The WRKY transcription factor family and senescence in switchgrass

Rinerson, Charles I.; Scully, Erin D.; Palmer, Nathan A.; Donze-Reiner, Teresa; Rabara, Roel C.; Tripathi, Prateek; Shen, Qingxi J.; Sattler, Scott E.; Rohila, Jai S.; Sarath, Gautam; Rushton, Paul J.

doi:10.1186/s12864-015-2057-4

Title: The WRKY transcription factor family and senescence in switchgrass

Journal Article · Mon Nov 09 00:00:00 EST 2015 · BMC Genomics

DOI:https://doi.org/10.1186/s12864-015-2057-4· OSTI ID:1626792

Rinerson, Charles I. ^[1]; Scully, Erin D. ^[2]; Palmer, Nathan A. ^[2]; Donze-Reiner, Teresa ^[3]; Rabara, Roel C. ^[1]; Tripathi, Prateek ^[4]; Shen, Qingxi J. ^[5]; Sattler, Scott E. ^[2]; Rohila, Jai S. ^[6]; Sarath, Gautam ^[2]; Rushton, Paul J. ^[7]

Texas A&M AgriLife Research and Extension Center, Dallas, TX, 75252, USA
Grain, Forage and Bioenergy Research Unit USDA-ARS UNL, Lincoln, NE, 68583-0937, USA
Department of Biology, West Chester University of Pennsylvania, West Chester, PA, 19382, USA
Molecular and Computational Biology Section, Dana & David Dornsife College of Letters, Arts and Sciences, University of Southern California, Los Angeles, CA, USA
School of Life Sciences, University of Nevada Las Vegas, Las Vegas, NV, 89154, USA
Department of Biology and Microbiology, South Dakota State University, Brookings, SD, 57007, USA
Texas A&M AgriLife Research and Extension Center, Dallas, TX, 75252, USA; 22nd Century Group Inc., Clarence, 14031, New York

Early aerial senescence in switchgrass (Panicum virgatum) can significantly limit biomass yields. WRKY transcription factors that can regulate senescence could be used to reprogram senescence and enhance biomass yields. All potential WRKY genes present in the version 1.0 of the switchgrass genome were identified and curated using manual and bioinformatic methods. Expression profiles of WRKY genes in switchgrass flag leaf RNA-Seq datasets were analyzed using clustering and network analyses tools to identify both WRKY and WRKY-associated gene co-expression networks during leaf development and senescence onset. We identified 240 switchgrass WRKY genes including members of the RW5 and RW6 families of resistance proteins. Weighted gene co-expression network analysis of the flag leaf transcriptomes across development readily separated clusters of co-expressed genes into thirteen modules. A visualization highlighted separation of modules associated with the early and senescence-onset phases of flag leaf growth. The senescence-associated module contained 3000 genes including 23 WRKYs. Putative promoter regions of senescence-associated WRKY genes contained several cis-element-like sequences suggestive of responsiveness to both senescence and stress signaling pathways. A phylogenetic comparison of senescence-associated WRKY genes from switchgrass flag leaf with senescence-associated WRKY genes from other plants revealed notable hotspots in Group I, IIb, and IIe of the phylogenetic tree. We have identified and named 240 WRKY genes in the switchgrass genome. Twenty three of these genes show elevated mRNA levels during the onset of flag leaf senescence. Eleven of the WRKY genes were found in hotspots of related senescence-associated genes from multiple species and thus represent promising targets for future switchgrass genetic improvement. Overall, individual WRKY gene expression profiles could be readily linked to developmental stages of flag leaves.

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Research Organization:: US Dept. of Agriculture (USDA), Washington, DC (United States). Agricultural Research Service (ARS)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); U. S. Department of Agriculture, National Institute of Food and Agriculture; U.S. Department of Agriculture, Agricultural Research Service, Central Regional Sun Grant Center

Grant/Contract Number:: SC0001490; AI02-09ER64829; 2011-67009-30096; 3042-21220-032-00D; 2008-35100-04519; 2008-35100-05969; 2010-38502-21861

OSTI ID:: 1626792

Journal Information:: BMC Genomics, Vol. 16, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 49 works

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References (84)

