ( X T X ), and environmental association analyses with eleven climate variables carried out with two different methods ( LFMM and BAYENV 2) identified genes putatively involved in local adaptation. Interestingly, many of these genes were also identified as adaptation candidates in another poplar species, Populus trichocarpa , indicating possible convergent evolution. This study constitutes the first assessment of genetic diversity and local adaptation in P. deltoides throughout the southern part of its range, information we expect to be of use to guide management and breeding strategies for this species in future, especially in the face of climate change.},
doi = {10.1002/ece3.3466},
journal = {Ecology and Evolution},
number = 22,
volume = 7,
place = {United Kingdom},
year = {Tue Oct 10 00:00:00 EDT 2017},
month = {Tue Oct 10 00:00:00 EDT 2017}
}
https://doi.org/10.1002/ece3.3466
Web of Science
Works referenced in this record:
FAST-TRACK: Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis): INTEGRATING QTL MAPPING AND GENOME SCANS
journal, December 2004
- Rogers, S. M.; Bernatchez, L.
- Molecular Ecology, Vol. 14, Issue 2
Populus: Arabidopsis for Forestry. Do We Need a Model Tree?
journal, October 2002
- Taylor, G.
- Annals of Botany, Vol. 90, Issue 6
Molecular Signatures of Natural Selection
journal, December 2005
- Nielsen, Rasmus
- Annual Review of Genetics, Vol. 39, Issue 1
Mathematical model for studying genetic variation in terms of restriction endonucleases.
journal, October 1979
- Nei, M.; Li, W. H.
- Proceedings of the National Academy of Sciences, Vol. 76, Issue 10
Nucleotide Polymorphism, Linkage Disequilibrium and Complex Trait Dissection in Populus
book, December 2009
- Ingvarson, Pär K.
- Genetics and Genomics of Populus
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline
journal, October 2013
- Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher
- Current Protocols in Bioinformatics, Vol. 43, Issue 1
A resource for characterizing genome-wide binding and putative target genes of transcription factors expressed during secondary growth and wood formation in Populus
journal, May 2015
- Liu, Lijun; Ramsay, Trevor; Zinkgraf, Matthew
- The Plant Journal, Vol. 82, Issue 5
Evidence for extensive parallelism but divergent genomic architecture of adaptation along altitudinal and latitudinal gradients in P opulus trichocarpa
journal, September 2015
- Holliday, Jason A.; Zhou, Lecong; Bawa, Rajesh
- New Phytologist, Vol. 209, Issue 3
The Populus Genome Integrative Explorer (PopGenIE): a new resource for exploring the Populus genome
journal, March 2009
- Sjödin, Andreas; Street, Nathaniel Robert; Sandberg, Göran
- New Phytologist, Vol. 182, Issue 4
MOSAIK: A Hash-Based Algorithm for Accurate Next-Generation Sequencing Short-Read Mapping
journal, March 2014
- Lee, Wan-Ping; Stromberg, Michael P.; Ward, Alistair
- PLoS ONE, Vol. 9, Issue 3
Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate
journal, March 2013
- Sork, V. L.; Aitken, S. N.; Dyer, R. J.
- Tree Genetics & Genomes, Vol. 9, Issue 4
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses
journal, September 2007
- Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe
- The American Journal of Human Genetics, Vol. 81, Issue 3
PopGenome: An Efficient Swiss Army Knife for Population Genomic Analyses in R
journal, April 2014
- Pfeifer, Bastian; Wittelsbürger, Ulrich; Ramos-Onsins, Sebastian E.
- Molecular Biology and Evolution, Vol. 31, Issue 7
The effect of deleterious mutations on neutral molecular variation.
journal, August 1993
- Charlesworth, B.; Morgan, M. T.; Charlesworth, D.
- Genetics, Vol. 134, Issue 4
Nucleotide diversity among natural populations of a North American poplar ( Populus balsamifera , Salicaceae)
journal, April 2009
- Breen, Amy L.; Glenn, Elise; Yeager, Adam
- New Phytologist, Vol. 182, Issue 3
4P: fast computing of population genetics statistics from large DNA polymorphism panels
journal, December 2014
- Benazzo, Andrea; Panziera, Alex; Bertorelle, Giorgio
- Ecology and Evolution, Vol. 5, Issue 1
Robust Identification of Local Adaptation from Allele Frequencies
journal, July 2013
- Günther, Torsten; Coop, Graham
- Genetics, Vol. 195, Issue 1
The relative power of genome scans to detect local adaptation depends on sampling design and statistical method
journal, February 2015
- Lotterhos, Katie E.; Whitlock, Michael C.
