Multitrait genome–wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
Abstract
Genome–wide association studies (GWAS) have great promise for identifying the loci that contribute to adaptive variation, but the complex genetic architecture of many quantitative traits presents a substantial challenge.We measured 14 morphological and physiological traits and identified single nucleotide polymorphism (SNP)–phenotype associations in a Populus trichocarpa population distributed from California, USA to British Columbia, Canada. We used whole–genome resequencing data of 882 trees with more than 6.78 million SNPs, coupled with multitrait association to detect polymorphisms with potentially pleiotropic effects. Candidate genes were validated with functional data.Broad–sense heritability (H2) ranged from 0.30 to 0.56 for morphological traits and 0.08 to 0.36 for physiological traits. In total, 4 and 20 gene models were detected using the single–trait and multitrait association methods, respectively. Several of these associations were corroborated by additional lines of evidence, including co–expression networks, metabolite analyses, and direct confirmation of gene function through RNAi.Multitrait association identified many more significant associations than single–trait association, potentially revealing pleiotropic effects of individual genes. Furthermore, this approach can be particularly useful for challenging physiological traits such as water–use efficiency or complex traits such as leaf morphology, for which we were able to identify credible candidate genes by combining multitrait association with gene co–expressionmore »
- Authors:
-
[1];
[2];
[2];
[2];
[2];
[2];
[1]
- West Virginia Univ., Morgantown, WV (United States)
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Univ. of Georgia, Athens, GA (United States)
- ArborGen, Inc., Ridgeville, SC (United States)
- Portland State Univ., Portland, OR (United States)
- Oregon State Univ., Corvallis, OR (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1545212
- Alternate Identifier(s):
- OSTI ID: 1505666
- Grant/Contract Number:
- AC05-00OR22725; AC05‐00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 223; Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; adaptation; drought tolerance; genome‐wide association studies (GWAS); leaf morphology; pleiotropy; Populus
Citation Formats
Chhetri, Hari B., Macaya‐Sanz, David, Kainer, David, Biswal, Ajaya K., Evans, Luke M., Chen, Jin ‐Gui, Collins, Cassandra, Hunt, Kimberly, Mohanty, Sushree S., Rosenstiel, Todd, Ryno, David, Winkeler, Kim, Yang, Xiaohan, Jacobson, Daniel A., Mohnen, Debra, Muchero, Wellington, Strauss, Steven H., Tschaplinski, Timothy J., Tuskan, Gerald A., and DiFazio, Stephen P. Multitrait genome–wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits. United States: N. p., 2019.
Web. doi:10.1111/nph.15777.
Chhetri, Hari B., Macaya‐Sanz, David, Kainer, David, Biswal, Ajaya K., Evans, Luke M., Chen, Jin ‐Gui, Collins, Cassandra, Hunt, Kimberly, Mohanty, Sushree S., Rosenstiel, Todd, Ryno, David, Winkeler, Kim, Yang, Xiaohan, Jacobson, Daniel A., Mohnen, Debra, Muchero, Wellington, Strauss, Steven H., Tschaplinski, Timothy J., Tuskan, Gerald A., & DiFazio, Stephen P. Multitrait genome–wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits. United States. https://doi.org/10.1111/nph.15777
Chhetri, Hari B., Macaya‐Sanz, David, Kainer, David, Biswal, Ajaya K., Evans, Luke M., Chen, Jin ‐Gui, Collins, Cassandra, Hunt, Kimberly, Mohanty, Sushree S., Rosenstiel, Todd, Ryno, David, Winkeler, Kim, Yang, Xiaohan, Jacobson, Daniel A., Mohnen, Debra, Muchero, Wellington, Strauss, Steven H., Tschaplinski, Timothy J., Tuskan, Gerald A., and DiFazio, Stephen P. Thu .
"Multitrait genome–wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits". United States. https://doi.org/10.1111/nph.15777. https://www.osti.gov/servlets/purl/1545212.