Molecular events in senescing Arabidopsis leaves Lin, Ji-Feng; Wu, Shu-Hsing The Plant Journal, Vol. 39, Issue 4 https://doi.org/10.1111/j.1365-313X.2004.02160.x	journal	August 2004
Nuclear targeted AtS40 modulates senescence associated gene expression in Arabidopsis thaliana during natural development and in darkness Fischer-Kilbienski, Isabell; Miao, Ying; Roitsch, Thomas Plant Molecular Biology, Vol. 73, Issue 4-5 https://doi.org/10.1007/s11103-010-9618-3	journal	March 2010
Molecular Analysis of viviparous-1: An Abscisic Acid-Insensitive Mutant of Maize. McCarty, D. R.; Carson, C. B.; Stinard, P. S. The Plant Cell https://doi.org/10.1105/tpc.1.5.523	journal	May 1989
Switchgrass (Panicum virgatum L) flag leaf transcriptomes reveal molecular signatures of leaf development, senescence, and mineral dynamics Palmer, Nathan A.; Donze-Reiner, Teresa; Horvath, David Functional & Integrative Genomics, Vol. 15, Issue 1 https://doi.org/10.1007/s10142-014-0393-0	journal	August 2014
WRKY42 Modulates Phosphate Homeostasis through Regulating Phosphate Translocation and Acquisition in Arabidopsis Su, Tong; Xu, Qian; Zhang, Fei-Cui Plant Physiology, Vol. 167, Issue 4 https://doi.org/10.1104/pp.114.253799	journal	March 2015
A Sorghum bicolor expression atlas reveals dynamic genotype-specific expression profiles for vegetative tissues of grain, sweet and bioenergy sorghums Shakoor, Nadia; Nair, Ramesh; Crasta, Oswald BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2229-14-35	journal	January 2014
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
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
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
Chlorophyll breakdown in higher plants Hörtensteiner, Stefan; Kräutler, Bernhard Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 8 https://doi.org/10.1016/j.bbabio.2010.12.007	journal	August 2011
WRKY transcription factors: key components in abscisic acid signalling: WRKY transcription factors in abscisic acid signalling Rushton, Deena L.; Tripathi, Prateek; Rabara, Roel C. Plant Biotechnology Journal, Vol. 10, Issue 1 https://doi.org/10.1111/j.1467-7652.2011.00634.x	journal	June 2011
The Switchgrass Genome: Tools and Strategies Casler, Michael D.; Tobias, Christian M.; Kaeppler, Shawn M. The Plant Genome Journal, Vol. 4, Issue 3 https://doi.org/10.3835/plantgenome2011.10.0026	journal	January 2011
Senescence, dormancy and tillering in perennial C4 grasses Sarath, Gautam; Baird, Lisa M.; Mitchell, Robert B. Plant Science, Vol. 217-218 https://doi.org/10.1016/j.plantsci.2013.12.012	journal	March 2014
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes: AtWRKY6 is associated with senescence and defence Robatzek, Silke; Somssich, Imre E. The Plant Journal, Vol. 28, Issue 2 https://doi.org/10.1046/j.1365-313X.2001.01131.x	journal	October 2001
Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence Hörtensteiner, Stefan Trends in Plant Science, Vol. 14, Issue 3 https://doi.org/10.1016/j.tplants.2009.01.002	journal	March 2009
Gene Network Analysis and Functional Studies of Senescence-associated Genes Reveal Novel Regulators of Arabidopsis Leaf SenescenceF Li, Zhonghai; Peng, Jinying; Wen, Xing Journal of Integrative Plant Biology, Vol. 54, Issue 8 https://doi.org/10.1111/j.1744-7909.2012.01136.x	journal	August 2012
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
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features Liao, Y.; Smyth, G. K.; Shi, W. Bioinformatics, Vol. 30, Issue 7 https://doi.org/10.1093/bioinformatics/btt656	journal	November 2013
WRKY transcription factors Rushton, Paul J.; Somssich, Imre E.; Ringler, Patricia Trends in Plant Science, Vol. 15, Issue 5 https://doi.org/10.1016/j.tplants.2010.02.006	journal	May 2010
Senescence Networking: WRKY18 is an Upstream Regulator, a Downstream Target Gene, and a Protein Interaction Partner of WRKY53 Potschin, Maren; Schlienger, Silke; Bieker, Stefan Journal of Plant Growth Regulation, Vol. 33, Issue 1 https://doi.org/10.1007/s00344-013-9380-2	journal	October 2013
Nomenclature report on rice WRKY's - Conflict regarding gene names and its solution Rice, Vol. 5, Issue 1 https://doi.org/10.1186/1939-8433-5-3	journal	February 2012
The evolution of WRKY transcription factors Rinerson, Charles I.; Rabara, Roel C.; Tripathi, Prateek BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0456-y	journal	January 2015
Leaf senescence and nutrient remobilisation in barley and wheat Gregersen, P. L.; Holm, P. B.; Krupinska, K. Plant Biology, Vol. 10 https://doi.org/10.1111/j.1438-8677.2008.00114.x	journal	September 2008
ARF1, a Transcription Factor That Binds to Auxin Response Elements Ulmasov, T. Science, Vol. 276, Issue 5320 https://doi.org/10.1126/science.276.5320.1865	journal	June 1997
Plant senescence and crop productivity Gregersen, Per L.; Culetic, Andrea; Boschian, Luca Plant Molecular Biology, Vol. 82, Issue 6 https://doi.org/10.1007/s11103-013-0013-8	journal	January 2013
Transcriptome of Arabidopsis leaf senescence Guo, Y.; Cai, Z.; Gan, S. Plant, Cell and Environment, Vol. 27, Issue 5 https://doi.org/10.1111/j.1365-3040.2003.01158.x	journal	May 2004
WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis Zhou, Xiang; Jiang, Yanjuan; Yu, Diqiu Molecules and Cells, Vol. 31, Issue 4 https://doi.org/10.1007/s10059-011-0047-1	journal	February 2011