- Molecular Ecology, Vol. 24, Issue 5
Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species
journal, September 2012
- Stölting, Kai N.; Nipper, Rick; Lindtke, Dorothea
- Molecular Ecology, Vol. 22, Issue 3
Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem
journal, September 2010
- Wegrzyn, Jill L.; Eckert, Andrew J.; Choi, Minyoung
- New Phytologist, Vol. 188, Issue 2
Genomewide patterns of variation in genetic diversity are shared among populations, species and higher-order taxa
journal, June 2017
- Vijay, Nagarjun; Weissensteiner, Matthias; Burri, Reto
- Molecular Ecology, Vol. 26, Issue 16
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014
- Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
- Nature Genetics, Vol. 46, Issue 10
Affinity Purification of the Arabidopsis 26 S Proteasome Reveals a Diverse Array of Plant Proteolytic Complexes
journal, June 2010
- Book, Adam J.; Gladman, Nicholas P.; Lee, Sang-Sook
- Journal of Biological Chemistry, Vol. 285, Issue 33
The Arabidopsis BEL1-LIKE HOMEODOMAIN Proteins SAW1 and SAW2 Act Redundantly to Regulate KNOX Expression Spatially in Leaf Margins
journal, September 2007
- Kumar, Ravi; Kushalappa, Kumuda; Godt, Dietmute
- The Plant Cell, Vol. 19, Issue 9
FactoMineR : An R Package for Multivariate Analysis
journal, January 2008
- Lê, Sébastien; Josse, Julie; Husson, François
- Journal of Statistical Software, Vol. 25, Issue 1
Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa
journal, April 2014
- McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D.
- New Phytologist, Vol. 203, Issue 2
Network analysis reveals the relationship among wood properties, gene expression levels and genotypes of natural Populus trichocarpa accessions
journal, July 2013
- Porth, Ilga; Klápště, Jaroslav; Skyba, Oleksandr
- New Phytologist, Vol. 200, Issue 3
Nucleotide diversity and linkage disequilibrium in Populus nigra cinnamyl alcohol dehydrogenase (CAD4) gene
journal, April 2011
- Marroni, Fabio; Pinosio, Sara; Zaina, Giusi
- Tree Genetics & Genomes, Vol. 7, Issue 5
LANDSCAPE GENOMICS OF POPULUS TRICHOCARPA : THE ROLE OF HYBRIDIZATION, LIMITED GENE FLOW, AND NATURAL SELECTION IN SHAPING PATTERNS OF POPULATION STRUCTURE : POPULATION DIFFERENTIATION IN
journal, September 2014
- Geraldes, Armando; Farzaneh, Nima; Grassa, Christopher J.
- Evolution, Vol. 68, Issue 11
Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms
journal, July 2013
- Porth, Ilga; Klapšte, Jaroslav; Skyba, Oleksandr
- New Phytologist, Vol. 200, Issue 3, p. 710-726
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data
journal, September 2011
- Li, H.
- Bioinformatics, Vol. 27, Issue 21
Ecological genomics of local adaptation
journal, October 2013
- Savolainen, Outi; Lascoux, Martin; Merilä, Juha
- Nature Reviews Genetics, Vol. 14, Issue 11
Evaluation of demographic history and neutral parameterization on the performance of F ST outlier tests
journal, April 2014
- Lotterhos, Katie E.; Whitlock, Michael C.
- Molecular Ecology, Vol. 23, Issue 9
Whole-genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep
journal, November 2015
- Kardos, Marty; Luikart, Gordon; Bunch, Rowan
- Molecular Ecology, Vol. 24, Issue 22
Determinants of genetic diversity
journal, June 2016
- Ellegren, Hans; Galtier, Nicolas
- Nature Reviews Genetics, Vol. 17, Issue 7
WD40 proteins propel cellular networks
journal, October 2010
- Stirnimann, Christian U.; Petsalaki, Evangelia; Russell, Robert B.