@article{osti_1545212,
title = {Multitrait genome–wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits},
author = {Chhetri, Hari B. and Macaya‐Sanz, David and Kainer, David and Biswal, Ajaya K. and Evans, Luke M. and Chen, Jin ‐Gui and Collins, Cassandra and Hunt, Kimberly and Mohanty, Sushree S. and Rosenstiel, Todd and Ryno, David and Winkeler, Kim and Yang, Xiaohan and Jacobson, Daniel A. and Mohnen, Debra and Muchero, Wellington and Strauss, Steven H. and Tschaplinski, Timothy J. and Tuskan, Gerald A. and DiFazio, Stephen P.},
abstractNote = {Genome–wide association studies (GWAS) have great promise for identifying the loci that contribute to adaptive variation, but the complex genetic architecture of many quantitative traits presents a substantial challenge.We measured 14 morphological and physiological traits and identified single nucleotide polymorphism (SNP)–phenotype associations in a Populus trichocarpa population distributed from California, USA to British Columbia, Canada. We used whole–genome resequencing data of 882 trees with more than 6.78 million SNPs, coupled with multitrait association to detect polymorphisms with potentially pleiotropic effects. Candidate genes were validated with functional data.Broad–sense heritability (H2) ranged from 0.30 to 0.56 for morphological traits and 0.08 to 0.36 for physiological traits. In total, 4 and 20 gene models were detected using the single–trait and multitrait association methods, respectively. Several of these associations were corroborated by additional lines of evidence, including co–expression networks, metabolite analyses, and direct confirmation of gene function through RNAi.Multitrait association identified many more significant associations than single–trait association, potentially revealing pleiotropic effects of individual genes. Furthermore, this approach can be particularly useful for challenging physiological traits such as water–use efficiency or complex traits such as leaf morphology, for which we were able to identify credible candidate genes by combining multitrait association with gene co–expression and co–methylation data.},
doi = {10.1111/nph.15777},
journal = {New Phytologist},
number = 1,
volume = 223,
place = {United States},
year = {Thu Mar 07 00:00:00 EST 2019},
month = {Thu Mar 07 00:00:00 EST 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 52 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
SNP discovery in black cottonwood ( Populus trichocarpa ) by population transcriptome resequencing : SNP DISCOVERY: NEXT GENERATION SEQUENCING
journal, February 2011
- Geraldes, Armando; Pang, Johnson; Thiessen, Nina
- Molecular Ecology Resources, Vol. 11
How relevant are flavonoids as antioxidants in plants?
journal, March 2009
- Hernández, Iker; Alegre, Leonor; Van Breusegem, Frank
- Trends in Plant Science, Vol. 14, Issue 3
Association genetics of complex traits in plants: Tansley review
journal, December 2010
- Ingvarsson, Pär K.; Street, Nathaniel R.
- New Phytologist, Vol. 189, Issue 4
Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis
journal, February 2018
- Biswal, Ajaya K.; Atmodjo, Melani A.; Li, Mi
- Nature Biotechnology, Vol. 36, Issue 3
Calcium at the Crossroads of Signaling
journal, May 2002
- Sanders, Dale; Pelloux, Jérôme; Brownlee, Colin
- The Plant Cell, Vol. 14, Issue suppl 1
Methods of integrating data to uncover genotype–phenotype interactions
journal, January 2015
- Ritchie, Marylyn D.; Holzinger, Emily R.; Li, Ruowang
- Nature Reviews Genetics, Vol. 16, Issue 2
Genome-wide efficient mixed-model analysis for association studies
journal, June 2012
- Zhou, Xiang; Stephens, Matthew
- Nature Genetics, Vol. 44, Issue 7
Statistical power and significance testing in large-scale genetic studies
journal, April 2014
- Sham, Pak C.; Purcell, Shaun M.
- Nature Reviews Genetics, Vol. 15, Issue 5
Characterization of the late embryogenesis abundant (LEA) proteins family and their role in drought stress tolerance in upland cotton
journal, January 2018
- Magwanga, Richard Odongo; Lu, Pu; Kirungu, Joy Nyangasi
- BMC Genetics, Vol. 19, Issue 1
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
POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana
journal, October 2017
- Rui, Yue; Xiao, Chaowen; Yi, Hojae
- The Plant Cell, Vol. 29, Issue 10
Xyloglucan endo -Transglycosylase-Mediated Xyloglucan Rearrangements in Developing Wood of Hybrid Aspen
journal, November 2010
- Nishikubo, Nobuyuki; Takahashi, Junko; Roos, Alexandra A.
