RESPONSE OF MANDARIN CULTIVARS AND HYBRIDS TO CITRUS LEPROSIS VIRUS

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1 017_JPP_179RP_ :29 Pagina 307 Journal of Plant Pathology (2008), 90 (2), Edizioni ETS Pisa, RESPONSE OF MANDARIN CULTIVARS AND HYBRIDS TO CITRUS LEPROSIS VIRUS M. Bastianel 1, J. Freitas-Astúa 1,2, F. Nicolini 1, N. Segatti 1, V.M. Novelli 1, V. Rodrigues 1, C.L. Medina 3 and M.A. Machado 1 1 Centro APTA Citros Sylvio Moreira/IAC, C.P.04, Cordeirópolis, SP, Brazil Embrapa Mandioca e Fruticultura Tropical, s/n, Cruz das Almas, BA, Brazil Grupo de Consultores de Citros/GCONCI, C.P.144, Cordeirópolis, SP, Brazil SUMMARY Mandarins and their hybrids are considered resistant to citrus leprosis. However, there are no studies addressing such resistance in the field under natural inoculation conditions. In this work we evaluated, through symptom analysis, the response to leprosis of 25 different genotypes of mandarins and hybrids from a ten-year-old orchard with a long history of the disease. We observed higher resistance levels among Citrus reticulata Blanco varieties and some of their hybrids, such as the Murcott tangor [C. reticulata x C. sinensis (L.) Osbeck], which did not show any leprosis symptoms. C. deliciosa Tenore and C. clementina hort. ex Tanaka accessions and hybrids, such as Lee tangelo [(C. clementina x (C. reticulata x C. paradisi Mac.)], were the most susceptible under natural conditions. However, even in those genotypes, most of the symptoms were observed in leaves and not in fruits, as often seen in sweet oranges (C. sinensis), considered the most susceptible species of citrus to leprosis. This suggests that even susceptible accessions of mandarins are likely to show some level of resistance when compared to sweet oranges. Key words: Mandarin, citrus, CiLV, leprosis, resistance. INTRODUCTION Leprosis is considered the main viral disease for Brazilian citrus production due to the high costs of chemical control of its vector Brevipalpus phoenicis (Acari: Tenuipalpidae). Additionally, the global importance of citrus leprosis has recently increased with the northbound spread of the virus to new areas in South and Central America (Rodrigues et al., 2003; Bastianel et al., 2006a). In all reports of the disease, sweet orange (Citrus sinensis) prevails as the most affected species. Corresponding author: M. Bastianel Fax: mbastianel@centrodecitricultura.br The common form of the virus is referred to as Citrus leprosis virus cytoplasmic type (CiLV-C) due to its cellular localization (Colariccio et al., 1995; Rodrigues et al., 2003). In contrast, a rare form of CiLV was first described in 1972 (CiLV-N) where virus particles accumulate in the nucleus of infected cells (Kitajima et al., 1972; Rodrigues et al., 2003). The latter type has been reported only once from Panama (Dominguez et al., 2001) and from a few municipalities in Brazil (Bastianel et al., 2006a). Because of its morphology and presence either in the cytoplasm or in the nucleus of infected cells, CiLV-C has been considered a tentative member of the Rhabdoviridae family (Rodrigues et al., 2003). However, molecular studies have shown that the nuclear and the cytoplasmic types of CiLV are completely different viruses (Freitas-Astúa et al., 2005) and that CiLV-C genome does not share sequence or organization similarity with rhabdoviruses (Locali-Fabris et al., 2006; Pascon et al., 2006). Hence, CiLV-C was proposed as the type member of a new plant virus genus named Cilevirus (Locali-Fabris et al., 2006). Leprosis can cause typical chlorotic to necrotic circular local lesions in citrus leaves, stems and fruits associated with mite feeding sites, since the virus does not infect its hosts systemically (Rodrigues et al., 2003). Even though there is a common pattern observed among leprosis lesions, they can vary in size, shape, and colour depending on the host species, developmental stage of the plant, pathogen isolate and probably, environmental conditions (Locali et al., 2003; Bastianel et al., 2006a). Marques et al. (2007) analyzing leaves and twigs of sweet oranges affected by CiLV, noted histological changes in the phloem such as hyperplasia of the cortical and phloem parenchyma cells, causing obliteration of the phloem vessels; this could explain why the virus does not become systemic. The relationship between the virus and its vector is still unclear, but recent studies have suggested that, contrary to what has been proposed (Rodrigues et al., 2003), it can be a persistent circulative rather than propagative type of interaction (Nicolini et al., 2007; Freitas-Astúa et al., 2008). Although plants of the genus Citrus are the only known natural hosts of CiLV (Rodrigues et al., 2003), the virus can be mite-transmitted to other plants usually

