Genome-wide identification of MAPK, MAPKK, and MAPKKK gene families and transcriptional profiling analysis during development and stress response in cucumber

BMC Genomics

Gang Lu²  Tao Zou²  Lifei Chen¹  Jian Wu¹  Lei Ye¹  Yan Wang¹  Changtian Pan²  Jie Wang² 

[1] Department of Horticulture, Zhejiang University, Hangzhou 310058, China;Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Hangzhou 310058, China

关键词: Plant hormones;    Biotic stress;    Abiotic stress;    MAPK;    MAPKK;    MAPKKK;    Cucumis sativus;   

Others  :  1203941
DOI  :  10.1186/s12864-015-1621-2

 received in 2014-12-23, accepted in 2015-05-05,  发布年份 2015

【 摘 要 】

Background

The mitogen-activated protein kinase (MAPK) cascade consists of three types of reversibly phosphorylated kinases, namely, MAPK, MAPK kinase (MAPKK/MEK), and MAPK kinase kinase (MAPKKK/MEKK), playing important roles in plant growth, development, and defense response. The MAPK cascade genes have been investigated in detail in model plants, including Arabidopsis, rice, and tomato, but poorly characterized in cucumber (Cucumis sativus L.), a major popular vegetable in Cucurbitaceae crops, which is highly susceptible to environmental stress and pathogen attack.

Results

A genome-wide analysis revealed the presence of at least 14 MAPKs, 6 MAPKKs, and 59 MAPKKKs in the cucumber genome. Phylogenetic analyses classified all the CsMAPK and CsMAPKK genes into four groups, whereas the CsMAPKKK genes were grouped into the MEKK, RAF, and ZIK subfamilies. The expansion of these three gene families was mainly contributed by segmental duplication events. Furthermore, the ratios of non-synonymous substitution rates (Ka) and synonymous substitution rates (Ks) implied that the duplicated gene pairs had experienced strong purifying selection. Real-time PCR analysis demonstrated that some MAPK, MAPKK and MAPKKK genes are preferentially expressed in specific organs or tissues. Moreover, the expression levels of most of these genes significantly changed under heat, cold, drought, and Pseudoperonospora cubensis treatments. Exposure to abscisic acid and jasmonic acid markedly affected the expression levels of these genes, thereby implying that they may play important roles in the plant hormone network.

Conclusion

A comprehensive genome-wide analysis of gene structure, chromosomal distribution, and evolutionary relationship of MAPK cascade genes in cucumber are present here. Further expression analysis revealed that these genes were involved in important signaling pathways for biotic and abiotic stress responses in cucumber, as well as the response to plant hormones. Our first systematic description of the MAPK, MAPKK, and MAPKKK families in cucumber will help to elucidate their biological roles in plant.

