Skip to main content
Log in

Severity and genetic diversity of Citrus tristeza virus complexes infecting ‘Pêra Bianchi’ sweet orange in Paraná, Brazil

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

The aggressiveness and genetic diversity of the Citrus tristeza virus (CTV) infecting sweet orange ‘Pêra Bianchi’ (Citrus sinensis) trees were evaluated under the environmental conditions of the state of Paraná, Brazil. Disease severity was assessed based on stem pitting symptoms in the citrus trees, while genetic diversity was determined by sequencing the virus coat protein (CP) gene. Stem pitting symptoms were less severe in trees maintained under greenhouse conditions and field experimental plots in the municipalities of Paranavaí and Umuarama, where the temperature is higher. In contrast, the most severe stem pitting symptoms were observed in trees from experimental orchards established in colder areas (i.e. municipalities of Arapongas, Cascavel and Londrina), suggesting a temperature effect on symptom development. Analysis of CP sequences indicated intra- and interspecific diversity of the CTV complex for most of the trees included in this study. Recombination analyses of the CP gene also allowed to identify recombinants with parentals related to PIAC-5, a mild isolate, and 1BL-3, found in trees from a field plot in Londrina. The CTV complex infecting ‘Pêra Bianchi’ trees under field conditions showed a high degree of genetic diversity, implying the possibility of multiple infections or even a dynamic rearrangement of the genotypes into different CTV complexes under the environmental conditions of the state of Paraná.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Albiach-Martí MR, Guerri J, Hermoso de Mendonza A, Laigret F, Ballester-Olmos JF, Moreno P (2000a) Aphid transmission alters the genomic and defective RNA populations of Citrus tristeza virus isolates. Phytopathology 90:134–138

    Article  PubMed  Google Scholar 

  • Albiach-Martí MR, Mawassi M, Gowda S, Satyanarayana T, Hilf ME, Shanker S, Almira EC, Vives MC, López C, Guerri J, Flores R, Moreno P, Garnsey SM, Dawson WO (2000b) Sequences of Citrus tristeza virus separated in time and space are essentially identical. Journal of Virology 74:6856–6865

    Article  PubMed  PubMed Central  Google Scholar 

  • Auler PAM, Fiori-Tutida ACG, Tazima ZH (2008) Comportamento da laranjeira ‘Valência’ sobre seis porta-enxertos no noroeste do Paraná. Revista Brasileira de Fruticultura 30:229–234

    Article  Google Scholar 

  • Auler PAM, Leite Júnior RPL, Tazima ZH, Andrade PFS (2014) A citricultura no Paraná. Citricultura Atual 99:17–20

    Google Scholar 

  • Ayllón MA, Rubio L, Moya A, Guerri J, Moreno P (1999) The haplotype distribution of two genes of Citrus tristeza virus is altered after host change or aphid transmission. Virology 255:32–39

    Article  PubMed  Google Scholar 

  • Ayllón MA, Rubio L, Sentandreu V, Moya A, Guerri J, Moreno P (2006) Variations in two gene sequences of Citrus tristeza virus after host passage. Virus Genes 32:119–128

    Article  PubMed  Google Scholar 

  • Baba VY, Giampani JS, Tazima ZH, Yada IFU, Paccola-Meirelles LD, Leite Júnior RP (2014) Agronomic performance of Pera and related sweet orange accessions naturally infected with Citrus tristeza virus in northern Paraná State, Brazil. Tropical Plant Pathology 39:442–448

    Article  Google Scholar 

  • Bar-Joseph M, Marcus R, Lee RF (1989) The continuous challenge of Citrus tristeza virus control. Annual Review of Phytopathology 27:291–316

    Article  Google Scholar 

  • Baruah BR, Kashyap A, Nath PD (2015) Citrus tristeza virus, a worldwide threat to citriculture: advances made in its research and future thrust. Research Journal of Agriculture and Forestry Sciences 3:7–14

    Google Scholar 

  • Benítez-Galeano MJ, Rubio L, Bertalmío A, Maeso D, Rivas F, Colina R (2015) Phylogenetic studies of the three RNA silencing suppressor genes of South American CTV isolates reveal the circulation of a novel genetic lineage. Virus 7:4152–4168

