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
Abstract
3–O–caffeoylquinic acid, also known as chlorogenic acid (CGA), functions as an intermediate in lignin biosynthesis in the phenylpropanoid pathway. It is widely distributed among numerous plant species and acts as an antioxidant in both plants and animals. Using GC–MS, we discovered consistent and extreme variation in CGA content across a population of 739 4–yr–old Populus trichocarpa accessions. We performed genome–wide association studies (GWAS) from 917 P. trichocarpa accessions and expression–based quantitative trait loci (eQTL) analyses to identify key regulators. The GWAS and eQTL analyses resolved an overlapped interval encompassing a hydroxycinnamoyl–CoA:shikimate hydroxycinnamoyl transferase 2 (PtHCT2) that was significantly associated with CGA and partially characterized metabolite abundances. PtHCT2 leaf expression was significantly correlated with CGA abundance and it was regulated by cis–eQTLs containing W–box for WRKY binding. Among all nine PtHCT homologs, PtHCT2 is the only one that responds to infection by the fungal pathogen Sphaerulina musiva (a Populus pathogen). Validation using protoplast–based transient expression system suggests that PtHCT2 is regulated by the defense–responsive WRKY. Finally, these results are consistent with reports of CGA functioning as an antioxidant in response to biotic stress. In conclusion, this study provides insights into data–driven and omics–based inference of gene function in woody species.
- Authors:
-
[1];
[1];
[1];
[1];
[1];
[1];
[1];
[1]
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
- Univ. of Tennessee, Knoxville, TN (United States)
- Oregon State Univ., Corvallis, OR (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1468259
- Alternate Identifier(s):
- OSTI ID: 1459725; OSTI ID: 1633225
- Grant/Contract Number:
- AC05-00OR22725; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 220; Journal Issue: 2; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; expression quantitative trait loci (eQTLs); genome‐wide association studies (GWAS); hydroxycinnamoyl‐CoA; metabolome; Populus trichocarpa; shikimate hydroxycinnamoyl transferase (HCT); WRKY
Citation Formats
Zhang, Jin, Yang, Yongil, Zheng, Kaijie, Xie, Meng, Feng, Kai, Jawdy, Sara S., Gunter, Lee E., Ranjan, Priya, Singan, Vasanth R., Engle, Nancy, Lindquist, Erika, Barry, Kerrie, Schmutz, Jeremy, Zhao, Nan, Tschaplinski, Timothy J., LeBoldus, Jared, Tuskan, Gerald A., Chen, Jin -Gui, and Muchero, Wellington. 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. United States: N. p., 2018.
Web. doi:10.1111/nph.15297.
Zhang, Jin, Yang, Yongil, Zheng, Kaijie, Xie, Meng, Feng, Kai, Jawdy, Sara S., Gunter, Lee E., Ranjan, Priya, Singan, Vasanth R., Engle, Nancy, Lindquist, Erika, Barry, Kerrie, Schmutz, Jeremy, Zhao, Nan, Tschaplinski, Timothy J., LeBoldus, Jared, Tuskan, Gerald A., Chen, Jin -Gui, & Muchero, Wellington. 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. United States. https://doi.org/10.1111/nph.15297
Zhang, Jin, Yang, Yongil, Zheng, Kaijie, Xie, Meng, Feng, Kai, Jawdy, Sara S., Gunter, Lee E., Ranjan, Priya, Singan, Vasanth R., Engle, Nancy, Lindquist, Erika, Barry, Kerrie, Schmutz, Jeremy, Zhao, Nan, Tschaplinski, Timothy J., LeBoldus, Jared, Tuskan, Gerald A., Chen, Jin -Gui, and Muchero, Wellington. Wed .
"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". United States. https://doi.org/10.1111/nph.15297. https://www.osti.gov/servlets/purl/1468259.
