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Characterization and genome analysis of Cucumber mosaic virus on commercial tobacco plants in Ecuador

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Abstract

Tobacco (Nicotiana tabacum L.), an endemic species of South America that is grown worldwide, is a member of the Solanaceae family. Although it is not a common crop in Ecuador, tobacco is important to the nation's economy and a significant source of employment. Viral infections are particularly devastating to tobacco as they can reduce both its yield and quality. In July 2021, symptoms of chlorosis, mosaic and leaf distortion were observed in four commercial fields in the provinces of Guayas and Los Ríos in Ecuador. This study aims to comprehensively characterize a viral isolate obtained from symptomatic plants. Using high throughput sequencing (HTS), phylogenetic analysis of the different open reading frames, and transmission electron microscopy (TEM) of symptomatic plants, we report for the first time the molecular characterization and genome sequence of Cucumber mosaic virus (CMV) isolated from commercial tobacco plants in Ecuador. The ability to detect and identify CMV in tobacco commercial plant fields enables the development of efficient control strategies, thereby mitigating constraints on the production of high-quality tobacco leaves.

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References

  • Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. Journal of Molecular Biology 215:403–410

    Article  CAS  PubMed  Google Scholar 

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

  • Apalowo OA, Adediji AO, Balogun OS et al (2022) Genetic structure of Cucumber mosaic virus from natural hosts in Nigeria reveals high diversity and occurrence of putative novel recombinant strains. Front Microbiol 13:753054

  • Aramburu J, Galipienso L, López C (2007) Reappearance of Cucumber mosaic virus isolates belonging to subgroup IB in tomato plants in north-eastern Spain. Journal of Phytopathology 155:513–518

    Article  CAS  Google Scholar 

  • Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barba M, Czosnek H, Hadidi A (2014) Historical perspective, development and applications of next-generation sequencing in plant virology. Viruses 6:106–136

    Article  PubMed  PubMed Central  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buitrón-Bustamante JL, Morillo-Velastegui LE (2017) Estandarización de un método de detección molecular del Cucumber mosaic virus (CMV) en banano ecuatoriano. Corpoica Ciencia y Tecnología Agropecuaria 18:113–124

    Article  Google Scholar 

  • Bujarski J, Gallitelli D, García-Arenal F et al (2019) ICTV virus taxonomy profile: Bromoviridae. J Gen Virol 100(8):1206–1207

    Article  CAS  PubMed  Google Scholar 

  • Canto T, Prior DAM, Hellwald KH et al (1997) Characterization of Cucumber mosaic virus. Virology 237:237–248

    Article  CAS  PubMed  Google Scholar 

  • Castellá M, Sueiro L, Machado J et al (2004) Comportamiento de plagas y enfermedades en el cultivo de tabaco tapado (Nicotiana tabacum L.) en la provincia de Granma. Fitosanidad 8:31–34

    Google Scholar 

  • Chen X, Krug L, Yang H et al (2020) Nicotiana tabacum seed endophytic communities share a common core structure and genotype-specific signatures in diverging cultivars. Computational and Structural Biotechnology Journal 18:287–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng L, Chen X, Jiang C et al (2019) High-density SNP genetic linkage map construction and quantitative trait locus mapping for resistance to Cucumber mosaic virus in tobacco (Nicotiana tabacum L.). Crop Journal 7:539–547

    Article  Google Scholar 

  • Chiurciu IA, Zaharia I, Soare E (2019) Aspects of the tobacco market within the european union and a brief moral reflection on smoking. Scientific Papers Series Management, Economic Engineering in Agriculture and Rural Development 19:59–68

    Google Scholar 

  • Dhawi F, El-Beltagi HS, Abdel-Mobdy YE et al (2021) Synergistic impact of the pomegranate peels and its nanoparticles against the infection of Tobacco mosaic virus (TMV). Fresenius Environmental Bulletin 30:731–746

    CAS  Google Scholar 

  • Duke M (2011) Ethnicity, well-being, and the organization of labor among shade tobacco workers. Medical Anthropology: Cross Cultural Studies in Health and Illness 30:409–424

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eiras M, Resende RO, Missiaggia AA et al (2001) RT-PCR and Dot Blot hybridization methods for a universal detection of tospoviruses. Fitopatol Bras 26:170–175

