Revisiting the Role of Transcription Factors in Coordinating the Defense Response Against Citrus Bark Cracking Viroid Infection in Commercial Hop (Humulus Lupulus L.)
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31060295
PubMed Central
PMC6563305
DOI
10.3390/v11050419
PII: v11050419
Knihovny.cz E-zdroje
- Klíčová slova
- hop stunt disease, management, transcriptional reprogramming, viroid pathogenesis,
- MeSH
- fylogeneze MeSH
- Humulus klasifikace genetika imunologie virologie MeSH
- kůra rostlin imunologie virologie MeSH
- nemoci rostlin genetika imunologie virologie MeSH
- rostlinné proteiny genetika imunologie MeSH
- stanovení celkové genové exprese MeSH
- transkripční faktory genetika imunologie MeSH
- viroidy genetika fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- rostlinné proteiny MeSH
- transkripční faktory MeSH
Transcription factors (TFs) play a major role in controlling gene expression by intricately regulating diverse biological processes such as growth and development, the response to external stimuli and the activation of defense responses. The systematic identification and classification of TF genes are essential to gain insight into their evolutionary history, biological roles, and regulatory networks. In this study, we performed a global mining and characterization of hop TFs and their involvement in Citrus bark cracking viroid CBCVd infection by employing a digital gene expression analysis. Our systematic analysis resulted in the identification of a total of 3,818 putative hop TFs that were classified into 99 families based on their conserved domains. A phylogenetic analysis classified the hop TFs into several subgroups based on a phylogenetic comparison with reference TF proteins from Arabidopsis thaliana providing glimpses of their evolutionary history. Members of the same subfamily and subgroup shared conserved motif compositions. The putative functions of the CBCVd-responsive hop TFs were predicted using their orthologous counterparts in A. thaliana. The analysis of the expression profiling of the CBCVd-responsive hop TFs revealed a massive differential modulation, and the expression of the selected TFs was validated using qRT-PCR. Together, the comprehensive integrated analysis in this study provides better insights into the TF regulatory networks associated with CBCVd infections in the hop, and also offers candidate TF genes for improving the resistance in hop against viroids.
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Moore J.W., Loake G.J., Spoel S.H. Transcription Dynamics in Plant Immunity. Plant Cell. 2011;23:2809–2820. doi: 10.1105/tpc.111.087346. PubMed DOI PMC
Singh K.B., Foley R.C., Oñate-Sánchez L. Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 2002;5:430–436. doi: 10.1016/S1369-5266(02)00289-3. PubMed DOI
Tsuda K., Somssich I.E. Tansley review Transcriptional networks in plant immunity. New Phytol. 2015;206:932–947. doi: 10.1111/nph.13286. PubMed DOI
Eulgem T., Somssich I.E. Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 2007;10:366–371. doi: 10.1016/j.pbi.2007.04.020. PubMed DOI
Stracke R., Werber M., Weisshaar B. The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 2001;4:447–456. doi: 10.1016/S1369-5266(00)00199-0. PubMed DOI
Toledo-Ortiz G., Huq E., Quail P.H. The Arabidopsis Basic/Helix-Loop-Helix Transcription Factor Family. Plant Cell. 2003;15:1749–1770. doi: 10.1105/tpc.013839. PubMed DOI PMC
Jakoby M., Weisshaar B., Dröge-Laser W., Vicente-Carbajosa J., Tiedemann J., Kroj T., Parcy F. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002;7:106–111. doi: 10.1016/S1360-1385(01)02223-3. PubMed DOI