- Plant Physiology, Vol. 155, Issue 1
Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression
journal, January 2012
- Vining, Kelly J.; Pomraning, Kyle R.; Wilhelm, Larry J.
- BMC Genomics, Vol. 13, Issue 1
The Evolution of Calcium-Based Signalling in Plants
journal, July 2017
- Edel, Kai H.; Marchadier, Elodie; Brownlee, Colin
- Current Biology, Vol. 27, Issue 13
Populus : A Model System for Plant Biology
journal, June 2007
- Jansson, Stefan; Douglas, Carl J.
- Annual Review of Plant Biology, Vol. 58, Issue 1
Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase12 (GAUT12) causes increased recalcitrance and decreased growth in Populus
journal, January 2018
- Biswal, Ajaya K.; Atmodjo, Melani A.; Pattathil, Sivakumar
- Biotechnology for Biofuels, Vol. 11, Issue 1
Geographic variation in ecophysiological traits of black cottonwood ( Populus trichocarpa )This article is one of a selection of papers published in the Special Issue on Poplar Research in Canada.
journal, December 2007
- Gornall, Jemma L.; Guy, Robert D.
- Canadian Journal of Botany, Vol. 85, Issue 12
10 Years of GWAS Discovery: Biology, Function, and Translation
journal, July 2017
- Visscher, Peter M.; Wray, Naomi R.; Zhang, Qian
- The American Journal of Human Genetics, Vol. 101, Issue 1
Identification of Genes Differentially Expressed in Shoot Apical Meristems and in Mature Xylem of Populus tomentosa
journal, October 2013
- Yang, Xiaohui; Li, Xinguo; Li, Bailian
- Plant Molecular Biology Reporter, Vol. 32, Issue 2
Forest-tree population genomics and adaptive evolution
journal, April 2006
- Gonzalez-Martinez, Santiago C.; Krutovsky, Konstantin V.; Neale, David B.
- New Phytologist, Vol. 170, Issue 2
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
Genome-wide association studies and expression-based quantitative trait loci analyses reveal roles of HCT2 in caffeoylquinic acid biosynthesis and its regulation by defense-responsive transcription factors in Populus
journal, July 2018
- Zhang, Jin; Yang, Yongil; Zheng, Kaijie
- New Phytologist, Vol. 220, Issue 2
Continental scale variability of foliar nitrogen and carbon isotopes in Populus balsamifera and their relationships with climate
journal, August 2017
- Elmore, Andrew J.; Craine, Joseph M.; Nelson, David M.
- Scientific Reports, Vol. 7, 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
Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar ( Populus balsamifera L.)
journal, December 2009
- Soolanayakanahally, Raju Y.; Guy, Robert D.; Silim, Salim N.
- Plant, Cell & Environment, Vol. 32, Issue 12
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
The ImageJ ecosystem: An open platform for biomedical image analysis: T
journal, July 2015
- Schindelin, Johannes; Rueden, Curtis T.; Hiner, Mark C.
- Molecular Reproduction and Development, Vol. 82, Issue 7-8
Effects of quercetin and its seven derivatives on the growth of Arabidopsis thaliana and Neurospora crassa
journal, July 2004
- Parvez, Mohammad Masud; Tomita-Yokotani, Kaori; Fujii, Yoshiharu
- Biochemical Systematics and Ecology, Vol. 32, Issue 7
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
Identification of Key Enzymes for Pectin Synthesis in Seed Mucilage
journal, September 2018
- Voiniciuc, Cătălin; Engle, Kristen A.; Günl, Markus
- Plant Physiology, Vol. 178, Issue 3
Downregulation of GAUT12 in Populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock
journal, January 2015
- Biswal, Ajaya K.; Hao, Zhangying; Pattathil, Sivakumar
- Biotechnology for Biofuels, Vol. 8, Issue 1
An Expanded View of Complex Traits: From Polygenic to Omnigenic
journal, June 2017
- Boyle, Evan A.; Li, Yang I.; Pritchard, Jonathan K.
