Skip to main content
SpringerLink
Log in

Complete genome sequence of a novel bipartite begomovirus infecting the legume weed Macroptilium erythroloma

  • Annotated Sequence Record
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The natural occurrence of mixed infections and large populations of the polyphagous vector (Bemisia tabaci) are the main factors associated with the intensification of the genetic flow among begomoviruses in Neotropical areas, contributing to the emergence of novel recombinants. Here, high-throughput sequencing and metagenomic analyses were employed to discover and characterize a novel recombinant bipartite begomovirus, tentatively named “macroptilium bright yellow interveinal virus” (MaBYIV) in the weed Macroptilium erythroloma (Fabaceae). Recombination signals were detected in MaBYIV, involving bean golden mosaic virus (BGMV) and tomato mottle leaf curl virus (ToMoLCV) genome components. All of the original MaBYIV-infected M. erythroloma plants were found to have mixed infections with BGMV. MaBYIV was transmitted to bean and soybean cultivars via B. tabaci MEAM 1, indicating that M. erythroloma may play a role as a year-round reservoir of a potential new viral pathogen of economically important legume crops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Stanley J, Bisaro DM, Briddon RW et al (2005) Family Geminiviridae. In: Virus taxon eighth rep int comm taxon viruses, pp 301–326

  2. Zerbini FM, Briddon RW, Idris A et al (2017) ICTV virus taxonomy profile: Geminiviridae. J Gen Virol 98:131–133. https://doi.org/10.1099/jgv.0.000738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rojas MR, Macedo MA, Maliano MR et al (2018) World management of geminiviruses. Annu Rev Phytopathol 56:637–677

    Article  CAS  PubMed  Google Scholar 

  4. Adams MJ, King AMQ, Carstens EB (2013) Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2013). Arch Virol 158:2023–2030

    Article  CAS  PubMed  Google Scholar 

  5. Brown JK, Zerbini FM, Navas-Castillo J et al (2015) Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 160:1593–1619

    Article  CAS  PubMed  Google Scholar 

  6. Varsani A, Roumagnac P, Fuchs M et al (2017) Capulavirus and Grablovirus: two new genera in the family Geminiviridae. Arch Virol 162:1819–1831. https://doi.org/10.1007/s00705-017-3268-6

    Article  CAS  PubMed  Google Scholar 

  7. Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248

    Article  CAS  PubMed  Google Scholar 

  8. de Reis L, NA dos, Fonseca ME de N, Ribeiro SG, et al (2020) Metagenomics of neotropical single-stranded DNA viruses in tomato cultivars with and without the Ty-1 gene. Viruses 12:819

    Article  CAS  Google Scholar 

  9. Galvao RM, Mariano AC, Luz DF et al (2003) A naturally occurring recombinant DNA-A of a typical bipartite begomovirus does not require the cognate DNA-B to infect Nicotiana benthamiana systemically. J Gen Virol 84:715–726

    Article  CAS  PubMed  Google Scholar 

  10. Ribeiro SG, Martin DP, Lacorte C et al (2007) Molecular and biological characterization of Tomato chlorotic mottle virus suggests that recombination underlies the evolution and diversity of Brazilian tomato begomoviruses. Phytopathology 97:702–711

    Article  CAS  PubMed  Google Scholar 

  11. Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT et al (2012) Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in northeastern Brazil. Plant Pathol 61:457–467

    Article  Google Scholar 

  12. Pita JS, Fondong VN, Sangare A et al (2001) Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J Gen Virol 82:655–665

    Article  CAS  PubMed  Google Scholar 

  13. Monci F, Sánchez-Campos S, Navas-Castillo J, Moriones E (2002) A natural recombinant between the geminiviruses tomato yellow leaf curl Sardinia virus and tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303:317–326

    Article  CAS  PubMed  Google Scholar 

  14. García-Andrés S, Monci F, Navas-Castillo J, Moriones E (2006) Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350:433–442

    Article  PubMed  CAS  Google Scholar 

  15. García-Andrés S, Accotto GP, Navas-Castillo J, Moriones E (2007) Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the Mediterranean basin. Virology 359:302–312