- Trends in Biochemical Sciences, Vol. 35, Issue 10
Genome-wide patterns of differentiation and spatially varying selection between postglacial recolonization lineages of Populus alba (Salicaceae), a widespread forest tree
journal, March 2015
- Stölting, Kai N.; Paris, Margot; Meier, Cécile
- New Phytologist, Vol. 207, Issue 3
Comparative SNP and Haplotype Analysis Reveals a Higher Genetic Diversity and Rapider LD Decay in Tropical than Temperate Germplasm in Maize
journal, September 2011
- Lu, Yanli; Shah, Trushar; Hao, Zhuanfang
- PLoS ONE, Vol. 6, Issue 9
Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa
journal, August 2012
- Slavov, Gancho T.; DiFazio, Stephen P.; Martin, Joel
- New Phytologist, Vol. 196, Issue 3, p. 713-725
Pervasive selection or is it…? why are F ST outliers sometimes so frequent?
journal, April 2013
- Bierne, Nicolas; Roze, Denis; Welch, John J.
- Molecular Ecology, Vol. 22, Issue 8
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
Variation in Linked Selection and Recombination Drive Genomic Divergence during Allopatric Speciation of European and American Aspens
journal, March 2016
- Wang, Jing; Street, Nathaniel R.; Scofield, Douglas G.
- Molecular Biology and Evolution, Vol. 33, Issue 7
On the number of segregating sites in genetical models without recombination
journal, April 1975
- Watterson, G. A.
- Theoretical Population Biology, Vol. 7, Issue 2
The mRNA decay factor PAT 1 functions in a pathway including MAP kinase 4 and immune receptor SUMM 2
journal, January 2015
- Roux, Milena Edna; Rasmussen, Magnus Wohlfahrt; Palma, Kristoffer
- The EMBO Journal, Vol. 34, Issue 5
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits
journal, February 2007
- Stinchcombe, J. R.; Hoekstra, H. E.
- Heredity, Vol. 100, Issue 2
Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa
journal, November 2013
- McKown, Athena D.; Guy, Robert D.; Klápště, Jaroslav
- New Phytologist, Vol. 201, Issue 4
Correcting Estimators of θ and Tajima's D for Ascertainment Biases Caused by the Single-Nucleotide Polymorphism Discovery Process
journal, December 2008
- Ramírez-Soriano, Anna; Nielsen, Rasmus
- Genetics, Vol. 181, Issue 2
Carbon sequestration: Managing forests in uncertain times
journal, February 2014
- Bellassen, Valentin; Luyssaert, Sebastiaan
- Nature, Vol. 506, Issue 7487
Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species
journal, December 2015
- Wang, J.; Street, N. R.; Scofield, D. G.
- Genetics, Vol. 202, Issue 3
Genome-wide scans for footprints of natural selection
journal, January 2010
- Oleksyk, Taras K.; Smith, Michael W.; O'Brien, Stephen J.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1537
Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study
journal, February 2013
- Vanholme, Bartel; Cesarino, Igor; Goeminne, Geert
- New Phytologist, Vol. 198, Issue 3
Conditions Under Which Genome-Wide Association Studies Will be Positively Misleading
journal, September 2010
- Platt, Alexander; Vilhjálmsson, Bjarni J.; Nordborg, Magnus
- Genetics, Vol. 186, Issue 3
Structure of linkage disequilibrium and phenotypic associations in the maize genome
journal, September 2001
- Remington, D. L.; Thornsberry, J. M.; Matsuoka, Y.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
Effective filtering strategies to improve data quality from population-based whole exome sequencing studies
journal, January 2014
- Carson, Andrew R.; Smith, Erin N.; Matsui, Hiroko
- BMC Bioinformatics, Vol. 15, Issue 1
Genome-wide association study reveals putative regulators of bioenergy traits in Populus deltoides
journal, September 2016
- Fahrenkrog, Annette M.; Neves, Leandro G.; Resende, Márcio F. R.
- New Phytologist, Vol. 213, Issue 2
Towards integration of population and comparative genomics in forest trees
journal, August 2016
- Ingvarsson, Pär K.; Hvidsten, Torgeir R.; Street, Nathaniel R.
- New Phytologist, Vol. 212, Issue 2
Testing for Associations between Loci and Environmental Gradients Using Latent Factor Mixed Models
journal, March 2013
- Frichot, Eric; Schoville, Sean D.; Bouchard, Guillaume
- Molecular Biology and Evolution, Vol. 30, Issue 7
Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow
journal, June 2014
- Cruickshank, Tami E.; Hahn, Matthew W.