Muthamilarasan M., Bonthala V.S., Mishra A.K., Khandelwal R., Khan Y., Roy R., Prasad M. C2H2 type of zinc finger transcription factors in foxtail millet define response to abiotic stresses. Funct. Integr. Genom. 2014;14:531–543. doi: 10.1007/s10142-014-0383-2. PubMed DOI
Muthamilarasan M., Bonthala V.S., Khandelwal R., Jaishankar J., Shweta S., Nawaz K., Prasad M. Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front. Plant Sci. 2015;6:1–15. doi: 10.3389/fpls.2015.00910. PubMed DOI PMC
Muthamilarasan M., Mangu V.R., Zandkarimi H., Prasad M., Baisakh N. Structure, organization and evolution of ADP-ribosylation factors in rice and foxtail millet, and their expression in rice. Sci. Rep. 2016;6:1–13. doi: 10.1038/srep24008. PubMed DOI PMC
Saidi M.N., Mergby D., Brini F. Identification and expression analysis of the NAC transcription factor family in durum wheat (Triticum turgidum L. ssp. durum) Plant Physiol. Biochem. 2017;112:117–128. doi: 10.1016/j.plaphy.2016.12.028. PubMed DOI
Yang J., Gao M., Huang L., Wang Y., van Nocker S., Wan R., Guo C., Wang X., Gao H. Identification and expression analysis of the apple (Malus × domestica) basic helix-loop-helix transcription factor family. Sci. Rep. 2017;7:28. doi: 10.1038/s41598-017-00040-y. PubMed DOI PMC
Wen C.L., Cheng Q., Zhao L., Mao A., Yang J., Yu S., Weng Y., Xu Y. Identification and characterisation of Dof transcription factors in the cucumber genome. Sci. Rep. 2016;6:1–11. doi: 10.1038/srep23072. PubMed DOI PMC
Hu W., Yang H., Yan Y., Wei Y., Tie W., Ding Z., Zuo J., Peng M., Li K. Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci. Rep. 2016;6 doi: 10.1038/srep22783. PubMed DOI PMC
Ding B. The Biology of Viroid-Host Interactions. Annu. Rev. Phytopathol. 2009;47:105–131. doi: 10.1146/annurev-phyto-080508-081927. PubMed DOI
Hernández C., Flores R., de Alba A.E.M., Daròs J.-A., Serio F. Di Viroids and Viroid-Host Interactions. Annu. Rev. Phytopathol. 2005;43:117–139. doi: 10.1146/annurev.phyto.43.040204.140243. PubMed DOI
Wilson C.R., Hay F.S., Eastwell K.C., Pethybridge S.J., Barbara D.J. Viruses and Viroids Infecting Hop: Significance, Epidemiology, and Management. Plant Dis. 2008;92:324–338. doi: 10.1094/pdis-92-3-0324. PubMed DOI
Pokorn T., Radišek S., Javornik B., Štajner N., Jakše J. Development of hop transcriptome to support research into host-viroid interactions. PLoS ONE. 2017;12:1–25. doi: 10.1371/journal.pone.0184528. PubMed DOI PMC
Jakse J., Radisek S., Pokorn T., Matousek J., Javornik B. Deep-sequencing revealed Citrus bark cracking viroid (CBCVd) as a highly aggressive pathogen on hop. Plant Pathol. 2015;64:831–842. doi: 10.1111/ppa.12325. DOI
Mishra A.K., Duraisamy G.S., Matoušek J., Radisek S., Javornik B., Jakse J. Identification and characterization of microRNAs in Humulus lupulus using high-throughput sequencing and their response to Citrus bark cracking viroid (CBCVd) infection. BMC Genomics. 2016;17 doi: 10.1186/s12864-016-3271-4. PubMed DOI PMC
Mishra K.A., Kumar A., Mishra D., Nath S.V., Jakše J., Kocábek T., Killi K.U., Morina F., Matoušek J. Genome-Wide Transcriptomic Analysis Reveals Insights into the Response to Citrus bark cracking viroid (CBCVd) in Hop (Humulus lupulus L.) Viruses. 2018;10:570. doi: 10.3390/v10100570. PubMed DOI PMC
Natsume S., Takagi H., Shiraishi A., Murata J., Toyonaga H., Patzak J., Takagi M., Yaegashi H., Uemura A., Mitsuoka C., et al. The draft genome of hop (Humulus lupulus), an essence for brewing. Plant Cell Physiol. 2015;56:428–441. doi: 10.1093/pcp/pcu169. PubMed DOI
