Pleiotropic and Epistatic Network-Based Discovery: Integrated Networks for Target Gene Discovery

Weighill, Deborah; Jones, Piet; Shah, Manesh; Ranjan, Priya; Muchero, Wellington; Schmutz, Jeremy; Sreedasyam, Avinash; Macaya-Sanz, David; Sykes, Robert; Zhao, Nan; Martin, Madhavi Z.; DiFazio, Stephen; Tschaplinski, Timothy J.; Tuskan, Gerald; Jacobson, Daniel

doi:10.3389/fenrg.2018.00030

Title: Pleiotropic and Epistatic Network-Based Discovery: Integrated Networks for Target Gene Discovery

Journal Article · Fri May 11 00:00:00 EDT 2018 · Frontiers in Energy Research

DOI:https://doi.org/10.3389/fenrg.2018.00030· OSTI ID:1436886

Weighill, Deborah; Jones, Piet; Shah, Manesh; Ranjan, Priya; Muchero, Wellington; Schmutz, Jeremy; Sreedasyam, Avinash; Macaya-Sanz, David; Sykes, Robert; Zhao, Nan; Martin, Madhavi Z.; DiFazio, Stephen; Tschaplinski, Timothy J.; Tuskan, Gerald; Jacobson, Daniel

Biological organisms are complex systems that are composed of functional networks of interacting molecules and macro-molecules. Complex phenotypes are the result of orchestrated, hierarchical, heterogeneous collections of expressed genomic variants. However, the effects of these variants are the result of historic selective pressure and current environmental and epigenetic signals, and, as such, their co-occurrence can be seen as genome-wide correlations in a number of different manners. Biomass recalcitrance (i.e., the resistance of plants to degradation or deconstruction, which ultimately enables access to a plant's sugars) is a complex polygenic phenotype of high importance to biofuels initiatives. This study makes use of data derived from the re-sequenced genomes from over 800 different Populus trichocarpa genotypes in combination with metabolomic and pyMBMS data across this population, as well as co-expression and co-methylation networks in order to better understand the molecular interactions involved in recalcitrance, and identify target genes involved in lignin biosynthesis/degradation. A Lines Of Evidence (LOE) scoring system is developed to integrate the information in the different layers and quantify the number of lines of evidence linking genes to target functions. This new scoring system was applied to quantify the lines of evidence linking genes to lignin-related genes and phenotypes across the network layers, and allowed for the generation of new hypotheses surrounding potential new candidate genes involved in lignin biosynthesis in P. trichocarpa, including various AGAMOUS-LIKE genes. Lastly, the resulting Genome Wide Association Study networks, integrated with Single Nucleotide Polymorphism (SNP) correlation, co-methylation, and co-expression networks through the LOE scores are proving to be a powerful approach to determine the pleiotropic and epistatic relationships underlying cellular functions and, as such, the molecular basis for complex phenotypes, such as recalcitrance.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); National Renewable Energy Laboratory (NREL), Golden, CO (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

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

Grant/Contract Number:: AC02-05CH11231; AC36-08GO28308; AC05-00OR22725

OSTI ID:: 1436886

Alternate ID(s):: OSTI ID: 1454749; OSTI ID: 1471945; OSTI ID: 1615272

Report Number(s):: NREL/JA-5100-71744; 30

Journal Information:: Frontiers in Energy Research, Journal Name: Frontiers in Energy Research Vol. 6; ISSN 2296-598X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: Switzerland

Language:: English

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Cited by: 18 works

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References (78)