    Article  Google Scholar 

  • Bennett CW, Costa AS (1949) Tristeza disease of citrus. Journal of Agricultural Research 78:207–237

    Google Scholar 

  • Bergua M, Phelan DM, Bak A, Bloom DC, Folimonova SY (2016) Simultaneous visualization of two Citrus tristeza virus genotypes provides new insights into the structure of multi-component virus populations in a host. Virology 491:10–19

    Article  CAS  PubMed  Google Scholar 

  • Biswas KK, Tarafdar A, Diwedi S, Lee RF (2012) Distribution, genetic diversity and recombination analysis of Citrus tristeza virus of India. Virus Genes 45:139–148

    Article  CAS  PubMed  Google Scholar 

  • Carraro BP, Nunes WMC, Corazza-Nunes MJ, Machado MA, Stach-Machado DR (2003) Avaliação de complexos do Citrus tristeza virus da região Norte do Paraná por meio de testes imunológicos e SSCP do gene da capa proteica. Acta Scientiarum (Agronomy) 25:269–273

    Google Scholar 

  • Carvalho SA, Machado MA, Baptista CR, Müller GW, Silvério JL (1997) Caracterização biológica de isolados do vírus da tristeza dos citros. Fitopatologia Brasileira 22:79–84

    Google Scholar 

  • Carvalho SA, Latado RR, Silva LFC, Müller GW (2015) Agronomic performance of thirty-two clones of ‘Pera’ sweet orange in São Paulo state, Brazil. Acta Horticulturae 1065:281–291

  • Caviglione JH, Kiihl LRB, Caramori PH, Oliveira D (2000) Cartas climáticas do Paraná. IAPAR, Londrina

    Google Scholar 

  • Corazza MJ, Zanutto CA, Zanineli-Ré ML, Müller GW, Nunes WMC (2012) Comparison of Citrus tristeza virus (CTV) isolates by RFLP analysis of the coat protein nucleotide sequences and by the severity of the symptoms. Tropical Plant Pathology 37:179–184

    Article  Google Scholar 

  • Costa AS, Müller GW (1980) Tristeza control by cross protection: a U.S.-Brazil cooperative successes. Plant Disease 64:538–541

    Article  Google Scholar 

  • Costa AT, Nunes WMC, Zanutto CA, Müller GW (2010) Stability of Citrus tristeza virus protective isolates in field conditions. Pesquisa Agropecuária Brasileira 45:693–700

    Article  Google Scholar 

  • D’Urso F, Ayllón MA, Rubio L, Sambade A, Hermoso de Mendoza A, Guerri J, Moreno P (2000) Contribution 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 Pathology 49:288–294

    Article  Google Scholar 

  • Dawson WO, Garnsey SM, Tatineni S, Folimonova SY, Harper SJ, Gowda S (2013) Citrus tristeza virus - host interactions. Frontiers in Microbiology 4:1–10

    Article  Google Scholar 

  • Dawson WO, Bar-Joseph M, Garnsey SM, Moreno P (2015) Citrus tristeza virus: making an ally from an enemy. Annual Review of Phytopathology 53:137–155

    Article  CAS  PubMed  Google Scholar 

  • Dodds JA, Jarupat T, Lee JG, Roistacher CN (1987) Effects of strain, host, time of harvest and virus concentration on double-stranded RNA analysis of Citrus tristeza virus. Phytopathology 77:442–447

    Article  CAS  Google Scholar 

  • Febres VJ, Ashoulin L, Mawassi M, Frank A, Bar-Joseph M, Manjunath KL, Lee RF, Niblett CL (1996) The p27 protein is present at one end of Citrus tristeza virus particles. Phytopathology 86:1331–1335

    CAS  Google Scholar 

  • Ferreira DF (2010) Sisvar: Sistema de análise de variância para dados balanceados, versão 5.3 Build 75. DEX/ UFLA, Lavras

    Google Scholar 

  • Folimonova SY (2013) Developing an understanding of cross-protection by Citrus tristeza virus. Frontiers in Microbiology 4:1–9

