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Occurrence of genetic bottlenecks during citrus tristeza virus acquisition by Toxoptera citricida under field conditions

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In this study, we address the involvement of T. citricida in strain segregation and genetic bottleneck events by comparing the nucleotide diversity of CTV coat protein (CP) gene variants present in field-grown trees with that of variants retrieved from single apterous aphids. Plant material and aphids were collected in orange orchards in the northern part of Portugal. Shoots from two trees that were found to be positive using ELISA and twenty-four apterous aphids from these same trees were selected for individual molecular assays. CTV was detected in 60% of the aphids by amplification of a 417-bp fragment of the CP gene. Analysis of molecular variance (AMOVA) of this fragment revealed that most of the variation of the virus was found among individual aphids (FSC: 0.766) within each location. Nucleotide diversity comparison between the pool of sequences obtained from a given shoot and sequences obtained from individual aphids present on that shoot showed a reduction of more than one order of magnitude in most cases. Computer simulations of random virus acquisition by single aphids showed that in 54% of the cases only a single CP gene phylogenetic group was acquired. However, a small number of aphids (e.g. 6) was enough to acquire the full complement of phylogenetic groups present.

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References

  • MR Albiach-Martí J Guerri A Hermoso de Mendoza F Laigret JF Ballester-Olmos P Moreno (2000) ArticleTitleAphid transmission alters the genomic and defective RNA populations of citrus tristeza virus isolates Phytopathology 90 134–138 Occurrence Handle10.1094/PHYTO.2000.90.2.134 Occurrence Handle18944601

    Article  PubMed  Google Scholar 

  • A Ali H Li WL Schneider DJ Sherman S Gray D Smith MJ Roossinck (2006) ArticleTitleAnalysis of genetic bottlenecks during horizontal transmission of Cucumber mosaic virus J Virol 80 8345–8350 Occurrence Handle16912285 Occurrence Handle10.1128/JVI.00568-06 Occurrence Handle1:CAS:528:DC%2BD28XovVOjtr4%3D

    Article  PubMed  CAS  Google Scholar 

  • M Bar-Joseph R Marcus RF Lee (1989) ArticleTitleThe continuous challenge of citrus tristeza virus control Annu Rev Phytopathol 27 291–316 Occurrence Handle10.1146/annurev.py.27.090189.001451

    Article  Google Scholar 

  • RH Brlansky VD Damsteegt DS Howd A Roy (2003) ArticleTitleMolecular analyses of Citrus tristeza virus sub-isolates separated by aphid transmission Plant Dis 87 397–401 Occurrence Handle10.1094/PDIS.2003.87.4.397 Occurrence Handle1:CAS:528:DC%2BD3sXivVGrsLc%3D

    Article  CAS  Google Scholar 

  • P Broadbent RH Brlansky J Indsto (1996) ArticleTitleBiological characterization of Australian isolates of citrus tristeza virus and separation of sub-isolates by single aphid transmissions Plant Dis 80 329–333 Occurrence Handle10.1094/PD-80-0329

    Article  Google Scholar 

  • Cambra M, Olmos A, Gorris MT, Marroquin C, Esteban O, Garnsey SM, Llauger R, Batista L, Pena I, Hermosos de Mendoza A (2000) Detection of Citrus tristeza virus by print capture and squash capture-PCR in plant tissues and single aphids. In: 14th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 42–49

  • F D’Urso MA Ayllon L Rubio A Sambade A Hermoso de Mendoza J Guerri P Moreno (2000) ArticleTitleContribution of uneven distribution of genomic RNA variants of Citrus tristeza virus (CTV) within the plant to changes in the viral population following aphid transmission Plant Pathol 49 288–294 Occurrence Handle10.1046/j.1365-3059.2000.00448.x Occurrence Handle1:CAS:528:DC%2BD3cXjslSltb4%3D

    Article  CAS  Google Scholar 

  • L Excoffier P Smouse J Quattro (1992) ArticleTitleAnalysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data Genetics 131 479–491 Occurrence Handle1644282 Occurrence Handle1:CAS:528:DyaK38XlsVCntro%3D

