Negative regulation of ABA Signaling By WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100

eLife

Volumn 4, Issue JUNE2015, 2015, Pages

  Liu, Shouan ^a,c   Kracher, Barbara ^a   Ziegler, Jörg ^b   Birkenbihl, Rainer P ^a   Somssich, Imre E ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; PHYTOHORMONE; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WRKY33 PROTEIN; 9-CIS-EPOXY-CAROTENOID DIOXYGENASE; ARABIDOPSIS PROTEIN; DIOXYGENASE; PLANT PROTEIN; TRANSCRIPTION FACTOR; WRKY33 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; BINDING SITE; BOTRYTIS CINEREA; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLANT GROWTH; PLANT IMMUNITY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ARABIDOPSIS; BIOSYNTHESIS; BOTRYTIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT DISEASE;

ARABIDOPSIS; BOTRYOTINIA FUCKELIANA; BOTRYTIS;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOSYNTHETIC PATHWAYS; BOTRYTIS; DIOXYGENASES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; PLANT DISEASES; PLANT PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84937061325     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07295     Document Type: Article

References (95)

1. Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R. 2007. ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. The Plant Cell 19:1665-1681. doi: 10.1105/tpc.106.048041.
2. Alexa A, Rahnenführer J. 2010. topGO: Enrichment analysis for Gene Ontology. R package version 2.18.0. http://www.bioconductor.org/packages/release/bioc/html/topGO.html.
3. Alexandre C, Vincent JP. 2003. Requirements for transcriptional repression and activation by Engrailed in Drosophila embryos. Development 130:729-739. doi: 10.1242/dev.00286.
4. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Nielsen HB, Hirt H, Somssich I, Mattsson O, Mundy J. 2005. The MAP kinase substrate MKS1 is a regulator of plant defense responses. The EMBO Journal 24:2579-2589. doi: 10.1038/sj.emboj.7600737.
5. Asselbergh B, De Vleesschauwer D, Höfte M. 2008. Global switches and fine-tuning-ABA modulates plant pathogen defense. Molecular Plant-Microbe Interactions 21:709-719. doi: 10.1094/MPMI-21-6-0709.
6. Bari R, Jones J. 2009. Role of plant hormones in plant defence responses. Plant Molecular Biology 69:473-488. doi: 10.1007/s11103-008-9435-0.
7. Berger N, Dubreucq B. 2012. Evolution goes GAGA: GAGA binding proteins across kingdoms. Biochimica et Biophysica Acta (BBA) 1819:863-868. doi: 10.1016/j.bbagrm.2012.02.022.
8. Berrocal-Lobo M, Molina A, Solano R. 2002. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. The Plant Journal 29:23-32. doi: 10.1046/j.1365-313x.2002.01191.x.
9. Birkenbihl RP, Diezel C, Somssich IE. 2012. Arabidopsis WRKY33 is a key transcriptional regulator of hormone and metabolic responses towards Botrytis cinerea infection. Plant Physiology 159:266-285. doi: 10.1104/pp.111.192641.
10. Birkenbihl RP, Somssich IE. 2011. Transcriptional plant responses critical for resistance towards necrotrophic pathogens. Frontiers in Plant Science 2:76. doi: 10.3389/fpls.2011.00076.
11. Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C. 2008. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Research 18:756-767. doi: 10.1038/cr.2008.53.
12. Carlson M. 2010. org.At.tair.db: Genome wide annotation for Arabidopsis. R package version 3.0.0. http://www.bioconductor.org/packages/release/data/annotation/html/org.At.tair.db.html.
13. Chang K, Zhong S, Weirauch M, Hon G, Pelizzola M, Li H, Huang SS, Schmitz R, Urich MA, Kuo D, Nery J, Qiao H, Yang A, Jamali A, Chen H, Ideker T, Ren B, Bar-Joseph Z, Hughes T, Ecker J. 2013. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife 2:00675. doi: 10.7554/eLife.00675.
14. Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, Chen JY, Wang F, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z. 2012. Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiology 159:810-825. doi: 10.1104/pp.112.196816.