Structure and function of the chloroplast signal recognition particle Sch�nemann, Danja Current Genetics, Vol. 44, Issue 6 https://doi.org/10.1007/s00294-003-0450-z	journal	January 2004
Silencing SlAGL6, a tomato AGAMOUS-LIKE6 lineage gene, generates fused sepal and green petal Yu, Xiaohui; Chen, Guoping; Guo, Xuhu Plant Cell Reports, Vol. 36, Issue 6 https://doi.org/10.1007/s00299-017-2129-9	journal	March 2017
Investigation of the crosstalk between the flg22 and the UV-B-induced flavonol pathway in Arabidopsis thaliana seedlings : UV-B-flg22 crosstalk is functional in planta Zhou, Zheng; Schenke, Dirk; Miao, Ying Plant, Cell & Environment, Vol. 40, Issue 3 https://doi.org/10.1111/pce.12869	journal	December 2016
ATHENA: Identifying interactions between different levels of genomic data associated with cancer clinical outcomes using grammatical evolution neural network Kim, Dokyoon; Li, Ruowang; Dudek, Scott M. BioData Mining, Vol. 6, Issue 1 https://doi.org/10.1186/1756-0381-6-23	journal	December 2013
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
ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
Variance component model to account for sample structure in genome-wide association studies Kang, Hyun Min; Sul, Jae Hoon; Service, Susan K. Nature Genetics, Vol. 42, Issue 4 https://doi.org/10.1038/ng.548	journal	March 2010
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
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher Current Protocols in Bioinformatics, Vol. 43, Issue 1 https://doi.org/10.1002/0471250953.bi1110s43	journal	October 2013
High-Throughput Screening of Plant Cell-Wall Composition Using Pyrolysis Molecular Beam Mass Spectroscopy Sykes, Robert; Yung, Matthew; Novaes, Evandro Biofuels https://doi.org/10.1007/978-1-60761-214-8_12	book	January 2009
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 MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis Zhong, R.; Richardson, E. A.; Ye, Z.-H. The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792 https://doi.org/10.1105/tpc.107.053678	journal	September 2007
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
Assessment of Populus wood chemistry following the introduction of a Bt toxin gene Davis, M. F.; Tuskan, G. A.; Payne, P. Tree Physiology, Vol. 26, Issue 5 https://doi.org/10.1093/treephys/26.5.557	journal	May 2006
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
Two Poplar-Associated Bacterial Isolates Induce Additive Favorable Responses in a Constructed Plant-Microbiome System Timm, Collin M.; Pelletier, Dale A.; Jawdy, Sara S. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00497	journal	April 2016
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
Involvement of the Chloroplast Signal Recognition Particle cpSRP43 in Acclimation to Conditions Promoting Photooxidative Stress in Arabidopsis Klenell, Markus; Morita, Shigeto; Tiemblo-Olmo, Mercedes Plant and Cell Physiology, Vol. 46, Issue 1 https://doi.org/10.1093/pcp/pci010	journal	January 2005
Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations Li, Yongchao; Tschaplinski, Timothy J.; Engle, Nancy L. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-2	journal	January 2012
Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production: Elicitor-mediated flavonol pathway suppression Schenke, Dirk; BÖTtcher, Christoph; Scheel, Dierk Plant, Cell & Environment, Vol. 34, Issue 11 https://doi.org/10.1111/j.1365-3040.2011.02381.x	journal	July 2011
Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads Jiang, Hongshan; Lei, Rong; Ding, Shou-Wei BMC Bioinformatics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2105-15-182	journal	June 2014
Synergistic effect of different levels of genomic data for cancer clinical outcome prediction Kim, Dokyoon; Shin, Hyunjung; Song, Young Soo Journal of Biomedical Informatics, Vol. 45, Issue 6 https://doi.org/10.1016/j.jbi.2012.07.008	journal	December 2012
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
The MADS-Domain Factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, Are Necessary to Block Floral Gene Expression during the Vegetative Phase Fernandez, Donna E.; Wang, Chieh-Ting; Zheng, Yumei Plant Physiology, Vol. 165, Issue 4 https://doi.org/10.1104/pp.114.242990	journal	June 2014