Dai X., Sinharoy S., Udvardi M., Zhao P.X. PlantTFcat: An online plant transcription factor and transcriptional regulator categorization and analysis tool. BMC Bioinform. 2013;14 doi: 10.1186/1471-2105-14-321. PubMed DOI PMC
Yu C.-S., Chen Y.-C., Lu C.-H., Hwang J.-K. Prediction of protein subcellular localization. Proteins Struct. Funct. Bioinforma. 2006;64:643–651. doi: 10.1002/prot.21018. PubMed DOI
Conesa A., Götz S. Blast2GO: A Comprehensive Suite for Functional Analysis in Plant Genomics. Int. J. Plant Genom. 2008;2008:1–12. doi: 10.1155/2008/619832. PubMed DOI PMC
Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC
Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D., Bowden J., Couger M.B., Eccles D., Li B., Lieber M., et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013;8:1494. doi: 10.1038/nprot.2013.084. PubMed DOI PMC
Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Benjamini Y., Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J. R. Stat. Soc. Ser. B. 1995;57:289–300. doi: 10.1111/j.2517-6161.1995.tb02031.x. DOI
Metsalu T., Vilo J. ClustVis: A web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 2015;43:W566–W570. doi: 10.1093/nar/gkv468. PubMed DOI PMC
Huerta-Cepas J., Forslund K., Coelho L.P., Szklarczyk D., Jensen L.J., Von Mering C., Bork P. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 2017;34:2115–2122. doi: 10.1093/molbev/msx148. PubMed DOI PMC
Huerta-Cepas J., Szklarczyk D., Forslund K., Cook H., Heller D., Walter M.C., Rattei T., Mende D.R., Sunagawa S., Kuhn M., et al. EGGNOG 4.5: A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 2016;44:D286–D293. doi: 10.1093/nar/gkv1248. PubMed DOI PMC
Morris J.H., Huerta-Cepas J., Junge A., Szklarczyk D., Jensen L.J., von Mering C., Lyon D., Gable A.L., Wyder S., Simonovic M., et al. STRING v11: Protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2018;47:D607–D613. doi: 10.1093/nar/gky1131. PubMed DOI PMC
Chin C.-H., Chen S.-H., Wu H.-H., Ho C.-W., Ko M.-T., Lin C.-Y. cytoHubba: Identifying hub objects and sub-networks from complex interactome. BMC Syst. Biol. 2014;8:S11. doi: 10.1186/1752-0509-8-S4-S11. PubMed DOI PMC
Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504. doi: 10.1101/gr.1239303. PubMed DOI PMC
Marshall O.J. PerlPrimer: Cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics. 2004;20:2471–2472. doi: 10.1093/bioinformatics/bth254. PubMed DOI
Ye J., Coulouris G., Zaretskaya I., Cutcutache I., Rozen S., Madden T.L. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012;13:134. doi: 10.1186/1471-2105-13-134. PubMed DOI PMC
Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI
Štajner N., Cregeen S., Javornik B. Evaluation of reference genes for RT-qPCR expression studies in hop (Humulus lupulus L.) during infection with vascular pathogen verticillium albo-atrum. PLoS ONE. 2013;8:e68228. doi: 10.1371/journal.pone.0068228. PubMed DOI PMC
McGrath K.C., Dombrecht B., Manners J.M., Schenk P.M., Edgar C.I., Maclean D.J., Scheible W.-R., Udvardi M.K., Kazan K. Repressor- and Activator-Type Ethylene Response Factors Functioning in Jasmonate Signaling and Disease Resistance Identified via a Genome-Wide Screen of Arabidopsis Transcription Factor Gene Expression. Plant Physiol. 2005;139:949–959. doi: 10.1104/pp.105.068544. PubMed DOI PMC
Seo E., Choi D. Functional studies of transcription factors involved in plant defenses in the genomics era. Brief. Funct. Genom. 2015;14:260–267. doi: 10.1093/bfgp/elv011. PubMed DOI
