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Diversity of Citrus Tristeza Virus in Jamaica

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Diversity of Citrus Tristeza Virus in Jamaica 026_JPP1393SC(Tennant)_201 19-03-2013 13:21 Pagina 201 Journal of Plant Pathology (2013), 95 (1), 201-206 Edizioni ETS Pisa, 2013 201 SHORT COMMUNICATION DIVERSITY OF CITRUS TRISTEZA VIRUS IN JAMAICA L. Fisher1,2*, P. Tennant1,2 and W.A. McLaughlin3 1 Department of Life Sciences, 4 Anguilla Close, The University of the West Indies, Mona Campus, Kingston, Jamaica 2 The Biotechnology Centre, 2 St. John’s Close, The University of the West Indies, Mona Campus, Kingston, Jamaica 3 Department of Basic Medical Sciences, Biochemistry Section, The University of the West Indies, Mona Campus, Kingston, Jamaica * Current address: Sciences Department, Plant Molecular and Cellular Biology Program, University of Florida, Gainesville, FL 32611, USA SUMMARY Middle East and North and South America, but it is al- so common to find relatively benign isolates that cause Citrus tristeza virus (CTV), one of the most serious no visible symptoms or loss of tree vigor. CTV originat- pathogens affecting Rutaceae species, causes consider- ed in southeast Asia and was most likely introduced into able economic losses to citrus production worldwide. other regions through the exchange of infected prop- While mild pathotypes have been known for many years agative materials and locally dispersed by several aphid in Jamaica, decline outbreaks were only recently recog- species including Toxoptera citricidus (synonym T. citri- nized after the introduction of the vector Toxoptera cit- cida) and Aphis gossypii, in a semipersistent manner ricidus in 1993. In this study, coat protein (CP) gene se- (Moreno et al., 2008). Typically the virus exists in infect- quences of isolates from four major citrus-growing re- ed trees as heterogeneous populations, with variants gions in Jamaica were obtained and their molecular di- and defective RNAs (Vives et al., 2005). Persistent in- versity compared with reference CTV genotypes from fection, coupled with repeated horizontal transmission other regions. CP sequences from Jamaican isolates mediated by aphids, has also created opportunities for showed identities between 90 to 100% at the nucleotide recombination between genotypes resulting in extensive level and shared similar identities with comparable se- virus diversity (Roy and Brlansky, 2010). quences reported for other Jamaican isolates in 2009 Since the 1990s, there have been increasing reports and 2010. Phylogenetic analysis revealed segregation in- of new incidences of CTV in Central America and the to five of seven lineages. One third of the Jamaican iso- Caribbean along with the northward movement of T. lates clustered with Florida-T30 and Spain-T385 geno- citricidus (Rocha-Peña et al., 1998). The virus was first types, with 99 to 100% identity within the lineage. The recorded in Jamaica in the early 1960s (Stell, 1961). A remaining isolates grouped closely with Florida T36-like low incidence of tristeza was noted and attributed to the genotypes or with the grapefruit and orange stem pit- presence of A. gossypii. T. citricidus was later detected in ting B249 from Venezuela and the New Zealand CTV- 1993 (Hoy et al., 2007). Island-wide surveys conducted resistance breaking genotypes. Identities among these in 2003 documented a more than 5-fold increase in groups ranged between 91 and 99%. The detection of CTV including isolates that react to the monoclonal an- genetic variants and potential recombination events in- tibody MCA-13 in more than half of the locations previ- volving parents from different lineages provide further ously assessed in 1999 shortly after the introduction of evidence of the diversity among Jamaican CTV isolates. T. citricidus (Fisher et al., 2005). Published reports, based on the analysis of a few isolates, indicated the Key words: CTV, phylogenetic analysis, nucleotide di- presence of both decline and stem pitting isolates (Fish- versity, citrus, tristeza. er et al., 2010; Nolasco et al., 2009). Although economic losses directly linked to CTV have only been document- Citrus tristeza virus (CTV) is the causal agent of de- ed in one of the main citrus-growing regions in Jamaica cline syndromes of scions grafted on sour orange and (Lee et al., 2002), an overall decline in citrus production stem pitting in citrus species, cultivars and hybrids. His- has been noted. Production of the Jamaican tangelo torically, CTV has been a devastating pathogen to citrus (Ugli) when compared to sweet orange and grapefruit, industries worldwide and is still of concern either from shows the greatest proportionate reduction. a disease or regulatory perspective (Albiach-Marti, Citrus is one of the important traditional crops in the 2012). Destructive isolates of CTV have caused epi- Jamaican agricultural sector, as it remains a major demics in citrus-growing regions of the Mediterranean, source of economic resilience. While the domestic mar- ket is the largest market for citrus fresh fruit and ac- counts for approximately 85% of production, fruits and Corresponding author: P. Tennant juices are exported to the United Kingdom, United Fax: +876.977.1075 E-mail: [email protected] States, Canada, and other countries in the Caribbean. 