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Transcriptome analysis reveals key defense-related genes upon SA induction in Cocos nucifera L.

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Abstract

Background

Salicylic acid (SA) is an important regulator of genes involved in plant defense and pathogen-triggered systemic acquired resistance (SAR). Coconut is an important crop affected by several pathogens. Reported evidence suggests SA involvement in defense responses, including SAR in coconut.

Objective

To identified differentially expressed genes in leaf and root tissues of coconut plantlets, as a result of SA, that might be involved in coconut defense responses.

Methods

Comparative transcriptomic analysis by RNA-Seq of leaf and root tissues from in vitro coconut plantlets unexposed and exposed to SA 2.5 mM for 48 h. And in silico validation of gene expression by qRT-PCR.

Results

We identified 4615 and 3940 differentially expressed unigenes (DEUs) in leaf and root tissues respectively. Our GO analysis showed functional categories related to the induction of defense responses, such as “systemic acquired resistance” and highly enriched hormone categories, such as abscisic acid. The most abundant KEGG pathway in our results was “Biosynthesis of antibiotics”. Our findings support that exogenous application of SA to plantlets induced the activation of PRs, RGAs, ICS2, NLTP2, PER4, TRXM and some WRKYs mediated by NPR1-dependent pathways. Also, we found DEUs, such as BZR1, HSL1, and WHY2 that support that SA could regulate defense-related genes through NPR1-independent pathways.

Conclusion

The present study of massive data analysis carried out on coconut plantlets exposed to SA, generates valuable information that increases our understanding of defense molecular mechanisms in coconut and open new venues for research for the improvement of management of coconut diseases.

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Availability of data and material

The data are included within the article or additional files and the generated raw sequence dataset can be accessed under accession number PRJNA622305 in the SRA of NCBI.

References

  • Albertazzi G, Milc J, Caffagni A et al (2009) Gene expression in grapevine cultivars in response to Bois Noir phytoplasma infection. Plant Sci 176:792–804. https://doi.org/10.1016/j.plantsci.2009.03.001

    Article  CAS  Google Scholar 

  • Andrews S (2010) FastQC: A quality control tool for high throughput sequence data. Software

  • Balconi C, Stevanato P, Motto M, Biancardi E (2012) Breeding for biotic stress resistance/tolerance in plants. In: Ashraf M, Öztürk M, Ahmad MSA, Aksoy A (eds) Crop production for agricultural improvement. Springer Netherlands, Dordrecht, pp 57–114

    Chapter  Google Scholar 

  • Blanco F, Salinas P, Cecchini NM et al (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102. https://doi.org/10.1007/s11103-009-9458-1

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao H, Bowling SA, Gordon AS, Xinnian D (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592. https://doi.org/10.1105/tpc.6.11.1583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by everexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95:6531–6536. https://doi.org/10.1073/pnas.95.11.6531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  Google Scholar 

  • Cui H, Qiu J, Zhou Y et al (2018) Antagonism of transcription factor MYC2 by EDS1/PAD4 complexes bolsters salicylic acid defense in arabidopsis effector-triggered immunity. Mol Plant 11:1053–1066. https://doi.org/10.1016/j.molp.2018.05.007

    Article  CAS  PubMed  Google Scholar 

  • Desveaux D, Subramaniam R, Després C et al (2004) A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev Cell 6:229–240

    Article  CAS  Google Scholar 

  • Ding Y, Sun T, Ao K et al (2018) Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173:1454-1467.e10. https://doi.org/10.1016/j.cell.2018.03.044

    Article  CAS  PubMed  Google Scholar 

  • Dollet M, De Franqueville H, Ducamp M (2012) Bud rot and other major diseases of coconut, a potential threat to oil palm.  In: 4th IOPRI-MPOB International Seminar, Bandung, Indonesia, 13–14 December 2012, 24 p 

  • Du M, Zhao J, Tzeng DTW et al (2017) MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell 29:1883–1906. https://doi.org/10.1105/tpc.16.00953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic Acquired Resistance. Annu Rev. Phytopathol 42:185–209. https://doi.org/10.1146/annurev.phyto.42.040803.140421

  • Durrant WE, Wang S, Dong X (2007) Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response. Proc Natl Acad Sci USA 104:4223–4227. https://doi.org/10.1073/pnas.0609357104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan W, Lou HQ, Gong YL et al (2015) Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol 208:456–468. https://doi.org/10.1111/nph.13456

    Article  CAS  PubMed  Google Scholar 

  • FAOSTAT. http://www.fao.org/faostat/. Accessed 15 Jan 2018

  • Finiti I, Leyva MO, López-Cruz J et al (2013) Functional analysis of endo-1,4-β-glucanases in response to Botrytis cinerea and Pseudomonas syringae reveals their involvement in plant-pathogen interactions. Plant Biol 15:819–831. https://doi.org/10.1111/j.1438-8677.2012.00701.x