【 授权许可】

   
2015 Wang et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Liu SQ, Xu L, Jia ZQ, Xu Y, Yang Q, Fei ZJ et al.. Genetic association of ETHYLENE-INSENSITIVE3-like sequence with the sex-determining M locus in cucumber (Cucumis sativus L.). Theor Appl Genet. 2008; 117(6):927-933.
• [2]Lee SH, Singh AP, Chung GC. Rapid accumulation of hydrogen peroxide in cucumber roots due to exposure to low temperature appears to mediate decreases in water transport. J Exp Bot. 2004; 55(403):1733-1741.
• [3]Janoudi AK, Widders IE, Flore JA. Water deficits and environmental-factors affect photosynthesis in leaves of cucumber (Cucumis sativus). J Am Soc Hortic Sci. 1993; 118(3):366-370.
• [4]Wyszogrodzka AJ, Williams PH, Peterson CE. Multiple-pathogen inoculation of cucumber (cucumis sativus) seedlings. Plant Dis. 1987; 71(3):275-280.
• [5]Huang SW, Li RQ, Zhang ZH, Li L, Gu XF, Fan W et al.. The genome of the cucumber, Cucumis sativus L. Nat Genet. 2009; 41(12):1275-1229.
• [6]Hu LF, Liu SQ. Genome-wide analysis of the MADS-box gene family in cucumber. Genome. 2012; 55(3):245-256.
• [7]Wan HJ, Yuan W, Bo KL, Shen J, Pang X, Chen JF. Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics. 2013; 14(109):1471-2164.
• [8]Li Q, Zhang CJ, Li J, Wang L, Ren ZH. Genome-wide identification and characterization of R2R3MYB family in Cucumis sativus. PLoS One. 2012; 7(10):e47576.
• [9]Baloglu MC, Eldem V, Hajyzadeh M, Unver T. Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS One. 2014; 9(4):e96014.
• [10]Ling J, Jiang WJ, Zhang Y, Yu HJ, Mao ZC, Gu XF et al.. Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics. 2011; 12(471):1471-2164.
• [11]Yu YJ, Liang Y, Lv ML, Wu J, Lu G, Cao JS. Genome-wide identification and characterization of polygalacturonase genes in Cucumis sativus and Citrullus lanatus. Plant Physiol Bioch. 2014; 74:263-275.
• [12]Tena G, Asai T, Chiu W-L, Sheen J. Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Bio. 2001; 4(5):392-400.
• [13]Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L et al.. Diverse signals converge at MAPK cascades in plant. Plant Physiol Bioch. 2006; 44(5–6):274-283.
• [14]Jimenez C, Cossio BR, Rivard CJ, Berl T, Capasso JM. Cell division in the unicellular microalga Dunaliella viridis depends on phosphorylation of extracellular signal-regulated kinases (ERKs). J Exp Bot. 2007; 58(5):1001-1011.
• [15]Xu J, Zhang SQ. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci. 2015; 20(1):56-64.
• [16]Pitzschke A, Schikora A, Hirt H. MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol. 2009; 12(4):421-426.
• [17]Heinrich M, Baldwin IT, Wu JQ. Two mitogen-activated protein kinase kinases, MKK1 and MEK2, are involved in wounding- and specialist lepidopteran herbivore Manduca sexta-induced responses in Nicotiana attenuata. J Exp Bot. 2011; 62(12):4355-4365.
• [18]Suarez LC, Fernandez RR. Signalling pathway in plants affected by salinity and drought. Itea-Inf Tec Econ Ag. 2010; 106(3):157-169.
• [19]Parages ML, Heinrich S, Wiencke C, Jimenez C. Rapid phosphorylation of MAP kinase-like proteins in two species of Arctic kelps in response to temperature and UV radiation stress. Environ Exp Bot. 2013; 91:30-37.
• [20]Samuel MA, Miles GP, Ellis BE. Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J. 2000; 22(4):367-376.
• [21]Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L et al.. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature. 2002; 415(6875):977-983.
• [22]Galletti R, Ferrari S, De Lorenzo G. Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide-or flagellin-induced resistance against Botrytis cinerea. Plant Physiol. 2011; 157(2):804-814.
• [23]Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K et al.. Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 2008; 148(1):212-222.
• [24]Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B et al.. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell. 2000; 103(7):1111-1120.
• [25]Furuya T, Matsuoka D, Nanmori T. Membrane rigidification functions upstream of the MEKK1-MKK2-MPK4 cascade during cold acclimation in Arabidopsis thaliana. FEBS Lett. 2014; 588(11):2025-2030.
• [26]Zeng Q, Chen JG, Ellis BE. AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J. 2011; 67(5):895-906.
• [27]Eckardt NA. A complete MAPK signaling cascade that functions in stomatal development and patterning in Arabidopsis. Plant Cell. 2007; 19 (1):7–7.
• [28]Liu Y, Schiff M, Dinesh-Kumar S. Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N‐mediated resistance to tobacco mosaic virus. Plant J. 2004; 38(5):800-809.
• [29]Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Gene Dev. 2003; 17(8):1055-1067.
