Archives of Virology

, Volume 156, Issue 12, pp 2205–2213 | Cite as

High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in northeastern Brazil

  • Sarah J. C. da Silva
  • Gloria P. Castillo-Urquiza
  • Braz T. Hora Júnior
  • Iraildes P. Assunção
  • Gaus S. A. Lima
  • Gilvan Pio-Ribeiro
  • Eduardo S. G. Mizubuti
  • F. Murilo Zerbini
Original Article
First Online:
Received:
Accepted:

Abstract

Diseases caused by begomoviruses are a serious constraint to crop production in many tropical and subtropical areas of the world, including Brazil. Begomoviruses are whitefly-transmitted, single-stranded DNA viruses that are often associated with weed plants, which may act as natural reservoirs of viruses that cause epidemics in crop plants. Cleome affinis (family Capparaceae) is an annual weed that is frequently associated with leguminous crops in Brazil. Samples of C. affinis were collected in four states in the northeast of Brazil. Analysis of 14 full-length DNA-A components revealed that only one begomovirus was present, with 91-96% identity to cleome leaf crumple virus (ClLCrV). In a phylogenetic tree, ClLCrV forms a basal group relative to all other Brazilian begomoviruses. Evidence of multiple recombination events was detected among the ClLCrV isolates, which also display a high degree of genetic variability. Despite ClLCrV being the only begomovirus found, its phylogenetic placement, high genetic variability and recombinant nature suggest that C. affinis may act as a source of novel viruses for crop plants. Alternatively, ClLCrV could be a genetically isolated begomovirus. Further studies on the biological properties of ClLCrV should help to clarify the role of C. affinis in the epidemiological scenario of Brazilian begomoviruses.

Keywords

Recombination Event Common Bean Tomato Spot Wilt Virus Recombination Analysis High Genetic Variability 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The authors wish to thank Poliane Alfenas-Zerbini for critical review of the manuscript. This work was carried out under the framework of a CAPES PROCAD-NF (no. 93-2008) collaborative project among UFAL, UFRPE and UFV, and was additionally funded by FAPEMIG grants CAG-666-08 and CAG-949-09 to FMZ. GPCU was the recipient of a CAPES-PNPD postdoctoral fellowship.

Supplementary material

705_2011_1119_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 29 kb)