    Article  CAS  PubMed  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644

    Article  CAS  Google Scholar 

  • Griffith R (1987) Red ring disease of coconut palm. Plant Dis 71:193–196

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Harrison NA, Oropeza C (2008) Coconut lethal yellowing. In: Harrison NA, Rao GP, Marcone C (eds) Characterization, Diagnosis and Management of Phytoplasmas. Studium Press LLC, Houston, TX, USA, pp 219–248

  • He CY, Wolyn DJ (2005) Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. sp. asparagi. Plant Pathol 54:227–232

    Article  CAS  Google Scholar 

  • Huang Y-Y, Lee C-P, Fu JL et al (2014) De novo transcriptome sequence assembly from coconut leaves and seeds with a focus on factors involved in RNA-directed DNA methylation. G3 (Bethesda) 4:2147–2157. https://doi.org/10.1534/g3.114.013409

    Article  Google Scholar 

  • Jendoubi W, Harbaoui K, Hamada W (2015) Salicylic acid-induced resistance against Fusarium oxysporum f. s. pradicis lycopercisi in hydroponic grown tomato plants. J New Sci 21:985–995

  • Jiang Y, Yu D (2016) The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise Botrytis cinerea resistance. Plant Physiol 171:2771–2782

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S, Sato Y et al (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357

    Article  CAS  Google Scholar 

  • Lantican DV, Strickler SR, Canama AO et al (2019) De novo genome sequence assembly of dwarf coconut (Cocos nucifera L. ’Catigan Green Dwarf’) provides insights into genomic variation between coconut types and related palm species. G3 Genes. Genomes, Genet 9:2377–2393. https://doi.org/10.1534/g3.119.400215

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

  • Lizama-Uc G, Estrada-Mota IA, Caamal-Chan MG et al (2007) Chitosan activates a MAP-kinase pathway and modifies abundance of defense-related transcripts in calli of Cocos nucifera L. Physiol Mol Plant Pathol 70:130–141. https://doi.org/10.1016/j.pmpp.2007.08.001

    Article  CAS  Google Scholar 

  • Molinari S, Fanelli E, Leonetti P (2014) Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Mol Plant Pathol 15:255–264

    Article  CAS  Google Scholar 

  • Nejat N, Cahill DM, Vadamalai G et al (2015) Transcriptomics-based analysis using RNA-Seq of the coconut (Cocos nucifera) leaf in response to yellow decline phytoplasma infection. Mol Genet Genom 290:1899–1910. https://doi.org/10.1007/s00438-015-1046-2

    Article  CAS  Google Scholar 

  • Nic-Matos G, Narváez M, Peraza-Echeverría S et al (2017) Molecular cloning of two novel NPR1 homologue genes in coconut palm and analysis of their expression in response to the plant defense hormone salicylic acid. Genes Genom 39:1007–1019. https://doi.org/10.1007/s13258-017-0566-z

    Article  CAS  Google Scholar 

  • Oropeza-Salín C, Sáenz L, Narvaez M, et al (2020) Dealing with lethal yellowing and related diseases in coconut. In: Adkins S, Foale M, Bourdeix R, Nguyen Q, Biddle J (eds) Coconut Biotechnology: Towards the Sustainability of the ‘Tree of Life.’ Springer, Cham, pp 169–197. https://doi.org/10.1007/978-3-030-44988-9_9 

  • Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316. https://doi.org/10.1038/nchembio.164

    Article  CAS  PubMed  Google Scholar 

  • Prades A, Salum UN, Pioch D (2016) New era for the coconut sector. What prospects for research? OCL 23:D607

    Article  Google Scholar 

  • Puch-Hau C, Oropeza-Salín C, Peraza-Echeverría S et al (2015) Molecular cloning and characterization of disease-resistance gene candidates of the nucleotide binding site (NBS) type from Cocos nucifera L. Physiol Mol Plant Pathol 89:87–96. https://doi.org/10.1016/j.pmpp.2015.01.002

    Article  CAS  Google Scholar 

  • Puch-Hau C, Oropeza C, Góngora-Paredes M et al (2016) New insights into the evolutionary history of resistance gene candidates in coconut palms and their expression profiles in palms affected by lethal yellowing disease. Genes Genom 38:793–807. https://doi.org/10.1007/s13258-016-0422-6

    Article  CAS  Google Scholar 

  • Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368–375

    Article  CAS  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  Google Scholar 

  • Rohde W, Randles JW, Langridge P, Hanold D (1990) Nucleotide sequence of a circular single-stranded DNA associated with coconut foliar decay virus. Virology 176:648–651. https://doi.org/10.1016/0042-6822(90)90038-S