Sakuma Y., Liu Q., Dubouzet J.G., Abe H., Shinozaki K., Yamaguchi- Shinozaki K. DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 2002;290:998–1009. doi: 10.1006/bbrc.2001.6299. PubMed DOI
Eulgem T. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 2005;10:71–78. doi: 10.1016/j.tplants.2004.12.006. PubMed DOI
Zhu T., Nevo E., Sun D., Peng J. Phylogenetic analyses unravel the evolutionary history of nac proteins in plants. Evolution. 2012;66:1833–1848. doi: 10.1111/j.1558-5646.2011.01553.x. PubMed DOI
Buscaill P., Rivas S. Transcriptional control of plant defence responses. Curr. Opin. Plant Biol. 2014;20:35–46. doi: 10.1016/j.pbi.2014.04.004. PubMed DOI
Riechmann J.L., Heard J., Martin G., Reuber L., Jiang C.-Z., Keddie J., Adam L., Pineda O., Ratcliffe O.J., Samaha R.R., et al. Transcription Factors: Genome-Wide Comparative Analysis Among Eukaryotes. Science. 2000;290:2105–2110. doi: 10.1126/science.290.5499.2105. PubMed DOI
Nakano T., Suzuki K., Fujimura T., Shinshi H. Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice. Plant Physiol. 2006;140:411–432. doi: 10.1104/pp.105.073783. PubMed DOI PMC
Fan K., Wang M., Miao Y., Ni M., Bibi N., Yuan S., Li F., Wang X. Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS ONE. 2014;9:e111837. doi: 10.1371/journal.pone.0111837. PubMed DOI PMC
Shiu S.-H., Shih M.-C., Li W.-H. Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol. 2005;139:18–26. doi: 10.1104/pp.105.065110. PubMed DOI PMC
Wen J., Zhang J.-Q., Nie Z.-L., Zhong Y., Sun H. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Front. Genet. 2014;5:4. doi: 10.3389/fgene.2014.00004. PubMed DOI PMC
Kaessmann H. Origins, evolution, and phenotypic impact of new genes. Genome Res. 2010;20:1313–1326. doi: 10.1101/gr.101386.109. PubMed DOI PMC
Muthamilarasan M., Khandelwal R., Yadav C.B., Bonthala V.S., Khan Y., Prasad M. Identification and molecular characterization of MYB Transcription Factor Superfamily in C4 model plant foxtail millet (Setaria italica L.) PLoS ONE. 2014;9:e109920. doi: 10.1371/journal.pone.0109920. PubMed DOI PMC
Tompa P., Davey N.E., Gibson T.J., Babu M.M. A Million peptide motifs for the molecular biologist. Mol. Cell. 2014;55:161–169. doi: 10.1016/j.molcel.2014.05.032. PubMed DOI
Wu K., Wu K., Guo Z., Guo Z., Wang H., Wang H., Li J., Li J. The WRKY Family of Transcription Factors in Rice and. Gene. 2005;26:9–26. doi: 10.1073/pnas.1420294112. PubMed DOI
Xie T., Chen C., Li C., Liu J., Liu C., He Y. Genome-wide investigation of WRKY gene family in pineapple: Evolution and expression profiles during development and stress. BMC Genom. 2018;19:1–18. doi: 10.1186/s12864-018-4880-x. PubMed DOI PMC
Nath V.S., Koyyappurath S., Alex T.E., Geetha K.A., Augustine L., Nasser A., Thomas G. Transcriptome-based mining and expression profiling of Pythium responsive transcription factors in Zingiber sp. Funct. Integr. Genom. 2018 doi: 10.1007/s10142-018-0644-6. PubMed DOI
Tatusov R.L., Koonin E.V., Lipman D.J. A genomic perspective on genomic families. Science. 1997;278:631–637. doi: 10.1126/science.278.5338.631. PubMed DOI
Thornton J.W., DeSalle R. Gene Family Evolution and Homology: Genomics Meets Phylogenetics. Annu. Rev. Genom. Hum. Genet. 2000;1:41–73. doi: 10.1146/annurev.genom.1.1.41. PubMed DOI
Chen R., Jeong S.S. Functional prediction: Identification of protein orthologs and paralogs. Protein Sci. 2000;9:2344–2353. doi: 10.1110/ps.9.12.2344. PubMed DOI PMC
