Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum

Molecular Genetics and Genomics

Volumn 287, Issue 6, 2012, Pages 495-513

  Huang, Shengxiong ^a,b   Gao, Yongfeng ^a,b   Liu, Jikai ^a,b   Peng, Xiaoli ^b   Niu, Xiangli ^b   Fei, Zhangjun ^c,d   Cao, Shuqing ^b   Liu, Yongsheng ^a,b  

^a SICHUAN UNIVERSITY   (China)

^b HEFEI UNIVERSITY OF TECHNOLOGY   (China)

^c United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^d ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

Expression pattern; Phylogenetic analysis; Tomato; Transcriptional factor; WRKY

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WRKY; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ABIOTIC STRESS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; BIOTIC STRESS; CHROMOSOME 5; CONTROLLED STUDY; DROUGHT STRESS; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PLANT DEVELOPMENT; PLANT GENE; PLANT GENOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PSEUDOMONAS SYRINGAE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; SALT STRESS; STRUCTURAL HOMOLOGY; TOMATO; WRKY GENE; CLASSIFICATION; COMPARATIVE STUDY; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY; PLANT CHROMOSOME; SPECIES DIFFERENCE;

ARABIDOPSIS; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; SOLANACEAE;

ARABIDOPSIS; CHROMOSOMES, PLANT; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION; GENES, PLANT; GENOME, PLANT; LYCOPERSICON ESCULENTUM; MULTIGENE FAMILY; ORYZA SATIVA; PHYLOGENY; PLANT PROTEINS; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84864324616     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-012-0696-6     Document Type: Article

References (61)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389-3402
2. Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, Kurabayashi A, Suzuki T, Tsugane T, Watanabe M, Ooga K, Torii M, Narita T, Shin IT, Kohara Y, Yamamoto N, Takahashi H, Watanabe Y, Egusa M, Kodama M, Ichinose Y, Kikuchi M, Fukushima S, Okabe A, Arie T, Sato Y, Yazawa K, Satoh S, Omura T, Ezura H, Shibata D (2010) Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 11:210
3. Atamian HS, Eulgem T, Kaloshian I (2011) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta. doi:10.1007/s00425-011-1509-6
4. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202-W208
5. Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T (2010) 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 63(2):229-240
6. Bombarely A, Menda N, Tecle IY, Buels RM, Strickler S, Fischer-York T, Pujar A, Leto J, Gosselin J, Mueller LA (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 39(Database issue):D1149-D1155
7. Burley SK, Kamada K (2002) Transcription factor complexes. Curr Opin Struct Biol 12(2):225-230
8. Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21(11):3554-3566
9. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10(1):281
10. 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(1-2):81-92
11. Cuartero J, Bolarin MC, Asins MJ, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57(5):1045-1058
12. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27(8):1164-1165
13. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143(4):1789-1801
14. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10(4):366-371
15. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199-206
16. Fei Z, Joung JG, Tang X, Zheng Y, Huang M, Lee JM, McQuinn R, Tieman DM, Alba R, Klee HJ, Giovannoni JJ (2011) Tomato Functional Genomics Database: a comprehensive resource and analysis package for tomato functional genomics. Nucleic Acids Res 39(Database issue):D1156-D1163
17. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(Database Issue):D211-D222
18. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun W-l, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. japonica). Science 296(5565):92-100
19. Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148(1):358-368
20. Higashi K, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Modulation of defense signal transduction by flagellininduced WRKY41 transcription factor in Arabidopsis thaliana. Mol Gen Genet 279(3):303-312
21. Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 50 upstream regions of genes coding for sporamin and β-amylase from sweet potato. Mol Gen Genet 244(6):563-571
22. Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69(1-2):91-105
23. Journot-Catalino N, Somssich IE, Roby D, Kroj T (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18(11):3289-3302
24. Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu Rev Entomol 48:51-72
25. Kim K-C, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with Histone Deacetylase 19 in basal defense. Plant Cell 20(9):2357-2371
26. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41-59
27. Lai Z, Vinod KM, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8(1):68
28. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40(Database issue):D1202-D1210
29. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947-2948
30. Letunic I, Bork P (2011) Interactive Tree Of Life v 2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39(Web Server issue):W475-W478
31. Letunic I, Doerks T, Bork P (2009) SMART 6: recent updates and new developments. Nucleic Acids Res 37(Database issue):D229-D232
32. Levee V, Major I, Levasseur C, Tremblay L, MacKay J, Seguin A (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184(1):48-70
33. Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233(6):1237-1252
34. Liu J-J, Ekramoddoullah AKM (2009) Identification and characterization of the WRKY transcription factor family in Pinus monticola. Genome 52(1):77-88
35. Mangelsen E, Kilian J, Berendzen K, Kolukisaoglu U, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9(1):194
36. 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. Plant Cell 23(4):1639-1653
37. Mukhtar MS, Deslandes L, Auriac M-C, Marco Y, Somssich IE (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J 56(6):935-947
38. Oh S-K, Baek K-H, Park JM, Yi SY, Yu SH, Kamoun S, Choi D (2008) Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol 177(4):977-989
39. Pan Y, Tsai CJ, Ma B, Nussinov R (2010) Mechanisms of transcription factor selectivity. Trends Genet 26(2):75-83
40. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648-1655
41. Pandey SP, Roccaro M, Schön M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64(6):912-923
42. Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2009) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38(Database issue):D822-D827
43. Plant AL, Cohen A, Moses MS, Bray EA (1991) Nucleotide sequence and spatial expression pattern of a drought-and abscisic acidinduced gene of tomato. Plant Physiol 97(3):900-906
44. Riechmann JL, Heard J, Martin G, Reuber L, Jiang ZC, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105-2110
45. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247-258
46. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) TM4 microarray software suite. Methods Enzymol 411:134-193
47. Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie AR (2008) Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20(3):509-523
48. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178-183
49. Shimono M, Koga H, Akagi AYA, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang C-J, Kaku H, Inoue H, Takatsuji H (2011) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol. doi:10.1111/j.1364-3703.2011.00732.x
50. Smith TF, Waterman MS (1981) Identification of common molecular subsequences. J Mol Biol 147(1):195-197
51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA 5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731-2739
52. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596-1604
53. UIker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7(5):491-498
54. Wu K-L, Guo Z-J, Wang H-H, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12(1):9-26
55. Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137(1):176-189
56. Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148(3):1189-1200
57. Yang B, Jiang Y, Rahman M, Deyholos M, Kav N (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9(1):68
58. Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5(1):1
59. Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2. 0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39(Database issue):D1114-D1117
60. Zhou Q-Y, Tian A-G, Zou H-F, Xie Z-M, Lei G, Huang J, Wang C-M, Wang H-W, Zhang J-S, Chen S-Y (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6(5):486-503
61. Zou C, Jiang W, Yu D (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot 61(14):3901-3914