    Article  PubMed  CAS  Google Scholar 

  16. García-Andrés S, Tomás DM, Sánchez-Campos S et al (2007) Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210–219

    Article  PubMed  CAS  Google Scholar 

  17. Gilbertson RL, Faria JC, Ahlquist P, Maxwell DP (1993) Genetic diversity in geminiviruses causing bean golden mosaic disease: the nucleotide sequence of the infectious cloned DNA components of a Brazilian isolate of bean golden mosaic geminivirus. Phytopathology 83:709

    Article  CAS  Google Scholar 

  18. Gilbertson RL, Faria JC, Hanson SF et al (1991) Cloning of the complete DNA genomes of four bean-infecting geminiviruses and determining their infectivity by electric discharge particle acceleration. Phytopathology 81:980–985

    Article  CAS  Google Scholar 

  19. Coco D, Calil IP, Brustolini OJB et al (2013) Soybean chlorotic spot virus, a novel begomovirus infecting soybean in Brazil. Arch Virol 158:457–462

    Article  CAS  PubMed  Google Scholar 

  20. Naito FYB, Melo FL, Fonseca MEN et al (2019) Nanopore sequencing of a novel bipartite new world begomovirus infecting cowpea. Arch Virol 164:1907–1910

    Article  CAS  PubMed  Google Scholar 

  21. Morales FJ (2006) History and current distribution of begomoviruses in Latin America. Adv Virus Res 67:127–162

    Article  PubMed  Google Scholar 

  22. Delgado-Salinas A, Lewis GP (2008) A new species of Macroptilium (Benth.) Urb. (Leguminosae: Papilionoideae: Phaseolinae) from North-Eastern Brazil. Kew Bull 63:151–154

    Article  Google Scholar 

  23. Passos LS, Rodrigues JS, Soares ÉCS et al (2017) Complete genome sequence of a new bipartite begomovirus infecting Macroptilium lathyroides in Brazil. Arch Virol 162:3551–3554

    Article  CAS  PubMed  Google Scholar 

  24. McLaughlin PD, McLaughlin WA, Maxwell DP et al (2011) Detection of begomoviruses in Caribbean crops and weeds in the islands of Antigua, Barbados and St Kitts & Nevis. Trop Agric 41:40211–40214

    Google Scholar 

  25. Martinez-Marrero N, Avalos-Calleros JA, Chiquito-Almanza E et al (2020) A new begomovirus isolated from a potyvirus-infected bean plant causes asymptomatic infections in bean and N. benthamiana. Arch Virol 165:1659–1665

    Article  CAS  PubMed  Google Scholar 

  26. Amarakoon II, Roye ME, Briddon RW et al (2008) Molecular and biological characterization of Macroptilium yellow mosaic virus from Jamaica. Plant Pathol 57:417–426

    Article  CAS  Google Scholar 

  27. Idris AM, Hiebert E, Bird J, Brown JK (2003) Two newly described begomoviruses of Macroptilium lathyroides and common bean. Phytopathology 93:774–783

    Article  CAS  PubMed  Google Scholar 

  28. Sobrinho RR, Xavier CAD, de Barros Pereira HM et al (2014) Contrasting genetic structure between two begomoviruses infecting the same leguminous hosts. J Gen Virol 95:2540–2552

    Article  PubMed  CAS  Google Scholar 

  29. Batista JG, Pereira-Carvalho RC, Malheiros MF et al (2020) Macroptilium erythroloma (Fabaceae): a natural weed host of bean golden mosaic virus in Brazil. Plant Dis 104:3270

    Article  Google Scholar 

  30. Idris AM, Bird J, Brown JK (1999) First report of a bean-infecting begomovirus from Macroptilium lathyroides in Puerto Rico that is distinct from bean golden mosaic virus. Plant Dis 83:1071

    Article  CAS  PubMed  Google Scholar 

  31. Ramos PL, Fernández A, Castrillo G et al (2002) Macroptilium yellow mosaic virus, a new begomovirus infecting Macroptilium lathyroides in Cuba. Plant Dis 86:1049

    Article  CAS  PubMed  Google Scholar 

  32. Benson DA, Cavanaugh M, Clark K et al (2012) GenBank. Nucleic Acids Res 41:D36–D42

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. De Faria JC, Aragão FJL, Souza T et al (2016) Golden mosaic of common beans in Brazil: management with a transgenic approach. APS Features. https://doi.org/10.1094/APSFeature-2016-10