- Cell, Vol. 169, Issue 7
A Statistical Approach for Testing Cross-Phenotype Effects of Rare Variants
journal, March 2016
- Broadaway, K. Alaine; Cutler, David J.; Duncan, Richard
- The American Journal of Human Genetics, Vol. 98, Issue 3
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
Genetical genomics of Populus leaf shape variation
journal, June 2015
- Drost, Derek R.; Puranik, Swati; Novaes, Evandro
- BMC Plant Biology, Vol. 15, Issue 1
Efficient multivariate linear mixed model algorithms for genome-wide association studies
journal, February 2014
- Zhou, Xiang; Stephens, Matthew
- Nature Methods, Vol. 11, Issue 4
Sap Pressure in Vascular Plants: Negative hydrostatic pressure can be measured in plants
journal, April 1965
- Scholander, P. F.; Bradstreet, E. D.; Hemmingsen, E. A.
- Science, Vol. 148, Issue 3668
A Multivariate Genome-Wide Association Analysis of 10 LDL Subfractions, and Their Response to Statin Treatment, in 1868 Caucasians
journal, April 2015
- Shim, Heejung; Chasman, Daniel I.; Smith, Joshua D.
- PLOS ONE, Vol. 10, Issue 4
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
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
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
EF-hand calcium-binding proteins
journal, December 2000
- Lewit-Bentley, Anita; Réty, Stéphane
- Current Opinion in Structural Biology, Vol. 10, Issue 6
Pleiotropic and Epistatic Network-Based Discovery: Integrated Networks for Target Gene Discovery
journal, May 2018
- Weighill, Deborah; Jones, Piet; Shah, Manesh
- Frontiers in Energy Research, Vol. 6
Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones
journal, March 2005
- Monclus, Romain; Dreyer, Erwin; Delmotte, Francis M.
- New Phytologist, Vol. 167, Issue 1
Arabidopsis AGDP1 links H3K9me2 to DNA methylation in heterochromatin
journal, October 2018
- Zhang, Cuijun; Du, Xuan; Tang, Kai
- Nature Communications, Vol. 9, Issue 1
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
Statistical methods to detect pleiotropy in human complex traits
journal, November 2017
- Hackinger, Sophie; Zeggini, Eleftheria
- Open Biology, Vol. 7, Issue 11
Abiotic Stress Signaling and Responses in Plants
journal, October 2016
- Zhu, Jian-Kang
- Cell, Vol. 167, 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
Powerful and Adaptive Testing for Multi-trait and Multi-SNP Associations with GWAS and Sequencing Data
journal, April 2016
- Kim, Junghi; Zhang, Yiwei; Pan, Wei
- Genetics, Vol. 203, Issue 2
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
A Unified Framework for Association Analysis with Multiple Related Phenotypes
journal, July 2013
- Stephens, Matthew
- PLoS ONE, Vol. 8, Issue 7
Evolving Views of Pectin Biosynthesis
journal, April 2013
- Atmodjo, Melani A.; Hao, Zhangying; Mohnen, Debra
- Annual Review of Plant Biology, Vol. 64, Issue 1
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
Productivity, water-use efficiency and tolerance to moderate water deficit correlate in 33 poplar genotypes from a Populus deltoides x Populus trichocarpa F1 progeny
journal, September 2009
- Monclus, R.; Villar, M.; Barbaroux, C.
- Tree Physiology, Vol. 29, Issue 11
Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase
journal, March 2006
- Sterling, J. D.; Atmodjo, M. A.; Inwood, S. E.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 13, p. 5236-5241
Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens
journal, July 2015
- Soolanayakanahally, Raju Y.; Guy, Robert D.; Street, Nathaniel R.