15. Ciolkowski I, Wanke D, Birkenbihl R, Somssich IE. 2008. Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Molecular Biology 68:81-92. doi: 10.1007/s11103-008-9353-1.
16. Cusanovich DA, Pavlovic B, Pritchard JK, Gilad Y. 2014. The functional consequences of variation in transcription factor binding. PLOS Genetics 10:e1004226. doi: 10.1371/journal.pgen.1004226.
17. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiology 139:5-17. doi: 10.1104/pp.105.063743.
18. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M. 2007. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. The EMBO Journal 26:1434-1443. doi: 10.1038/sj.emboj.7601575.
19. Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13:414-430. doi: 10.1111/j.1364-3703.2011.00783.x.
20. Eulgem T. 2006. Dissecting the WRKY web of plant defense regulators. PLOS Pathogens 2:e126. doi: 10.1371/journal.ppat.0020126.
21. Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH, Kim SK, Mudgett MB, Wang ZY. 2014. The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. The Plant Cell 26:828-841. doi: 10.1105/tpc.113.121111.
22. Finkelstein R. 2013. Abscisic acid synthesis and response. The Arabidopsis Book 11:e0166. doi: 10.1199/tab.0166.
23. Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A. 2012. Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. The Plant Journal 70:501-512. doi: 10.1111/j.1365-313X.2011.04887.x.
24. Gachon C, Saindrenan P. 2004. Real-time PCR monitoring of fungal development in Arabidopsis thaliana infected by Alternaria brassicicola and Botrytis cinerea. Plant Physiology and Biochemistry 42:367-371. doi: 10.1016/j.plaphy.2004.04.001.
25. Gendrel AV, Lippman Z, Martienssen R, Colot V. 2005. Profiling histone modification patterns in plants using genomic tiling microarrays. Nature Methods 2:213-218. doi: 10.1038/nmeth0305-213.
26. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Reviews of Phytopathology 43:205-227. doi: 10.1146/annurev.phyto.43.040204.135923.
27. Gonzalez-Lamothe R, Boyle P, Dulude A, Roy V, Lezin-Doumbou C, Kaur GS, Bouarab K, Despres C, Brisson N. 2008. The transcriptional activator Pti4 is required for the recruitment of a repressosome nucleated by repressor SEBF at the potato PR-10a gene. The Plant Cell 20:3136-3147. doi: 10.1105/tpc.108.061721.
28. González-Lamothe R, El Oirdi M, Brisson N, Bouarab K. 2012. The conjugated auxin indole-3-acetic acid—aspartic acid promotes plant disease development. The Plant Cell 24:762-777.
29. Grant C, Bailey T, Noble W. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017-1018. doi: 10.1093/bioinformatics/btr064.
30. Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C. 2012. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. The Plant Cell Online 24:2515-2527. doi: 10.1105/tpc.112.099119.
31. Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y, Zhang S. 2010. Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. The Plant Journal 64:114-127.
32. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Molecular Cell 38:576-589. doi: 10.1016/j.molcel.2010.05.004.
33. Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D. 2013. JAV1 controls jasmonate-regulated plant defense. Molecular Cell 50:504-515. doi: 10.1016/j.molcel.2013.04.027.
34. Huang PY, Yeh YH, Liu AC, Cheng CP, Zimmerli L. 2014. The Arabidopsis LecRK-VI.2 associates with the patternrecognition receptor FLS2 and primes Nicotiana benthamiana pattern-triggered immunity. The Plant Journal 79: 243-255. doi: 10.1111/tpj.12557.
35. Ikeda M, Mitsuda N, Ohme-Takagi M. 2009. Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. The Plant Cell 21:3493-3505. doi: 10.1105/tpc.109.069997.
36. Jensen MK, Hagedorn PH, De Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF. 2008. Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. The Plant Journal 56:867-880. doi: 10.1111/j.1365-313X.2008.03646.x.
37. Jensen MK, Lindemose S, Fd Masi, Reimer JJ, Nielsen M, Perera V, Workman CT, Turck F, Grant MR, Mundy J, Petersen M, Skriver K. 2013. ATAF1 transcription factor directly regulates abscisic acid biosynthetic gene NCED3 in Arabidopsis thaliana. FEBS Open Bio 3:321-327. doi: 10.1016/j.fob.2013.07.006.