    PubMed  CAS  Google Scholar 

  • L Excoffier G Laval S Schneider (2005) ArticleTitleArlequin ver. 3.0: An integrated software package for population genetics data analysis Evol Bioinform Online 1 47–50 Occurrence Handle1:CAS:528:DC%2BD28XjsFSltg%3D%3D Occurrence Handle19325852

    CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2006) Arlequin ver 3.1 user manual. Computational and Molecular Population Genetics Lab (CMPG), Institute of Zoology, University of Berne

  • VJ Febres L Ashoulin M Mawassi A Frank M Bar-Joseph KL Manjunath RF Lee CL Niblett (1996) ArticleTitleThe P 27 protein is present at one end of citrus tristeza virus particles Phytopathology 86 1331–1335 Occurrence Handle1:CAS:528:DyaK2sXjs1Gmsg%3D%3D

    CAS  Google Scholar 

  • Garnsey SM, Christie RG, Derrick KS, Bar-Joseph M (1980) Detection of citrus tristeza virus. II. Light and electron microscopy of inclusions and viral particles. In: Proc. 8th Conf. Intern. Org. Citrus Virol IOCV, Riverside, pp 9–15

  • M Gillings P Broadbent J Indsto R Lee (1993) ArticleTitleCharacterisation of isolates and strains of citrus tristeza closterovirus using restriction analysis of the coat protein gene amplified by the polymerase chain reaction J Virol Methods 44 305–317 Occurrence Handle7903310 Occurrence Handle10.1016/0166-0934(93)90065-Y Occurrence Handle1:CAS:528:DyaK2cXitl2qt7c%3D

    Article  PubMed  CAS  Google Scholar 

  • TR Gottwald SM Garnsey J Borbon (1998) ArticleTitleIncrease and spread of Citrus tristeza virus infections in Costa Rica and Dominican Republic in the presence of the brown citrus aphid, Toxoptera citricida Phytopathology 88 621–636 Occurrence Handle10.1094/PHYTO.1998.88.7.621 Occurrence Handle1:STN:280:DC%2BD1cjjvVagsw%3D%3D Occurrence Handle18944934

    Article  CAS  PubMed  Google Scholar 

  • SE Halbert H Genc B Cevik LG Brown IM Rosales KL Manjunath M Pomerinke DA Davison RF Lee CL Niblett (2004) ArticleTitleDistribution and characterization of Citrus tristeza virus in south Florida following the establishment of Toxoptera citricida Plant Dis 88 935–941 Occurrence Handle10.1094/PDIS.2004.88.9.935

    Article  Google Scholar 

  • JS Hall R French GL Hein TJ Morris DC Stenger (2001) ArticleTitleThree distinct mechanisms facilitate genetic isolation of sympatric wheat streak mosaic virus lineages Virology 282 230–236 Occurrence Handle11289805 Occurrence Handle10.1006/viro.2001.0841 Occurrence Handle1:CAS:528:DC%2BD3MXisVWlsbw%3D

    Article  PubMed  CAS  Google Scholar 

  • CM Herron TE Mirkov N Solís-Gracia CJ Kahlke M Skaria JV da Graça (2005) ArticleTitleSeverity of Citrus tristeza virus isolates from Texas Plant Dis 89 575–580 Occurrence Handle10.1094/PD-89-0575 Occurrence Handle1:CAS:528:DC%2BD2MXltlOgu7o%3D

    Article  CAS  Google Scholar 

  • FA Ilharco CR Sousa-Silva AA Alvarez (2005) ArticleTitleFirst report on Toxoptera citricidus (Kirkaldy) in Spain and Continental Portugal Agronomia Lusitana 51 19–21

    Google Scholar 

  • C Jridi JF Martin V Marie-Jeanne G Labonne S Blanc (2006) ArticleTitleDistinct viral populations differentiate and evolve independently in a single perennial host plant J Virol 80 2349–2357 Occurrence Handle16474141 Occurrence Handle10.1128/JVI.80.5.2349-2357.2006 Occurrence Handle1:CAS:528:DC%2BD28XhvFyht7s%3D

