skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa

Abstract

Populus trichocarpa is an important forest tree species for the generation of lignocellulosic ethanol. Understanding the genomic basis of biomass production and chemical composition of wood is fundamental in supporting genetic improvement programs. Considerable variation has been observed in this species for complex traits related to growth, phenology, ecophysiology and wood chemistry. Those traits are influenced by both polygenic control and environmental effects, and their genome architecture and regulation are only partially understood. Genome wide association studies (GWAS) represent an approach to advance that aim using thousands of single nucleotide polymorphisms (SNPs). Genotyping using exome capture methodologies represent an efficient approach to identify specific functional regions of genomes underlying phenotypic variation. We identified 813 K SNPs, which were utilized for genotyping 461 P. trichocarpa clones, representing 101 provenances collected from Oregon and Washington, and established in California. A GWAS performed on 20 traits, considering single SNP-marker tests identified a variable number of significant SNPs ( p-value < 6.1479E-8) in association with diameter, height, leaf carbon and nitrogen contents, and δ 15N. The number of significant SNPs ranged from 2 to 220 per trait. Additionally, multiple-marker analyses by sliding-windows tests detected between 6 and 192 significant windows for the analyzed traits.more » The significant SNPs resided within genes that encode proteins belonging to different functional classes as such protein synthesis, energy/metabolism and DNA/RNA metabolism, among others. SNP-markers within genes associated with traits of importance for biomass production were detected. They contribute to characterize the genomic architecture of P. trichocarpa biomass required to support the development and application of marker breeding technologies.« less

Authors:
 [1];  [2];  [2];  [3];  [3];  [3];  [4];  [4];  [5]; ORCiD logo [5];  [3]
  1. Univ. of California, Davis, CA (United States); Univ. de Talca, Talca (Chile)
  2. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
  3. Univ. of California, Davis, CA (United States)
  4. GreenWood Resources, Portland, OR (United States)
  5. National Renewable Energy Lab. (NREL), Golden, CO (United States)
Publication Date:
Research Org.:
National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1578253
Report Number(s):
NREL/JA-2700-74675
Journal ID: ISSN 1471-2164
Grant/Contract Number:  
AC36-08GO28308
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; populus; GWAS; sequence capture; growth; stable isotopes; lignin; cellulose; wood metabolome

Citation Formats

Guerra, Fernando P., Suren, Haktan, Holliday, Jason, Richards, James H., Fiehn, Oliver, Famula, Randi, Stanton, Brian J., Shuren, Richard, Sykes, Robert W., Davis, Mark F., and Neale, David B. Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa. United States: N. p., 2019. Web. doi:10.1186/s12864-019-6160-9.
Guerra, Fernando P., Suren, Haktan, Holliday, Jason, Richards, James H., Fiehn, Oliver, Famula, Randi, Stanton, Brian J., Shuren, Richard, Sykes, Robert W., Davis, Mark F., & Neale, David B. Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa. United States. doi:10.1186/s12864-019-6160-9.
Guerra, Fernando P., Suren, Haktan, Holliday, Jason, Richards, James H., Fiehn, Oliver, Famula, Randi, Stanton, Brian J., Shuren, Richard, Sykes, Robert W., Davis, Mark F., and Neale, David B. Wed . "Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa". United States. doi:10.1186/s12864-019-6160-9. https://www.osti.gov/servlets/purl/1578253.
@article{osti_1578253,
title = {Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa},
author = {Guerra, Fernando P. and Suren, Haktan and Holliday, Jason and Richards, James H. and Fiehn, Oliver and Famula, Randi and Stanton, Brian J. and Shuren, Richard and Sykes, Robert W. and Davis, Mark F. and Neale, David B.},
abstractNote = {Populus trichocarpa is an important forest tree species for the generation of lignocellulosic ethanol. Understanding the genomic basis of biomass production and chemical composition of wood is fundamental in supporting genetic improvement programs. Considerable variation has been observed in this species for complex traits related to growth, phenology, ecophysiology and wood chemistry. Those traits are influenced by both polygenic control and environmental effects, and their genome architecture and regulation are only partially understood. Genome wide association studies (GWAS) represent an approach to advance that aim using thousands of single nucleotide polymorphisms (SNPs). Genotyping using exome capture methodologies represent an efficient approach to identify specific functional regions of genomes underlying phenotypic variation. We identified 813 K SNPs, which were utilized for genotyping 461 P. trichocarpa clones, representing 101 provenances collected from Oregon and Washington, and established in California. A GWAS performed on 20 traits, considering single SNP-marker tests identified a variable number of significant SNPs (p-value < 6.1479E-8) in association with diameter, height, leaf carbon and nitrogen contents, and δ15N. The number of significant SNPs ranged from 2 to 220 per trait. Additionally, multiple-marker analyses by sliding-windows tests detected between 6 and 192 significant windows for the analyzed traits. The significant SNPs resided within genes that encode proteins belonging to different functional classes as such protein synthesis, energy/metabolism and DNA/RNA metabolism, among others. SNP-markers within genes associated with traits of importance for biomass production were detected. They contribute to characterize the genomic architecture of P. trichocarpa biomass required to support the development and application of marker breeding technologies.},
doi = {10.1186/s12864-019-6160-9},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United States},
year = {2019},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Using Populus as a lignocellulosic feedstock for bioethanol
journal, February 2015