@article{osti_1468259,
title = {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},
author = {Zhang, Jin and Yang, Yongil and Zheng, Kaijie and Xie, Meng and Feng, Kai and Jawdy, Sara S. and Gunter, Lee E. and Ranjan, Priya and Singan, Vasanth R. and Engle, Nancy and Lindquist, Erika and Barry, Kerrie and Schmutz, Jeremy and Zhao, Nan and Tschaplinski, Timothy J. and LeBoldus, Jared and Tuskan, Gerald A. and Chen, Jin -Gui and Muchero, Wellington},
abstractNote = {3–O–caffeoylquinic acid, also known as chlorogenic acid (CGA), functions as an intermediate in lignin biosynthesis in the phenylpropanoid pathway. It is widely distributed among numerous plant species and acts as an antioxidant in both plants and animals. Using GC–MS, we discovered consistent and extreme variation in CGA content across a population of 739 4–yr–old Populus trichocarpa accessions. We performed genome–wide association studies (GWAS) from 917 P. trichocarpa accessions and expression–based quantitative trait loci (eQTL) analyses to identify key regulators. The GWAS and eQTL analyses resolved an overlapped interval encompassing a hydroxycinnamoyl–CoA:shikimate hydroxycinnamoyl transferase 2 (PtHCT2) that was significantly associated with CGA and partially characterized metabolite abundances. PtHCT2 leaf expression was significantly correlated with CGA abundance and it was regulated by cis–eQTLs containing W–box for WRKY binding. Among all nine PtHCT homologs, PtHCT2 is the only one that responds to infection by the fungal pathogen Sphaerulina musiva (a Populus pathogen). Validation using protoplast–based transient expression system suggests that PtHCT2 is regulated by the defense–responsive WRKY. Finally, these results are consistent with reports of CGA functioning as an antioxidant in response to biotic stress. In conclusion, this study provides insights into data–driven and omics–based inference of gene function in woody species.},
doi = {10.1111/nph.15297},
journal = {New Phytologist},
number = 2,
volume = 220,
place = {United States},
year = {2018},
month = {7}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 12 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:
Elicitor-induced transcription factors for metabolic reprogramming of secondary metabolism in Medicago truncatula
journal, January 2008
- Naoumkina, Marina A.; He, XianZhi; Dixon, Richard A.
- BMC Plant Biology, Vol. 8, Issue 1
Lignin Biosynthesis
journal, June 2003
- Boerjan, Wout; Ralph, John; Baucher, Marie
- Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546
Wheat cells accumulate a syringyl-rich lignin during the hypersensitive resistance response
journal, February 2007
- Menden, Barbara; Kohlhoff, Markus; Moerschbacher, Bruno M.
- Phytochemistry, Vol. 68, Issue 4
Maize Homologs of CCoAOMT and HCT, Two Key Enzymes in Lignin Biosynthesis, Form Complexes with the NLR Rp1 Protein to Modulate the Defense Response
journal, May 2016
- Wang, Guan-Feng; Balint-Kurti, Peter J.
- Plant Physiology, Vol. 171, Issue 3
COFACTOR: improved protein function prediction by combining structure, sequence and protein–protein interaction information
journal, May 2017
- Zhang, Chengxin; Freddolino, Peter L.; Zhang, Yang
- Nucleic Acids Research, Vol. 45, Issue W1
I-TASSER server: new development for protein structure and function predictions
journal, April 2015
- Yang, Jianyi; Zhang, Yang
- Nucleic Acids Research, Vol. 43, Issue W1
Circumventing multiple testing: A multilocus Monte Carlo approach to testing for association
journal, January 2000
- McIntyre, Lauren M.; Martin, Eden R.; Simonsen, Katy L.
- Genetic Epidemiology, Vol. 19, Issue 1
Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007
- Chen, Fang; Dixon, Richard A.
- Nature Biotechnology, Vol. 25, Issue 7, p. 759-761
Genome-wide efficient mixed-model analysis for association studies
journal, June 2012
- Zhou, Xiang; Stephens, Matthew
- Nature Genetics, Vol. 44, Issue 7
Impact of Phenolic Compounds and Related Enzymes in Sorghum Varieties for Resistance and Susceptibility to Biotic and Abiotic Stresses
journal, October 2005
- Dicko, Mamoudou H.; Gruppen, Harry; Barro, Clarisse
- Journal of Chemical Ecology, Vol. 31, Issue 11
The phenylpropanoid pathway and plant defence-a genomics perspective
journal, September 2002
- Dixon, Richard A.; Achnine, Lahoucine; Kota, Parvathi
- Molecular Plant Pathology, Vol. 3, Issue 5
Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize
journal, June 2007
- Salvi, S.; Sponza, G.; Morgante, M.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 27
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Genome Biology, Vol. 14, Issue 4
Two Classes of Plant Antibiotics: Phytoalexins versus "Phytoanticipins"
journal, September 1994
- VanEtten, H. D.; Mansfield, J. W.; Bailey, J. A.
