Identification and functional analysis of mitogen-activated protein kinase kinase kinase (MAPKKK) genes in canola (Brassica napus L.)

Journal of Experimental Botany

Volumn 65, Issue 8, 2014, Pages 2171-2188

  Sun, Yun ^a   Wang, Chen ^a   Yang, Bo ^a   Wu, Feifei ^a   Hao, Xueyu ^a   Liang, Wanwan ^a   Niu, Fangfang ^a   Yan, Jingli ^a   Zhang, Hanfeng ^a   Wang, Boya ^a   Deyholos, Michael K ^b   Jiang, Yuan Qing ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Abiotic stress; Brassica napus; Cell death; MAPKKK; MKK; Sclerotinia sclerotiorum

Indexed keywords

COMPLEMENTARY DNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGICAL STRESS; POLYMERASE CHAIN REACTION; RAPESEED; SEQUENCE ALIGNMENT; TWO HYBRID SYSTEM;

AMINO ACID SEQUENCE; BRASSICA NAPUS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION REGULATION, PLANT; MAP KINASE KINASE KINASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STRESS, PHYSIOLOGICAL; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84898952340     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru092     Document Type: Article

References (69)

1. Amselem J, Cuomo CA, van Kan JA, et al. 2011. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genetics 7, e1002230
2. Andreasson E, Jenkins T, Brodersen P, et al. 2005. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO Journal 24, 2579-2589
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. Bardwell AJ, Flatauer LJ, Matsukuma K, Thorner J, Bardwell L. 2001. A conserved docking site in MEKs mediates high-Affinity binding to MAP kinases and cooperates with a scaffold protein to enhance signal transmission. Journal of Biological Chemistry 276, 10374-10386
5. Becerra C, Jahrmann T, Puigdomenech P, Vicient CM. 2004. Ankyrin repeat-containing proteins in Arabidopsis: Characterization of a novel and abundant group of genes coding ankyrin-Transmembrane proteins. Gene 340, 111-121
6. Campanella JJ, Bitincka L, Smalley J. 2003. MatGAT: An application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4, 29
7. Cessna SG, Sears VE, Dickman MB, Low PS. 2000. Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. The Plant Cell 12, 2191-2200
8. Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M. 2007. Botrytis cinerea virulence factors: New insights into a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters 277, 1-10
9. Clark KL, Larsen PB, Wang X, Chang C. 1998. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proceedings of the National Academy of Sciences, USA 95, 5401-5406
10. Colcombet J, Hirt H. 2008. Arabidopsis MAPKs: A complex signalling network involved in multiple biological processes. Biochemical Journal 413, 217-226
11. Daudi A, Cheng Z, O'Brien JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP. 2012. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-Triggered immunity. The Plant Cell 24, 275-287
12. del Pozo O, Pedley KF, Martin GB. 2004. MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO Journal 23, 3072-3082
13. Doczi R, Brader G, Pettko-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H. 2007. The Arabidopsis mitogen-Activated protein kinase kinase MKK3 is upstream of group C mitogen-Activated protein kinases and participates in pathogen signaling. The Plant Cell 19, 3266-3279
14. Feller A, Hernandez JM, Grotewold E. 2006. An ACT-like domain participates in the dimerization of several plant basic-helix-loop-helix transcription factors. Journal of Biological Chemistry 281, 28964-28974
15. Frye CA, Tang D, Innes RW. 2001. Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proceedings of the National Academy of Sciences, USA 98, 373-378
16. Galletti R, Ferrari S, De Lorenzo G. 2011. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide-or flagellininduced resistance against Botrytis cinerea. Plant Physiology 157, 804-814
17. Gentile AC. 1954. Carbohydrate metabolism and oxalic acid synthesis by Botrytis cinerea. Plant Physiology 29, 257-261
18. Grewal S, Molina DM, Bardwell L. 2006. Mitogen-Activated protein kinase (MAPK)-Docking sites in MAPK kinases function as tethers that are crucial for MAPK regulation in vivo. Cell Signaling 18, 123-134
19. Guimaraes RL, Stotz HU. 2004. Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiology 136, 3703-3711