Jiang Z., Dong X., Zhang Z. Network-Based Comparative Analysis of Arabidopsis Immune Responses to Golovinomyces orontii and Botrytis cinerea Infections. Sci. Rep. 2016;6:19149. doi: 10.1038/srep19149. PubMed DOI PMC
Reményi A., Good M.C., Bhattacharyya R.P., Lim W.A. The Role of Docking Interactions in Mediating Signaling Input, Output, and Discrimination in the Yeast MAPK Network. Mol. Cell. 2005;20:951–962. doi: 10.1016/j.molcel.2005.10.030. PubMed DOI
Alves M.S., Dadalto S.P., Gonçalves A.B., de Souza G.B., Barros V.A., Fietto L.G. Transcription Factor Functional Protein-Protein Interactions in Plant Defense Responses. Proteomes. 2014;2:85–106. doi: 10.3390/proteomes2010085. PubMed DOI PMC
Geisler-Lee J., O’Toole N., Ammar R., Provart N.J., Millar A.H., Geisler M. A predicted interactome for Arabidopsis. Plant Physiol. 2007;145:317–329. doi: 10.1104/pp.107.103465. PubMed DOI PMC
Musungu B., Bhatnagar D., Brown R.L., Fakhoury A.M., Geisler M. A predicted protein interactome identifies conserved global networks and disease resistance subnetworks in maize. Front. Genet. 2015;6:201. doi: 10.3389/fgene.2015.00201. PubMed DOI PMC
Chi Y., Yang Y., Zhou Y., Zhou J., Fan B., Yu J.-Q., Chen Z. Protein–Protein Interactions in the Regulation of WRKY Transcription Factors. Mol. Plant. 2013;6:287–300. doi: 10.1093/mp/sst026. PubMed DOI
Owens R.A., Tech K.B., Shao J.Y., Sano T., Baker C.J. Global Analysis of Tomato Gene Expression During Potato spindle tuber viroid Infection Reveals a Complex Array of Changes Affecting Hormone Signaling. Mol. Plant-Microbe Interact. 2012;25:582–598. doi: 10.1094/MPMI-09-11-0258. PubMed DOI
Katsarou K., Wu Y., Zhang R., Bonar N., Morris J., Hedley P.E., Bryan G.J., Kalantidis K., Hornyik C. Insight on Genes Affecting Tuber Development in Potato upon Potato spindle tuber viroid (PSTVd) Infection. PLoS One. 2016;11:e0150711. doi: 10.1371/journal.pone.0150711. PubMed DOI PMC
Więsyk A., Iwanicka-Nowicka R., Fogtman A., Zagórski-Ostoja W., Góra-Sochacka A. Time-Course Microarray Analysis Reveals Differences between Transcriptional Changes in Tomato Leaves Triggered by Mild and Severe Variants of Potato Spindle Tuber Viroid. Viruses. 2018;10:257. doi: 10.3390/v10050257. PubMed DOI PMC
Dubos C., Stracke R., Grotewold E., Weisshaar B., Martin C., Lepiniec L. MYB transcription factors in Arabidopsis. Trends Plant Sci. 2010;15:573–581. doi: 10.1016/j.tplants.2010.06.005. PubMed DOI
Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W.-L., Gomez-Gomez L., Boller T., Ausubel F.M., Sheen J. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002;415:977. doi: 10.1038/415977a. PubMed DOI
Zheng Y., Wang Y., Ding B., Fei Z. Comprehensive Transcriptome Analyses Reveal that Potato Spindle Tuber Viroid Triggers Genome-Wide Changes in Alternative Splicing, Inducible trans-Acting Activity of Phased Secondary Small Interfering RNAs, and Immune Responses. J. Virol. 2017;91:e00247-17. doi: 10.1128/JVI.00247-17. PubMed DOI PMC
Maldonado A.M., Amil-Ruiz F., Muñoz-Blanco J., Encinas-Villarejo S., Caballero J.L., de los Santos B., Romero F., Pliego-Alfaro F. Evidence for a positive regulatory role of strawberry (Fragaria×ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J. Exp. Bot. 2009;60:3043–3065. doi: 10.1093/jxb/erp152. PubMed DOI
Bhattarai K.K., Atamian H.S., Kaloshian I., Eulgem T. WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J. 2010;63:229–240. doi: 10.1111/j.1365-313X.2010.04232.x. PubMed DOI
Shi W., Hao L., Li J., Liu D., Guo X., Li H. The Gossypium hirsutum WRKY gene GhWRKY39-1 promotes pathogen infection defense responses and mediates salt stress tolerance in transgenic Nicotiana benthamiana. Plant Cell Rep. 2014;33:483–498. doi: 10.1007/s00299-013-1548-5. PubMed DOI
