Abstract
The CORONATINE INSENSITIVE (COI) plays pivotal roles in plant growth and development, including pollen fertility, defence against pests, trichome formation, and seed germination. In this study, we performed bioinformatics characterization of COI proteins in tomato and analysed their expression profile analysis under abiotic stress. A total of nine members of the COI gene family were isolated and phylogenetically clustered into five distinct clades with Arabidopsis, rice, maize, and other related plant species. Subcellular localization showed selected COI proteins predominantly localized in the nucleus. The reverse transcription quantitative real-time polymerase chain reaction analysis revealed distinct spatial expression patterns SlCOIs among different tissues mainly found in the root and fruits of different developmental stages. In addition, we examined different hormone and abiotic stresses related to cis-regulatory sequences in upstream regions of these genes. Further, we examined differential changes in SlCOIs transcripts accumulation in response to different hormones (ABA, IAA, GA, SA and MeJA), salinity, drought, and cold. It was found that SlCOI1, SlCOI2, SlCOI3, SlCOI4, SlCOI5 and SlCOI7 was peaked under ABA, GA, SA and MeJA while, SlCOI1, SlCOI3, SlCOI6 and SlCOI8 were upregulated under salt, drought, and cold. These results provide invaluable insights into functional and protein functional features. Our research also provides a foundation for further functional characterization of COI genes in tomato.
Similar content being viewed by others
References
Abdelkareem A., Thagun C., Nakayasu M., Mizutani M., Hashimoto T. and Shoji T. 2017 Jasmonate-induced biosynthesis of steroidal glycoalkaloids depends on COI1 proteins in tomato. Biochem. Biophys. Res. Commun. 489, 206–210.
Abuqamar S., Chai M. F., Luo H., Song F. and Mengiste T. 2008 Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 20, 1964–1983.
Acosta I. F., Laparra H., Romero S. P., Schmelz E., Hamberg M., Mottinger J. P. et al. 2009 tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323, 262–265.
Adams E. and Turner J. 2010 COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J. Exp. Bot. 61, 4373–4386.
Bailey T. L. and Elkan C. 1994 Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28–36.
Bauer A. M., Bo Y., Han L., He J., Lanczycki C. J., Lu S. et al. 2017 CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic. Acids Res. 45, D200–D203.
Castillo M. C. and Leon J. 2008 Expression of the beta-oxidation gene 3-ketoacyl-CoA thiolase 2 (KAT2) is required for the timely onset of natural and dark-induced leaf senescence in Arabidopsis. J. Exp. Bot. 59, 2171–2179.
Cheng Z., Li S., Qi T., Zhang B., Peng W., Liu Y. et al. 2011 The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate Jasmonate response in Arabidopsis. Mol. Plant 4, 279–288.
Chico J. M., Chini A., Fonseca S. and Solano R. 2008 JAZ repressors set the rhythm in jasmonate signaling. Curr. Opin. Plant Biol. 11, 486–494.
Comeron J. M. 1999 K-estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15, 763–764.
Creelman R. A. and Mullet J. E. 1997 Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 355–381.
Devoto A., Nieto-Rostro M., Xie D., Ellis C., Harmston R., Patrick E. et al. 2002 COI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32, 457–466.
Devoto A., Ellis C., Magusin A., Chang H. S., Chilcott C., Zhu T. et al. 2005 Expression profiling reveals COI1 to be a key regulator of genes involved in wound- and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol. Biol. 58, 497–513.
Farmer E. E., Almeras E. and Krishnamurthy V. 2003 Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6, 372–378.
Fernandez-Pozo N., Menda N., Edwards J. D., Saha S., Tecle I. Y., Strickler S. R. et al. 2015 The sol genomics network (SGN)–from genotype to phenotype to breeding. Nucleic. Acids Res. 43, D1036–D1041.
Feys B., Benedetti C. E., Penfold C. N. and Turner J. G. 1994 Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751–759.