20. Hamel LP, Nicole MC, Sritubtim S, et al. 2006. Ancient signals: Comparative genomics of plant MAPK and MAPKK gene families. Trends in Plant Science 11, 192-198
21. Hashimoto M, Komatsu K, Maejima K, Okano Y, Shiraishi T, Ishikawa K, Takinami Y, Yamaji Y, Namba S. 2012. Identification of three MAPKKKs forming a linear signaling pathway leading to programmed cell death in Nicotiana benthamiana. BMC Plant Biology 12, 103
22. Heller J, Tudzynski P. 2011. Reactive oxygen species in phytopathogenic fungi: Signaling, development, and disease. Annual Review of Phytopathology 49, 369-390
23. Ichimura K, Casais C, Peck S, Shinozaki K, Shirasu K. 2006. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-Dependent cell death in Arabidopsis. Journal of Biological Chemistry 281, 36969-36976
24. Ichimura K, Shinozaki K, Tena G, et al. 2002. Mitogen-Activated protein kinase cascades in plants: A new nomenclature. Trends in Plant Science 7, 301-308
25. Jaspers P, Kangasjarvi J. 2010. Reactive oxygen species in abiotic stress signaling. Physiologia Plantarum 138, 405-413
26. Jin H, Axtell MJ, Dahlbeck D, Ekwenna O, Zhang S, Staskawicz B, Baker B. 2002. NPK1, an MEKK1-like mitogen-Activated protein kinase kinase kinase, regulates innate immunity and development in plants. Developmeental Cell 3, 291-297
27. Jonak C, Okresz L, Bogre L, Hirt H. 2002. Complexity, cross talk and integration of plant MAP kinase signalling. Current Opinion in Plant Biology 5, 415-424
28. Jouannic S, Hamal A, Leprince AS, Tregear JW, Kreis M, Henry Y. 1999. Plant MAP kinase kinase kinases structure, classification and evolution. Gene 233, 1-11
29. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427-441
30. Kim KS, Min JY, Dickman MB. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Molecular Plant-Microbe Interactions 21, 605-612
31. Kong Q, Qu N, Gao M, et al. 2012. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogenactivated protein kinase kinase kinase in Arabidopsis. The Plant Cell 24, 2225-2236
32. Kong X, Lv W, Zhang D, Jiang S, Zhang S, Li D. 2013. Genome-wide identification and analysis of expression profiles of maize mitogen-Activated protein kinase kinase kinase. PLoS One 8, e57714
33. Kumar K, Rao KP, Biswas DK, Sinha AK. 2011. Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signaling and Behavior 6, 316-320
34. Lanier W, Moustafa A, Bhattacharya D, Comeron JM. 2008. EST analysis of Ostreococcus lucimarinus, the most compact eukaryotic genome, shows an excess of introns in highly expressed genes. PLoS One 3, e2171
35. Li S, Wilkinson MF. 1997. Site-Directed mutagenesis: A two-step method using PCR and DpnI. Biotechniques 23, 588-590
36. Liang W, Yang B, Yu B, et al. 2013. Identification and analysis of MKK and MPK gene families in canola (Brassica napus L). BMC Genomics 14, 392
37. Liu H, Wang Y, Xu J, Su T, Liu G, Ren D. 2008. Ethylene signaling is required for the acceleration of cell death induced by the activation of AtMEK5 in Arabidopsis. Cell Research 18, 422-432
38. Liu Y, Schiff M, Dinesh-Kumar SP. 2004. Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. The Plant Journal 38, 800-809
39. Lysak MA, Cheung K, Kitschke M, Bures P. 2007. Ancestral chromosomal blocks are triplicated in Brassiceae species with varying chromosome number and genome size. Plant Physiology 145, 402-410
40. Lysak MA, Koch MA, Pecinka A, Schubert I. 2005. Chromosome triplication found across the tribe Brassiceae. Genome Research 15, 516-525
41. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S. 2011. Phosphorylation of a WRKY transcription factor by two pathogenresponsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. The Plant Cell 23, 1639-1653
42. Melech-Bonfil S, Sessa G. 2010. Tomato MAPKKKepsilon is a positive regulator of cell-Death signaling networks associated with plant immunity. The Plant Journal 64, 379-391
43. Meng X, Zhang S. 2013. MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology 51, 245-266
44. Miao Y, Laun TM, Smykowski A, Zentgraf U. 2007. Arabidopsis MEKK1 can take a short cut: It can directly interact with senescencerelated WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Molecular Biology 65, 63-76