- The Plant Cell
Transcriptional regulation of secondary metabolite biosynthesis in plants
journal, November 2013
- Patra, Barunava; Schluttenhofer, Craig; Wu, Yongmei
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1829, Issue 11
A Structural Basis for the Biosynthesis of the Major Chlorogenic Acids Found in Coffee
journal, July 2012
- Lallemand, Laura A.; Zubieta, Chloe; Lee, Soon Goo
- Plant Physiology, Vol. 160, Issue 1
Salicylic acid mediates the reduced growth of lignin down-regulated plants
journal, November 2011
- Gallego-Giraldo, L.; Escamilla-Trevino, L.; Jackson, L. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
Wounding-Induced WRKY8 Is Involved in Basal Defense in Arabidopsis
journal, May 2010
- Chen, Ligang; Zhang, Liping; Yu, Diqiu
- Molecular Plant-Microbe Interactions, Vol. 23, Issue 5
Purification, Cloning, and Properties of an Acyltransferase Controlling Shikimate and Quinate Ester Intermediates in Phenylpropanoid Metabolism
journal, October 2002
- Hoffmann, Laurent; Maury, Stéphane; Martz, Françoise
- Journal of Biological Chemistry, Vol. 278, Issue 1
Regulation of Specialized Metabolism by WRKY Transcription Factors
journal, December 2014
- Schluttenhofer, Craig; Yuan, Ling
- Plant Physiology, Vol. 167, Issue 2
The nature of lignin-like compounds in cucumber hypocotyls induced by alpha-1,4-linked oligogalacturonides
journal, July 1990
- Robertsen, Borre; Svalheim, Oystein
- Physiologia Plantarum, Vol. 79, Issue 3
Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants
journal, December 2010
- Wang, H.; Avci, U.; Nakashima, J.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 51, p. 22338-22343
Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism
journal, July 2006
- Wuyts, N.
- Journal of Experimental Botany, Vol. 57, Issue 11
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
Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.)
journal, January 2011
- Gallego-Giraldo, Lina; Jikumaru, Yusuke; Kamiya, Yuji
- New Phytologist, Vol. 190, Issue 3
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance
journal, April 2006
- Truman, William; Zabala, Marta Torres; Grant, Murray
- The Plant Journal, Vol. 46, Issue 1
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
The potential effects of chlorogenic acid, the main phenolic components in coffee, on health: a comprehensive review of the literature
journal, April 2017
- Tajik, Narges; Tajik, Mahboubeh; Mack, Isabelle
- European Journal of Nutrition, Vol. 56, Issue 7
Production of novel antioxidative phenolic amides through heterologous expression of the plant’s chlorogenic acid biosynthesis genes in yeast
journal, May 2010
- Andrea, Moglia; Cinzia, Comino; Sergio, Lanteri
- Metabolic Engineering, Vol. 12, Issue 3
Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis
journal, January 2012
- Grunewald, W.; De Smet, I.; Lewis, D. R.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 5
The I-TASSER Suite: protein structure and function prediction
journal, December 2014
- Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
- Nature Methods, Vol. 12, Issue 1
Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus
journal, October 2006
- Tsai, Chung-Jui; Harding, Scott A.; Tschaplinski, Timothy J.
- New Phytologist, Vol. 172, Issue 1
Quantification of Lignin Formation in Almond Bark in Response to Wounding and Infection by Phytophthora Species
journal, January 1988
- Doster, M. A.
- Phytopathology, Vol. 78, Issue 4
Silencing of Hydroxycinnamoyl-Coenzyme A Shikimate/Quinate Hydroxycinnamoyltransferase Affects Phenylpropanoid Biosynthesis
journal, May 2004
- Hoffmann, Laurent; Besseau, Sébastien; Geoffroy, Pierrette
- The Plant Cell, Vol. 16, Issue 6
Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes
journal, December 2009
- Shi, Rui; Sun, Ying-Hsuan; Li, Quanzi
- Plant and Cell Physiology, Vol. 51, Issue 1
Chlorogenic acids and related depsides
journal, October 1964
- Sondheimer, Ernest
- The Botanical Review, Vol. 30, Issue 4
Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses
journal, September 2014
- Jiang, Yuanzhong; Duan, Yanjiao; Yin, Jia
- Journal of Experimental Botany, Vol. 65, Issue 22
Role of HXXXD-motif/BAHD acyltransferases in the biosynthesis of extracellular lipids
journal, December 2014
- Molina, Isabel; Kosma, Dylan
- Plant Cell Reports, Vol. 34, Issue 4
Linking Metabolic QTLs with Network and cis-eQTLs Controlling Biosynthetic Pathways
journal, January 2007
- Wentzell, Adam M.; Rowe, Heather C.; Hansen, Bjarne Gram
- PLoS Genetics, Vol. 3, Issue 9
Highly Efficient Isolation of Populus Mesophyll Protoplasts and Its Application in Transient Expression Assays
journal, September 2012
- Guo, Jianjun; Morrell-Falvey, Jennifer L.; Labbé, Jessy L.