Ecophysiology of short rotation forest crops
journal, January 1992


Analysis of the genetic variation in growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa provenances
journal, January 2016

  • Guerra, Fernando P.; Richards, James H.; Fiehn, Oliver
  • Tree Genetics & Genomes, Vol. 12, Issue 1
  • DOI: 10.1007/s11295-015-0965-8

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
  • DOI: 10.1111/nph.12601

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
  • DOI: 10.1038/ng.3075

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
  • DOI: 10.1111/nph.12419

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
  • DOI: 10.1111/nph.12422

Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations
journal, December 2012

  • Porth, Ilga; Klápště, Jaroslav; Skyba, Oleksandr
  • New Phytologist, Vol. 197, Issue 3, p. 777-790
  • DOI: 10.1111/nph.12014

Production physiology and morphology of Populus species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones
journal, March 1997

  • Scaracia-Mugnozza, G. E.; Ceulemans, R.; Heilman, P. E.
  • Canadian Journal of Forest Research, Vol. 27, Issue 3
  • DOI: 10.1139/x96-180

Biomass equations and carbon content of aboveground leafless biomass of hybrid poplar in Coastal British Columbia
journal, March 2006


Ecological genomics of variation in bud-break phenology and mechanisms of response to climate warming in Populus trichocarpa
journal, July 2018

  • McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D.
  • New Phytologist, Vol. 220, Issue 1
  • DOI: 10.1111/nph.15273

Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
journal, April 2019

  • Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David
  • New Phytologist, Vol. 223, Issue 1
  • DOI: 10.1111/nph.15777

Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs
journal, November 2014

  • McKown, Athena D.; Guy, Robert D.; Quamme, Linda
  • Molecular Ecology, Vol. 23, Issue 23
  • DOI: 10.1111/mec.12969

Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem
journal, September 2010


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
  • DOI: 10.1111/nph.12815

Association genetics of chemical wood properties in black poplar ( Populus nigra )
journal, November 2012

  • Guerra, Fernando P.; Wegrzyn, Jill L.; Sykes, Robert
  • New Phytologist, Vol. 197, Issue 1
  • DOI: 10.1111/nph.12003

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
  • DOI: 10.1111/nph.14154

Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing
journal, February 2009

  • Gnirke, Andreas; Melnikov, Alexandre; Maguire, Jared
  • Nature Biotechnology, Vol. 27, Issue 2
  • DOI: 10.1038/nbt.1523

From Genomes to GENE-omes: Exome Sequencing Concept and Applications in Crop Improvement
journal, December 2017


Targeted enrichment of the black cottonwood (Populus trichocarpa) gene space using sequence capture
journal, January 2012


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
  • DOI: 10.1111/nph.13643

High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus
journal, January 2015


Genome sequence and genetic diversity of European ash trees
journal, December 2016