    Article  Google Scholar 

  • Giampani JS, Tazima ZH, Baba VY, Yada IFU, Leite Júnior RP (2016) Citrus tristeza disease severity and agronomic performance of ‘Pêra’ sweet orange cultivars and selections in the North and Northwest regions of the state of Paraná, Brazil. Revista Brasileira de Fruticultura 38:e-073

    Article  Google Scholar 

  • Harper SJ (2013) Citrus tristeza virus: evolution of complex and varied genotypic groups. Frontiers in Microbiology 4:1–18

    Article  Google Scholar 

  • Hilf ME, Mavrodieva VA, Garnsey SM (2005) Genetic marker analysis of a global collection of isolates of Citrus tristeza virus: characterization and distribution of CTV genotypes and association with symptoms. Phytopathology 95:909–917

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Rundell PA, Guan X, Powell CA (2004) Detection and isolate differentiation of Citrus tristeza virus in infected field trees based on reverse transcription - polymerase chain reaction. Plant Disease 88:625–629

    Article  CAS  Google Scholar 

  • IAPAR - Instituto Agronômico do Paraná. Agrometeorologia. Estações Meteorológicas. Médias Históricas. Available at: http://www.iapar.br/modules/conteudo/conteudo.php?conteudo=1070. Accessed on May 20, 2016

  • Karasev AV (2000) Genetic diversity and evolution of closteroviruses. Annual Review of Phytopathology 38:293–324

    Article  CAS  PubMed  Google Scholar 

  • Karasev AV, Boyko VP, Gowda S, Nikolaeva OV, Hilf ME, Koonin EV, Niblett CL, Cline K, Gumpf DJ, Lee RF, Garnsey SM, Dawson WO (1995) Complete sequence of the Citrus tristeza virus RNA genome. Virology 208:511–520

    Article  CAS  PubMed  Google Scholar 

  • Kitajima EW, Silva DM, Oliveira AR, Müller GW, Costa AS (1964) Thread-like particles associated with tristeza disease of citrus. Nature 201:1011–1012

    Article  CAS  PubMed  Google Scholar 

  • Koller OL, Soprano E (1998) Aumento na severidade do vírus da tristeza dos citros em dois clones de laranja ‘Valência’. Ciência e Agrotecnologia 22:219–225

    Google Scholar 

  • Kong P, Rubio L, Polek M, Falk BW (2000) Population structure and genetic diversity within California Citrus tristeza virus (CTV) isolates. Virus Genes 21:139–145

    Article  CAS  PubMed  Google Scholar 

  • Leonel WMS, Corazza MJ, Zanutto CA, Müller GW, Carvalho AS, Nunes WMC (2015) Stability of Citrus tristeza virus protective isolate ‘Pêra IAC’ according to SSCP analysis of old and new lines of three sweet Orange varieties. Summa Phytopathologica 41:8–12

    Article  Google Scholar 

  • Lu R, Folimonov A, Shintaku M, Li WX, Falk BW, Dawson WO, Ding SW (2004) Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proceedings of the National Academy of Sciences, USA 101:15742–15747

    Article  CAS  Google Scholar 

  • Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumura EE, Coletta Filho HD, Nouri S, Falk WB, Nerva L, Oliveira TS, Dorta SO, Machado MA (2017) Deep sequencing analysis of RNAs from citrus plants grown in a citrus sudden death-affected area reveals diverse known and putative novel viruses. Virus 92:1–19

    Google Scholar 

  • Meissner Filho PE, Soares Filho WS, Velame KVC, Diamantino EP, Diamantino MSAS (2002) Reação de porta-enxertos híbridos ao Citrus tristeza virus. Fitopatologia Brasileira 27:312–315

    Article  Google Scholar 

  • Miller EM, Nickoloff JA (1995) Escherichia coli electrotransformation. Methods in Molecular Biology 47:105–113

    CAS  PubMed  Google Scholar 

  • Moreno P, Ambrós S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9:251–268

    Article  CAS  PubMed  Google Scholar 

  • Müller GW, Targon MLN, Machado MA (1999) Trinta anos de uso do clone pré-imunizado ‘Pêra’ IAC na citricultura paulista. Laranja 20:399–408