    Article  Google Scholar 

  34. Boiteux L, Fonseca MEN, Simon PW (1999) Effects of plant tissue and DNA purification method on randomly amplified polymorphic DNA-based genetic fingerprinting analysis in carrot. J Am Soc Hortic Sci 124:32–38

    Article  CAS  Google Scholar 

  35. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T (2004) A simple method for cloning the complete Begomovirus genome using the bacteriophage phi29 DNA Polymerase. J Virol Methods 116:209–211

    Article  CAS  PubMed  Google Scholar 

  36. Bonfim K, Faria JC, Nogueira EOPL et al (2007) RNAi-mediated resistance to Bean golden mosaic virus in genetically engineered common bean (Phaseolus vulgaris). Mol Plant-Microbe Interact 20:717–726

    Article  CAS  PubMed  Google Scholar 

  37. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Martin DP, Murrell B, Golden M et al (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003

    Article  PubMed  PubMed Central  Google Scholar 

  41. Jovel J, Reski G, Rothenstein D et al (2004) Sida micrantha mosaic is associated with a complex infection of begomoviruses different from abutilon mosaic virus. Arch Virol 149:829–841

    Article  CAS  PubMed  Google Scholar 

  42. Chagas CM, Vicente M, Barradas MM (1981) Macroptilium erythroloma (Mart. ex Benth.) Urb.-Leguminosae-a possible reservoir of bean golden mosaic virus (BGMV). Arq do Inst Biol São Paulo 48:113–116

    Google Scholar 

  43. Gilbertson RL, Rojas MR, Russell DR, Maxwell DP (1991) Use of the asymmetric polymerase chain reaction and DNA sequencing to determine genetic variability of bean golden mosaic geminivirus in the Dominican Republic. J Gen Virol 72:2843–2848

    Article  CAS  PubMed  Google Scholar 

  44. Bedford ID, Kelly A, Banks GK et al (1998) Solanum nigrum: an indigenous weed reservoir for a Tomato yellow leaf curl geminivirus in southern Spain. Eur J Plant Pathol 104:221–222

    Article  Google Scholar 

  45. Tan PHN, Wong SM, Wu M et al (1995) Genome organization of ageratum yellow vein virus, a monopartite whitefly-transmitted geminivirus isolated from a common weed. J Gen Virol 76:2915–2922

    Article  CAS  PubMed  Google Scholar 

  46. Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This research was carried out with financial support from grants from Embrapa, Conselho Nacional de Desenvolvimento Científico e Tecnológico–CNPq and Fundação de Apoio à Pesquisa do Distrito Federal–FAP/DF. This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Finance Code 001.

Author information

Author notes

  1. Josiane G. Batista and Flávia M. B. Nery contributed equally.

Authors and Affiliations

  1. Department of Plant Pathology, Universidade de Brasília (UnB), Brasília-DF, 70910-900, Brazil

    Josiane G. Batista, Flávia M. B. Nery, Felipe F. Silva Melo, Mateus F. Malheiros, Denise V. Rezende, Bruno Eduardo Cardozo de Miranda & Rita C. Pereira-Carvalho

  2. National Center for Vegetable Crops Research (CNPH), Embrapa Hortaliças, Brasília-DF, 70275-970, Brazil

    Leonardo S. Boiteux & Maria Esther N. Fonseca

Authors
  1. Josiane G. Batista
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Flávia M. B. Nery
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Felipe F. Silva Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mateus F. Malheiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Denise V. Rezende
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leonardo S. Boiteux
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maria Esther N. Fonseca
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bruno Eduardo Cardozo de Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rita C. Pereira-Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: RCPC and LSB. Performance of experiments: JGM, FFSM, MFM, and RCPC. Data analysis: JGM, FMBN, and RCPC. Writing—original draft: DVR, LSB, MENF, and RCPC. Writing—review and editing: JGB, FMBN, DVR, LSB, MENF, BECM, and RCPC. Supervision: RCPC. All of the authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Rita C. Pereira-Carvalho.

Ethics declarations

Conflict of interest

The authors declare that no conflict of interest exists.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Jesús Navas-Castillo.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Supplementary file2 (TIF 17175 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Batista, J.G., Nery, F.M.B., Melo, F.F.S. et al. Complete genome sequence of a novel bipartite begomovirus infecting the legume weed Macroptilium erythroloma. Arch Virol 167, 1597–1602 (2022). https://doi.org/10.1007/s00705-022-05410-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-022-05410-0

Search

Navigation