Data Integration in Poplar: ‘Omics Layers and Integration Strategies

Weighill, Deborah A.; Tschaplinski, Timothy J.; Tuskan, Gerald A.; Jacobson, Daniel A.

doi:10.3389/fgene.2019.00874

Data Integration in Poplar: ‘Omics Layers and Integration Strategies

Journal Article · Wed Sep 25 00:00:00 EDT 2019 · Frontiers in Genetics

DOI:https://doi.org/10.3389/fgene.2019.00874· OSTI ID:1616837

^[1]; ^[2]; ^[3]; ^[2]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Harvard Univ., Boston, MA (United States)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Populus trichocarpa is an important biofuel feedstock that has been the target of extensive research and is emerging as a model organism for plants, especially woody perennials. This research has generated several large ‘omics datasets. However, only few studies in Populus have attempted to integrate various data types. This review will summarize various ‘omics data layers, focusing on their application in Populus species. Subsequently, network and signal processing techniques for the integration and analysis of these data types will be discussed, with particular reference to examples in Populus.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1616837

Journal Information:: Frontiers in Genetics, Journal Name: Frontiers in Genetics Journal Issue: na Vol. 10; ISSN 1664-8021

Publisher:: FrontiersCopyright Statement

Country of Publication:: United States

Language:: English

References (202)

Poplar as a feedstock for biofuels: A review of compositional characteristics Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A. Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2 https://doi.org/10.1002/bbb.206	journal	March 2010
A Custom Correlation Coefficient (CCC) Approach for Fast Identification of Multi-SNP Association Patterns in Genome-Wide SNPs Data: Fast Identification of Multi-SNP Patterns in GWAS Climer, Sharlee; Yang, Wei; de las Fuentes, Lisa Genetic Epidemiology, Vol. 38, Issue 7 https://doi.org/10.1002/gepi.21833	journal	August 2014
Advances in plant proteomics Chen, Sixue; Harmon, Alice C. PROTEOMICS, Vol. 6, Issue 20 https://doi.org/10.1002/pmic.200600143	journal	October 2006
Identification of Open Chromatin Regions in Plant Genomes Using ATAC-Seq Bajic, Marko; Maher, Kelsey A.; Deal, Roger B. Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-7318-7_12	book	October 2017
Voluntary exposure to a toxin: the genetic influence on ethanol consumption Hoffman, Paula L.; Saba, Laura M.; Vanderlinden, Lauren A. Mammalian Genome, Vol. 29, Issue 1-2 https://doi.org/10.1007/s00335-017-9726-3	journal	December 2017
A database for poplar gene co-expression analysis for systematic understanding of biological processes, including stress responses Ogata, Yoshiyuki; Suzuki, Hideyuki; Shibata, Daisuke Journal of Wood Science, Vol. 55, Issue 6 https://doi.org/10.1007/s10086-009-1058-9	journal	December 2009
An atlas of gene expression from seed to seed through barley development Druka, Arnis; Muehlbauer, Gary; Druka, Ilze Functional & Integrative Genomics, Vol. 6, Issue 3 https://doi.org/10.1007/s10142-006-0025-4	journal	March 2006
Modification of plant cell wall chemistry impacts metabolome and microbiome composition in Populus PdKOR1 RNAi plants Veach, Allison M.; Yip, Daniel; Engle, Nancy L. Plant and Soil, Vol. 429, Issue 1-2 https://doi.org/10.1007/s11104-018-3692-8	journal	June 2018
Analysis of the Drought Stress-Responsive Transcriptome of Black Cottonwood (Populus trichocarpa) Using Deep RNA Sequencing Tang, Sha; Dong, Yan; Liang, Dan Plant Molecular Biology Reporter, Vol. 33, Issue 3 https://doi.org/10.1007/s11105-014-0759-4	journal	July 2014
Visualization of DNA methylation results through a GPU-based parallelization of the wavelet transform Fernández, Lisardo; Pérez, Mariano; Orduña, Juan M. The Journal of Supercomputing, Vol. 75, Issue 3 https://doi.org/10.1007/s11227-018-2670-5	journal	October 2018
The use of the Mexican Hat and the Morlet wavelets for detection of ecological patterns Mi, Xiangcheng; Ren, Haibao; Ouyang, Zisheng Plant Ecology, Vol. 179, Issue 1 https://doi.org/10.1007/s11258-004-5089-4	journal	July 2005
A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome Cossu, Rosa Maria; Buti, Matteo; Giordani, Tommaso Tree Genetics & Genomes, Vol. 8, Issue 1 https://doi.org/10.1007/s11295-011-0421-3	journal	August 2011
Comparative genome-wide analysis of repetitive DNA in the genus Populus L. Usai, Gabriele; Mascagni, Flavia; Natali, Lucia Tree Genetics & Genomes, Vol. 13, Issue 5 https://doi.org/10.1007/s11295-017-1181-5	journal	August 2017
Detection of structural DNA variation from next generation sequencing data: a review of informatic approaches Abel, Haley J.; Duncavage, Eric J. Cancer Genetics, Vol. 206, Issue 12 https://doi.org/10.1016/j.cancergen.2013.11.002	journal	December 2013
Poplar under drought: Comparison of leaf and cambial proteomic responses Durand, Thomas C.; Sergeant, Kjell; Renaut, Jenny Journal of Proteomics, Vol. 74, Issue 8 https://doi.org/10.1016/j.jprot.2011.03.013	journal	August 2011
Comparative proteomic analysis of Populus trichocarpa early stem from primary to secondary growth Liu, Jinwen; Hai, Guanghui; Wang, Chong Journal of Proteomics, Vol. 126 https://doi.org/10.1016/j.jprot.2015.05.032	journal	August 2015
Epigenetic regulation of stress responses in plants Chinnusamy, Viswanathan; Zhu, Jian-Kang Current Opinion in Plant Biology, Vol. 12, Issue 2 https://doi.org/10.1016/j.pbi.2008.12.006	journal	April 2009
Network-assisted crop systems genetics: network inference and integrative analysis Lee, Tak; Kim, Hyojin; Lee, Insuk Current Opinion in Plant Biology, Vol. 24 https://doi.org/10.1016/j.pbi.2015.02.001	journal	April 2015