YANG S., ZHOU L., MIAO L., SHI J., SUN C., FAN W., LAN J., CHEN H., LIU L., DOU S., et al. The expression and binding properties of the rice WRKY68 protein in the Xa21-mediated resistance response to Xanthomonas oryzae pv. Oryzae. J. Integr. Agric. 2016;15:2451–2460. doi: 10.1016/S2095-3119(15)61265-5. DOI
Fan S., Dong L., Han D., Zhang F., Wu J., Jiang L., Cheng Q., Li R., Lu W., Meng F., et al. GmWRKY31 and GmHDL56 Enhances Resistance to Phytophthora sojae by Regulating Defense-Related Gene Expression in Soybean. Front. Plant Sci. 2017;8:781. doi: 10.3389/fpls.2017.00781. PubMed DOI PMC
Shearer H.L., Wang L., DeLong C., Despres C., Fobert P.R. NPR1 enhances the DNA binding activity of the Arabidopsis bZIP transcription factor TGA7This paper is one of a selection of papers published in a Special Issue from the National Research Council of Canada – Plant Biotechnology Institute. Botany. 2009;87:561–570. doi: 10.1139/B08-143. DOI
Kan J., Liu T., Ma N., Li H., Li X., Wang J., Zhang B., Chang Y., Lin J. Transcriptome analysis of Callery pear (Pyrus calleryana) reveals a comprehensive signalling network in response to Alternaria alternata. PLoS ONE. 2017;12:e0184988. doi: 10.1371/journal.pone.0184988. PubMed DOI PMC
Berens M.L., Berry H.M., Mine A., Argueso C.T., Tsuda K. Evolution of Hormone Signaling Networks in Plant Defense. Annu. Rev. Phytopathol. 2017;55:401–425. doi: 10.1146/annurev-phyto-080516-035544. PubMed DOI
Dang F., Wang Y., She J., Lei Y., Liu Z., Eulgem T., Lai Y., Lin J., Yu L., Lei D., et al. Overexpression of CaWRKY27, a subgroup IIe WRKY transcription factor of Capsicum annuum, positively regulates tobacco resistance to Ralstonia solanacearum infection. Physiol. Plant. 2014;150:397–411. doi: 10.1111/ppl.12093. PubMed DOI
Li J., Brader G., Kariola T., Tapio Palva E. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 2006;46:477–491. doi: 10.1111/j.1365-313X.2006.02712.x. PubMed DOI
Phukan U.J., Jeena G.S., Shukla R.K. WRKY Transcription Factors: Molecular Regulation and Stress Responses in Plants. Front. Plant Sci. 2016;7:1–14. doi: 10.3389/fpls.2016.00760. PubMed DOI PMC
Cai X.-T., Xu P., Zhao P.-X., Liu R., Yu L.-H., Xiang C.-B. Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat. Commun. 2014;5:5833. doi: 10.1038/ncomms6833. PubMed DOI
Scheideler M., Schlaich N.L., Fellenberg K., Beissbarth T., Hauser N.C., Vingron M., Slusarenko A.J., Hoheisel J.D. Monitoring the Switch from Housekeeping to Pathogen Defense Metabolism in Arabidopsis thaliana Using cDNA Arrays. J. Biol. Chem. 2002;277:10555–10561. doi: 10.1074/jbc.M104863200. PubMed DOI
Windram O., Madhou P., McHattie S., Hill C., Hickman R., Cooke E., Jenkins D.J., Penfold C.A., Baxter L., Breeze E., et al. Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis. Plant Cell. 2012;24:3530–3557. doi: 10.1105/tpc.112.102046. PubMed DOI PMC
Shi J.X., Malitsky S., de Oliveira S., Branigan C., Franke R.B., Schreiber L., Aharoni A. SHINE transcription factors act redundantly to pattern the archetypal surface of arabidopsis flower organs. PLoS Genet. 2011;7 doi: 10.1371/journal.pgen.1001388. PubMed DOI PMC
Hasson A., Plessis A., Blein T., Adroher B., Grigg S., Tsiantis M., Boudaoud A., Damerval C., Laufs P. Evolution and Diverse Roles of the CUP-SHAPED COTYLEDON Genes in Arabidopsis Leaf Development. Plant Cell. 2011;23:54–68. doi: 10.1105/tpc.110.081448. PubMed DOI PMC
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