45. Nakagami H, Kiegerl S, Hirt H. 2004. OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. Journal of Biological Chemistry 279, 26959-26966
46. Ning J, Li X, Hicks L, Xiong L. 2010. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiology 152, 876-890
47. Oh CS, Hwang J, Choi MS, Kang BC, Martin GB. 2013. Two leucines in the N-Terminal MAPK-Docking site of tomato SlMKK2 are critical for interaction with a downstream MAPK to elicit programmed cell death associated with plant immunity. FEBS Letters 587, 1460-1465
48. Oh CS, Martin GB. 2011. Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-Associated programmed cell death mediated by diverse disease resistance proteins. Journal of Biological Chemistry 286, 14129-14136
49. Oh CS, Pedley KF, Martin GB. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-Associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK α. The Plant Cell 22, 260-272
50. Osborn TC. 2004. The contribution of polyploidy to variation in Brassica species. Physiologia Plantarum 121, 531-536
51. Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ. 2005. Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171, 765-781
52. Petersen K, Qiu JL, Lutje J, Fiil BK, Hansen S, Mundy J, Petersen M. 2010. Arabidopsis MKS1 is involved in basal immunity and requires an intact N-Terminal domain for proper function. PLoS One 5, e14364
53. Petersen M, Brodersen P, Naested H, et al. 2000. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111-1120
54. Popescu S, Popescu G, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar S. 2009. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes and Development 23, 80-92
55. Qiu JL, Fiil BK, Petersen K, et al. 2008. Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO Journal 27, 2214-2221
56. Rana D, Van Den Boogaart T, O'Neill CM, Hynes L, Bent E, Macpherson L, Park JY, Lim YP, Bancroft I. 2004. Conservation of the microstructure of genome segments in Brassica napus and its diploid relatives. The Plant Journal 40, 725-733
57. Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK. 2010. In silico analysis reveals 75 members of mitogen-Activated protein kinase kinase kinase gene family in rice. DNA Research 17, 139-153
58. Rietz S, Bernsdorff FE, Cai D. 2012. Members of the germin-like protein family in Brassica napus are candidates for the initiation of an oxidative burst that impedes pathogenesis of Sclerotinia sclerotiorum. Journal of Experimental Botany 63, 5507-5519
59. Rodriguez MC, Petersen M, Mundy J. 2010. Mitogen-Activated protein kinase signaling in plants. Annual Review of Plant Biology 61, 621-649
60. Sedgwick SG, Smerdon SJ. 1999. The ankyrin repeat: A diversity of interactions on a common structural framework. Trends in Biochemical Science 24, 311-316
61. Singh R, Lee MO, Lee JE, et al. 2012. Rice mitogen-Activated protein kinase interactome analysis using the yeast two-hybrid system. Plant Physiology 160, 477-487
62. Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K. 2007. The mitogen-Activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. The Plant Cell 19, 805-818
63. Torres MA, Dangl JL. 2005. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Current Opinion in Plant Biology 8, 397-403
64. Waadt R, Schmidt LK, Lohse M, Hashimoto K, Bock R, Kudla J. 2008. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. The Plant Journal 56, 505-516
65. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. 2007. Stomatal development and patterning are regulated by environmentally responsive mitogen-Activated protein kinases in Arabidopsis. The Plant Cell 19, 63-73
66. Wang Y, Liu K, Liao H, Zhuang C, Ma H, Yan X. 2008. The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biology (Stuttgart) 10, 548-562
67. Xu B, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, Cobb MH. 2000. WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. Journal of Biological Chemistry 275, 16795-16801
68. Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN. 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 Biology 9, 68
69. Yang B, Srivastava S, Deyholos MK, Kav NNV. 2007. Transcriptional profiling of canola (Brassica napus L) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Science 173, 156-171