    Article  PubMed  CAS  Google Scholar 

  • Kano T, Koizumi M (1991) Separation of Citrus tristeza virus (CTV) serotypes through aphid transmission. In: Proc. 11th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 82–85

  • AV Karasev VP Boyko S Gowda OV Nikolaeva ME Hilf EV Koonin CL Niblett K Cline DJ Gumpf RF Lee et al. (1995) ArticleTitleComplete sequence of the citrus tristeza virus RNA genome Virology 208 511–520 Occurrence Handle7747424 Occurrence Handle10.1006/viro.1995.1182 Occurrence Handle1:CAS:528:DyaK2MXlsF2ht7s%3D

    Article  PubMed  CAS  Google Scholar 

  • S Kumar K Tamura M Nei (2004) ArticleTitleMEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment Brief Bioinform 5 150–163 Occurrence Handle15260895 Occurrence Handle10.1093/bib/5.2.150 Occurrence Handle1:CAS:528:DC%2BD2cXntFGqu7s%3D

    Article  PubMed  CAS  Google Scholar 

  • H Li MJ Roossinck (2004) ArticleTitleGenetic bottlenecks reduce population variation in an experimental RNA virus population J Virol 78 10582–10587 Occurrence Handle15367625 Occurrence Handle10.1128/JVI.78.19.10582-10587.2004 Occurrence Handle1:CAS:528:DC%2BD2cXotVemtro%3D

    Article  PubMed  CAS  Google Scholar 

  • Marais LJ, Manjunath KL, Barthe G, Febres VJ, Derrick KS, Niblett CL, Lee RF (2000) Separation and characterization of strains of citrus tristeza virus useful in mild strain cross protection in South Africa. In: Proc. 14th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 416

  • P Mehta RH Brlansky S Gowda RK Yokomi (1997) ArticleTitleReverse-transcription polymerase chain reaction detection of Citrus tristeza virus in aphids Plant Dis 81 1066–1069 Occurrence Handle10.1094/PDIS.1997.81.9.1066 Occurrence Handle1:CAS:528:DyaK2sXmtlCqtLg%3D

    Article  CAS  Google Scholar 

  • CL Niblett H Genc B Cevik S Halbert L Brown G Nolasco B Bonacalza KL Manjunath VJ Febres HR Pappu RF Lee (2000) ArticleTitleProgress on strain differentiation of Citrus tristeza virus and its application to the epidemiology of citrus tristeza disease Virus Res 71 97–106 Occurrence Handle11137165 Occurrence Handle10.1016/S0168-1702(00)00191-X Occurrence Handle1:CAS:528:DC%2BD3MXptVSntQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S Ogino RB Wilson (2002) ArticleTitleQuantification of PCR bias caused by a single nucleotide polymorphism in SMN gene dosage analysis J Mol Diagn 4 185–190 Occurrence Handle12411585 Occurrence Handle1:CAS:528:DC%2BD38Xps1Khtr8%3D

    PubMed  CAS  Google Scholar 

  • H Pappu S Pappu C Niblett R Lee E Civerolo (1993) ArticleTitleComparative sequence analysis of the coat proteins of biologically distinct citrus tristeza closterovirus isolates Virus Genes 7 255–264 Occurrence Handle8279124 Occurrence Handle10.1007/BF01702586 Occurrence Handle1:CAS:528:DyaK2cXitlymsro%3D

    Article  PubMed  CAS  Google Scholar 

  • HR Pappu SS Pappu KL Manjunath RF Lee CL Niblett (1993) ArticleTitleMolecular characterization of a structural epitope that is largely conserved among severe isolates of a plant virus Proc Natl Acad Sci USA 90 3641–3644 Occurrence Handle7682715 Occurrence Handle10.1073/pnas.90.8.3641 Occurrence Handle1:CAS:528:DyaK3sXkvV2gsLY%3D