    Article  CAS  Google Scholar 

  • Farzadfar S, Pourrahim R, Arafati N (2013) Molecular identification of Cucumber mosaic virus subgroup IB isolates in South Iran. Journal of Plant Pathology 95:423–428

    Google Scholar 

  • Ganchozo-Mendoza E, Flores FJ, Garcés-Fiallos FR (2023) Virosis en el cultivo de tabaco. Revista Bionatura 8(4):30

    Google Scholar 

  • Gibbs A, Mackenzie A (1997) A primer pair for amplifying part of the genome of all potyvirids by RT-PCR. J Virol Methods 63(1–2):9–16

    Article  CAS  PubMed  Google Scholar 

  • Gonsalves D, Provvidenti R, Edwards MC (1982) Tomato white leaf: the relation of an apparent satellite RNA and cucumber mosaic virus. Phytopathology 72:1533–1538

    Article  Google Scholar 

  • Hayes RJ, Buck KW (1990) Complete replication of a eukaryotic virus RNA in vitro by a purified RNA-dependent RNA polymerase. Cell 63:363–368

    Article  CAS  PubMed  Google Scholar 

  • Heo KJ, Kwon SJ, Kim MK et al (2020) Newly emerged resistance-breaking variants of Cucumber mosaic virus represent ongoing host-interactive evolution of an RNA virus. Virus Evolution 6:2

    Article  Google Scholar 

  • Jacquemond M (2012) Cucumber mosaic virus. Adv Virus Res 84:439–504

    Article  PubMed  Google Scholar 

  • Kakar KU, Nawaz Z, Cui Z et al (2018) Molecular breeding approaches for production of disease-resilient commercially important tobacco. Briefings in Functional Genomics 19:10–25

    Article  Google Scholar 

  • Kayode AB, Odu BO, Ako-Nai KA et al (2014) Occurrence of Cucumber mosaic virus subgroups IA and IB isolates in tomatoes in Nigeria. Plant Dis 98:1750–1750

    Article  CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kidanemariam DB, Sukal AC, Abraham AD et al (2019) Characterization of a subgroup IB isolate of Cucumber mosaic virus from Xanthosoma sp. in sub-Saharan Africa. Australasian Plant Pathology 48:457–460

    Article  Google Scholar 

  • Kim MK, Jeong RD, Kwak HR et al (2014) First report of Cucumber mosaic virus isolated from wild Vigna angularis var. nipponensis in Korea. Plant Pathology Journal 30:200–207

    Article  PubMed  PubMed Central  Google Scholar 

  • Konakalla NC, Bag S, Deraniyagala AS et al (2021) Induction of plant resistance in tobacco (Nicotiana tabacum) against Tomato spotted wilt orthotospovirus through foliar application of dsRNA. Viruses 13:4

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M et al (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari R, Bhardwaj P, Singh L et al (2013) Biological and molecular characterization of Cucumber mosaic virus subgroup II isolate causing severe mosaic in cucumber. Indian Journal of Virology 24:27–34

    Article  PubMed  PubMed Central  Google Scholar 

  • Letschert B, Adam G, Lesemann DE et al (2002) Detection and differentiation of serologically cross-reacting tobamoviruses of economical importance by RT-PCR and RT-PCR-RFLP. J Virol Methods 106:1–10

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Nelson RS (2013) The cell biology of Tobacco mosaic virus replication and movement. Front Plant Sci 4:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu T, Gu Y, Zhou Z et al (2021) Ecological strategies of biological and chemical control agents on wildfire disease of tobacco (Nicotiana tabacum L.). BMC Microbiology 21:1–11

    Article  CAS  Google Scholar 

  • Lu J, Du Z-X, Kong J et al (2012) Transcriptome analysis of Nicotiana tabacum infected by Cucumber mosaic virus during systemic symptom development. PLoS One 7:e43447

  • Maree HJ, Fox A, Al Rwahnih M et al (2018) Application of HTS for routine plant virus diagnostics: state of the art and challenges. Frontiers in Plant Science 9:1082

    Article  PubMed  PubMed Central  Google Scholar 

  • Mochizuki T, Ohki ST (2012) Cucumber mosaic virus: Viral genes as virulence determinants. Molecular Plant Pathology 13:217–225

    Article  CAS  PubMed  Google Scholar 

  • Mrkvová M, Hančinský R, Predajňa L et al (2022) High-throughput sequencing discloses the Cucumber mosaic virus (CMV) diversity in Slovakia and reveals new hosts of CMV from the Papaveraceae Family. Plants 11:1665