References

  1. 1.
    Andrade EC, Manhani GG, Alfenas PF, Calegario RF, Fontes EPB, Zerbini FM (2006) Tomato yellow spot virus a tomato-infecting begomovirus from Brazil with a closer relationship to viruses from Sida sp., forms pseudorecombinants with begomoviruses from tomato but not from Sida. J Gen Virol 87:3687–3696PubMedCrossRefGoogle Scholar
  2. 2.
    Castillo-Urquiza GP, Beserra JEA Jr, Bruckner FP, Lima ATM, Varsani A, Alfenas-Zerbini P, Zerbini FM (2008) Six novel begomoviruses infecting tomato and associated weeds in Southeastern Brazil. Arch Virol 153:1985–1989PubMedCrossRefGoogle Scholar
  3. 3.
    Castillo-Urquiza GP, Alfenas-Zerbini P, Beserra-Junior JEA, Mizubuti ESG, Varsani A, Martin DP, Zerbini FM (2010) Genetic structure of tomato-infecting begomovirus populations in two tomato-growing regions of Southeastern Brazil. In: Program and Abstracts, 6th International Geminivirus Symposium and 4th International ssDNA Comparative Virology Workshop, Guanajuato, MexicoGoogle Scholar
  4. 4.
    Costa AS (1975) Increase in the populational density of Bemisia tabaci, a threat to widespread virus infection of legume crops in Brazil. In: Bird J, Maramorosch K (eds) Tropical diseases of legumes. Academic Press, New York, p 171Google Scholar
  5. 5.
    Costa AS (1976) Whitefly-transmitted plant diseases. Annu Rev Phytopathol 14:429–440CrossRefGoogle Scholar
  6. 6.
    Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  7. 7.
    Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50Google Scholar
  8. 8.
    Faria JC, Bezerra IC, Zerbini FM, Ribeiro SG, Lima MF (2000) Current status of geminivirus diseases in Brazil (in Portuguese). Fitopatol Bras 25:125–137Google Scholar
  9. 9.
    Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini FM, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821PubMedCrossRefGoogle Scholar
  10. 10.
    Fiallo-Olive E, Martinez-Zubiaur Y, Moriones E, Navas-Castillo J (2010) Complete nucleotide sequence of Sida golden mosaic Florida virus and phylogenetic relationships with other begomoviruses infecting malvaceous weeds in the Caribbean. Arch Virol 155:1535–1537PubMedCrossRefGoogle Scholar
  11. 11.
    Frischmuth T, Engel M, Lauster S, Jeske H (1997) Nucleotide sequence evidence for the occurrence of three distinct whitefly-transmitted, Sida-infecting bipartite geminiviruses in Central America. J Gen Virol 78:2675–2682PubMedGoogle Scholar
  12. 12.
    Garcia-Andres 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 350:433–442PubMedCrossRefGoogle Scholar
  13. 13.
    Graham AP, Martin DP, Roye ME (2010) Molecular characterization and phylogeny of two begomoviruses infecting Malvastrum americanum in Jamaica: Evidence of the contribution of inter-species recombination to the evolution of malvaceous weed-associated begomoviruses from the Northern Caribbean. Virus Genes 40:256–266PubMedCrossRefGoogle Scholar
  14. 14.
    Guo XJ, Zhou XP (2006) Molecular characterization of a new begomovirus infecting Sida cordifolia and its associated satellite DNA molecules. Virus Genes 33:279–285PubMedGoogle Scholar
  15. 15.
    Hagen C, Rojas MR, Sudarshana MR, Xoconostle-Cazares B, Natwick ET, Turini TA, Gilbertson RL (2008) Biology and molecular characterization of Cucurbit leaf crumple virus, an emergent cucurbit-infecting begomovirus in the Imperial Valley of California. Plant Dis 92:781–793CrossRefGoogle Scholar
  16. 16.
    Hanssen IM, Lapidot M, Thomma B (2010) Emerging viral diseases of tomato crops. Mol Plant-Microbe Int 23:539–548CrossRefGoogle Scholar
  17. 17.
    Hofer P, Engel M, Jeske H, Frischmuth T (1997) Nucleotide sequence of a new bipartite geminivirus isolated from the common weed Sida rhombifolia in Costa Rica. Virology 78:1785–1790Google Scholar
  18. 18.
    Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  19. 19.
    Ilyas M, Qazi J, Mansoor S, Briddon RW (2010) Genetic diversity and phylogeography of begomoviruses infecting legumes in Pakistan. J Gen Virol 91:2091–2101PubMedCrossRefGoogle Scholar
  20. 20.
    Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage phi 29 DNA polymerase. J Virol Met 116:209–211CrossRefGoogle Scholar
  21. 21.
    Jones RAC (2009) Plant virus emergence and evolution: Origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res 141:113–130PubMedCrossRefGoogle Scholar
  22. 22.
    Jovel J, Reski G, Rothenstein D, Ringel M, Frischmuth T, Jeske H (2004) Sida micrantha mosaic is associated with a complex infection of begomoviruses different from Abutilon mosaic virus. Arch Virol 149:829–841PubMedCrossRefGoogle Scholar
  23. 23.