  • Sollars, Elizabeth S. A.; Harper, Andrea L.; Kelly, Laura J.
  • Nature, Vol. 541, Issue 7636
  • DOI: 10.1038/nature20786

Genetic diversity, linkage disequilibrium, population structure and construction of a core collection of Prunus avium L. landraces and bred cultivars
journal, February 2016

  • Campoy, José Antonio; Lerigoleur-Balsemin, Emilie; Christmann, Hélène
  • BMC Plant Biology, Vol. 16, Issue 1
  • DOI: 10.1186/s12870-016-0712-9

Genomic prediction in contrast to a genome-wide association study in explaining heritable variation of complex growth traits in breeding populations of Eucalyptus
journal, July 2017

  • Müller, Bárbara S. F.; Neves, Leandro G.; de Almeida Filho, Janeo E.
  • BMC Genomics, Vol. 18, Issue 1
  • DOI: 10.1186/s12864-017-3920-2

Genomic selection in forest tree breeding: the concept and an outlook to the future
journal, March 2014


Maize Leaf Epiphytic Bacteria Diversity Patterns Are Genetically Correlated with Resistance to Fungal Pathogen Infection
journal, April 2010

  • Balint-Kurti, Peter; Simmons, Susan J.; Blum, James E.
  • Molecular Plant-Microbe Interactions, Vol. 23, Issue 4
  • DOI: 10.1094/MPMI-23-4-0473

Relaxed Significance Criteria for Linkage Analysis
journal, June 2006


Fast implementation of a scan statistic for identifying chromosomal patterns of genome wide association studies
journal, March 2009

  • Sun, Yan V.; Jacobsen, Douglas M.; Turner, Stephen T.
  • Computational Statistics & Data Analysis, Vol. 53, Issue 5
  • DOI: 10.1016/j.csda.2008.04.013

A scan statistic for identifying chromosomal patterns of SNP association
journal, November 2006

  • Sun, Yan V.; Levin, Albert M.; Boerwinkle, Eric
  • Genetic Epidemiology, Vol. 30, Issue 7
  • DOI: 10.1002/gepi.20173

Regression models, scan statistics and reappearance probabilities to detect regions of association between gene expression and copy number
journal, February 2011

  • Asimit, Jennifer L.; Andrulis, Irene L.; Bull, Shelley B.
  • Statistics in Medicine, Vol. 30, Issue 10
  • DOI: 10.1002/sim.4193

Structural and biochemical studies of the 5′→3′ exoribonuclease Xrn1
journal, February 2011

  • Chang, Jeong Ho; Xiang, Song; Xiang, Kehui
  • Nature Structural & Molecular Biology, Vol. 18, Issue 3
  • DOI: 10.1038/nsmb.1984

The Exoribonuclease XRN4 Is a Component of the Ethylene Response Pathway in Arabidopsis
journal, November 2006

  • Potuschak, Thomas; Vansiri, Amérin; Binder, Brad M.
  • The Plant Cell, Vol. 18, Issue 11
  • DOI: 10.1105/tpc.106.046508

XRN4 and LARP1 Are Required for a Heat-Triggered mRNA Decay Pathway Involved in Plant Acclimation and Survival during Thermal Stress
journal, December 2013


Activation of 5'-3' exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast
journal, May 2012

  • Sinturel, F.; Brechemier-Baey, D.; Kiledjian, M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 21
  • DOI: 10.1073/pnas.1120090109

Plant δ 15 N Correlates with the Transpiration Efficiency of Nitrogen Acquisition in Tropical Trees
journal, September 2009

  • Cernusak, Lucas A.; Winter, Klaus; Turner, Benjamin L.
  • Plant Physiology, Vol. 151, Issue 3
  • DOI: 10.1104/pp.109.145870

The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana
journal, July 2013

  • Easlon, Hsien Ming; Nemali, Krishna S.; Richards, James H.
  • Photosynthesis Research, Vol. 119, Issue 1-2
  • DOI: 10.1007/s11120-013-9891-5

Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


The Sequence Alignment/Map format and SAMtools
journal, June 2009


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
  • DOI: 10.1038/ng.806

The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


GCTA: A Tool for Genome-wide Complex Trait Analysis
journal, January 2011

  • Yang, Jian; Lee, S. Hong; Goddard, Michael E.
  • The American Journal of Human Genetics, Vol. 88, Issue 1
  • DOI: 10.1016/j.ajhg.2010.11.011

TASSEL: software for association mapping of complex traits in diverse samples
journal, June 2007


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
  • DOI: 10.1086/519795

Eigenanalysis of SNP data with an identity by descent interpretation
journal, February 2016


Some Distance Properties of Latent Root and Vector Methods Used in Multivariate Analysis
journal, December 1966


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
  • DOI: 10.1073/pnas.201394398

    Works referencing / citing this record:

    Using Populus as a lignocellulosic feedstock for bioethanol
    journal, February 2015


    A scan statistic for identifying chromosomal patterns of SNP association
    journal, November 2006

    • Sun, Yan V.; Levin, Albert M.; Boerwinkle, Eric
    • Genetic Epidemiology, Vol. 30, Issue 7
    • DOI: 10.1002/gepi.20173

    Regression models, scan statistics and reappearance probabilities to detect regions of association between gene expression and copy number
    journal, February 2011

    • Asimit, Jennifer L.; Andrulis, Irene L.; Bull, Shelley B.
    • Statistics in Medicine, Vol. 30, Issue 10
    • DOI: 10.1002/sim.4193

    Genomic selection in forest tree breeding: the concept and an outlook to the future
    journal, March 2014


    The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana
    journal, July 2013

    • Easlon, Hsien Ming; Nemali, Krishna S.; Richards, James H.
    • Photosynthesis Research, Vol. 119, Issue 1-2
    • DOI: 10.1007/s11120-013-9891-5

    Analysis of the genetic variation in growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa provenances
    journal, January 2016

    • Guerra, Fernando P.; Richards, James H.; Fiehn, Oliver
    • Tree Genetics & Genomes, Vol. 12, Issue 1
    • DOI: 10.1007/s11295-015-0965-8

    Ecophysiology of short rotation forest crops
    journal, January 1992


    GCTA: A Tool for Genome-wide Complex Trait Analysis
    journal, January 2011

    • Yang, Jian; Lee, S. Hong; Goddard, Michael E.
    • The American Journal of Human Genetics, Vol. 88, Issue 1
    • DOI: 10.1016/j.ajhg.2010.11.011

    XRN4 and LARP1 Are Required for a Heat-Triggered mRNA Decay Pathway Involved in Plant Acclimation and Survival during Thermal Stress
    journal, December 2013


    Fast implementation of a scan statistic for identifying chromosomal patterns of genome wide association studies
    journal, March 2009

    • Sun, Yan V.; Jacobsen, Douglas M.; Turner, Stephen T.
    • Computational Statistics & Data Analysis, Vol. 53, Issue 5
    • DOI: 10.1016/j.csda.2008.04.013

    Biomass equations and carbon content of aboveground leafless biomass of hybrid poplar in Coastal British Columbia
    journal, March 2006


    Eigenanalysis of SNP data with an identity by descent interpretation
    journal, February 2016


    Genome sequence and genetic diversity of European ash trees
    journal, December 2016

    • Sollars, Elizabeth S. A.; Harper, Andrea L.; Kelly, Laura J.
    • Nature, Vol. 541, Issue 7636
    • DOI: 10.1038/nature20786

    Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing
    journal, February 2009

    • Gnirke, Andreas; Melnikov, Alexandre; Maguire, Jared
    • Nature Biotechnology, Vol. 27, Issue 2
    • DOI: 10.1038/nbt.1523

    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
    • DOI: 10.1038/ng.3075

    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
    • DOI: 10.1038/ng.806

    Structural and biochemical studies of the 5′→3′ exoribonuclease Xrn1
    journal, February 2011

    • Chang, Jeong Ho; Xiang, Song; Xiang, Kehui
    • Nature Structural & Molecular Biology, Vol. 18, Issue 3
    • DOI: 10.1038/nsmb.1984

    Activation of 5'-3' exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast
    journal, May 2012

    • Sinturel, F.; Brechemier-Baey, D.; Kiledjian, M.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 21
    • DOI: 10.1073/pnas.1120090109