    Article  PubMed  PubMed Central  Google Scholar 

  • Muhire BM, Varsani A, Martin DP (2014) SDT: A Virus classification tool based on pairwise sequence alignment and identity calculation. PLOS One 9(9):e108277

  • Mutuku MJ, Wamonje FO, Mukeshimana G et al (2018) Metagenomic analysis of plant virus occurrence in common bean (Phaseolus vulgaris) in Central Kenya. Frontiers in Microbiology 9:1–12

    Article  Google Scholar 

  • Palukaitis P, García-Arenal F (2003) Cucumoviruses. Advances in Virus Research 62:241–323

    Article  CAS  PubMed  Google Scholar 

  • Palukaitis P, Roossinck MJ, Dietzgen RG et al (1992) Cucumber mosaic virus. Adv Virus Res 41:281–348

    Article  CAS  PubMed  Google Scholar 

  • Pratap D, Kumar S, Snehi SK, Raj SK (2012) Biological and molecular characterization of Cucumber mosaic virus isolate causing shoestring disease of tomato in India which has closer affinity to European or east Asian isolates of CMV. Indian Journal of Virology 23:57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizos H, Gunn LV, Pares RD et al (1992) Differentiation of cucumber mosaic virus isolates using the polymerase chain reaction. J Gen Virol 73:2099–2103

    Article  CAS  PubMed  Google Scholar 

  • Roossinck MJ (2001) Cucumber mosaic virus, a model for RNA virus evolution. Molecular Plant Pathology 2:59–63

    Article  CAS  PubMed  Google Scholar 

  • Roossinck MJ (2002) Evolutionary History of Cucumber Mosaic Virus Deduced by Phylogenetic Analyses. Journal of Virology 76:3382–3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roossinck MJ, Martin DP, Roumagnac P (2015) Plant virus metagenomics: Advances in virus discovery. Phytopathology 105:716–727

    Article  CAS  PubMed  Google Scholar 

  • Roossinck MJ, Zhang L, Hellwald K-H (1999) Rearrangements in the 5 nontranslated region and phylogenetic analyses of Cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J Virol 73:8

    Article  Google Scholar 

  • Russell EA, Rahman E (2015) The Master Plant: Tobacco in Lowland South America. Bloomsbury Academic 259

  • Sierro N, Ivanov N V. (2020) Background and History of Tobacco Genome Resources. In: The Tobacco plant genome. Compendium of plants Genomes. pp 1–19

  • Soler S, López C, Nuez F (2005) Natural occurrence of viruses in Lycopersicon spp. in Ecuador. Plant Dis 89:1244–1244

    Article  CAS  PubMed  Google Scholar 

  • Swapna Geetanjali A, Kumar R, Srivastava PS, Mandal B (2011) Biological and molecular characterization of two distinct tomato strains of Cucumber mosaic virus based on complete RNA-3 genome and subgroup specific diagnosis. Indian Journal of Virology 22:117–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tovar J (2018) El cultivo del tabaco en América Latina. SSRN Electronic Journal

  • Tungadi T, Donnelly R, Qing L et al (2019) Cucumber mosaic virus 2b proteins inhibit virus-induced aphid resistance in tobacco. Molecular Plant Pathology 21:250–257

    Article  PubMed  PubMed Central  Google Scholar 

  • Valachas CA, Giantsis IA, Sareli K et al (2021) Molecular analysis of Greek isolates of Cucumber mosaic virus from vegetables shows a low prevalence of satellite RNAs and suggests the presence of host-associated virus strains. Archives of Virology 166:2199–2208

    Article  CAS  PubMed  Google Scholar 

  • Vélez-Olmedo JB, Quiñonez LC, Vélez-Zambrano SM et al (2021) Low virus diversity and spread in wild Capsicum spp. accessions from Ecuador under natural inoculum pressure. Archives of Virology 166:1447–1453

    Article  PubMed  Google Scholar 

  • Verdugo-Morales N, Andrade-Díaz V (2018) Productos tradicionales y no tradicionales del Ecuador: Posicionamiento y eficiencia en el mercado internacional para el período 2013–2017. X-Pendientes Económicos 2:84–102