• [30]Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A et al.. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 2002; 7(7):301-308.
• [31]Colcombet J, Hirt H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J. 2008; 413:217-226.
• [32]Jonak C, Ökrész L, Bögre L, Hirt H. Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol. 2002; 5(5):415-424.
• [33]Rohila JS, Yang Y. Rice mitogen-activated protein kinase gene family and its role in biotic and abiotic stress response. J Integr Plant Bio. 2007; 49(6):751-759.
• [34]Wankhede DP, Misra M, Singh P, Sinha AK. Rice mitogen activated protein kinase kinase and mitogen activated protein kinase interaction network revealed by in-silico docking and yeast two-hybrid approaches. PLoS One. 2013; 8(5):e65011.
• [35]Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK. In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res. 2010; 17(3):139-153.
• [36]Liu Y, Zhang D, Wang L, Li D. Genome-wide analysis of mitogen-activated protein kinase gene family in maize. Plant Mol Biol Rep. 2013; 31(6):1446-1460.
• [37]Kong XP, Pan JW, Zhang D, Jiang SS, Cai GH, Wang L et al.. Identification of mitogen-activated protein kinase kinase gene family and MKK-MAPK interaction network in maize. Biochem Bioph Res Co. 2013; 441(4):964-969.
• [38]Kong X, Lv W, Zhang D, Jiang S, Zhang S, Li D. Genome-wide identification and analysis of expression profiles of maize mitogen-activated protein kinase kinase kinase. PLoS One. 2013; 8(2):e57714.
• [39]Kong F, Wang J, Cheng L, Liu S, Wu J, Peng Z et al.. Genome-wide analysis of the mitogen-activated protein kinase gene family in Solanum lycopersicum. Gene. 2012; 499(1):108-120.
• [40]Wu J, Wang J, Pan C, Guan X, Wang Y, Liu S et al.. Genome-wide identification of MAPKK and MAPKKK gene families in tomato and transcriptional profiling analysis during development and stress response. PLoS One. 2014; 9(7):e103032.
• [41]Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K et al.. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 2009; 150(2):801-814.
• [42]Xu HN, Wang XF, Sun XD, Shi QH, Yang FJ, Du DL. Molecular cloning and characterization of a cucumber MAP kinase gene in response to excess NO3− and other abiotic stresses. Sci Hortic. 2008; 117(1):1-8.
• [43]Xu HN, Sun XD, Wang XF, Shi QH, Yang XY, Yang FJ. Involvement of a cucumber MAPK gene (CsNMAPK) in positive regulation of ROS scavengence and osmotic adjustment under salt stress. Sci Hortic. 2011; 127(4):488-493.
• [44]Shoresh M, Gal-On A, Leibman D, Chet I. Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol. 2006; 142(3):1169-1179.
• [45]Bie B, Sun J, Pan J, He H, Cai R. Ectopic expression of CsCTR1, a cucumber CTR-like gene, attenuates constitutive ethylene signaling in an Arabidopsis ctr1-1 mutant and expression pattern analysis of CsCTR1 in cucumber (Cucumis sativus). Int J Mol Sci. 2014; 15(9):16331-16350.
• [46]Neupane A, Nepal MP, Piya S, Subramanian S, Rohila JS, Reese RN et al.. Identification, nomenclature, and evolutionary relationships of mitogen-activated protein kinase (MAPK) genes in soybean. Evol Bioinform. 2013; 9:363.
• [47]Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J et al.. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 2006; 11(4):192-198.
• [48]Chen LH, Hu W, Tan SL, Wang M, Ma ZB, Zhou SY et al.. Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One. 2012; 7(10):e46744.
• [49]Liang W, Yang B, Yu B-J, Zhou Z, Li C, Jia M et al.. Identification and analysis of MKK and MPK gene families in canola (Brassica napus L.). BMC Genomics. 2013; 14(1):392.
• [50]Wrzaczek M, Hirt H. Plant MAP kinase pathways: how many and what for? Bio Cell. 2001; 93(1–2):81-87.
• [51]Sun Y, Wang C, Yang B, Wu FF, Hao XY, Liang WW et al.. Identification and functional analysis of mitogen-activated protein kinase kinase kinase (MAPKKK) genes in canola (Brassica napus L.). J Exp Bot. 2014; 65(8):2171-2188.
• [52]Wang G, Lovato A, Polverari A, Wang M, Liang YH, Ma YC et al.. Genome-wide identification and analysis of mitogen activated protein kinase kinase kinase gene family in grapevine (Vitis vinifera). BMC Plant Biol. 2014; 14(219):1471-2229.
• [53]Tanoue T, Adachi M, Moriguchi T, Nishida E. A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat Cell Biol. 2000; 2(2):110-116.
• [54]Murakami-Kojima M, Nakamichi N, Yamashino T, Mizuno T. The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana. Plant Cell Physiol. 2002; 43(6):675-683.
• [55]Wang Y, Liu K, Liao H, Zhuang C, Ma H, Yan X. The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol. 2008; 10(5):548-562.
• [56]Kumar K, Rao KP, Biswas DK, Sinha AK. Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal Behav. 2011; 6(3):316-320.