Gene Networks in Plant Biology: Approaches in Reconstruction and Analysis Li, Yupeng; Pearl, Stephanie A.; Jackson, Scott A. Trends in Plant Science, Vol. 20, Issue 10 https://doi.org/10.1016/j.tplants.2015.06.013	journal	October 2015
Wavelet analysis of human DNA Machado, J. A. Tenreiro; Costa, António C.; Quelhas, Maria Dulce Genomics, Vol. 98, Issue 3 https://doi.org/10.1016/j.ygeno.2011.05.010	journal	September 2011
Integrated Analysis of Transcript, Protein and Metabolite Data To Study Lignin Biosynthesis in Hybrid Aspen Bylesjö, Max; Nilsson, Robert; Srivastava, Vaibhav Journal of Proteome Research, Vol. 8, Issue 1 https://doi.org/10.1021/pr800298s	journal	January 2009
The (in)famous GWAS P-value threshold revisited and updated for low-frequency variants Fadista, João; Manning, Alisa K.; Florez, Jose C. European Journal of Human Genetics, Vol. 24, Issue 8 https://doi.org/10.1038/ejhg.2015.269	journal	January 2016
Human gephyrin is encompassed within giant functional noncoding yin–yang sequences Climer, Sharlee; Templeton, Alan R.; Zhang, Weixiong Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7534	journal	March 2015
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli Nature Genetics, Vol. 46, Issue 10 https://doi.org/10.1038/ng.3075	journal	August 2014
DNA methylome analysis using short bisulfite sequencing data Krueger, Felix; Kreck, Benjamin; Franke, Andre Nature Methods, Vol. 9, Issue 2 https://doi.org/10.1038/nmeth.1828	journal	January 2012
Mapping genome-wide transcription-factor binding sites using DAP-seq Bartlett, Anna; O'Malley, Ronan C.; Huang, Shao-shan Carol Nature Protocols, Vol. 12, Issue 8 https://doi.org/10.1038/nprot.2017.055	journal	July 2017
Recombination: an underappreciated factor in the evolution of plant genomes Gaut, Brandon S.; Wright, Stephen I.; Rizzon, Carène Nature Reviews Genetics, Vol. 8, Issue 1 https://doi.org/10.1038/nrg1970	journal	January 2007
Transposable elements and the epigenetic regulation of the genome Slotkin, R. Keith; Martienssen, Robert Nature Reviews Genetics, Vol. 8, Issue 4 https://doi.org/10.1038/nrg2072	journal	April 2007
DNA methylation landscapes: provocative insights from epigenomics Suzuki, Miho M.; Bird, Adrian Nature Reviews Genetics, Vol. 9, Issue 6 https://doi.org/10.1038/nrg2341	journal	June 2008
Principles and challenges of genome-wide DNA methylation analysis Laird, Peter W. Nature Reviews Genetics, Vol. 11, Issue 3 https://doi.org/10.1038/nrg2732	journal	February 2010
Genotype and SNP calling from next-generation sequencing data Nielsen, Rasmus; Paul, Joshua S.; Albrechtsen, Anders Nature Reviews Genetics, Vol. 12, Issue 6 https://doi.org/10.1038/nrg2986	journal	May 2011
Methods of integrating data to uncover genotype–phenotype interactions Ritchie, Marylyn D.; Holzinger, Emily R.; Li, Ruowang Nature Reviews Genetics, Vol. 16, Issue 2 https://doi.org/10.1038/nrg3868	journal	January 2015
Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis Wang, Jack P.; Matthews, Megan L.; Williams, Cranos M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03863-z	journal	April 2018
Comparative transcriptomic analysis reveals conserved programmes underpinning organogenesis and reproduction in land plants Julca, Irene; Ferrari, Camilla; Flores-Tornero, María Nature Plants, Vol. 7, Issue 8 https://doi.org/10.1038/s41477-021-00958-2	journal	July 2021
Genetic regulation of amphioxus somitogenesis informs the evolution of the vertebrate head mesoderm Aldea, Daniel; Subirana, Lucie; Keime, Celine Nature Ecology & Evolution, Vol. 3, Issue 8 https://doi.org/10.1038/s41559-019-0933-z	journal	July 2019
A latent subset of human hematopoietic stem cells resists regenerative stress to preserve stemness Kaufmann, Kerstin B.; Zeng, Andy G. X.; Coyaud, Etienne Nature Immunology, Vol. 22, Issue 6 https://doi.org/10.1038/s41590-021-00925-1	journal	May 2021
Expression and integrated network analyses revealed functional divergence of NHX-type Na+/H+ exchanger genes in poplar Tian, Fengxia; Chang, Ermei; Li, Yu Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-02894-8	journal	June 2017
Preterm infants with isolated cerebellar hemorrhage show bilateral cortical alterations at term equivalent age Dijkshoorn, Aicha B. C.; Turk, Elise; Hortensius, Lisa M. Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-62078-9	journal	March 2020
Network-based integration of systems genetics data reveals pathways associated with lignocellulosic biomass accumulation and processing Mizrachi, Eshchar; Verbeke, Lieven; Christie, Nanette Proceedings of the National Academy of Sciences, Vol. 114, Issue 5 https://doi.org/10.1073/pnas.1620119114	journal	January 2017
Exploring regulation in tissues with eQTL networks Fagny, Maud; Paulson, Joseph N.; Kuijjer, Marieke L. Proceedings of the National Academy of Sciences, Vol. 114, Issue 37 https://doi.org/10.1073/pnas.1707375114	journal	August 2017
A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Frommer, M.; McDonald, L. E.; Millar, D. S. Proceedings of the National Academy of Sciences, Vol. 89, Issue 5 https://doi.org/10.1073/pnas.89.5.1827	journal	March 1992
The nature of the progression of drought stress drives differential metabolomic responses in Populus deltoides Tschaplinski, Timothy James; Abraham, Paul E.; Jawdy, Sara S. Annals of Botany, Vol. 124, Issue 4 https://doi.org/10.1093/aob/mcz002	journal	January 2019
Wavelets in bioinformatics and computational biology: state of art and perspectives Lio, P. Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1093/bioinformatics/19.1.2	journal	January 2003
SPTEdb: a database for transposable elements in salicaceous plants Yi, Fei; Jia, Zirui; Xiao, Yao Database, Vol. 2018 https://doi.org/10.1093/database/bay024	journal	January 2018
GFDP: the gene family database in poplar Wang, Hao; Yan, Hanwei; Liu, Huanlong Database, Vol. 2018 https://doi.org/10.1093/database/bay107	journal	January 2018
Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa Shuai, Peng; Liang, Dan; Tang, Sha Journal of Experimental Botany, Vol. 65, Issue 17 https://doi.org/10.1093/jxb/eru256	journal	June 2014
Single nucleotide polymorphism arrays: a decade of biological, computational and technological advances LaFramboise, T. Nucleic Acids Research, Vol. 37, Issue 13 https://doi.org/10.1093/nar/gkp552	journal	July 2009
Approaches for Extracting Practical Information from Gene Co-expression Networks in Plant Biology Aoki, K.; Ogata, Y.; Shibata, D. Plant and Cell Physiology, Vol. 48, Issue 3 https://doi.org/10.1093/pcp/pcm013	journal	January 2007
Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes Shi, Rui; Sun, Ying-Hsuan; Li, Quanzi Plant and Cell Physiology, Vol. 51, Issue 1 https://doi.org/10.1093/pcp/pcp175	journal	December 2009
Methods for biological data integration: perspectives and challenges Gligorijević, Vladimir; Pržulj, Nataša Journal of The Royal Society Interface, Vol. 12, Issue 112 https://doi.org/10.1098/rsif.2015.0571	journal	November 2015
JBrowse: A next-generation genome browser Skinner, M. E.; Uzilov, A. V.; Stein, L. D. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.094607.109	journal	July 2009
The Grapevine Expression Atlas Reveals a Deep Transcriptome Shift Driving the Entire Plant into a Maturation Program Fasoli, Marianna; Dal Santo, Silvia; Zenoni, Sara The Plant Cell, Vol. 24, Issue 9 https://doi.org/10.1105/tpc.112.100230	journal	September 2012
Comparative co-expression analysis in plant biology: Comparative transcriptomics in plants Movahedi, Sara; Van Bel, Michiel; Heyndrickx, Ken S. Plant, Cell & Environment, Vol. 35, Issue 10 https://doi.org/10.1111/j.1365-3040.2012.02517.x	journal	May 2012
A dynamic gene expression atlas covering the entire life cycle of rice Wang, Lei; Xie, Weibo; Chen, Ying The Plant Journal, Vol. 61, Issue 5 https://doi.org/10.1111/j.1365-313x.2009.04100.x	journal	March 2010
Modular gene expression in Poplar: a multilayer network approach Grönlund, Andreas; Bhalerao, Rishikesh P.; Karlsson, Jan New Phytologist, Vol. 181, Issue 2 https://doi.org/10.1111/j.1469-8137.2008.02668.x	journal	November 2008
The developmental dynamics of the Populus stem transcriptome Chao, Qing; Gao, Zhi-Fang; Zhang, Dong Plant Biotechnology Journal, Vol. 17, Issue 1 https://doi.org/10.1111/pbi.12958	journal	June 2018
Development of an integrated transcript sequence database and a gene expression atlas for gene discovery and analysis in switchgrass ( Panicum virgatum L.) Zhang, Ji-Yi; Lee, Yi-Ching; Torres-Jerez, Ivone The Plant Journal, Vol. 74, Issue 1 https://doi.org/10.1111/tpj.12104	journal	February 2013
The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization McCormick, Ryan F.; Truong, Sandra K.; Sreedasyam, Avinash The Plant Journal, Vol. 93, Issue 2 https://doi.org/10.1111/tpj.13781	journal	December 2017
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) Tuskan, G. A.; DiFazio, S.; Jansson, S. Science, Vol. 313, Issue 5793, p. 1596-1604 https://doi.org/10.1126/science.1128691	journal	September 2006
Integration of omic networks in a developmental atlas of maize Walley, J. W.; Sartor, R. C.; Shen, Z. Science, Vol. 353, Issue 6301 https://doi.org/10.1126/science.aag1125	journal	August 2016
Using the Bipartite Human Phenotype Network to Reveal Pleiotropy and Epistasis Beyond the gene Darabos, Christian; Harmon, Samantha H.; Moore, Jason H. Proceedings of the Pacific Symposium, Biocomputing 2014 https://doi.org/10.1142/9789814583220_0019	conference	November 2013
The Contributions of Transposable Elements to the Structure, Function, and Evolution of Plant Genomes Bennetzen, Jeffrey L.; Wang, Hao Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-035811	journal	April 2014
Dna Methylation in Plants Finnegan, E. J.; Genger, R. K.; Peacock, W. J. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev.arplant.49.1.223	journal	June 1998
Structure of Linkage Disequilibrium in Plants Flint-Garcia, Sherry A.; Thornsberry, Jeffry M.; Buckler, Edward S. Annual Review of Plant Biology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.arplant.54.031902.134907	journal	June 2003
Populus : A Model System for Plant Biology Jansson, Stefan; Douglas, Carl J. Annual Review of Plant Biology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.arplant.58.032806.103956	journal	June 2007
RepPop: a database for repetitive elements in Populus trichocarpa Zhou, Fengfeng; Xu, Ying BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-14	journal	January 2009
Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects van Eijk, Kristel R.; de Jong, Simone; Boks, Marco PM BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-636	journal	January 2012
Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis Shuai, Peng; Liang, Dan; Zhang, Zhoujia BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-233	journal	January 2013
Methylome reorganization during in vitro dedifferentiation and regeneration of Populus trichocarpa Vining, Kelly; Pomraning, Kyle R.; Wilhelm, Larry J. BMC Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2229-13-92	journal	January 2013
The advantages and limitations of trait analysis with GWAS: a review Korte, Arthur; Farlow, Ashley Plant Methods, Vol. 9, Issue 1 https://doi.org/10.1186/1746-4811-9-29	journal	January 2013
Integrated genome-wide association, coexpression network, and expression single nucleotide polymorphism analysis identifies novel pathway in allergic rhinitis Bunyavanich, Supinda; Schadt, Eric E.; Himes, Blanca E. BMC Medical Genomics, Vol. 7, Issue 1 https://doi.org/10.1186/1755-8794-7-48	journal	August 2014