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
Gene Ontology: tool for the unification of biology Ashburner, Michael; Ball, Catherine A.; Blake, Judith A. Nature Genetics, Vol. 25, Issue 1 https://doi.org/10.1038/75556	journal	May 2000
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
Functional Analysis of the Arlequin Mutant Corroborates the Essential Role of the ARLEQUIN/TAGL1 Gene during Reproductive Development of Tomato Giménez, Estela; Pineda, Benito; Capel, Juan PLoS ONE, Vol. 5, Issue 12 https://doi.org/10.1371/journal.pone.0014427	journal	December 2010
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
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
Pinoresinol reductase 1 impacts lignin distribution during secondary cell wall biosynthesis in Arabidopsis Zhao, Qiao; Zeng, Yining; Yin, Yanbin Phytochemistry, Vol. 112 https://doi.org/10.1016/j.phytochem.2014.07.008	journal	April 2015
Graph Clustering Via a Discrete Uncoupling Process Van Dongen, Stijn SIAM Journal on Matrix Analysis and Applications, Vol. 30, Issue 1 https://doi.org/10.1137/040608635	journal	January 2008
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 Biswal, Ajaya K.; Hao, Zhangying; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0218-y	journal	January 2015
The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation Cosio, Claudia; Ranocha, Philippe; Francoz, Edith New Phytologist, Vol. 213, Issue 1 https://doi.org/10.1111/nph.14127	journal	August 2016
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
Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data: Mercator: sequence functional annotation server Lohse, Marc; Nagel, Axel; Herter, Thomas Plant, Cell & Environment, Vol. 37, Issue 5 https://doi.org/10.1111/pce.12231	journal	December 2013
Reshaping Data with the reshape Package Wickham, Hadley Journal of Statistical Software, Vol. 21, Issue 12 https://doi.org/10.18637/jss.v021.i12	journal	January 2007
LNK1 and LNK2 Corepressors Interact with the MYB3 Transcription Factor in Phenylpropanoid Biosynthesis Zhou, Meiliang; Zhang, Kaixuan; Sun, Zhanmin Plant Physiology, Vol. 174, Issue 3 https://doi.org/10.1104/pp.17.00160	journal	May 2017
The MYB36 transcription factor orchestrates Casparian strip formation Kamiya, Takehiro; Borghi, Monica; Wang, Peng Proceedings of the National Academy of Sciences, Vol. 112, Issue 33 https://doi.org/10.1073/pnas.1507691112	journal	June 2015
Lignin Biosynthesis and Structure Vanholme, R.; Demedts, B.; Morreel, K. Plant Physiology, Vol. 153, Issue 3, p. 895-905 https://doi.org/10.1104/pp.110.155119	journal	May 2010
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
Mergeomics: multidimensional data integration to identify pathogenic perturbations to biological systems Shu, Le; Zhao, Yuqi; Kurt, Zeyneb BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-3198-9	journal	November 2016
Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development Yu, Hao; Ito, Toshiro; Wellmer, Frank Nature Genetics, Vol. 36, Issue 2 https://doi.org/10.1038/ng1286	journal	January 2004
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
Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood Davies, Matthew N.; Volta, Manuela; Pidsley, Ruth Genome Biology, Vol. 13, Issue 6 https://doi.org/10.1186/gb-2012-13-6-r43	journal	January 2012
MYB Transcription Factors as Regulators of Phenylpropanoid Metabolism in Plants Liu, Jingying; Osbourn, Anne; Ma, Pengda Molecular Plant, Vol. 8, Issue 5 https://doi.org/10.1016/j.molp.2015.03.012	journal	May 2015
schwimmbad: A uniform interface to parallel processing pools in Python M. Price-Whelan, Adrian; Foreman-Mackey, Daniel The Journal of Open Source Software, Vol. 2, Issue 17 https://doi.org/10.21105/joss.00357	journal	September 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
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
Rapid method for high-quality RNA isolation from seed endosperm containing high levels of starch Li, Zhiwu; Trick, Harold N. BioTechniques, Vol. 38, Issue 6 https://doi.org/10.2144/05386BM05	journal	June 2005
Molecular characterization of the pyrolysis of biomass Evans, Robert J.; Milne, Thomas A. Energy & Fuels, Vol. 1, Issue 2 https://doi.org/10.1021/ef00002a001	journal	March 1987