38. Jiang H, Li H, Bu Q, Li C. 2009. The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signaling & Behavior 4:464-466. doi: 10.1104/pp.109.135269.
39. Kazan K, Manners JM. 2013. MYC2: the master in action. Molecular Plant 6:686-703. doi: 10.1093/mp/sss128.
40. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/gb-2013-14-4-r36.
41. Kliebenstein DJ, Rowe HC, Denby KJ. 2005. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. The Plant Journal 44:25-36. doi: 10.1111/j.1365-313X.2005.02508.x.
42. Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ, Chen Z. 2011. Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. The Plant Cell 23:3824-3841. doi: 10.1105/tpc.111.090571.
43. Langmead B, Trapnell C, Pop M, Salzberg S. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10:R25. doi: 10.1186/gb-2009-10-3-r25.
44. Law C, Chen Y, Shi W, Smyth G. 2014. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biology 15:R29. doi: 10.1186/gb-2014-15-2-r29.
45. Łázniewska J, Macioszek V, Lawrence C, Kononowicz A. 2010. Fight to the death: Arabidopsis thaliana defense response to fungal necrotrophic pathogens. Acta Physiologiae Plantarum 32:1-10. doi: 10.1007/s11738-009-0372-6.
46. Leng P, Yuan B, Guo Y, Chen P. 2014. The role of abscisic acid in fruit ripening and responses to abiotic stress. Journal of Experimental Botany 65:4577-4588. doi: 10.1093/jxb/eru204.
47. Léon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JAD, Koornneef M. 1996. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. The Plant Journal 10:655-661. doi: 10.1046/j.1365-313X.1996.10040655.x.
48. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S. 2012. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLOS Genetics 8:e1002767. doi: 10.1371/journal.pgen.1002767.
49. Lippok B, Birkenbihl RP, Rivory G, Brümmer J, Schmelzer E, Logemann E, Somssich IE. 2007. Expression of AtWRKY33 encoding a pathogen-/PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Molecular Plant-Microbe Interactions 20:420-429. doi: 10.1094/MPMI-20-4-0420.
50. Llorca CM, Potschin M, Zentgraf U. 2014. bZIPS and WRKYs: two large transcription factor families executing two different functional strategies. Frontiers in Plant Science 5:169. doi: 10.3389/fpls.2014.00169.
51. Luo H, Laluk K, Lai Z, Veronese P, Song F, Mengiste T. 2010. The Arabidopsis Botrytis Susceptible1 Interactor defines a subclass of RING E3 ligases that regulate pathogen and stress responses. Plant Physiology 154: 1766-1782. doi: 10.1104/pp.110.163915.
52. Machanick P, Bailey T. 2011. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27:1696-1697. doi: 10.1093/bioinformatics/btr189.
53. Machens F, Becker M, Umrath F, Hehl R. 2014. Identification of a novel type of WRKY transcription factor binding site in elicitor-responsive cis-sequences from Arabidopsis thaliana. Plant Molecular Biology 84:371-385. doi: 10.1007/s11103-013-0136-y.
54. MacQuarrie KL, Fong AP, Morse RH, Tapscott SJ. 2011. Genome-wide transcription factor binding: beyond direct target regulation. Trends in Genetics 27:141-148. doi: 10.1016/j.tig.2011.01.001.
55. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S. 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. The Plant Cell 23:1639-1653. doi: 10.1105/tpc.111.084996.
56. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17:10-12. doi: 10.14806/ej.17.1.200.
57. Mengiste T. 2012. Plant immunity to necrotrophs. Annual Review of Phytopathology 50:267-294. doi: 10.1146/annurev-phyto-081211-172955.
58. Miao Y, Laun T, Zimmermann P, Zentgraf U. 2004. Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Molecular Biology 55:853-867. doi: 10.1007/s11103-005-2142-1.
59. Miyakawa T, Fujita Y, Yamaguchi-Shinozaki K, Tanokura M. 2013. Structure and function of abscisic acid receptors. Trends in Plant Science 18:259-266. doi: 10.1016/j.tplants.2012.11.002.