    Google Scholar 

  • Vitti A, Pagán I, Bochicchio B (2022) Cucumber mosaic virus is unable to self-assemble in tobacco plants when transmitted by seed. Plants 11:3217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warner KE (2000) The economics of tobacco: Myths and realities. Tobacco control 9:78–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu Y, Wang C, Zhu S (2018) A review on the pathogenicity of Cucumber mosaic virus. Agric Biotechnol 7:87–91

    CAS  Google Scholar 

  • Yeturu S, Paz L, Intriago D et al (2017) First report of mosaic disease caused by Cucumber mosaic virus infecting passion fruit in Ecuador. Plant Disease 102:458

    Article  Google Scholar 

  • Zecevic K, Stankovic I, Petrovic B et al (2023) Molecular characterization and differentiation of Cucumber mosaic virus subgroups in Serbia by RT-PCR-RFLP. Arch Biol Sci 75:431–442

    Article  Google Scholar 

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Funding

EGM and FRGF gratefully acknowledges the financial support of the Technical University of Manabi: BECA PARA EL DESARROLLO DE LA INVESTIGACIÓN A TRAVÉS DE SU TITULACIÓN. FMZ is research members of the National Council for Scientific and Technological Development (CNPq).

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Authors and Affiliations

  1. Maestría en Sanidad Vegetal, Instituto de Posgrado, Universidad Técnica de Manabí, Portoviejo, 130105, Manabí, Ecuador

    Enny Ganchozo-Mendoza

  2. Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Ayane F. Ferreira Quadros & Francisco Murilo Zerbini

  3. Departamento de Ciencias de la Vida y la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, 170501, Ecuador

    Francisco J. Flores

  4. Centro de Investigación de Alimentos, Facultad de Ciencias de la Ingeniería e Industrias, CIAL, Universidad UTE, Quito, Ecuador

    Francisco J. Flores

  5. Laboratory of Phytopathology, Faculty of Agronomic Engineering, Experimental Campus La Teodomira, Technical University of Manabí, Santa Ana, Manabi, EC131301, Ecuador

    Felipe R. Garcés-Fiallos

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  1. Enny Ganchozo-Mendoza
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  2. Ayane F. Ferreira Quadros
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  3. Francisco Murilo Zerbini
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  4. Francisco J. Flores
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  5. Felipe R. Garcés-Fiallos
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by EG-M and AFFQ. The first draft of the manuscript was written by EG-M, FMZ, and FRGF and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Felipe R. Garcés-Fiallos.

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40858_2024_643_MOESM1_ESM.jpg

Supplementary file1 Figure S1 Phylogenetic tree based on the complete coding sequence of ORF1a of CMV. The scale bar indicates genetic distance. Bootstrap values (1000 replication) are indicated at the branches. The tree was inferred using the maximum likelihood method implemented in MEGA X. (JPG 7125 KB)

40858_2024_643_MOESM2_ESM.jpg

Supplementary file2 Figure S2 Phylogenetic tree based on the complete coding sequence of ORF2a of CMV. The scale bar indicates genetic distance. Bootstrap values (1000 replications) indicated. The tree was inferred using the maximum likelihood method implemented in MEGA X. (JPG 7494 KB)

40858_2024_643_MOESM3_ESM.jpg

Supplementary file3 Figure S3 Phylogenetic tree based on the complete coding sequence of ORF3a of CMV. The scale bar indicates genetic distance. Bootstrap values (1000 replications) are indicated. The tree was inferred using the maximum likelihood method implemented in MEGA X. (JPG 6771 KB)

40858_2024_643_MOESM4_ESM.jpg

Supplementary file4 Figure S4 RT-PCR-based detection of viruses in plants inoculated with symptomatic tobacco leaves from samples in which CMV-TabEC was detected by HTS. Lane 1: Nicotiana glutinosa; 2: N. tabacum cv. TNN; 3: N. tabacum cv. Havana; 4: N. debneyi; +: positive control, and nc: negative control. (JPG 359 KB)

40858_2024_643_MOESM5_ESM.jpg

Supplementary file5 Figure S5 Nucleotide and amino acid multiple sequence alignments showing polymorphisms among CMV-TabEC variants and references CTL and Pichilingue 1. (JPG 1526 KB)

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Ganchozo-Mendoza, E., Quadros, A.F.F., Zerbini, F.M. et al. Characterization and genome analysis of Cucumber mosaic virus on commercial tobacco plants in Ecuador. Trop. plant pathol. (2024). https://doi.org/10.1007/s40858-024-00643-7

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