    Google Scholar 

  • Niblett CL, Genc H, Cevik B, Halbert S, Brown L, Nolasco G, Bonacalza B, Manjunath KL, Febres VJ, Pappu HR, Lee RF (2000) Progress on strain differentiation of Citrus tristeza virus and its application to the epidemiology of citrus tristeza disease. Virus Research 71:97–106

    Article  CAS  PubMed  Google Scholar 

  • Pappu HR, Pappu SS, Niblett CL, Lee RF, Civerolo E (1993) Comparative analysis of the coat proteins of biologically distinct citrus tristeza closterovirus isolates. Virus Genes 73:255–264

    Article  Google Scholar 

  • Rubio L, Ayllón MA, Kong P, Fernández A, Polek M, Guerri J, Moreno P, Falk BW (2001) Genetic variation of Citrus tristeza virus isolates from California and Spain: evidence for mixed infections and recombination. Journal of Virology 75:8054–8062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salibe AA, Teófilo Sobrinho J, Müller GW (2002) Sinopse de conhecimentos e pesquisas sobre a laranja ‘Pêra. Laranja 23:231–245

    Google Scholar 

  • Sambade A, Ambrós S, López C, Ruiz-Ruiz S, Hermoso de Mendoza A, Flores R, Guerri J, Moreno P (2007) Preferential accumulation of severe variants of Citrus tristeza virus in plants coinoculated with mild and severe variants. Archives of Virology 152:1115–1126

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning - a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Satyanarayana T, Bar-Joseph M, Mawassi M, Albiach-Martí MR, Ayllón MA, Gowda S, Hilf ME, Moreno P, Garnsey SM, Dawson WO (2001) Amplification of Citrus tristeza virus from a cDNA clone and infection of citrus trees. Virology 280:87–96

    Article  CAS  PubMed  Google Scholar 

  • Satyanarayana T, Gowda S, Ayllón MA, Dawson WO (2004) Closterovirus bipolar virion: evidence for initiation of assembly by minor coat protein and its restriction to the genomic RNA 5′ region. Proceedings of the National Academy of Sciences, USA 101:799–804

    Article  CAS  Google Scholar 

  • Souza AA, Müller GW (2006) A premunização no controle da tristeza dos citros. Laranja 27:57–70

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teófilo Sobrinho J, Müller GW, Figueiredo JO, Laranjeira FF, Salibe AA (2001) Laranja ‘Pêra IAC 2000’. Laranja 22:495–501

    Google Scholar 

  • Vives MC, Rubio L, Sambade A, Mirkov TE, Moreno P, Guerri J (2005) Evidence of multiple recombination events between two RNA sequence variants within a Citrus tristeza virus isolate. Virology 331:232–237

    Article  CAS  PubMed  Google Scholar 

  • Weng Z, Barthelson R, Gowda S, Hilf ME, Dawson WO, Galbraith DW, Xiong Z (2007) Persistent infection and promiscuous recombination of multiples genotypes of an RNA virus within a single host generate extensive diversity. PloS One 2:e917

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu GW, Tang M, Wang GP, Jin FY, Yang ZK, Cheng LJ, Hong N (2015) Genetic diversity and evolution of two capsid protein genes of Citrus tristeza virus isolates from China. Archives of Virology 160:787–794

    Article  CAS  PubMed  Google Scholar 

  • Zanutto CA, Corazza MJ, Nunes WMC, Müller GW (2013) Evaluation of the protective capacity of new mild Citrus tristeza virus (CTV) isolates selected for a preimmunization program. Scientia Agricola 70:116–124

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Instituto Agronômico do Paraná (IAPAR) for providing access to infrastructure and to the support offered; Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Paraná, CAPES and CNPq for financial support; Dr. Sérgio A. Carvalho (Centro de Citricultura ‘Sylvio Moreira’) for providing CTV isolates, and Dr. Douglas S. Domingues for assistance in sequence analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rúbia de Oliveira Molina.

Additional information

Section Editor: Jorge Rezende

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giampani, J.S., Santos, K.S., Silva, C.C. et al. Severity and genetic diversity of Citrus tristeza virus complexes infecting ‘Pêra Bianchi’ sweet orange in Paraná, Brazil. Trop. plant pathol. 43, 59–68 (2018). https://doi.org/10.1007/s40858-017-0185-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-017-0185-x

Keywords

Navigation