- PLoS ONE, Vol. 7, Issue 9
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
Early lignin pathway enzymes and routes to chlorogenic acid in switchgrass (Panicum virgatum L.)
journal, November 2013
- Escamilla-Treviño, Luis L.; Shen, Hui; Hernandez, Timothy
- Plant Molecular Biology, Vol. 84, Issue 4-5
The Growth Reduction Associated with Repressed Lignin Biosynthesis in Arabidopsis thaliana Is Independent of Flavonoids
journal, May 2010
- Li, Xu; Bonawitz, Nicholas D.; Weng, Jing-Ke
- The Plant Cell, Vol. 22, Issue 5
Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors
journal, April 2006
- Xu, Xinping; Chen, Chunhong; Fan, Baofang
- The Plant Cell, Vol. 18, Issue 5
Cytoscape 2.8: new features for data integration and network visualization
journal, December 2010
- Smoot, M. E.; Ono, K.; Ruscheinski, J.
- Bioinformatics, Vol. 27, Issue 3
Haploview: analysis and visualization of LD and haplotype maps
journal, August 2004
- Barrett, J. C.; Fry, B.; Maller, J.
- Bioinformatics, Vol. 21, Issue 2
Elicitor-Induced Spruce Stress Lignin (Structural Similarity to Early Developmental Lignins)
journal, July 1995
- Lange, B. M.; Lapierre, C.; Sandermann Jr, H.
- Plant Physiology, Vol. 108, Issue 3
NMR Characterization of C3H and HCT Down-Regulated Alfalfa Lignin
journal, October 2009
- Pu, Yunqiao; Chen, Fang; Ziebell, Angela
- BioEnergy Research, Vol. 2, Issue 4
Production of the Isoflavones Genistein and Daidzein in Non-Legume Dicot and Monocot Tissues
journal, October 2000
- Yu, Oliver; Jung, Woosuk; Shi, June
- Plant Physiology, Vol. 124, Issue 2
The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco
journal, November 2009
- Guillaumie, Sabine; Mzid, Rim; Méchin, Valérie
- Plant Molecular Biology, Vol. 72, Issue 1-2
Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens?†
journal, January 2013
- Sattler, Scott E.; Funnell-Harris, Deanna L.
- Frontiers in Plant Science, Vol. 4
Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study
journal, February 2013
- Vanholme, Bartel; Cesarino, Igor; Goeminne, Geert
- New Phytologist, Vol. 198, Issue 3
Systemic acquired resistance: the elusive signal(s)
journal, August 2008
- Vlot, A. Corina; Klessig, Daniel F.; Park, Sang-Wook
- Current Opinion in Plant Biology, Vol. 11, Issue 4
The Transcription Factors WRKY11 and WRKY17 Act as Negative Regulators of Basal Resistance in Arabidopsis thaliana
journal, November 2006
- Journot-Catalino, Noëllie; Somssich, Imre E.; Roby, Dominique
- The Plant Cell, Vol. 18, Issue 11
Transcription factors WRKY70 and WRKY11 served as regulators in rhizobacterium Bacillus cereus AR156-induced systemic resistance to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis
journal, October 2015
- Jiang, Chun-Hao; Huang, Zi-Yang; Xie, Ping
- Journal of Experimental Botany, Vol. 67, Issue 1
High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus
journal, January 2015
- Muchero, Wellington; Guo, Jianjun; DiFazio, Stephen P.
- BMC Genomics, Vol. 16, Issue 1
Dissecting the WRKY Web of Plant Defense Regulators
journal, January 2006
- Eulgem, Thomas
- PLoS Pathogens, Vol. 2, Issue 11
Modification of phenolic metabolism in soybean hairy roots through down regulation of chalcone synthase or isoflavone synthase
journal, August 2006
- Lozovaya, Vera V.; Lygin, Anatoliy V.; Zernova, Olga V.
- Planta, Vol. 225, Issue 3
Identifying the molecular basis of QTLs: eQTLs add a new dimension
journal, February 2008
- Hansen, Bjarne G.; Halkier, Barbara A.; Kliebenstein, Daniel J.