Finn R. D., Tate J., Mistry J., Coggill P. C., Sammut S. J., Hotz H. R. et al. 2008 The Pfam protein families database. Nucleic. Acids Res. 36, D281–D288.
Finn R. D., Clements J. and Eddy S. R. 2011 HMMER web server: interactive sequence similarity searching. Nucleic. Acids Res. 39, W29–W37.
Goodstein D. M., Shu S., Howson R., Neupane R., Hayes R. D., Fazo J. et al. 2012 Phytozome: a comparative platform for green plant genomics. Nucleic. Acids Res. 40, D1178–D1186.
Goossens J., Fernandez-Calvo P., Schweizer F. and Goossens A. 2016 Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol. Biol. 91, 673–689.
Horton P., Park K. J., Obayashi T., Fujita N., Harada H., Adams-Collier C. J. et al. 2007 WoLF PSORT: protein localization predictor. Nucleic. Acids Res. 35, W585–W587.
Hu B., Jin J., Guo A. Y., Zhang H., Luo J. and Gao G. 2015 GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31, 1296–1297.
Ishiga Y., Ishiga T., Uppalapati S. R. and Mysore K. S. 2013 Jasmonate ZIM-domain (JAZ) protein regulates host and nonhost pathogen-induced cell death in tomato and Nicotiana benthamiana. PLoS One 8, e75728.
Jian-fang B., Wang Y. K., Wang P., Yuan S. H., Gao J. G., Duan W. J. et al. 2018 Genome-wide identification and analysis of the COI gene family in wheat (Triticum aestivum L.). BMC Genom. 19, 754.
Kim J., Dotson B., Rey C., Lindsey J., Bleecker A. B., Binder B. M. et al. 2013 New clothes for the jasmonic acid receptor COI1: delayed abscission, meristem arrest and apical dominance. PLoS One 8, e60505.
Koch M. A., Haubold B. and Olds T. M. 2000 Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17, 1483–1498.
Kondo S., Tomiyama A. and Seto H. 2000 Changes of endogenous jasmonic acid and methyl jasmonate in apples and sweet cherries during fruit development. J. Am. Soc. Hortic. Sci. 125, 282–287.
Kumar S., Stecher G., Li M., Knyaz C. and Tamura K. 2018 MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549.
Lee S. H., Sakuraba Y., Lee T., Kim K. W., An G., Lee H. Y. et al. 2015 Mutation of Oryza sativa CORONATINE INSENSITIVE 1b (OsCOI1b) delays leaf senescence. J. Integr. Plant Biol. 57, 562–576.
Lescot M., Dehais P., Thijs G., Marchal K., Moreau Y., Van de Peer Y. et al. 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 X. 2011 Infiltration of Nicotiana benthamiana protocol for transient expression via agrobacterium. Bio. Protoc. 1, e95.
Li L., Zhao Y., McCaig B. C., Wingerd B. A., Wang J., Whalon M. E. et al. 2004 The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16, 126–143.
Liao Y., Wei J., Xu Y. and Zhang Z. 2015 Cloning, expression and characterization of COI1 gene (AsCOI1) from Aquilaria sinensis (Lour.) Gilg. Acta Pharm. Sin. B 5, 473–481.
Liu K., Yuan C., Feng S., Zhong S., Li H., Zhong J. et al. 2017 Genome-wide analysis and characterization of aux/IAA family genes related to fruit ripening in papaya (Carica papaya L.). BMC Genom. 18, 1–11.
Livak K. J. and Schmittgen T. D. 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methethods 25, 402–448.
Mcconn M., Creelman R. A., Bell E., Mullet J. E. and Browse J. 1997 Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 94, 5473–5477.
McConn M. and Browse J. 1996 The critical requirement for linolenic acid is pollen development, not photosynthesis, in an arabidopsis mutant. Plant Cell 8, 146–403.
Meissner R., Jacobson Y., Melamed S., Levyatuv S., Shalev G., Ashri A. et al. 2002 A new model system for tomato genetics. Plant J. 12, 1465–1472.