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals Yu, H.; Xu, Y.; Tan, E. L. Proceedings of the National Academy of Sciences, Vol. 99, Issue 25 https://doi.org/10.1073/pnas.212624599	journal	November 2002
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
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
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
The Phosphoenolpyruvate/Phosphate Translocator Is Required for Phenolic Metabolism, Palisade Cell Development, and Plastid-Dependent Nuclear Gene Expression Streatfield, Stephen J.; Weber, Andreas; Kinsman, Elizabeth A. The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.1105/tpc.11.9.1609	journal	September 1999
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
BamTools: a C++ API and toolkit for analyzing and managing BAM files Barnett, D. W.; Garrison, E. K.; Quinlan, A. R. Bioinformatics, Vol. 27, Issue 12 https://doi.org/10.1093/bioinformatics/btr174	journal	April 2011
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus Muchero, Wellington; Guo, Jianjun; DiFazio, Stephen P. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1215-z	journal	January 2015
Arabidopsis cpSRP54 regulates carotenoid accumulation in Arabidopsis and Brassica napus Yu, Bianyun; Gruber, Margaret Y.; Khachatourians, George G. Journal of Experimental Botany, Vol. 63, Issue 14 https://doi.org/10.1093/jxb/ers179	journal	July 2012
Differential DNA methylation marks and gene comethylation of COPD in African-Americans with COPD exacerbations Busch, Robert; Qiu, Weiliang; Lasky-Su, Jessica Respiratory Research, Vol. 17, Issue 1 https://doi.org/10.1186/s12931-016-0459-8	journal	November 2016
Negative Regulation of the SHATTERPROOF Genes by FRUITFULL During Arabidopsis Fruit Development Ferrandiz, C. Science, Vol. 289, Issue 5478 https://doi.org/10.1126/science.289.5478.436	journal	July 2000
The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis Lee, H. Genes & Development, Vol. 14, Issue 18 https://doi.org/10.1101/gad.813600	journal	September 2000
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
MYB transcription factors in Arabidopsis Dubos, Christian; Stracke, Ralf; Grotewold, Erich Trends in Plant Science, Vol. 15, Issue 10 https://doi.org/10.1016/j.tplants.2010.06.005	journal	October 2010
Detecting outliers: Do not use standard deviation around the mean, use absolute deviation around the median Leys, Christophe; Ley, Christophe; Klein, Olivier Journal of Experimental Social Psychology, Vol. 49, Issue 4 https://doi.org/10.1016/j.jesp.2013.03.013	journal	July 2013
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Two High-Throughput Techniques for Determining Wood Properties as Part of a Molecular Genetics Analysis of Hybrid Poplar and Loblolly Pine Tuskan, Gerald; West, Darrell; Bradshaw, Harvy D. Applied Biochemistry and Biotechnology, Vol. 77, Issue 1-3 https://doi.org/10.1385/ABAB:77:1-3:55	journal	January 1999
A Bayesian Integrative Genomic Model for Pathway Analysis of Complex Traits: Bayesian Model for Analysis of Multiple Genomic Data Types Fridley, Brooke L.; Lund, Steven; Jenkins, Gregory D. Genetic Epidemiology, Vol. 36, Issue 4 https://doi.org/10.1002/gepi.21628	journal	March 2012
Measurement of mRNA abundance using RNA-seq data: RPKM measure is inconsistent among samples Wagner, Günter P.; Kin, Koryu; Lynch, Vincent J. Theory in Biosciences, Vol. 131, Issue 4 https://doi.org/10.1007/s12064-012-0162-3	journal	August 2012
Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-71	journal	January 2012
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
Overexpression of AGAMOUS-LIKE 28 (AGL28) promotes flowering by upregulating expression of floral promoters within the autonomous pathway Yoo, Seung Kwan; Lee, Jong Seob; Ahn, Ji Hoon Biochemical and Biophysical Research Communications, Vol. 348, Issue 3 https://doi.org/10.1016/j.bbrc.2006.07.121	journal	September 2006
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Optimizing illumina next-generation sequencing library preparation for extremely at-biased genomes Oyola, Samuel O.; Otto, Thomas D.; Gu, Yong BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-1	journal	January 2012

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