026_JPP1393SC(Tennant)_201 19-03-2013 13:21 Pagina 202 202 Genetic diversity of Jamaican CTV isolates Journal of Plant Pathology (2013), 95 (1), 201-206 Given that genetic diversity, studies of CTV in Jamaica ent SSCP patterns. Amplicons of 16 isolates were puri- are limited to a few isolates and since estimation of the fied with the QIAquick system (Roche Diagnostics, genetic variation of CTV is necessary for proper diagno- Germany), TA cloned into the pGEM-T Easy vector sis and the development of long-term management (Promega, USA) and sequenced (1-2 clones per loca- strategies, the molecular characterization of Jamaican tion) in both directions using the universal M13 forward CTV isolates was extended in this study by nucleotide and reverse primers (University at Albany, USA). Vector sequence analysis of the coat protein (CP) gene of iso- and primer sequences from the CTV p27 and p18 gene lates from four major citrus growing regions. Various regions were removed and multiple sequence align- CTV strain typing methods target the CP gene (Niblett ments with those of previous studies (Fisher et al., 2010; et al., 2000; Yokomi et al., 2010), the sequences of Nolasco et al., 2009) and reference CTV sequences were which parallel the genetic structure of the terminal 3 kb performed using the ClustalX 1.8 (Thompson et al., region of the genome and allow for strain differentia- 1997). MEGA4 was used to assess the phylogenetic re- tion. lationships among the isolates using the neighbor-join- Eleven of 16 CTV isolates from four main citrus- ing method after bootstrapping to 1000 replicates for growing Jamaican regions were characterized on Dun- tree construction and inter and intra nucleotide dis- can grapefruit (Citrus aurantifolia Macf.), sweet orange tances based on the Kimura 2-parameter model (Saitou (Citrus sinensis (L.) Osb.) or sweet orange grafted onto and Nei, 1987; Nei and Kumar, 2000; Tamura et al., sour orange (Citrus aurantium L.) (Fisher et al., 2010). 2007). The recombination detection program, RDP4 Samples were collected from sweet orange grafted version Beta 4.16, was used to assess and identify poten- onto the sour orange rootstock that exhibited signs of tial recombination events and possible parental se- decline including swelling at the bud union, sparse fo- quences in the CP gene (Martin et al., 2010). The algo- liage and heavy crops of small fruits, and tested by rithms RDP (Martin and Rybicki, 2000), GENECONV DAS-ELISA using polyclonal and MCA-13 monoclonal (Padidam et al., 1999), BOOTSCAN (Martin et al., antibodies to confirm infection with CTV (Fisher et al., 2005), MaxChi (Smith, 1992), CHIMAERA (Posada 2010). Amplicons were generated by RT-PCR using the and Crandall, 2001), SISCAN (Gibbs et al., 2000), primer pairs CTV-SF15851 and CTV-SR17262 or CTV- 3SEQ (Boni et al., 2007) were employed. By default a MF15920 and CTV-MR17236 (Fisher et al., 2010). Pre- Bonferroni correction highest acceptable P-value of liminary assessment of CP amplicons by single-strand 0.05 was used throughout. conformation polymorphism (SSCP) revealed 24 differ- More than half of the Jamaican CTV isolates induced Table 1. Characteristics of Jamaican CTV isolates cloned in the study. Symptoms on GenBank Field MCA-13 Isolate Origin DG, SwO or accession symptoms1 reactivity3 SwO+SO2 Nos Clarendon Park 10 Clarendon Clarendon park - SwO+SO-St + HM160505 Frankfield 11 Frankfield + SwO-St + HM160506 Montpelier 12 Hanover Montpelier - SwO-ns - GU983384 Montpelier 18 - nt + HM160508 DG-SP, Knockalva 1 Knockalva + + HM160517 SwO+SO-St&B DG-SP, Knockalva 11 - + HM160518 SwO+SO-St Arscott 13 Manchester Arscott - SwO-ns + HM160512 DG-ns, Arscott 28 + + HM160513 SwO+SO-B Arscott 38 + nt + HM160514 Mile Gully 9 Mile Gully + SwO-St + HM160516 Wakefield 21 St. Catherine Wakefield + nt - GU983389 Wakefield 24 - SwO-ns - GU983388 DG-ns, Bybrook 5 Bybrook - SwO-ns, - GU983387 SwO+SO-ns DG-SP, HM160502, Linstead 2 Linstead + - SwO+SO-St GU983386 Linstead 5 + nt + HM160500 Linstead 3 + nt + HM160501 1Symptoms characteristic of CTV, such as swelling at the bud union, twig dieback, sparse foliage and canopy, heavy crops of small fruit size and quality. 2DG ‘Duncan’ grapefruit, SwO sweet orange, SwO+SO sweet orange grafted onto sour orange rootstock, B bud union phloem necrosis, St stunting, SP severe stem pitting, ns no symptom expression, nt not tested. 3Reaction with monoclonal antibody MCA-13 in DAS-ELISA. 026_JPP1393SC(Tennant)_201 19-03-2013 13:21 Pagina 203 Journal of Plant Pathology (2013), 95 (1), 201-206 Fisher et al. 203 stunting or stem pitting symptoms on Duncan grape- fruit or sweet orange or bud union necrosis on sweet or- ange grafted on sour orange (Table 1). Symptoms typi- cal of seedling yellows were not observed. All isolates tested positive for universal CTV reactivity in DAS- ELISA (data not shown) and most, including those de- rived from apparently asymptomatic field trees, showed MCA-13 reactivity (Table 1).
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