- Molecular Ecology, Vol. 23, Issue 13
Recent Y chromosome divergence despite ancient origin of dioecy in poplars ( Populus )
journal, April 2015
- Geraldes, A.; Hefer, C. A.; Capron, A.
- Molecular Ecology, Vol. 24, Issue 13
Exome resequencing reveals signatures of demographic and adaptive processes across the genome and range of black cottonwood ( Populus trichocarpa )
journal, May 2014
- Zhou, L.; Bawa, R.; Holliday, J. A.
- Molecular Ecology, Vol. 23, Issue 10
A practical guide to environmental association analysis in landscape genomics
journal, August 2015
- Rellstab, Christian; Gugerli, Felix; Eckert, Andrew J.
- Molecular Ecology, Vol. 24, Issue 17
Multilocus Patterns of Nucleotide Polymorphism and the Demographic History of Populus tremula
journal, August 2008
- Ingvarsson, Pär K.
- Genetics, Vol. 180, Issue 1
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010
- McKenna, A.; Hanna, M.; Banks, E.
- Genome Research, Vol. 20, Issue 9
Evolutionary Quantitative Genomics of Populus trichocarpa
journal, November 2015
- Porth, Ilga; Klápště, Jaroslav; McKown, Athena D.
- PLOS ONE, Vol. 10, Issue 11
Postglacial history of a widespread conifer produces inverse clines in selective neutrality tests: POSTGLACIAL HISTORY OF SITKA SPRUCE
journal, August 2010
- Holliday, J. A.; Yuen, M.; Ritland, K.
- Molecular Ecology, Vol. 19, Issue 18
How much of the Variation in Adaptive Divergence can be Explained by gene Flow? an Evaluation Using Lake-Stream Stickleback Pairs
journal, October 2004
- Hendry, Andrew P.; Taylor, Eric B.
- Evolution, Vol. 58, Issue 10
The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem
journal, March 2016
- Puechmaille, Sebastien J.
- Molecular Ecology Resources, Vol. 16, Issue 3
Recombination and the power of statistical tests of neutrality
journal, August 1999
- Wall, Jeffrey D.
- Genetical Research, Vol. 74, Issue 1
Demographic History Has Influenced Nucleotide Diversity in European Pinus sylvestris Populations
journal, November 2007
- Pyhäjärvi, Tanja; García-Gil, M. Rosario; Knürr, Timo
- Genetics, Vol. 177, Issue 3
NADP-malic enzyme from plants
journal, June 1992
- Gerald E., Edwards; Carlos S., Andreo
- Phytochemistry, Vol. 31, Issue 6
Genetics in geographically structured populations: defining, estimating and interpreting FST
journal, September 2009
- Holsinger, Kent E.; Weir, Bruce S.
- Nature Reviews Genetics, Vol. 10, Issue 9
Convergent local adaptation to climate in distantly related conifers
journal, September 2016
- Yeaman, S.; Hodgins, K. A.; Lotterhos, K. E.
- Science, Vol. 353, Issue 6306
Molecular evidence for glacial refugia of mountain plants in the European Alps
journal, October 2005
- Schonswetter, P.; Stehlik, I.; Holderegger, R.
- Molecular Ecology, Vol. 14, Issue 11
Adaptation, migration or extirpation: climate change outcomes for tree populations: Climate change outcomes for tree populations
journal, January 2008
- Aitken, Sally N.; Yeaman, Sam; Holliday, Jason A.
- Evolutionary Applications, Vol. 1, Issue 1
Comparative phylogeography of unglaciated eastern North America: PHYLOGEOGRAPHY OF UNGLACIATED EASTERN NORTH AMERICA
journal, November 2006
- Soltis, Douglas E.; Morris, Ashley B.; McLACHLAN, Jason S.
- Molecular Ecology, Vol. 15, Issue 14
Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion
journal, January 2009
- Bhuiyan, N. H.; Selvaraj, G.; Wei, Y.
- Journal of Experimental Botany, Vol. 60, Issue 2
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w
journal, April 2012
- Cingolani, Pablo; Platts, Adrian; Wang, Le Lily
- Fly, Vol. 6, Issue 2