• [57]Altenhoff AM, Studer RA, Robinson-Rechavi M, Dessimoz C. Resolving the ortholog conjecture: orthologs tend to be weakly, but significantly, more similar in function than paralogs. Plos Comput Biol. 2012;8(5):e1002514.
• [58]Mattick JS. Introns: evolution and function. Curr Opin Genet Dev. 1994; 4(6):823-831.
• [59]Holub EB. The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet. 2001; 2(7):516-527.
• [60]Gu ZL, Cavalcanti A, Chen FC, Bouman P, Li WH. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol. 2002; 19(3):256-262.
• [61]Liu Q, Xue Q. Computational identification and phylogenetic analysis of the MAPK gene family in Oryza sativa. Plant Physiol Bioch. 2007; 45(1):6-14.
• [62]Liu W, Li W, He Q, Daud MK, Chen J, Zhu S. Genome-wide survey and expression analysis of Calcium-Dependent Protein Kinase in Gossypium raimondii. PLoS One. 2014; 9(6):e98189.
• [63]Schnable PS, Ware D, Fulton RS, Stein JC, Wei FS, Pasternak S et al.. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009; 326(5956):1112-1115.
• [64]Sato S, Tabata S, Hirakawa H, Asamizu E, Shirasawa K, Isobe S et al.. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012; 485(7400):635-641.
• [65]Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ et al.. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature. 2005; 434(7036):980-986.
• [66]Kaul S, Koo HL, Jenkins J, Rizzo M, Rooney T, Tallon LJ et al.. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000; 408(6814):796-815.
• [67]Hord CLH, Suna YJ, Pillitteri LJ, Torii KU, Wang HC, Zhang SQ et al.. Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol Plant. 2008; 1(4):645-658.
• [68]Meng XZ, Wang HC, He YX, Liu YD, Walker JC, Torii KU et al.. A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell. 2012; 24(12):4948-4960.
• [69]Lopez-Bucio JS, Dubrovsky JG, Raya-Gonzalez J, Ugartechea-Chirino Y, Lopez-Bucio J, de Luna-Valdez LA et al.. Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J Exp Bot. 2014; 65(1):169-183.
• [70]Zhou CJ, Cai ZH, Guo YF, Gan SS. An Arabidopsis mitogen-activated protein kinase cascade, MKK9-MPK6, plays a role in leaf senescence. Plant Physiol. 2009; 150(1):167-177.
• [71]Liu JZ, Horstman HD, Braun E, Graham MA, Zhang CQ, Navarre D et al.. Soybean homologs of MPK4 negatively regulate defense responses and positively regulate growth and development. Plant Physiol. 2011; 157(3):1363-1378.
• [72]Shi J, An HL, Zhang LA, Gao Z, Guo XQ. GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol. 2010; 74(1–2):1-17.
• [73]Duan PG, Rao YC, Zeng DL, Yang YL, Xu R, Zhang BL et al.. SMALL GRAIN 1, which encodes a mitogen-activated protein kinase kinase 4, influences grain size in rice. Plant J. 2014; 77(4):547-557.
• [74]Teige M, Scheikl E, Eulgem T, Doczi F, Ichimura K, Shinozaki K et al.. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell. 2004; 15(1):141-152.
• [75]Nakagami H, Soukupova H, Schikora A, Zarsky V, Hirt H. A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem. 2006; 281(50):38697-38704.
• [76]Xing Y, Jia WS, Zhangl JH. AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 2008; 54(3):440-451.
• [77]Cristina MS, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol. 2010; 61:621-649.
• [78]Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M et al.. The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell. 2007; 19(3):805-818.
• [79]Wang Q, Li JC, Hu LF, Zhang TF, Zhang GR, Lou YG. OsMPK3 positively regulates the JA signaling pathway and plant resistance to a chewing herbivore in rice. Plant Cell Rep. 2013; 32(7):1075-1084.
• [80]Lu C, Han MH, Guevara-Garcia A, Fedoroff NV. Mitogen-activated protein kinase signaling in postgermination arrest of development by abscisic acid. Pro Nat Acad Sci USA. 2002; 99(24):15812-15817.
• [81]Yu CS, Lin CJ, Hwang JK. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci. 2004; 13(5):1402-1406.
• [82]Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997; 25(24):4876-4882.
• [83]Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006; 34(suppl 2):W369-W373.
• [84]Saitou N, Nei M. The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-425.
• [85]Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25(11):1451-1452.
• [86]Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S. A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol. 2008; 49(6):865-879.
• [87]Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (T) (−Delta Delta C) method. Methods. 2001; 25(4):402-408.
• [88]Saeed AI, Hagabati NK, Braisted JC, Liang W, Sharov V, Howe EA et al.. TM4 microarray software suite. Methods Enzymol. 2006; 411:134-193.