Molecules as documents of evolutionary history Zuckerkandl, Emile; Pauling, Linus Journal of Theoretical Biology, Vol. 8, Issue 2 https://doi.org/10.1016/0022-5193(65)90083-4	journal	March 1965
The WRKY transcription factor family in Brachypodium distachyon Tripathi, Prateek; Rabara, Roel C.; Langum, Tanner J. BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-270	journal	January 2012
Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C ₄ Kranz anatomy Wang, Peng; Kelly, Steven; Fouracre, Jim P. The Plant Journal, Vol. 75, Issue 4 https://doi.org/10.1111/tpj.12229	journal	June 2013
Identification of early senescence-associated genes in rice flag leaves Liu, Li; Zhou, Yong; Zhou, Gang Plant Molecular Biology, Vol. 67, Issue 1-2 https://doi.org/10.1007/s11103-008-9300-1	journal	March 2008
Anatomical and transcriptional dynamics of maize embryonic leaves during seed germination Liu, W. -Y.; Chang, Y. -M.; Chen, S. C. -C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 10 https://doi.org/10.1073/pnas.1301009110	journal	February 2013
Wheat (Triticum aestivum) NAM proteins regulate the translocation of iron, zinc, and nitrogen compounds from vegetative tissues to grain Waters, Brian M.; Uauy, Cristobal; Dubcovsky, Jorge Journal of Experimental Botany, Vol. 60, Issue 15 https://doi.org/10.1093/jxb/erp257	journal	November 2009
Opportunities and roadblocks in utilizing forages and small grains for liquid fuels Sarath, Gautam; Mitchell, Robert B.; Sattler, Scott E. Journal of Industrial Microbiology & Biotechnology, Vol. 35, Issue 5 https://doi.org/10.1007/s10295-007-0296-3	journal	January 2008
Targets of AtWRKY6 regulation during plant senescence and pathogen defense Robatzek, S. Genes & Development, Vol. 16, Issue 9 https://doi.org/10.1101/gad.222702	journal	May 2002
Registration of ‘Liberty’ Switchgrass Vogel, K. P.; Mitchell, R. B.; Casler, M. D. Journal of Plant Registrations, Vol. 8, Issue 3 https://doi.org/10.3198/jpr2013.12.0076crc	journal	January 2014
Confidence Limits on Phylogenies: An Approach Using the Bootstrap Felsenstein, Joseph Evolution, Vol. 39, Issue 4, p. 783-791 https://doi.org/10.2307/2408678	journal	July 1985
Heterosis in Switchgrass: Spaced Plants Martinez-Reyna, Juan M.; Vogel, Kenneth P. Crop Science, Vol. 48, Issue 4 https://doi.org/10.2135/cropsci2007.12.0695	journal	January 2008
PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors Jin, Jinpu; Zhang, He; Kong, Lei Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1016	journal	October 2013
Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. Rushton, P. J.; Torres, J. T.; Parniske, M. The EMBO Journal, Vol. 15, Issue 20 https://doi.org/10.1002/j.1460-2075.1996.tb00953.x	journal	October 1996
A travel guide to Cytoscape plugins Saito, Rintaro; Smoot, Michael E.; Ono, Keiichiro Nature Methods, Vol. 9, Issue 11 https://doi.org/10.1038/nmeth.2212	journal	November 2012
Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation Wang, Hui; Xu, Qian; Kong, You-Han Plant Physiology, Vol. 164, Issue 4 https://doi.org/10.1104/pp.113.235077	journal	February 2014
Characterization of WRKY co-regulatory networks in rice and Arabidopsis Berri, Stefano; Abbruscato, Pamela; Faivre-Rampant, Odile BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-120	journal	January 2009
Arabidopsis Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes Riechmann, J. L.; Heard, J.; Martin, G. Science, Vol. 290, Issue 5499 https://doi.org/10.1126/science.290.5499.2105	journal	December 2000
Plant cis-acting regulatory DNA elements (PLACE) database: 1999 Higo, K.; Ugawa, Y.; Iwamoto, M. Nucleic Acids Research, Vol. 27, Issue 1 https://doi.org/10.1093/nar/27.1.297	journal	January 1999
Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation: Role of AtGDPD1 in phosphate starvation Cheng, Yuxiang; Zhou, Wenbin; El sheery, Nabil Ibrahim The Plant Journal, Vol. 66, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04538.x	journal	April 2011
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Developmental dynamics of Kranz cell transcriptional specificity in maize leaf reveals early onset of C4-related processes Tausta, S. Lori; Li, Pinghua; Si, Yaqing Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru152	journal	April 2014
The WRKY6 Transcription Factor Modulates PHOSPHATE1 Expression in Response to Low Pi Stress in Arabidopsis Chen, Yi-Fang; Li, Li-Qin; Xu, Qian The Plant Cell, Vol. 21, Issue 11 https://doi.org/10.1105/tpc.108.064980	journal	November 2009
Global analysis of the Gossypium hirsutum L. Transcriptome during leaf senescence by RNA-Seq Lin, Min; Pang, Chaoyou; Fan, Shuli BMC Plant Biology, Vol. 15, Issue 1 https://doi.org/10.1186/s12870-015-0433-5	journal	January 2015
Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence Ricachenevsky, Felipe Klein; Sperotto, Raul Antonio; Menguer, Paloma Koprovski Molecular Biology Reports, Vol. 37, Issue 8 https://doi.org/10.1007/s11033-010-0027-0	journal	March 2010
Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis Miao, Y.; Laun, T.; Zimmermann, P. Plant Molecular Biology, Vol. 55, Issue 6 https://doi.org/10.1007/s11103-005-2142-1	journal	August 2004