Poplar trees reconfigure the transcriptome and metabolome in response to drought in a genotype- and time-of-day-dependent manner Hamanishi, Erin T.; Barchet, Genoa LH; Dauwe, Rebecca BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1535-z	journal	April 2015
A multi-omics approach reveals function of Secretory Carrier-Associated Membrane Proteins in wood formation of Populus trees Obudulu, Ogonna; Mähler, Niklas; Skotare, Tomas BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-017-4411-1	journal	January 2018
Integrated chromatin accessibility and DNA methylation analysis to reveal the critical epigenetic modification and regulatory mechanism in gonadal differentiation of the sequentially hermaphroditic fish, Monopterus albus Hu, Qiaomu; Lian, Zitong; Xia, Xueping Biology of Sex Differences, Vol. 13, Issue 1 https://doi.org/10.1186/s13293-022-00484-6	journal	December 2022
A DNA Methylation Network Interaction Measure, and Detection of Network Oncomarkers Bartlett, Thomas E.; Olhede, Sofia C.; Zaikin, Alexey PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0084573	journal	January 2014
Site-Dependent Differences in DNA Methylation and Their Impact on Plant Establishment and Phosphorus Nutrition in Populus trichocarpa Schönberger, Brigitte; Chen, Xiaochao; Mager, Svenja PLOS ONE, Vol. 11, Issue 12 https://doi.org/10.1371/journal.pone.0168623	journal	December 2016
Quantitative proteome profile of water deficit stress responses in eastern cottonwood (Populus deltoides) leaves Abraham, Paul E.; Garcia, Benjamin J.; Gunter, Lee E. PLOS ONE, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pone.0190019	journal	February 2018
Defining the genetic components of callus formation: A GWAS approach Tuskan, Gerald A.; Mewalal, Ritesh; Gunter, Lee E. PLOS ONE, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pone.0202519	journal	August 2018
Gene network analysis of poplar root transcriptome in response to drought stress identifies a PtaJAZ3PtaRAP2.6-centered hierarchical network Dash, Madhumita; Yordanov, Yordan S.; Georgieva, Tatyana PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0208560	journal	December 2018
The developing xylem transcriptome and genome-wide analysis of alternative splicing in Populus trichocarpa (black cottonwood) populations Bao, Hua; Li, Eryang; Mansfield, Shawn D. BioMed Central https://doi.org/10.14288/1.0221338	text	January 2013
Knowledge Discovery in Biological Databases for Revealing Candidate Genes Linked to Complex Phenotypes Hassani-Pak, Keywan; Rawlings, Christopher Journal of Integrative Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1515/jib-2016-0002	journal	March 2017
Systems-Level Analysis of Genome-Wide Association Data Farber, Charles R. G3: Genes\|Genomes\|Genetics, Vol. 3, Issue 1 https://doi.org/10.1534/g3.112.004788	journal	January 2013
A Variable Polyglutamine Repeat Affects Subcellular Localization and Regulatory Activity of a Populus ANGUSTIFOLIA Protein Bryan, Anthony C.; Zhang, Jin; Guo, Jianjun G3: Genes\|Genomes\|Genetics, Vol. 8, Issue 8 https://doi.org/10.1534/g3.118.200188	journal	June 2018
Wavelets for Agriculture and Biology: A Tutorial with Applications and Outlook Dong, Xuejun; Nyren, Paul; Patton, Bob BioScience, Vol. 58, Issue 5 https://doi.org/10.1641/b580512	journal	May 2008
An introduction to wavelet transforms: a tutorial approach Leavey, C. M.; James, M. N.; Summerscales, J. Insight - Non-Destructive Testing and Condition Monitoring, Vol. 45, Issue 5 https://doi.org/10.1784/insi.45.5.344.52875	journal	May 2003
Scale-Specific Inference Using Wavelets Keitt, Timothy H.; Urban, Dean L. Ecology, Vol. 86, Issue 9 https://doi.org/10.1890/04-1016	journal	September 2005
Methyl-DNA immunoprecipitation (MeDIP): Hunting down the DNA methylome Jacinto, Filipe V.; Ballestar, Esteban; Esteller, Manel BioTechniques, Vol. 44, Issue 1 https://doi.org/10.2144/000112708	journal	January 2008
Wavelet-Based Genomic Signal Processing for Centromere Identification and Hypothesis Generation Weighill, Deborah; Macaya-Sanz, David; DiFazio, Stephen Paul Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00487	journal	May 2019
Multi-Omics Approach Identifies Molecular Mechanisms of Plant-Fungus Mycorrhizal Interaction Larsen, Peter E.; Sreedasyam, Avinash; Trivedi, Geetika Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01061	journal	January 2016
Wavelet-based genetic association analysis of functional phenotypes arising from high-throughput sequencing assays Shim, Heejung; Stephens, Matthew arXiv https://doi.org/10.48550/arxiv.1307.7203	preprint	January 2013
The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Szklarczyk, D.; Franceschini, A.; Kuhn, M. Oxford University Press https://doi.org/10.5167/uzh-41629	text	January 2011
ATAC‐seq: A Method for Assaying Chromatin Accessibility Genome‐Wide Buenrostro, Jason D.; Wu, Beijing; Chang, Howard Y. Current Protocols in Molecular Biology, Vol. 109, Issue 1 https://doi.org/10.1002/0471142727.mb2129s109	journal	January 2015
Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress Zhang, Sheng; Chen, Fugui; Peng, Shuming PROTEOMICS, Vol. 10, Issue 14 https://doi.org/10.1002/pmic.200900650	journal	May 2010
Transposable elements: genome innovation, chromosome diversity, and centromere conflict Klein, Savannah J.; O’Neill, Rachel J. Chromosome Research, Vol. 26, Issue 1-2 https://doi.org/10.1007/s10577-017-9569-5	journal	January 2018
The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis Tuskan, Gerald A.; DiFazio, Steve; Faivre-Rampant, Patricia Tree Genetics & Genomes, Vol. 8, Issue 3 https://doi.org/10.1007/s11295-012-0495-6	journal	March 2012
A survey of Gypsy and Copia LTR-retrotransposon superfamilies and lineages and their distinct dynamics in the Populus trichocarpa (L.) genome Natali, Lucia; Cossu, Rosa Maria; Mascagni, Flavia Tree Genetics & Genomes, Vol. 11, Issue 5 https://doi.org/10.1007/s11295-015-0937-z	journal	September 2015