60. Moffat CS, Ingle RA, Wathugala DL, Saunders NJ, Knight H, Knight MR. 2012. ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PLOS ONE 7:e35995. doi: 10.1371/journal.pone.0035995.
61. Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA, Glazebrook J. 2007. Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. The Plant Cell 19:2039-2052. doi: 10.1105/tpc.107.051383.
62. Nurmberg PL, Knox KA, Yun BW, Morris PC, Shafiei R, Hudson A, Loake GJ. 2007. The developmental selector AS1 is an evolutionarily conserved regulator of the plant immune response. Proceedings of the National Academy of Sciences of USA 104:18795-18800. doi: 10.1073/pnas.0705586104.
63. Pandey SP, Somssich IE. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiology 150: 1648-1655. doi: 10.1104/pp.109.138990.
64. Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, Uhrig J, Weyhe M, Scheel D, Lee J. 2014. The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of ‘VQ-motif’-containing proteins to regulate immune responses. New Phytologist 203:592-606. doi: 10.1111/nph.12817.
65. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5:308-316. doi: 10.1038/nchembio.164.
66. Pré M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J. 2008. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiology 147:1347-1357. doi: 10.1104/pp.108.117523.
67. Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M. 2008. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. The EMBO Journal 27:2214-2221. doi: 10.1038/emboj.2008.147.
68. Quinlan A, Hall I. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842. doi: 10.1093/bioinformatics/btq033.
69. Ramírez V, Agorio A, Coego A, García-Andrade J, Hernández MJ, Balaguer B, Ouwerkerk PB, Zarra I, Vera P. 2011. MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiology 155: 1920-1935. doi: 10.1104/pp.110.171843.
70. Robatzek S, Somssich IE. 2002. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes & Development 16:1139-1149. doi: 10.1101/gad.222702.
71. Robert-Seilaniantz A, Grant M, Jones JD. 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology 49:317-343. doi: 10.1146/annurev-phyto-073009-114447.
72. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. doi: 10.1093/bioinformatics/btp616.
73. Rowe HC, Kliebenstein DJ. 2008. Complex genetics control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. Genetics 180:2237-2250. doi: 10.1534/genetics.108.091439.
74. Rushton PJ, Somssich IE, Ringler P, Shen QJ. 2010. WRKY transcription factors. Trends in Plant Science 15: 247-258. doi: 10.1016/j.tplants.2010.02.006.
75. Sakabe NJ, Aneas I, Shen T, Shokri L, Park SY, Bulyk ML, Evans SM, Nobrega MA. 2012. Dual transcriptional activator and repressor roles of TBX20 regulate adult cardiac structure and function. Human Molecular Genetics 21:2194-2204. doi: 10.1093/hmg/dds034.
76. Sánchez-Vallet A, López G, Ramos B, Delgado-Cerezo M, Riviere MP, Llorente F, Fernández PV, Miedes E, Estevez JM, Grant M, Molina A. 2012. Disruption of abscisic acid signaling constitutively activates Arabidopsis resistance to the necrotrophic fungus. Plectosphaerella Cucumerina. Plant Physiology 160:2109-2124. doi: 10.1104/pp.112.200154.
77. Sánchez-Vallet A, Ramos B, Bednarek P, López G, Piślewska-Bednarek M, Schulze-Lefert P, Molina A. 2010. Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. The Plant Journal 63:115-127. doi: 10.1111/j.1365-313X.2010.04224.x.
78. Schmieder R, Edwards R. 2011. Quality control and preprocessing of metagenomic datasets. Bioinformatics 27: 863-864. doi: 10.1093/bioinformatics/btr026.
79. Shankaranarayanan P, Mendoza-Parra MA, Walia M, Wang L, Li N, Trindade LM, Gronemeyer H. 2011. Single-tube linear DNA amplification (LinDA) for robust ChIP-seq. Nature Methods 8:565-567. doi: 10.1038/nmeth.1626.