OsWRKY42 Represses OsMT1d and Induces Reactive Oxygen Species and Leaf Senescence in Rice Han, Muho; Kim, Chi-Yeol; Lee, Junok Molecules and Cells, Vol. 37, Issue 7 https://doi.org/10.14348/molcells.2014.0128	journal	July 2014
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays Popescu, S. C.; Popescu, G. V.; Bachan, S. Genes & Development, Vol. 23, Issue 1 https://doi.org/10.1101/gad.1740009	journal	December 2008
Heterologous expression of OsWRKY23 gene enhances pathogen defense and dark-induced leaf senescence in Arabidopsis Jing, Shaojuan; Zhou, Xiang; Song, Yu Plant Growth Regulation, Vol. 58, Issue 2 https://doi.org/10.1007/s10725-009-9366-z	journal	February 2009
Senescence, ageing and death of the whole plant Thomas, Howard New Phytologist, Vol. 197, Issue 3 https://doi.org/10.1111/nph.12047	journal	November 2012
Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice Zhang, Yu; Xu, Yong-Han; Yi, Hong-Yin The Plant Journal, Vol. 72, Issue 3 https://doi.org/10.1111/j.1365-313X.2012.05088.x	journal	August 2012
PvNAC1 and PvNAC2 Are Associated with Leaf Senescence and Nitrogen Use Efficiency in Switchgrass Yang, Jiading; Worley, Eric; Torres-Jerez, Ivone BioEnergy Research, Vol. 8, Issue 2 https://doi.org/10.1007/s12155-014-9566-x	journal	December 2014
WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana Besseau, Sébastien; Li, Jing; Palva, E. Tapio Journal of Experimental Botany, Vol. 63, Issue 7 https://doi.org/10.1093/jxb/err450	journal	January 2012
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis Miao, Y.; Laun, T.; Zimmermann, P. Plant Molecular Biology, Vol. 55, Issue 6 https://doi.org/10.1007/s11103-004-2142-6	journal	August 2004
Draft genome of a novel methanotrophic Methylobacter sp. from the volcanic soils of Pantelleria Island Hogendoorn, Carmen; Picone, Nunzia; van Hout, Femke Antonie van Leeuwenhoek, Vol. 114, Issue 3 https://doi.org/10.1007/s10482-021-01525-7	journal	February 2021
Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis) Boonanuntanasarn, Surintorn; Jangprai, Araya; Na-Nakorn, Uthairat Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-61738-0	journal	March 2020
Probing the floral developmental stages, bisexuality and sex reversions in castor (Ricinus communis L.) Parvathy, Sujatha Thankeswaran; Prabakaran, Amala Joseph; Jayakrishna, Thadakamalla Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-81781-9	journal	February 2021
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Molecular Analysis of viviparous-1: An Abscisic Acid-Insensitive Mutant of Maize McCarty, Donald R.; Carson, Christian B.; Stinard, Philip S. The Plant Cell, Vol. 1, Issue 5 https://doi.org/10.2307/3868973	journal	May 1989
Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence S., Hörtensteiner, Elsevier https://doi.org/10.5167/uzh-18971	text	January 2009
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Nature Precedings https://doi.org/10.1038/npre.2010.4282.2	journal	April 2010
Chlorophyll breakdown in higher plants. Hörtensteiner, S.; Kräutler, B. Elsevier https://doi.org/10.5167/uzh-53843	text	January 2011
Confidence Limits on Phylogenies: an Approach Using the Bootstrap Felsenstein, Joseph Evolution, Vol. 39, Issue 4 https://doi.org/10.1111/j.1558-5646.1985.tb00420.x	journal	July 1985
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Springer Nature https://doi.org/10.13016/7jyb-2sdy	text	January 2013
featureCounts: An efficient general-purpose program for assigning sequence reads to genomic features Liao, Yang; Smyth, Gordon K.; Shi, Wei arXiv https://doi.org/10.48550/arxiv.1305.3347	text	January 2013
Switchgrass Breeding, Genetics, and Genomics Casler, Michael D. Green Energy and Technology (book series) https://doi.org/10.1007/978-1-4471-2903-5_2	book	January 2012
The WRKY superfamily of plant transcription factors Eulgem, Thomas; Rushton, Paul J.; Robatzek, Silke Trends in Plant Science, Vol. 5, Issue 5, p. 199-206 https://doi.org/10.1016/s1360-1385(00)01600-9	journal	May 2000
IL-1-dependent enteric gliosis guides intestinal inflammation and dysmotility and modulates macrophage function Schneider, Reiner; Leven, Patrick; Mallesh, Shilpashree Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03772-4	journal	August 2022
NADPH-dependent Reductases Involved in the Detoxification of Reactive Carbonyls in Plants Yamauchi, Yasuo; Hasegawa, Ayaka; Taninaka, Ai Journal of Biological Chemistry, Vol. 286, Issue 9 https://doi.org/10.1074/jbc.m110.202226	journal	December 2010
Structural Basis for Sequence-specific DNA Recognition by an Arabidopsis WRKY Transcription Factor Yamasaki, Kazuhiko; Kigawa, Takanori; Watanabe, Satoru Journal of Biological Chemistry, Vol. 287, Issue 10 https://doi.org/10.1074/jbc.m111.279844	journal	January 2012
SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements Prestridge, Dan S. Bioinformatics, Vol. 7, Issue 2 https://doi.org/10.1093/bioinformatics/7.2.203	journal	January 1991
The neighbor-joining method: a new method for reconstructing phylogenetic trees. Saitou, N.; Nei, M. Molecular Biology and Evolution, Vol. 4, Issue 4, p. 406-425 https://doi.org/10.1093/oxfordjournals.molbev.a040454	journal	July 1987
A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53: E3 ubiquitin ligase regulates senescence Miao, Ying; Zentgraf, Ulrike The Plant Journal, Vol. 63, Issue 2 https://doi.org/10.1111/j.1365-313x.2010.04233.x	journal	April 2010