Gene co-expression network reconstruction: a review on computational methods for inferring functional information from plant-based expression data Emamjomeh, Abbasali; Saboori Robat, Elham; Zahiri, Javad Plant Biotechnology Reports, Vol. 11, Issue 2 https://doi.org/10.1007/s11816-017-0433-z	journal	April 2017
Integrative Networks Illuminate Biological Factors Underlying Gene–Disease Associations Krishnan, Arjun; Taroni, Jaclyn N.; Greene, Casey S. Current Genetic Medicine Reports, Vol. 4, Issue 4 https://doi.org/10.1007/s40142-016-0102-5	journal	September 2016
An introduction to wavelet transforms for chemometricians: A time-frequency approach Alsberg, Bjørn K.; Woodward, Andrew M.; Kell, Douglas B. Chemometrics and Intelligent Laboratory Systems, Vol. 37, Issue 2 https://doi.org/10.1016/S0169-7439(97)00029-4	journal	June 1997
Histone acetylation: lessons from the plant kingdom Lusser, Alexandra; Kölle, Doris; Loidl, Peter Trends in Plant Science, Vol. 6, Issue 2 https://doi.org/10.1016/S1360-1385(00)01839-2	journal	February 2001
Five Years of GWAS Discovery Visscher, Peter M.; Brown, Matthew A.; McCarthy, Mark I. The American Journal of Human Genetics, Vol. 90, Issue 1 https://doi.org/10.1016/j.ajhg.2011.11.029	journal	January 2012
10 Years of GWAS Discovery: Biology, Function, and Translation Visscher, Peter M.; Wray, Naomi R.; Zhang, Qian The American Journal of Human Genetics, Vol. 101, Issue 1 https://doi.org/10.1016/j.ajhg.2017.06.005	journal	July 2017
Developing integrated crop knowledge networks to advance candidate gene discovery Hassani-Pak, Keywan; Castellote, Martin; Esch, Maria Applied & Translational Genomics, Vol. 11 https://doi.org/10.1016/j.atg.2016.10.003	journal	December 2016
Unraveling gene function in agricultural species using gene co-expression networks Schaefer, Robert J.; Michno, Jean-Michel; Myers, Chad L. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1860, Issue 1 https://doi.org/10.1016/j.bbagrm.2016.07.016	journal	January 2017
On the Dependency of Cellular Protein Levels on mRNA Abundance Liu, Yansheng; Beyer, Andreas; Aebersold, Ruedi Cell, Vol. 165, Issue 3 https://doi.org/10.1016/j.cell.2016.03.014	journal	April 2016
Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape O’Malley, Ronan C.; Huang, Shao-shan Carol; Song, Liang Cell, Vol. 165, Issue 5 https://doi.org/10.1016/j.cell.2016.04.038	journal	May 2016
Integrating GWAS and Co-expression Network Data Identifies Bone Mineral Density Genes SPTBN1 and MARK3 and an Osteoblast Functional Module Calabrese, Gina M.; Mesner, Larry D.; Stains, Joseph P. Cell Systems, Vol. 4, Issue 1 https://doi.org/10.1016/j.cels.2016.10.014	journal	January 2017
Network analysis of GWAS data Leiserson, Mark DM; Eldridge, Jonathan V.; Ramachandran, Sohini Current Opinion in Genetics & Development, Vol. 23, Issue 6 https://doi.org/10.1016/j.gde.2013.09.003	journal	December 2013
Green systems biology — From single genomes, proteomes and metabolomes to ecosystems research and biotechnology Weckwerth, Wolfram Journal of Proteomics, Vol. 75, Issue 1 https://doi.org/10.1016/j.jprot.2011.07.010	journal	December 2011
Parallel accelerated Custom Correlation Coefficient calculations for genomics applications Joubert, Wayne; Nance, James; Climer, Sharlee Parallel Computing, Vol. 84 https://doi.org/10.1016/j.parco.2019.02.003	journal	May 2019
How does multiple testing correction work? Noble, William S. Nature Biotechnology, Vol. 27, Issue 12 https://doi.org/10.1038/nbt1209-1135	journal	December 2009
A gene expression map of Arabidopsis thaliana development Schmid, Markus; Davison, Timothy S.; Henz, Stefan R. Nature Genetics, Vol. 37, Issue 5 https://doi.org/10.1038/ng1543	journal	April 2005
Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription Zilberman, Daniel; Gehring, Mary; Tran, Robert K. Nature Genetics, Vol. 39, Issue 1 https://doi.org/10.1038/ng1929	journal	November 2006
Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position Buenrostro, Jason D.; Giresi, Paul G.; Zaba, Lisa C. Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2688	journal	October 2013
Network biology: understanding the cell's functional organization Barabási, Albert-László; Oltvai, Zoltán N. Nature Reviews Genetics, Vol. 5, Issue 2 https://doi.org/10.1038/nrg1272	journal	February 2004
A unified classification system for eukaryotic transposable elements Wicker, Thomas; Sabot, François; Hua-Van, Aurélie Nature Reviews Genetics, Vol. 8, Issue 12 https://doi.org/10.1038/nrg2165	journal	December 2007
Establishing, maintaining and modifying DNA methylation patterns in plants and animals Law, Julie A.; Jacobsen, Steven E. Nature Reviews Genetics, Vol. 11, Issue 3 https://doi.org/10.1038/nrg2719	journal	February 2010
Analysing and interpreting DNA methylation data Bock, Christoph Nature Reviews Genetics, Vol. 13, Issue 10 https://doi.org/10.1038/nrg3273	journal	September 2012
Pleiotropy in complex traits: challenges and strategies Solovieff, Nadia; Cotsapas, Chris; Lee, Phil H. Nature Reviews Genetics, Vol. 14, Issue 7 https://doi.org/10.1038/nrg3461	journal	June 2013
Metabolomics: the apogee of the omics trilogy Patti, Gary J.; Yanes, Oscar; Siuzdak, Gary Nature Reviews Molecular Cell Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nrm3314	journal	March 2012
Characterization of DWARF14 Genes in Populus Zheng, Kaijie; Wang, Xiaoping; Weighill, Deborah A. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep21593	journal	February 2016
PoplarGene: poplar gene network and resource for mining functional information for genes from woody plants Liu, Qi; Ding, Changjun; Chu, Yanguang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep31356	journal	August 2016
