Abstract
Mitogen-activated protein kinases (MAPKs) are important components of the tripartite mitogen-activated protein kinase signaling cascade and play an important role in plant growth and development. Although members of the MAPK gene family have been identified in model plants, little information is available regarding this gene family in fruit crops. In this study, we carried out a computational analysis using the Musa Genome database to identify members of the MAPK gene family in banana, an economically important crop and the most popular fruit worldwide. Our analysis identified 25 members of the MAP kinase (MAPK or MPK) gene family. Phylogenetic analyses of MPKs in Arabidopsis, Oryza, and Populus have classified these MPKs into four subgroups. The presence of conserved domains in the deduced amino acid sequences, phylogeny, and genomic organization strongly support their identity as members of the MPK gene family. Expression analysis during ethylene-induced banana fruit ripening suggests the involvement of several MPKs in the ethylene signal transduction pathway that are necessary for banana fruit ripening. Analysis of the cis-regulatory elements in the promoter regions and the involvement of the identified MPKs in various cellular processes, as analyzed using Pathway Studio, suggest a role for the banana MPK gene family in diverse functions related to growth, development, and the stress response. This report is the first concerning the identification of members of a gene family and the elucidation of their role in various processes using the Musa Genome database.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asif M, Trivedi P, Solomos T, Tucker M (2006) Isolation of high-quality RNA from apple (Malus domestica) fruit. J Agric Food Chem 54:5227–5229
Asif MH, Trivedi PK, Misra P, Nath P (2009a) Prolyl-4-hydroxylase (AtP4H1) mediates and mimics low oxygen response in Arabidopsis thaliana. Funct Integr Genomics 9:525–535
Asif MH, Pathak N, Solomos T, Trivedi PK (2009b) Effect of low oxygen, temperature and 1-methylcyclopropene on the expression of genes regulating ethylene biosynthesis and perception during ripening in apple. S Afr J Bot 75:137–144
Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR et al (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28:94–107
Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, Kumar S, Rai A, Pandey A, Nigam D, Tripathi RD, Tuli R (2009) Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere 74:688–702
Chen L, Hu W, Tan S, Wang M, Ma Z, Zhou S, Deng X, Zhang Y, Huang C, Yang G, He G (2012) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One 7:e46744
Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972
D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, Garsmeur O, Noel B, Bocs S, Droc G, Rouard M, Da Silva C, Jabbari K, Cardi C, Poulain J, Souquet M, Labadie K, Jourda C, Lengelle J, Rodier-Goud M, Alberti A, Bernard M, Correa M, Ayyampalayam S, McKain MR, Leebens-Mack J, Burgess D, Freeling M, Mbeguie AMD, Chabannes M, Wicker T, Panaud O, Barbosa J, Hribova E, Heslop-Harrison P, Habas R, Rivallan R, Francois P, Poiron C, Kilian A, Burthia D, Jenny C, Bakry F, Brown S, Guignon V, Kema G, Dita M, Waalwijk C, Joseph S, Dievart A, Jaillon O, Leclercq J, Argout X, Lyons E, Almeida A, Jeridi M, Dolezel J, Roux N, Risterucci AM, Weissenbach J, Ruiz M, Glaszmann JC, Quetier F, Yahiaoui N, Wincker P (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217
Doczi R, Okresz L, Romero AE, Paccanaro A, Bogre L (2012) Exploring the evolutionary path of plant MAPK networks. Trends Plant Sci 17:518–525
Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr (VI) stress. BMC Genomics 11:648
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–37
Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40:D26–32
Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198
Janitza P, Ullrich KK, Quint M (2012) Toward a comprehensive phylogenetic reconstruction of the evolutionary history of mitogen-activated protein kinases in the plant kingdom. Front Plant Sci 3:271
Kesari R, Trivedi PK, Nath P (2007) Ethylene-induced ripening in banana evokes expression of defense and stress related genes in fruit tissue. Postharvest Biol Technol 46:136–143
Kesari R, Trivedi PK, Nath P (2010) Gene expression of pathogenesis-related protein during banana ripening and after treatment with 1-MCP. Postharvest Biol Technol 56:64–70
Kong F, Wang J, Cheng L, Liu S, Wu J, Peng Z, Lu G (2012) Genome-wide analysis of the mitogen-activated protein kinase gene family in Solanum lycopersicum. Gene 499:108–120
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:D1202–D1210
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li CY, Deng GM, Yang J, Viljoen A, Jin Y, Kuang RB, Zuo CW, Lv ZC, Yang QS, Sheng O, Wei YR, Hu CH, Dong T, Yi GJ (2012) Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genomics 13:374
Lohani S, Trivedi PK, Nath P (2004) Changes in activities of cell wall hydrolases during ethylene-induced ripening in banana: effect of 1-MCP, ABA and IAA. Postharvest Biol Technol 31:119–126
Misra P, Pandey A, Tiwari M, Chandrashekar K, Sidhu OP, Asif MH, Chakrabarty D, Singh PK, Trivedi PK, Nath P, Tuli R (2010) Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol 152:2258–2268
Nikitin A, Egorov S, Daraselia N, Mazo I (2003) Pathway studio—the analysis and navigation of molecular networks. Bioinformatics 19:2155–2157
Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35:D883–887
Pathak N, Asif MH, Dhawan P, Srivastava MK, Nath P (2003) Expression and activities of ethylene biosynthesis enzymes during ripening of banana fruits and effect of 1-MCP treatment. Plant Growth Regul 40:11–19
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 Res 17:139–153
Samajova O, Plihal O, Al-Yousif M, Hirt H, Samaj J (2013) Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. Biotechnol Adv 31:118–128
Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH et al. (2013) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 38(Database issue):D5–16.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2012) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Trivedi PK, Nath P (2004) MaExp1, an ethylene-induced expansin from ripening banana fruit. Plant Sci 167:1351–1358
Zhang X, Cheng T, Wang G, Yan Y, Xia Q (2013) Cloning and evolutionary analysis of tobacco MAPK gene family. Mol Biol Rep 40:1407–1415
Acknowledgments
This work was supported by a research grant from the Council of Scientific and Industrial Research, New Delhi, as Network Project (BSC-107). SP acknowledges Council of Scientific and Industrial Research Govt. of India for Senior Research Fellowships. The authors acknowledge Dr. Shirish A. Ranade, Chief Scientist, CSIR-NBRI for editing the manuscript to refine the language.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table S1
(DOCX 12 kb)
Supplementary Table S2
(XLS 266 kb)
Rights and permissions
About this article
Cite this article
Asif, M.H., Lakhwani, D., Pathak, S. et al. Genome-wide identification and expression analysis of the mitogen-activated protein kinase gene family from banana suggest involvement of specific members in different stages of fruit ripening. Funct Integr Genomics 14, 161–175 (2014). https://doi.org/10.1007/s10142-013-0349-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-013-0349-9