80. Singh P, Kuo YC, Mishra S, Tsai CH, Chien CC, Chen CW, Desclos-Theveniau M, Chu PW, Schulze B, Chinchilla D, Boller T, Zimmerli L. 2012. The lectin receptor kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. The Plant Cell 24:1256-1270. doi: 10.1105/tpc.112.095778.
81. Ton J, Flors V, Mauch-Mani B. 2009. The multifaceted role of ABA in disease resistance. Trends in Plant Science 14: 310-317. doi: 10.1016/j.tplants.2009.03.006.
82. Valouev A, Johnson DS, Sundquist A, Medina C, Anton E, Batzoglou S, Myers RM, Sidow A. 2008. Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nature Methods 5:829-834. doi: 10.1038/nmeth.1246.
83. Wang X, Basnayake BM, Zhang H, Li G, Li W, Virk N, Mengiste T, Song F. 2009. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Molecular Plant-Microbe Interactions 22:1227-1238. doi: 10.1094/MPMI-22-10-1227.
84. Williamson B, Tudzynski B, Tudzynski P, Van Kan JAL. 2007. Botrytis cinerea: the cause of grey mould disease. Molecular Plant Pathology 8:561-580. doi: 10.1111/j.1364-3703.2007.00417.x.
85. Windram O, Madhou P, McHattie S, Hill C, Hickman R, Cooke E, Jenkins DJ, Penfold CA, Baxter L, Breeze E, Kiddle SJ, Rhodes J, Atwell S, Kliebenstein DJ, Ys Kim, Stegle O, Borgwardt K, Zhang C, Tabrett A, Legaie R, Moore J, Finkenstadt B, Wild DL, Mead A, Rand D, Beynon J, Ott S, Buchanan-Wollaston V, Denby KJ. 2012. Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. The Plant Cell 24:3530-3557. doi: 10.1105/tpc.112.102046.
86. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. 2010. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. The Plant Cell 22:508-522. doi: 10.1105/tpc.109.068874.
87. Young M, Wakefield M, Smyth G, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11:R14. doi: 10.1186/gb-2010-11-2-r14.
88. Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y. 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. The Plant Journal 65:634-646. doi: 10.1111/j.1365-313X.2010.04449.x.
89. Zander M, Thurow C, Gatz C. 2014. TGA transcription factors activate the salicylic acid-suppressible branch of the ethylene-induced defense program by regulating ORA59 expression. Plant Physiology 165:1671-1683. doi: 10.1104/pp.114.243360.
90. Zhao Y, Wei T, Yin KQ, Chen Z, Gu H, Qu LJ, Qin G. 2012. Arabidopsis RAP2.2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytologist 195:450-460. doi: 10.1111/j.1469-8137.2012.04160.x.
91. Zheng XY, Spivey Natalie W, Zeng W, Liu PP, Fu Zheng Q, Klessig Daniel F, He Sheng Y, Dong X. 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host & Microbe 11:587-596. doi: 10.1016/j.chom.2012.04.014.
92. Zheng Z, Qamar SA, Chen Z, Mengiste T. 2006. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. The Plant Journal 48:592-605. doi: 10.1111/j.1365-313X.2006.02901.x.
93. Zhou N, Tootle TL, Glazebrook J. 1999. Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. The Plant Cell 11:2419-2428. doi: 10.1105/tpc.11.12.2419.
94. Zhu X, Wang Y, Pi W, Liu H, Wickrema A, Tuan D. 2012. NF-Y recruits both transcription activator and repressor to modulate tissue-and developmental stage-specific expression of human γ-globin gene. PLOS ONE 7:e47175. doi: 10.1371/journal.pone.0047175.
95. Ziegler J, Qwegwer J, Schubert M, Erickson JL, Schattat M, Bürstenbinder K, Grubb CD, Abel S. 2014. Simultaneous analysis of apolar phytohormones and 1-aminocyclopropan-1-carboxylic acid by high performance liquid chromatography/electrospray negative ion tandem mass spectrometry via 9-fluorenylmethoxycarbonyl chloride derivatization. Journal of Chromatography A 1362:102-109. doi: 10.1016/j.chroma.2014.08.029.