Drought response transcriptomes are altered in poplar with reduced tonoplast sucrose transporter expression Xue, Liang-Jiao; Frost, Christopher J.; Tsai, Chung-Jui Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep33655	journal	September 2016
Overexpression of a serine hydroxymethyltransferase increases biomass production and reduces recalcitrance in the bioenergy crop Populus Zhang, Jin; Li, Mi; Bryan, Anthony C. Sustainable Energy & Fuels, Vol. 3, Issue 1 https://doi.org/10.1039/C8SE00471D	journal	January 2019
Stress and transposable elements: co-evolution or useful parasites? Capy, Pierre; Gasperi, Giuliano; Biémont, Christian Heredity, Vol. 85, Issue 2 https://doi.org/10.1046/j.1365-2540.2000.00751.x	journal	January 2000
The human disease network Goh, K. -I.; Cusick, M. E.; Valle, D. Proceedings of the National Academy of Sciences, Vol. 104, Issue 21 https://doi.org/10.1073/pnas.0701361104	journal	May 2007
A comparison of methods for LTR-retrotransposon insertion time profiling in the Populus trichocarpa genome Mascagni, F.; Usai, G.; Natali, L. Caryologia, Vol. 71, Issue 1 https://doi.org/10.1080/00087114.2018.1429749	journal	January 2018
Populus: Arabidopsis for Forestry. Do We Need a Model Tree? Taylor, G. Annals of Botany, Vol. 90, Issue 6 https://doi.org/10.1093/aob/mcf255	journal	October 2002
DINGO: differential network analysis in genomics Ha, Min Jin; Baladandayuthapani, Veerabhadran; Do, Kim-Anh Bioinformatics, Vol. 31, Issue 21 https://doi.org/10.1093/bioinformatics/btv406	journal	July 2015
Network-based integration of multi-omics data for prioritizing cancer genes Dimitrakopoulos, Christos; Hindupur, Sravanth Kumar; Häfliger, Luca Bioinformatics, Vol. 34, Issue 14 https://doi.org/10.1093/bioinformatics/bty148	journal	March 2018
Fine-Scale Population Recombination Rates, Hotspots, and Correlates of Recombination in the Medicago truncatula Genome Paape, Timothy; Zhou, Peng; Branca, Antoine Genome Biology and Evolution, Vol. 4, Issue 5 https://doi.org/10.1093/gbe/evs046	journal	January 2012
DNA co-methylation analysis suggests novel functional associations between gene pairs in breast cancer samples Akulenko, Ruslan; Helms, Volkhard Human Molecular Genetics, Vol. 22, Issue 15 https://doi.org/10.1093/hmg/ddt158	journal	April 2013
A network perspective on nitrogen metabolism from model to crop plants using integrated ‘omics’ approaches Fukushima, Atsushi; Kusano, Miyako Journal of Experimental Botany, Vol. 65, Issue 19 https://doi.org/10.1093/jxb/eru322	journal	August 2014
An efficient algorithm for large-scale detection of protein families Enright, A. J. Nucleic Acids Research, Vol. 30, Issue 7 https://doi.org/10.1093/nar/30.7.1575	journal	April 2002
STRING: a database of predicted functional associations between proteins Mering, C. v. Nucleic Acids Research, Vol. 31, Issue 1 https://doi.org/10.1093/nar/gkg034	journal	January 2003
The Gene Ontology (GO) database and informatics resource No authors listed Nucleic Acids Research, Vol. 32, Issue 90001 https://doi.org/10.1093/nar/gkh036	journal	January 2004
The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Szklarczyk, D.; Franceschini, A.; Kuhn, M. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq973	journal	November 2010
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes Lu, Zefu; Hofmeister, Brigitte T.; Vollmers, Christopher Nucleic Acids Research, Vol. 45, Issue 6 https://doi.org/10.1093/nar/gkw1179	journal	November 2016
The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible Szklarczyk, Damian; Morris, John H.; Cook, Helen Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw937	journal	October 2016
Revisiting the sequencing of the first tree genome: Populus trichocarpa Wullschleger, S. D.; Weston, D. J.; DiFazio, S. P. Tree Physiology, Vol. 33, Issue 4 https://doi.org/10.1093/treephys/tps081	journal	October 2012
Populus trichocarpa and Populus deltoides Exhibit Different Metabolomic Responses to Colonization by the Symbiotic Fungus Laccaria bicolor Tschaplinski, Timothy J.; Plett, Jonathan M.; Engle, Nancy L. Molecular Plant-Microbe Interactions, Vol. 27, Issue 6 https://doi.org/10.1094/MPMI-09-13-0286-R	journal	June 2014
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data McKenna, A.; Hanna, M.; Banks, E. Genome Research, Vol. 20, Issue 9 https://doi.org/10.1101/gr.107524.110	journal	July 2010
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Identification of higher-order functional domains in the human ENCODE regions Thurman, R. E.; Day, N.; Noble, W. S. Genome Research, Vol. 17, Issue 6 https://doi.org/10.1101/gr.6081407	journal	June 2007
Genome structure and emerging evidence of an incipient sex chromosome in Populus Yin, T.; DiFazio, S. P.; Gunter, L. E. Genome Research, Vol. 18, Issue 3 https://doi.org/10.1101/gr.7076308	journal	February 2008
Profiling of Accessible Chromatin Regions across Multiple Plant Species and Cell Types Reveals Common Gene Regulatory Principles and New Control Modules Maher, Kelsey A.; Bajic, Marko; Kajala, Kaisa The Plant Cell, Vol. 30, Issue 1 https://doi.org/10.1105/tpc.17.00581	journal	December 2017
Attacking the Opioid Epidemic: Determining the Epistatic and Pleiotropic Genetic Architectures for Chronic Pain and Opioid Addiction Joubert, Wayne; Weighill, Deborah; Kainer, David SC18: International Conference for High Performance Computing, Networking, Storage and Analysis https://doi.org/10.1109/SC.2018.00060	conference	November 2018
A 34K SNP genotyping array for Populus trichocarpa : Design, application to the study of natural populations and transferability to other Populus species Geraldes, A.; DiFazio, S. P.; Slavov, G. T. Molecular Ecology Resources, Vol. 13, Issue 2, p. 306-323 https://doi.org/10.1111/1755-0998.12056	journal	January 2013
mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Thimm, Oliver; Bläsing, Oliver; Gibon, Yves The Plant Journal, Vol. 37, Issue 6, p. 914-939 https://doi.org/10.1111/j.1365-313X.2004.02016.x	journal	March 2004
Genetical metabolomics of flavonoid biosynthesis in Populus : a case study Morreel, Kris; Goeminne, Geert; Storme, Véronique The Plant Journal, Vol. 47, Issue 2 https://doi.org/10.1111/j.1365-313X.2006.02786.x	journal	July 2006
Data integration in plant biology: the O2PLS method for combined modeling of transcript and metabolite data Bylesjö, Max; Eriksson, Daniel; Kusano, Miyako The Plant Journal, Vol. 52, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03293.x	journal	December 2007
A gene expression atlas of the model legume Medicago truncatula Benedito, Vagner A.; Torres-Jerez, Ivone; Murray, Jeremy D. The Plant Journal, Vol. 55, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03519.x	journal	August 2008
A dynamic gene expression atlas covering the entire life cycle of rice Wang, Lei; Xie, Weibo; Chen, Ying The Plant Journal, Vol. 61, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.04100.x	journal	March 2010
BAR expressolog identification: expression profile similarity ranking of homologous genes in plant species: Expression profile similarity ranking of homologous genes Patel, Rohan V.; Nahal, Hardeep K.; Breit, Robert The Plant Journal, Vol. 71, Issue 6 https://doi.org/10.1111/j.1365-313X.2012.05055.x	journal	July 2012
Comparative analysis of the transcriptomes of Populus trichocarpa and Arabidopsis thaliana suggests extensive evolution of gene expression regulation in angiosperms Quesada, Tania; Li, Zhen; Dervinis, Christopher New Phytologist, Vol. 180, Issue 2, p. 408-420 https://doi.org/10.1111/j.1469-8137.2008.02586.x	journal	October 2008
Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa Slavov, Gancho T.; DiFazio, Stephen P.; Martin, Joel New Phytologist, Vol. 196, Issue 3, p. 713-725 https://doi.org/10.1111/j.1469-8137.2012.04258.x	journal	August 2012
Populus trichocarpa cell wall chemistry and ultrastructure trait variation, genetic control and genetic correlations Porth, Ilga; Klápště, Jaroslav; Skyba, Oleksandr New Phytologist, Vol. 197, Issue 3, p. 777-790 https://doi.org/10.1111/nph.12014	journal	December 2012
Methylome of DNase I sensitive chromatin in Populus trichocarpa shoot apical meristematic cells: a simplified approach revealing characteristics of gene-body DNA methylation in open chromatin state Lafon-Placette, Clément; Faivre-Rampant, Patricia; Delaunay, Alain New Phytologist, Vol. 197, Issue 2 https://doi.org/10.1111/nph.12026	journal	December 2012
Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D. New Phytologist, Vol. 203, Issue 2 https://doi.org/10.1111/nph.12815	journal	April 2014
Towards integration of population and comparative genomics in forest trees Ingvarsson, Pär K.; Hvidsten, Torgeir R.; Street, Nathaniel R. New Phytologist, Vol. 212, Issue 2 https://doi.org/10.1111/nph.14153	journal	August 2016
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 Zhang, Jin; Yang, Yongil; Zheng, Kaijie New Phytologist, Vol. 220, Issue 2 https://doi.org/10.1111/nph.15297	journal	July 2018
Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15777	journal	April 2019
UV-B mediated metabolic rearrangements in poplar revealed by non-targeted metabolomics: Poplar metabolome under UV stress Kaling, Moritz; Kanawati, Basem; Ghirardo, Andrea Plant, Cell & Environment, Vol. 38, Issue 5 https://doi.org/10.1111/pce.12348	journal	May 2014
Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation Verdier, Jerome; Torres-Jerez, Ivone; Wang, Mingyi The Plant Journal, Vol. 74, Issue 2 https://doi.org/10.1111/tpj.12119	journal	March 2013
Two‐stage identification of SNP effects on dynamic poplar growth Liu, Jingyuan; Ye, Meixia; Zhu, Sheng The Plant Journal, Vol. 93, Issue 2 https://doi.org/10.1111/tpj.13777	journal	December 2017
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
Histone Methylation in Higher Plants Liu, Chunyan; Lu, Falong; Cui, Xia Annual Review of Plant Biology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.091939	journal	June 2010
Gene network interconnectedness and the generalized topological overlap measure Yip, Andy M.; Horvath, Steve BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-22	journal	January 2007
WGCNA: an R package for weighted correlation network analysis Langfelder, Peter; Horvath, Steve BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-559	journal	December 2008
Single-base-resolution methylomes of populus trichocarpa reveal the association between DNA methylation and drought stress Liang, Dan; Zhang, Zhoujia; Wu, Honglong BMC Genetics, Vol. 15, Issue Suppl 1 https://doi.org/10.1186/1471-2156-15-S1-S9	journal	January 2014
Accounting for multiple comparisons in a genome-wide association study (GWAS) Johnson, Randall C.; Nelson, George W.; Troyer, Jennifer L. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-724	journal	December 2010
Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression Vining, Kelly J.; Pomraning, Kyle R.; Wilhelm, Larry J. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-27	journal	January 2012
The developing xylem transcriptome and genome-wide analysis of alternative splicing in Populus trichocarpa (black cottonwood) populations Bao, Hua; Li, Eryang; Mansfield, Shawn D. BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-359	journal	January 2013
ComPlEx: conservation and divergence of co-expression networks in A. thaliana, Populus and O. sativa Netotea, Sergiu; Sundell, David; Street, Nathaniel R. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-106	journal	January 2014
Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms Janz, Dennis; Behnke, Katja; Schnitzler, Jörg-Peter BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-150	journal	January 2010