- Frontiers in Plant Science, Vol. 6
Analysis of EF-Hand Proteins in Soybean Genome Suggests Their Potential Roles in Environmental and Nutritional Stress Signaling
journal, May 2017
- Zeng, Houqing; Zhang, Yaxian; Zhang, Xiajun
- Frontiers in Plant Science, Vol. 8
Multivariate simulation framework reveals performance of multi-trait GWAS methods
journal, March 2017
- Porter, Heather F.; O’Reilly, Paul F.
- Scientific Reports, Vol. 7, Issue 1
The Evolution of Forest Genetics and Tree Improvement Research in the United States
journal, September 2015
- Wheeler, Nicholas C.; Steiner, Kim C.; Schlarbaum, Scott E.
- Journal of Forestry, Vol. 113, Issue 5
Calcium Sensors as Key Hubs in Plant Responses to Biotic and Abiotic Stresses
journal, March 2016
- Ranty, Benoît; Aldon, Didier; Cotelle, Valérie
- Frontiers in Plant Science, Vol. 7
Forest tree genomics: growing resources and applications
journal, January 2011
- Neale, David B.; Kremer, Antoine
- Nature Reviews Genetics, Vol. 12, Issue 2
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
Pleiotropy in complex traits: challenges and strategies
journal, June 2013
- Solovieff, Nadia; Cotsapas, Chris; Lee, Phil H.
- Nature Reviews Genetics, Vol. 14, Issue 7
The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides
journal, January 2019
- Tschaplinski, Timothy James; Abraham, Paul E.; Jawdy, Sara S.
- Annals of Botany, Vol. 124, Issue 4
Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012
- Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
- Biotechnology for Biofuels, Vol. 5, Issue 1
Efficient set tests for the genetic analysis of correlated traits
journal, June 2015
- Casale, Francesco Paolo; Rakitsch, Barbara; Lippert, Christoph
- Nature Methods, Vol. 12, Issue 8
Substantial role for carbonic anhydrase in latitudinal variation in mesophyll conductance of Populus trichocarpa Torr. & Gray : Mesophyll conductance of cottonwood
journal, November 2016
- Momayyezi, Mina; Guy, Robert D.
- Plant, Cell & Environment, Vol. 40, Issue 1
Population Genomics for Understanding Adaptation in Wild Plant Species
journal, November 2015
- Weigel, Detlef; Nordborg, Magnus
- Annual Review of Genetics, Vol. 49, Issue 1
Prominent Vessel Sign on Susceptibility-Weighted Imaging in Acute Stroke: Prediction of Infarct Growth and Clinical Outcome
journal, June 2015
- Chen, Chia-Yuen; Chen, Chin-I; Tsai, Fong Y.
- PLOS ONE, Vol. 10, Issue 6
Fabrication of functional hollow microspheres constructed from MOF shells: Promising drug delivery systems with high loading capacity and targeted transport
journal, November 2016
- Gao, Xuechuan; Hai, Xiao; Baigude, Huricha
- Scientific Reports, Vol. 6, Issue 1
Identification of deleterious recessive haplotypes and candidate deleterious recessive mutations in Japanese Black cattle
journal, March 2021
- Sasaki, Shinji; Watanabe, Toshio; Ibi, Takayuki
- Scientific Reports, Vol. 11, Issue 1
Works referencing / citing this record:
Association mapping for yield traits in Paeonia rockii based on SSR markers within transcription factors of comparative transcriptome
journal, June 2020
- Liu, Na; Cheng, Fangyun
- BMC Plant Biology, Vol. 20, Issue 1
A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees
journal, June 2019
- Bastiaanse, Héloïse; Zinkgraf, Matthew; Canning, Courtney
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 27
Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa
journal, November 2019
- Guerra, Fernando P.; Suren, Haktan; Holliday, Jason
- BMC Genomics, Vol. 20, Issue 1
Going with the flow: Intraspecific variation may act as a natural ally to counterbalance the impacts of global change for the riparian species Populus deltoides
journal, June 2019
- Godbout, Julie; Gros-Louis, Marie‐Claude; Lamothe, Manuel
- Evolutionary Applications, Vol. 13, Issue 1
Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa
journal, November 2019
- Guerra, Fernando P.; Suren, Haktan; Holliday, Jason
- BMC Genomics, Vol. 20, Issue 1