Integration of Bioinformatics and synthetic promoters leads to the discovery of novel elicitor-responsive cis-regulatory sequences in Arabidopsis

Plant Physiology

Volumn 160, Issue 1, 2012, Pages 178-191

  Koschmann, Jeannette ^a   Machens, Fabian ^a   Becker, Marlies ^a   Niemeyer, Julia ^a   Schulze, Jutta ^a   Bülow, Lorenz ^a   Stahl, Dietmar J ^b   Hehl, Reinhard ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^b KWS SAAT SE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIUM TUMEFACIENS; ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA BENTHAMIANA; PETROSELINUM CRISPUM;

EID: 84865859719     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.198259     Document Type: Article

References (85)

1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63-78.
2. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K (1997) Role of Arabidopsis MYC and MYB homologs in droughtand abscisic acid-regulated gene expression. Plant Cell 9: 1859-1868.
3. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
4. Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3: 21-29.
5. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436.
6. Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106: 8067-8072.
7. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
9. Brady SM, Provart NJ (2009) Web-queryable large-scale data sets for hypothesis generation in plant biology. Plant Cell 21: 1034-1051.
10. Bülow L, Brill Y, Hehl R (2010) AthaMap-assisted transcription factor target gene identification in Arabidopsis thaliana. Database (Oxford) 2010: baq034.
11. Bülow L, Engelmann S, Schindler M, Hehl R (2009) AthaMap, integrating transcriptional and post-transcriptional data. Nucleic Acids Res 37: D983-D986.
12. Bülow L, Schindler M, Choi C, Hehl R (2004) PathoPlant: a database on plant-pathogen interactions. In Silico Biol 4: 529-536.
13. Bülow L, Schindler M, Hehl R (2007) PathoPlant: a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses. Nucleic Acids Res 35: D841-D845.
14. Bülow L, Steffens NO, Galuschka C, Schindler M, Hehl R (2006) Atha-Map: from in silico data to real transcription factor binding sites. In Silico Biol 6: 243-252.
15. Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: plant promoter analysis navigator, for identifying combinatorial cisregulatory elements with distance constraint in plant gene groups. BMC Genomics 9: 561.
16. Che D, Jensen S, Cai L, Liu JS (2005) BEST: binding-site estimation suite of tools. Bioinformatics 21: 2909-2911.
17. Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129: 706-716.
18. Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68: 81-92.
19. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
20. Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinformatics 4: 25.
21. de Pater S, Greco V, Pham K, Memelink J, Kijne J (1996) Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucleic Acids Res 24: 4624-4631.
22. De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon L, Smeekens SC, Pieterse CM (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1: 305-311.
23. de Wet JR, Wood KV, DeLuca M, Helinski DR, Subramani S (1987) Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol 7: 725-737.
24. Du L, Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogenand salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J 24: 837-847.
25. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573-581.
26. Eskin E, Pevzner PA (2002) Finding composite regulatory patterns in DNA sequences. Bioinformatics (suppl 1) 18: S354-S363.
27. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206.
28. Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66: 94-116.
29. Galuschka C, Schindler M, Bülow L, Hehl R (2007) AthaMap web tools for the analysis and identification of co-regulated genes. Nucleic Acids Res 35: D857-D862.
30. Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA, et al (2002) TAIR: a resource for integrated Arabidopsis data. Funct Integr Genomics 2: 239-253.
31. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60: 425-449.
32. GuhaThakurta D, Stormo GD (2001) Identifying target sites for cooperatively binding factors. Bioinformatics 17: 608-621.
33. Guo Y, Gan S (2011) AtMYB2 regulates whole plant senescence by inhibiting cytokinin-mediated branching at late stages of development in Arabidopsis. Plant Physiol 156: 1612-1619.
34. Gurr SJ, Rushton PJ (2005) Engineering plants with increased disease resistance: how are we going to express it? Trends Biotechnol 23: 283-290.
35. Hahlbrock K, Scheel D, Logemann E, Nürnberger T, Parniske M, Reinold S, Sacks WR, Schmelzer E (1995) Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proc Natl Acad Sci USA 92: 4150-4157.
36. Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B (2005) Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 57: 155-171.
37. Hehl R, Bülow L (2008) Internet resources for gene expression analysis in Arabidopsis thaliana. Curr Genomics 9: 375-380.
38. Hehl R, Steffens NO, Wingender E (2004) Isolation and analysis of gene regulatory sequences. In P Christou, H Klee, eds, Handbook of Plant Biotechnology. John Wiley and Sons, Hoboken, NJ, pp 81-102.
39. Hehl R, Wingender E (2001) Database-assisted promoter analysis. Trends Plant Sci 6: 251-255.
40. Hertz GZ, Stormo GD (1999) Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15: 563-577.
41. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300.
42. Hoeren FU, Dolferus R, Wu Y, Peacock WJ, Dennis ES (1998) Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase gene (ADH1) by low oxygen. Genetics 149: 479-490.
43. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: b-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