    Article  CAS  PubMed  Google Scholar 

  • Sáenz L, Chan JL, Narvaez M, Oropeza C (2018) Protocol for the micropropagation of coconut from plumule explants. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Plant cell culture protocols. Springer New York, New York, pp 161–170

    Chapter  Google Scholar 

  • Santos MO, Aragão FJL (2009) Role of SERK genes in plant environmental response. Plant Signal Behav 4:10–13. https://doi.org/10.4161/psb.4.12.9900

    Article  Google Scholar 

  • Sood A, Chauhan RS (2017) Comparative NGS transcriptomics unravels molecular components associated with mosaic virus infection in a bioenergy plant species, Jatropha curcas L. Bioenergy Res 10:129–145. https://doi.org/10.1007/s12155-016-9783-6

    Article  CAS  Google Scholar 

  • Team RC (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Trapnell C, Williams BA, Pertea G et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511

    Article  CAS  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206. https://doi.org/10.1146/annurev.phyto.050908.135202

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Tao F, Tian W et al (2017) The wheat WRKY transcription factors TaWRKY49 and TaWRKY62 confer differential high-temperature seedling-plant resistance to Puccinia striiformis f. sp. tritici. PLoS ONE 12:1–23. https://doi.org/10.1371/journal.pone.0181963

    Article  CAS  Google Scholar 

  • Xoca-Orozco LÁ, Cuellar-Torres EA, González-Morales S et al (2017) Transcriptomic analysis of avocado hass (Persea americana Mill) in the interaction system Fruit-Chitosan-Colletotrichum. Front Plant Sci 8:1–13. https://doi.org/10.3389/fpls.2017.00956

    Article  Google Scholar 

  • Xu Y, Zheng X, Song Y et al (2018) NtLTP4, a lipid transfer protein that enhances salt and drought stresses tolerance in Nicotiana tabacum. Sci Rep 8:1–14

    Google Scholar 

  • Zhang X, Dong J, Liu H et al (2016) Transcriptome sequencing in response to salicylic acid in salvia miltiorrhiza. PLoS ONE 11:1–27. https://doi.org/10.1371/journal.pone.0147849

    Article  CAS  Google Scholar 

  • Zhang YT, Zhang YL, Chen SX et al (2015) Proteomics of methyl jasmonate induced defense response in maize leaves against Asian corn borer. BMC Genom 16:224. https://doi.org/10.1186/s12864-015-1363-1

    Article  CAS  Google Scholar 

  • Zizumbo-Villarreal D, Colunga-GarcíaMarín P, Fernández-Barrera M et al (2008) Mortality of Mexican coconut germplasm due to lethal yellowing. Plant Genet Resour Newsl 156:23–33

    Google Scholar 

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Acknowledgments

Research partially funded by CONACYT (Ciencia Básica 2009—2013) NO. CB12977 and Centro de Investigación Científica de Yucatán, México. Postgraduate scholarship awarded by CONACYT to Carmen Silverio-Gómez No.286531.

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Authors and Affiliations

  1. Centro de Investigación Científica de Yucatán A. C., Unidad de Biotecnología, Calle 43 No. 130 x 32 y 34., Chuburná de Hidalgo, C.P. 97205, Mérida, Yucatán, Mexico

    C. Silverio-Gómez, G. Nic-Matos, M. Narváez-Cab, L. Sáenz-Carbonell & C. Oropeza

  2. UNAM: Escuela Nacional de Estudios Superiores Unidad León (ENES-León), Ciencias Agrogenómicas, Blv. UNAM #2011, Predio El Saucillo y, Comunidad de los Tepetates, El Potrero, C.P. 37684, León, Guanajuato, Mexico

    J. Vega-Arreguín

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  1. C. Silverio-Gómez
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  2. J. Vega-Arreguín
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  3. G. Nic-Matos
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  4. M. Narváez-Cab
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  5. L. Sáenz-Carbonell
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  6. C. Oropeza
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Contributions

CSG conducted most of the experiments, and drafted the article. JVA helped in massive data analyze and edited the manuscript. GNM helped in primer design, data collection and edited the manuscript. MNC helped in collection, sample preparation and edited the manuscript. LSC helped in designed the experiments. CO coordinated the project, conceived and designed the experiments and edited the manuscript.

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Correspondence to C. Oropeza.

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Silverio-Gómez, C., Vega-Arreguín, J., Nic-Matos, G. et al. Transcriptome analysis reveals key defense-related genes upon SA induction in Cocos nucifera L.. Genes Genom 44, 197–210 (2022). https://doi.org/10.1007/s13258-021-01068-1

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