    Kaye AC, Moyer JW, Parks EJ, Carbone I, Cubeta MA (2011) Population genetic analysis of Tomato spotted wilt virus on peanut in North Carolina and Virginia. Phytopathology 101:147–153PubMedCrossRefGoogle Scholar
  24. 24.
    Lefeuvre P, Martin DP, Hoareau M, Naze F, Delatte H, Thierry M, Varsani A, Becker N, Reynaud B, Lett JM (2007) Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: Molecular diversity and evolution through recombination. J Gen Virol 88:3458–3468PubMedCrossRefGoogle Scholar
  25. 25.
    Lefeuvre P, Lett JM, Varsani A, Martin DP (2009) Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707PubMedCrossRefGoogle Scholar
  26. 26.
    Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463PubMedCrossRefGoogle Scholar
  27. 27.
    Morales FJ, Anderson PK (2001) The emergence and dissemination of whitefly-transmitted geminiviruses in Latin America. Arch Virol 146:415–441PubMedCrossRefGoogle Scholar
  28. 28.
    Paprotka T, Metzler V, Jeske H (2010) The first DNA 1-like alpha satellites in association with New World begomoviruses in natural infections. Virology 404:148–157PubMedCrossRefGoogle Scholar
  29. 29.
    Qazi J, Ilyas M, Mansoor S, Briddon RW (2007) Legume yellow mosaic viruses: genetically isolated begomoviruses. Mol Plant Pathol 8:343–348PubMedCrossRefGoogle Scholar
  30. 30.
    Ribeiro SG, Ávila AC, Bezerra IC, Fernandes JJ, Faria JC, Lima MF, Gilbertson RL, Zambolim EM, Zerbini FM (1998) Widespread occurrence of tomato geminiviruses in Brazil, associated with the new biotype of the whitefly vector. Plant Dis 82:830CrossRefGoogle Scholar
  31. 31.
    Rojas MR, Gilbertson RL, Russell DR, Maxwell DP (1993) Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77:340–347CrossRefGoogle Scholar
  32. 32.
    Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394PubMedCrossRefGoogle Scholar
  33. 33.
    Romay G, Chirinos D, Geraud-Pouey F, Desbiez C (2010) Association of an atypical alphasatellite with a bipartite New World begomovirus. Arch Virol 155:1843–1847PubMedCrossRefGoogle Scholar
  34. 34.
    Roye ME, McLaughlin WA, Nakhla MK, Maxwell DP (1997) Genetic diversity among geminiviruses associated with the weed species Sida spp., Macroptilium lathyroides, and Wissadula amplissima from Jamaica. Plant Dis 81:1251–1258CrossRefGoogle Scholar
  35. 35.
    Roye ME, Spence J, McLaughlin WA, Maxwell DP (1999) The common weed Macroptilium lathyroides is not a source of crop-infecting geminiviruses from Jamaica. Trop Agric 76:256–262Google Scholar
  36. 36.
    Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 537:337–350PubMedCrossRefGoogle Scholar
  37. 37.
    Sanz AI, Fraile A, García-Arenal F, Zhou X, Robinson DJ, Khalid S, Butt T, Harrison BD (2000) Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. J Gen Virol 81:1839–1849PubMedGoogle Scholar
  38. 38.
    Seal SE, Jeger MJ, Van den Bosch F (2006) Begomovirus evolution and disease management. Adv Virus Res 67:297–316PubMedCrossRefGoogle Scholar
  39. 39.
    Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM (2011) Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in Northeastern Brazil. Plant Pathol. doi: 10.1111/j.1365-3059.2011.02543.x
  40. 40.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739Google Scholar
  41. 41.
    Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associated Inc, Sunderland, MassachusettsGoogle Scholar
  42. 42.
    Wyant PS, Gotthardt D, Schafer B, Krenz B, Jeske H (2011) The genomes of four novel begomoviruses and a new Sida micrantha mosaic virus strain from Bolivian weeds. Arch Virol 156:347–352PubMedCrossRefGoogle Scholar
  43. 43.
    Yahara T, Ooi K, Oshita S, Ishii I, Ikegami M (1998) Molecular evolution of a host-range gene in geminiviruses infecting asexual populations of Eupatorium makinoi. Genes Genet Syst 73:137–141PubMedCrossRefGoogle Scholar
  44. 44.
    Zerbini FM, Andrade EC, Barros DR, Ferreira SS, Lima ATM, Alfenas PF, Mello RN (2005) Traditional and novel strategies for geminivirus management in Brazil. Australas Plant Path 34:475–480CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sarah J. C. da Silva
    • 1
    • 3
  • Gloria P. Castillo-Urquiza
    • 1
  • Braz T. Hora Júnior
    • 1
  • Iraildes P. Assunção
    • 2
  • Gaus S. A. Lima
    • 2
    • 3
  • Gilvan Pio-Ribeiro
    • 3
  • Eduardo S. G. Mizubuti
    • 1
  • F. Murilo Zerbini
    • 1
  1. 1.Departamento de Fitopatologia/BIOAGROUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento of Fitossanidade/CECAUniversidade Federal de AlagoasRio LargoBrazil
  3. 3.Departamento de AgronomiaUniversidade Federal Rural de PernambucoRecifeBrazil

Personalised recommendations