- Trends in Plant Science, Vol. 13, Issue 2
Patterns of differential gene expression in Brassica napus cultivars infected with Sclerotinia sclerotiorum
journal, September 2009
- Zhao, Jianwei; Buchwaldt, Lone; Rimmer, Samuel Roger
- Molecular Plant Pathology, Vol. 10, Issue 5
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis
journal, January 2007
- Mockler, T. C.; Michael, T. P.; Priest, H. D.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 72, Issue 1
The effect of chlorogenic acid on blood pressure: a systematic review and meta-analysis of randomized clinical trials
journal, June 2014
- Onakpoya, I. J.; Spencer, E. A.; Thompson, M. J.
- Journal of Human Hypertension, Vol. 29, Issue 2
Engineering plants with increased levels of the antioxidant chlorogenic acid
journal, April 2004
- Niggeweg, Ricarda; Michael, Anthony J.; Martin, Cathie
- Nature Biotechnology, Vol. 22, Issue 6
WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis
journal, May 2013
- Chen, L.; Zhang, L.; Li, D.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 21
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
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
Two Classes of Plant Antibiotics: Phytoalexins versus "Phytoanticipins"
journal, September 1994
- VanEtten, Hans D.; Mansfield, John W.; Bailey, John A.
- The Plant Cell, Vol. 6, Issue 9
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture
journal, March 2021
- Rajewski, Alex; Carter-House, Derreck; Stajich, Jason
- BMC Genomics, Vol. 22, Issue 1
The nature of lignin-like compounds in cucumber hypocotyls induced by alpha-1,4-linked oligogalacturonides
journal, July 1990
- Robertsen, Borre; Svalheim, Oystein
- Physiologia Plantarum, Vol. 79, Issue 3
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
text, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Springer Nature
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features
text, January 2013
- Liao, Yang; Smyth, Gordon K.; Shi, Wei
- arXiv
Works referencing / citing this record:
The viability of a breeding programme for ash in the British Isles in the face of ash dieback
journal, July 2019
- Plumb, William J.; Coker, Timothy L. R.; Stocks, Jonathan J.
- PLANTS, PEOPLE, PLANET, Vol. 2, Issue 1
Agronomic performance of 27 Populus clones evaluated after two 3‐year coppice rotations in Henan, China
journal, December 2019
- Zhang, Jin; Song, Xueqin; Zhang, Lei
- GCB Bioenergy, Vol. 12, Issue 2
Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits
journal, April 2019
- Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David
- New Phytologist, Vol. 223, Issue 1
Comparative transcriptome analysis to identify candidate genes related to chlorogenic acid biosynthesis in Eucommia ulmoides Oliv.
journal, May 2019
- Ye, Jing; Han, Wenjing; Deng, Peng
- Trees, Vol. 33, Issue 5
Recent Advances in the Transcriptional Regulation of Secondary Cell Wall Biosynthesis in the Woody Plants
journal, October 2018
- Zhang, Jin; Xie, Meng; Tuskan, Gerald A.
- Frontiers in Plant Science, Vol. 9
Regulation of Lignin Biosynthesis and Its Role in Growth-Defense Tradeoffs
journal, September 2018
- Xie, Meng; Zhang, Jin; Tschaplinski, Timothy J.
- Frontiers in Plant Science, Vol. 9
Metabolic and physiological analyses reveal that Populus cathayana males adopt an energy-saving strategy to cope with phosphorus deficiency
journal, June 2019
- Zhang, Sheng; Tang, Duoteng; Korpelainen, Helena
- Tree Physiology, Vol. 39, Issue 9
Genome-wide association studies of bark texture in Populus trichocarpa
journal, February 2019
- Bdeir, Roba; Muchero, Wellington; Yordanov, Yordan
- Tree Genetics & Genomes, Vol. 15, Issue 1
Genome-Wide Association Studies to Improve Wood Properties: Challenges and Prospects
journal, December 2018
- Du, Qingzhang; Lu, Wenjie; Quan, Mingyang
- Frontiers in Plant Science, Vol. 9
Systems and Synthetic Biology of Forest Trees: A Bioengineering Paradigm for Woody Biomass Feedstocks
journal, June 2019
- Myburg, Alexander A.; Hussey, Steven G.; Wang, Jack P.
- Frontiers in Plant Science, Vol. 10
A High-Performance Computing Implementation of Iterative Random Forest for the Creation of Predictive Expression Networks
journal, December 2019
- Cliff, Ashley; Romero, Jonathon; Kainer, David
- Genes, Vol. 10, Issue 12