44. Jensen ST, Liu JS (2004) BioOptimizer: a Bayesian scoring function approach to motif discovery. Bioinformatics 20: 1557-1564.
45. Kim KC, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20: 2357-2371.
46. Kirsch C, Takamiya-Wik M, Schmelzer E, Hahlbrock K, Somssich IE (2000) A novel regulatory element involved in rapid activation of parsley ELI7 gene family members by fungal elicitor or pathogen infection. Mol Plant Pathol 1: 243-251.
47. Liu X, Brutlag DL, Liu JS (2001) BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 6: 127-138.
48. Mahony S, Benos PV (2007) STAMP: a Web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 35: W253-W258.
49. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410.
50. Matys V, Fricke E, Geffers R, Gössling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, et al (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31: 374-378.
51. Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15: 2551-2565.
52. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55: 853-867.
53. Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, Scheel D (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78: 449-460.
54. Palaniswamy SK, James S, Sun H, Lamb RS, Davuluri RV, Grotewold E (2006) AGRIS and AtRegNet. a platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiol 140: 818-829.
55. Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38: D822-D827.
56. Pitzschke A, Djamei A, Teige M, Hirt H (2009) VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc Natl Acad Sci USA 106: 18414-18419.
57. Priest HD, Filichkin SA, Mockler TC (2009) Cis-regulatory elements in plant cell signaling. Curr Opin Plant Biol 12: 643-649.
58. Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, et al (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27: 2214-2221.
59. Reiser L, Rhee SY (2005) Using The Arabidopsis Information Resource (TAIR) to find information about Arabidopsis genes. Curr Protoc Bioinformatics June: Chapter 1: Unit 1.11.
60. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16: 1139-1149.
61. Roth FP, Hughes JD, Estep PW, Church GM (1998) Finding DNA regulatory motifs within unaligned noncoding sequences clustered by whole-genome mRNA quantitation. Nat Biotechnol 16: 939-945.
62. Rushton PJ, Reinstädler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14: 749-762.
63. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15: 247-258.
64. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15: 5690-5700.
65. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, Ed 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
66. Sandelin A, Wasserman WW (2004) Constrained binding site diversity within families of transcription factors enhances pattern discovery bioinformatics. J Mol Biol 338: 207-215.
67. Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66: 361-378.
68. Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Biophys Res Commun 361: 1048-1053.
69. Sprenger-Haussels M, Weisshaar B (2000) Transactivation properties of parsley proline-rich bZIP transcription factors. Plant J 22: 1-8.
70. Stahl DJ, Kloos DU, Hehl R (2004) A sugar beet chlorophyll a/b binding protein promoter void of G-box like elements confers strong and leaf specific reporter gene expression in transgenic sugar beet. BMC Biotechnol 4: 31.
71. Steffens NO, Galuschka C, Schindler M, Bülow L, Hehl R (2004) Atha-Map: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome. Nucleic Acids Res 32: D368-D372.
72. Steffens NO, Galuschka C, Schindler M, Bülow L, Hehl R (2005) Atha-Map Web tools for database-assisted identification of combinatorial cis-regulatory elements and the display of highly conserved transcription factor binding sites in Arabidopsis thaliana. Nucleic Acids Res 33: W397-W402.
73. Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, Wang H, Su SH, Jester PJ, Zhang S, Bent AF, Krysan PJ (2007) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol 143: 661-669.
74. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
75. Tena G, Boudsocq M, Sheen J (2011) Protein kinase signaling networks in plant innate immunity. Curr Opin Plant Biol 14: 519-529.
76. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M, Chow A, Steinhauser D, Persson S, Provart NJ (2009) Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ 32: 1633-1651.
77. van de Löcht U, Meier I, Hahlbrock K, Somssich IE (1990) A 125 bp promoter fragment is sufficient for strong elicitor-mediated gene activation in parsley. EMBO J 9: 2945-2950.
78. Van der Ent S, Verhagen BW, Van Doorn R, Bakker D, Verlaan MG, Pel MJ, Joosten RG, Proveniers MC, Van Loon LC, Ton J, et al (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146: 1293-1304.
79. van Verk MC, Pappaioannou D, Neeleman L, Bol JF, Linthorst HJM (2008) A novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol 146: 1983-1995.
80. Venter M (2007) Synthetic promoters: genetic control through cis engineering. Trends Plant Sci 12: 118-124.
81. Wroblewski T, Tomczak A, Michelmore R (2005) Optimization of Agrobacterium-mediated transient assays of gene expression in lettuce, tomato and Arabidopsis. Plant Biotechnol J 3: 259-273.
82. Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18: 1310-1326.
83. Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E (2011) AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res 39: D1118-D1122.
84. Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR gene expression. Plant Cell 13: 1527-1540.
85. Zou C, Sun K, Mackaluso JD, Seddon AE, Jin R, Thomashow MF, Shiu SH (2011) Cis-regulatory code of stress-responsive transcription in Arabidopsis thaliana. Proc Natl Acad Sci USA 108: 14992-14997.