Mosblech A., Thurow C., Gatz G., Feussner I. and Heilmann I. 2011 Jasmonic acid perception by COI1 involves inositol polyphosphates in Arabidopsis thaliana. Plant J. 65, 949–957.
Pauwels L., Morreel K., Witte E. D., Lammertyn F., Montagu M. V., Boerjan W. et al. 2008 Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc. Natl. Acad. Sci. USA 105, 1380–1385.
Pfeifer M., Kugler K. G., Sandve S. R., Zhan B., Rudi H., Hvidsten T. R. et al. 2014 Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345, 1250091.
Qiang C., Yuan Z., Chen M., Yin C., Luo Z., Zhao X. et al. 2014 Jasmonic acid regulates spikelet development in rice. Nat. Commun. 5, 3476.
Reinbothe C., Springer A., Samol I. and Reinbothe S. 2009 Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. Febs J. 276, 4666–4681.
Reiser L., Subramaniam S., Li D. and Huala E. 2017 Using the Arabidopsis information resource (TAIR) to find information about Arabidopsis genes. Curr. Protoc. Bioinform. 60, 1.11.1-1.11.45.
Saitou N. and Nei M. 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.
Sanders P. M., Lee P. Y., Biesgen C., Boone J. D., Beals T. P., Weiler E. W. et al. 2000 The arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12, 1041–1461.
Schultz J., Milpetz F., Bork P. and Ponting C. P. 1998 SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. USA 95, 5857.
Seo J. S., Joo J., Kim M. J., Kim Y. K., Nahm B. H., Song S. I. et al. 2011 OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J. 65, 907–921.
Stothard P. 2000 The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28, 1104.
Turner J. G., Ellis C. and Devoto A. 2002 The jasmonate signal pathway. Plant Cell 14, S153–S164.
VanDoorn A., Bonaventure G., Schmidt D. D. and Baldwin I. T. 2011 Regulation of jasmonate metabolism and activation of systemic signaling in Solanum nigrum: COI1 and JAR4 play overlapping yet distinct roles. New Phytol. 190, 640–652.
Wang Y., Qiao L., Bai J., Peng W., Duan W., Yuan S. et al. 2017 Genome-wide characterization of JASMONATE-ZIM DOMAIN transcription repressors in wheat (Triticum aestivum L.). BMC Genom. 18, 1–19.
Waseem M., Ahmad F., Habib S., Gao Y. and Li Z. 2018 Genome-wide identification of FK506-binding domain protein gene family, its characterization, and expression analysis in tomato (Solanum lycopersicum L.). Gene 678, 143–154.
Wasternack C. and Hause B. 2013 Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. an update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021–1058.
Weidhase R. A., Kramell H. M., Lehmann J., Liebisch H. W., Lerbs W. and Parthier B. 1987 Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments. Plant Sci. 51, 177–186.
Xie D. X., Feys B. F., James S., Rostro M. N. and Turner J. G. 1998 COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094.
Xu L., Liu F., Lechner E., Genschik P., Crosby W. L., Ma H., Peng W. et al. 2002 The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935.
Yan J., Zhang C., Gu M., Bai Z., Zhang W., Qi T. et al. 2009 The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220–2236.
Zhang Y.-M., Ni X.-I., Ma H.-Q. and Qiu W. 2009 Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J. Exp. Bot. 60, 3849–3860.
Author information
Authors and Affiliations
Contributions
MW performed the experiments, MW and IS carried out the analyses and MW, MMA, and IS drafted the manuscript and revised it. All authors approved the final version of the manuscript.
Corresponding author
Additional information
Corresponding editor: Manoj Prasad
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Waseem, M., Aslam, M.M. & Shaheen, I. Tomato COI gene family identification and expression under abiotic and phytohormone stress. J Genet 100, 80 (2021). https://doi.org/10.1007/s12041-021-01331-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12041-021-01331-0