    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
    • DOI: 10.1073/pnas.201394398

    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
    • DOI: 10.1086/519795

    TASSEL: software for association mapping of complex traits in diverse samples
    journal, June 2007


    Fast and accurate short read alignment with Burrows-Wheeler transform
    journal, May 2009


    The Sequence Alignment/Map format and SAMtools
    journal, June 2009


    The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
    journal, July 2010


    Plant δ 15 N Correlates with the Transpiration Efficiency of Nitrogen Acquisition in Tropical Trees
    journal, September 2009

    • Cernusak, Lucas A.; Winter, Klaus; Turner, Benjamin L.
    • Plant Physiology, Vol. 151, Issue 3
    • DOI: 10.1104/pp.109.145870

    The Exoribonuclease XRN4 Is a Component of the Ethylene Response Pathway in Arabidopsis
    journal, November 2006

    • Potuschak, Thomas; Vansiri, Amérin; Binder, Brad M.
    • The Plant Cell, Vol. 18, Issue 11
    • DOI: 10.1105/tpc.106.046508

    Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem
    journal, September 2010


    Association genetics, geography and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs
    journal, November 2014

    • McKown, Athena D.; Guy, Robert D.; Quamme, Linda
    • Molecular Ecology, Vol. 23, Issue 23
    • DOI: 10.1111/mec.12969

    Association genetics of chemical wood properties in black poplar ( Populus nigra )
    journal, November 2012

    • Guerra, Fernando P.; Wegrzyn, Jill L.; Sykes, Robert
    • New Phytologist, Vol. 197, Issue 1
    • DOI: 10.1111/nph.12003

    Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations
    journal, December 2012

    • Porth, Ilga; Klápště, Jaroslav; Skyba, Oleksandr
    • New Phytologist, Vol. 197, Issue 3, p. 777-790
    • DOI: 10.1111/nph.12014

    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
    • DOI: 10.1111/nph.12419

    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
    • DOI: 10.1111/nph.12422

    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
    • DOI: 10.1111/nph.12601

    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
    • DOI: 10.1111/nph.12815

    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
    • DOI: 10.1111/nph.13643

    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
    • DOI: 10.1111/nph.14154

    Ecological genomics of variation in bud-break phenology and mechanisms of response to climate warming in Populus trichocarpa
    journal, July 2018

    • McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D.
    • New Phytologist, Vol. 220, Issue 1
    • DOI: 10.1111/nph.15273

    Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
    journal, April 2019

    • Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David
    • New Phytologist, Vol. 223, Issue 1
    • DOI: 10.1111/nph.15777

    Production physiology and morphology of Populus species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones
    journal, March 1997

    • Scaracia-Mugnozza, G. E.; Ceulemans, R.; Heilman, P. E.
    • Canadian Journal of Forest Research, Vol. 27, Issue 3
    • DOI: 10.1139/x96-180

    Targeted enrichment of the black cottonwood (Populus trichocarpa) gene space using sequence capture
    journal, January 2012


    High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus
    journal, January 2015


    Genomic prediction in contrast to a genome-wide association study in explaining heritable variation of complex growth traits in breeding populations of Eucalyptus
    journal, July 2017

    • Müller, Bárbara S. F.; Neves, Leandro G.; de Almeida Filho, Janeo E.
    • BMC Genomics, Vol. 18, Issue 1
    • DOI: 10.1186/s12864-017-3920-2

    Genetic diversity, linkage disequilibrium, population structure and construction of a core collection of Prunus avium L. landraces and bred cultivars
    journal, February 2016

    • Campoy, José Antonio; Lerigoleur-Balsemin, Emilie; Christmann, Hélène
    • BMC Plant Biology, Vol. 16, Issue 1
    • DOI: 10.1186/s12870-016-0712-9

    Relaxed Significance Criteria for Linkage Analysis
    journal, June 2006


    Some Distance Properties of Latent Root and Vector Methods Used in Multivariate Analysis
    journal, December 1966


    From Genomes to GENE-omes: Exome Sequencing Concept and Applications in Crop Improvement
    journal, December 2017