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Genome-wide survey of switchgrass NACs family provides new insights into motif and structure arrangements and reveals stress-related and tissue-specific NACs Yan, Haidong; Zhang, Ailing; Ye, Yuntian Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-03435-z	journal	June 2017
Targeted mutagenesis in tetraploid switchgrass ( Panicum virgatum L.) using CRISPR/Cas9 Liu, Yang; Merrick, Paul; Zhang, Zhengzhi Plant Biotechnology Journal, Vol. 16, Issue 2 https://doi.org/10.1111/pbi.12778	journal	August 2017
Genome-wide promoter analysis, homology modeling and protein interaction network of Dehydration Responsive Element Binding (DREB) gene family in Solanum tuberosum ain-Ali, Qurat-ul; Mushtaq, Nida; Amir, Rabia PLOS ONE, Vol. 16, Issue 12 https://doi.org/10.1371/journal.pone.0261215	journal	December 2021
Proteomic Responses of Switchgrass and Prairie Cordgrass to Senescence Paudel, Bimal; Das, Aayudh; Tran, Michaellong Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00293	journal	March 2016
Functional and RNA-Sequencing Analysis Revealed Expression of a Novel Stay-Green Gene from Zoysia japonica (ZjSGR) Caused Chlorophyll Degradation and Accelerated Senescence in Arabidopsis Teng, Ke; Chang, Zhihui; Li, Xiao Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01894	journal	December 2016
A Novel WRKY Transcription Factor, MuWRKY3 (Macrotyloma uniflorum Lam. Verdc.) Enhances Drought Stress Tolerance in Transgenic Groundnut (Arachis hypogaea L.) Plants Kiranmai, Kurnool; Lokanadha Rao, Gunupuru; Pandurangaiah, Merum Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00346	journal	March 2018
Arabidopsis WRKY53, a Node of Multi-Layer Regulation in the Network of Senescence Zentgraf, Ulrike; Doll, Jasmin Plants, Vol. 8, Issue 12 https://doi.org/10.3390/plants8120578	journal	December 2019
Characterization of the PAO/phyllobilin Pathway of Chlorophyll Breakdown in Grasses A., Das, University of Zurich https://doi.org/10.5167/uzh-129333	dissertation	January 2016