    Article  PubMed  CAS  Google Scholar 

  • M Raymond F Rousset (1995) ArticleTitleAn exact test for population differentiation Evolution 49 1280–1283 Occurrence Handle10.2307/2410454

    Article  Google Scholar 

  • Roistacher CN, Moreno P (1991) The worldwide threat from destructive isolates of citrus tristeza virus. A review. In: Proc. 11th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 7–19

  • S Sacristan JM Malpica A Fraile F Garcia-Arenal (2003) ArticleTitleEstimation of population bottlenecks during systemic movement of tobacco mosaic virus in tobacco plants J Virol 77 9906–9911 Occurrence Handle12941900 Occurrence Handle10.1128/JVI.77.18.9906-9911.2003 Occurrence Handle1:CAS:528:DC%2BD3sXntFShsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • Sasaki A, Tsuchizaki T, Saito Y (1980) Distribution of citrus tristeza virus antigen in citrus tissues. In: Proc. 8th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 17–19

  • V Sentandreu JA Castro MA Ayllon L Rubio J Guerri F Gonzalez-Candelas P Moreno A Moya (2006) ArticleTitleEvolutionary analysis of genetic variation observed in citrus tristeza virus (CTV) after host passage Arch Virol 151 875–894 Occurrence Handle16329002 Occurrence Handle10.1007/s00705-005-0683-x Occurrence Handle1:CAS:528:DC%2BD28Xjs1KlurY%3D

    Article  PubMed  CAS  Google Scholar 

  • Z Sequeira G Nolasco (2002) ArticleTitleBacterial expressed coat protein: development of a single antiserum for routine detection of Citrus tristeza virus Phytopathologia Mediterranea 41 55–62 Occurrence Handle1:CAS:528:DC%2BD38Xltlyjs7o%3D

    CAS  Google Scholar 

  • F Tajima (1983) ArticleTitleEvolutionary relationship of DNA sequences in finite populations Genetics 105 437–460 Occurrence Handle6628982 Occurrence Handle1:CAS:528:DyaL3sXlsFCjs74%3D

    PubMed  CAS  Google Scholar 

  • JH Tsai YH Liu JJ Wang RF Lee (2000) ArticleTitleRecovery of orange stem pitting strains of Citrus tristeza virus (CTV) following single aphid transmissions with Toxoptera citricida from a Florida decline isolate of CTV Proc Fla State Hort Soc 113 75–78

    Google Scholar 

  • van Vuuren SP, van Vyver, Luttig M (2000) Diversity among sub-isolates of cross protecting Citrus tristeza virus isolates in South Africa. In: Proc. 14th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 103–110

  • Walsh PS, Erlich HA, Higuchi R (1992) Preferential PCR amplification of alleles: mechanisms and solutions. PCR methods and applications, vol 1, pp 241–250

  • BS Weir CC Cockerham (1984) ArticleTitleEstimating F-statistics for the analysis of population structure Evolution 38 1358–1370 Occurrence Handle10.2307/2408641

    Article  Google Scholar 

  • T Weissensteiner JS Lanchbury (1996) ArticleTitleStrategy for controlling preferential amplification and avoiding false negatives in PCR typing BioTechniques 21 1102–1108 Occurrence Handle8969839 Occurrence Handle1:CAS:528:DyaK28XntlGgsrk%3D

    PubMed  CAS  Google Scholar 

  • Zemzami M, Soares CM, Bailey AM, Niblett CL, Nolasco G (2002) Molecular characterization and classification of Moroccan isolates of Citrus tristeza closterovirus. In: Proc. 15th Conf. Intern. Org. Citrus Virol. IOCV, Riverside, pp 8–12

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Correspondence to G. Nolasco.

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Correspondence: Gustavo Nolasco, Adress: University of Algarve, FERN, Campus de Gambelas, 8005-139 Faro, Portugal

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Nolasco, G., Fonseca, F. & Silva, G. Occurrence of genetic bottlenecks during citrus tristeza virus acquisition by Toxoptera citricida under field conditions. Arch Virol 153, 259–271 (2008). https://doi.org/10.1007/s00705-007-1089-8

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