RNA-Seq Atlas of Glycine max: A guide to the soybean transcriptome Severin, Andrew J.; Woody, Jenna L.; Bolon, Yung-Tsi BMC Plant Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2229-10-160	journal	January 2010
Weighted Interaction SNP Hub (WISH) network method for building genetic networks for complex diseases and traits using whole genome genotype data Kogelman, Lisette JA; Kadarmideen, Haja N. BMC Systems Biology, Vol. 8, Issue Suppl 2 https://doi.org/10.1186/1752-0509-8-S2-S5	journal	January 2014
Populus resequencing: towards genome-wide association studies Tuskan, Gerald; Slavov, Gancho; DiFazio, Steve BMC Proceedings, Vol. 5, Issue S7 https://doi.org/10.1186/1753-6561-5-S7-I21	journal	September 2011
Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis Gutiérrez, Rodrigo A.; Lejay, Laurence V.; Dean, Alexis Genome Biology, Vol. 8, Issue 1 https://doi.org/10.1186/gb-2007-8-1-r7	journal	January 2007
Quantitative proteomics reveals protein profiles underlying major transitions in aspen wood development Obudulu, Ogonna; Bygdell, Joakim; Sundberg, Björn BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2458-z	journal	February 2016
Mergeomics: a web server for identifying pathological pathways, networks, and key regulators via multidimensional data integration Arneson, Douglas; Bhattacharya, Anindya; Shu, Le BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3057-8	journal	September 2016
Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants Lämke, Jörn; Bäurle, Isabel Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1263-6	journal	June 2017
Population Structure and Cryptic Relatedness in Genetic Association Studies Astle, William; Balding, David J. Statistical Science, Vol. 24, Issue 4 https://doi.org/10.1214/09-STS307	journal	November 2009
Wavelet-based genetic association analysis of functional phenotypes arising from high-throughput sequencing assays Shim, Heejung; Stephens, Matthew The Annals of Applied Statistics, Vol. 9, Issue 2 https://doi.org/10.1214/14-AOAS776	journal	June 2015
Geometric Interpretation of Gene Coexpression Network Analysis Horvath, Steve; Dong, Jun PLoS Computational Biology, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pcbi.1000117	journal	August 2008
Chapter 11: Genome-Wide Association Studies Bush, William S.; Moore, Jason H. PLoS Computational Biology, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pcbi.1002822	journal	December 2012
Allele-Specific Network Reveals Combinatorial Interaction That Transcends Small Effects in Psoriasis GWAS Climer, Sharlee; Templeton, Alan R.; Zhang, Weixiong PLoS Computational Biology, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pcbi.1003766	journal	September 2014
The Influence of Recombination on Human Genetic Diversity Spencer, Chris C. A.; Deloukas, Panos; Hunt, Sarah PLoS Genetics, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pgen.0020148	journal	January 2006
A Network-Based Approach to Prioritize Results from Genome-Wide Association Studies Akula, Nirmala; Baranova, Ancha; Seto, Donald PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0024220	journal	September 2011
Wavelets for Agriculture and Biology: A Tutorial with Applications and Outlook Dong, Xuejun; Nyren, Paul; Patton, Bob BioScience, Vol. 58, Issue 5 https://doi.org/10.1641/B580512	journal	May 2008
A General Framework for Weighted Gene Co-Expression Network Analysis Zhang, Bin; Horvath, Steve Statistical Applications in Genetics and Molecular Biology, Vol. 4, Issue 1 https://doi.org/10.2202/1544-6115.1128	journal	January 2005
Pleiotropic and Epistatic Network-Based Discovery: Integrated Networks for Target Gene Discovery Weighill, Deborah; Jones, Piet; Shah, Manesh Frontiers in Energy Research, Vol. 6 https://doi.org/10.3389/fenrg.2018.00030	journal	May 2018
Multi-Phenotype Association Decomposition: Unraveling Complex Gene-Phenotype Relationships Weighill, Deborah; Jones, Piet; Bleker, Carissa Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00417	journal	May 2019
Learning from Co-expression Networks: Possibilities and Challenges Serin, Elise A. R.; Nijveen, Harm; Hilhorst, Henk W. M. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00444	journal	April 2016
Advances in Integrating Genomics and Bioinformatics in the Plant Breeding Pipeline Hu, Haifei; Scheben, Armin; Edwards, David Agriculture, Vol. 8, Issue 6 https://doi.org/10.3390/agriculture8060075	journal	May 2018
Integrated Transcriptome Analysis Reveals Plant Hormones Jasmonic Acid and Salicylic Acid Coordinate Growth and Defense Responses upon Fungal Infection in Poplar Luo, Jie; Xia, Wenxiu; Cao, Pei Biomolecules, Vol. 9, Issue 1 https://doi.org/10.3390/biom9010012	journal	January 2019
Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa D. McKown, Athena; Geraldes, Armando; Mansfield,, Shawn D. , Zenodo https://doi.org/10.5281/zenodo.7129888	dataset	January 2022
Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa D. McKown, Athena; Geraldes, Armando; Mansfield,, Shawn D. , Zenodo https://doi.org/10.5281/zenodo.7129891	dataset	January 2022
Mergeomics: a web server for identifying pathological pathways, networks, and key regulators via multidimensional data integration Arneson, Douglas; Bhattacharya, Anindya; Shu, Le figshare https://doi.org/10.6084/m9.figshare.c.3607511	collection	January 2016
Quantitative proteomics reveals protein profiles underlying major transitions in aspen wood development Obudulu, Ogonna; Bygdell, Joakim; Sundberg, Björn Figshare https://doi.org/10.6084/m9.figshare.c.3640562.v1	collection	January 2016
Accounting for multiple comparisons in a genome-wide association study (GWAS) Johnson, Randall C.; Nelson, George W.; Troyer, Jennifer L. figshare https://doi.org/10.6084/m9.figshare.c.4872699	collection	January 2020