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Similar Records

Identification, characterization, and gene expression analysis of nucleotide binding site (NB)-type resistance gene homologues in switchgrass

Journal Article · Tue Nov 08 00:00:00 EST 2016 · BMC Genomics · OSTI ID:1626792

Frazier, Taylor P.; Palmer, Nathan A.; Xie, Fuliang; +10 more

Transcriptional analysis of defense mechanisms in upland tetraploid switchgrass to greenbugs

Journal Article · Thu Feb 16 00:00:00 EST 2017 · BMC Plant Biology · OSTI ID:1626792

Donze-Reiner, Teresa; Palmer, Nathan A.; Scully, Erin D.; +8 more

Global changes in mineral transporters in tetraploid switchgrasses (Panicum virgatum L.)

Journal Article · Thu Jan 02 00:00:00 EST 2014 · Frontiers in Plant Science · OSTI ID:1626792

Palmer, Nathan A.; Saathoff, Aaron J.; Waters, Brian M.; +5 more

Related Subjects

Biotechnology & Applied Microbiology
Genetics & Heredity

The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337 The current record is supplemented by this collection	collection	January 2015
The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337.v1 The current record is supplemented by this collection	collection	January 2015
Additional file 5: Figure S3. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d1.v1 The current record is supplemented by this text	text	January 2015
Additional file 4: Figure S2. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d2 The current record is supplemented by this text	text	January 2015
Additional file 4: Figure S2. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d2.v1 The current record is supplemented by this text	text	January 2015
Additional file 3: Figure S1. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d3 The current record is supplemented by this text	text	January 2015
Additional file 3: Figure S1. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d3.v1 The current record is supplemented by this text	text	January 2015
Additional file 2: Table S2. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d4.v1 The current record is supplemented by this dataset	dataset	January 2015
Additional file 5: Figure S3. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d1 The current record is supplemented by this text	text	January 2015
Additional file 2: Table S2. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d4 The current record is supplemented by this dataset	dataset	January 2015
Additional file 1: Table S1. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d5 The current record is supplemented by this dataset	dataset	January 2015
Additional file 1: Table S1. of The WRKY transcription factor family and senescence in switchgrass Rinerson, Charles; Scully, Erin; Palmer, Nathan https://doi.org/10.6084/m9.figshare.c.3646337_d5.v1 The current record is supplemented by this dataset	dataset	January 2015