2 Table 1. Citrus accessions evaluated for the presence of leprosis symptoms in different organs, disease incidence (%), and severity. Species Citrus reticulata C. deliciosa C. suhuiensis Common name Number of plants evaluated Symptoms on: Leaf Branch Fruit Percentage of symptomatic plants Vermelha mandarin Cravo mandarin Emperor mandarin Harris mandarin Muscia mandarin Ponkan mandarin África do Sul mandarin De Wildt mandarin Loose Jacket mandarin Span Americana mandarin Sunburst mandarin Rosehaugh Nartjee mandarin Empress mandarin Tardia da Sicilia mandarin mandarin Mogi das Cruzes mandarin Swzinkon mandarin Swzinkon x Swzinkon-Tizon hybrid Clementine Caçula 3 mandarin C. clementina x. C. reticulata Clementine Caçula 2 mandarin C. clementina x (C. reticulata x C. paradisi) C. sinensis x C. reticulata Lee tangelo Osceola tangelo Nova tangelo Ortanique tangor Murcott tangor Score (see text) 308 Mandarin and hybrids response to CiLV Journal of Plant Pathology (2008), 90 (2), _JPP_179RP_ :29 Pagina 308

3 017_JPP_179RP_ :29 Pagina 309 Journal of Plant Pathology (2008), 90 (2), Bastianel et al. 309 found in citrus orchards, such as weeds, windbreaks and hedgerows (Nunes, 2007). This may have consequences for the epidemiology of the disease. Sweet oranges are considered the most susceptible citrus species and, even though there are differences in susceptibility amongst them, none of the commercial varieties are resistant (Rodrigues et al., 2000; Bastianel et al., 2006a). In Brazil leprosis is important in large areas cultivated with sweet orange, associated with the yearround presence of the vector and abundant source of inoculum in most orchards. In fact, approximately 80% of the citrus trees grown in São Paulo State, the main producer in Brazil, are sweet orange varieties, highly susceptible to CiLV. In 1995, more than 60% of the State s citrus orchards had plants with leprosis symptoms, which explains why chemical control of the vector is widely used (Salva and Massari, 1995). Mandarins and some of their hybrids exhibit high levels of resistance to the disease (Rodrigues et al., 2003; Bastianel et al., 2006a), but there is very little if any information on the behaviour of these genotypes under natural CiLV mite inoculation. This information is crucial for countries, like those of the Mediterranean basin, where mandarins are economically important and the mite is present. MATERIALS AND METHODS Plant material. The response to leprosis of twentyfive genotypes of mandarins and hybrids (Table 1) was studied under natural conditions of CiLV inoculation and based on the symptoms observed in the field, in a ten-year-old orchard with a long history of the disease, located in Mogi Mirim, São Paulo State, Brazil, a region of endemic leprosis. The experimental design was eight randomized blocks with two replicates for each genotype, with 5 m spacing between rows and 6 m within rows. The area studied was surrounded by orchards of Cravo and Satsuma mandarins. Disease assessment. Symptoms were evaluated every two months over a year period. Disease incidence was scored in the leaves, branches and fruits, and the percentage of symptomatic plants was determined. Severity was scored according to an empirical scale from 0 (no lesions) to 5 (Rodrigues, 2000). In particular: 1 = few lesions restricted to a particular region of the plant; 2 = lesions in more than one plant organ and/or distributed in more than one sector of the plant; 3 = plentiful lesions throughout the plant; 4 = plentiful lesions throughout the plant accompanied by leaf and/or fruit drop; 5 = like 4 plus dieback of branches. RESULTS AND DISCUSSION From the 25 genotypes studied, 16 showed various levels of leprosis symptoms, which remained unaltered throughout the six assessments (Table 1). Although symptoms were similar to those observed in sweet oranges (Fig. 1), they occurred mainly in the leaves and rarely in branches and fruits. High disease variability was observed particularly within varieties of C. reticulata, which correlates with the high genetic variability within the group (Machado et al., 1996). The two varieties showing highest leprosis incidence and severity were Vermelha and Cravo mandarins (Table 1), both possible hybrids of C. reticulata with C. deliciosa (Machado et al., 1996; Coletta Filho et al., 1998). While Vermelha mandarin is not an important variety in Brazil, Cravo is grown in commercial orchards and, reportedly, often shows leprosis symptoms on leaves and branches (Salvo Filho et al., 1997), which corroborates our data. Interestingly, other C. reticulata accessions, considered true varieties, showed low leprosis or remained symptomless throughout (Table 1). Overall, C. deliciosa (Mediterranean mandarin) varieties were more susceptible than those of C. reticulata. Machado et al. (1996), using molecular markers, observed complete genetic similarity in approximately 20 accessions of Mediterranean mandarins, suggesting very low genetic variability and, possibly, widespread susceptibility to CiLV within the group. The Swzinkon mandarin (C. suhuiensis) and hybrids were also susceptible to leprosis, as were most C. clementina hybrids (Table 1). Interestingly, the two C. clementina x C. reticulata hybrids evaluated (Clementine Caçula 2 and Clementine Caçula 3) have a Cravo mandarin parent (Pio et al., 2000), and may have inherited their susceptibility from that genotype. Amongst tangelos [C. clementina x (C. reticulata x C. paradisi)], Lee exhibited the highest susceptibility, while Osceola showed few symptomatic plants and Nova remained symptomless throughout (Table 1). Differential response to CiLV was also observed beetwen Ortanique and Temple tangors (C. sinensis x C. reticulata). In the field, Ortanique showed high disease incidence, similar to that observed by Freitas-Astúa et al. (unpublished data) under greenhouse conditions for Temple. Ortanique (and Temple) have likely inherited their susceptibility from the sweet orange parent, but Murcott tangor, which remained symptomless throughout the evaluation, may have inherited the resistance trait from its C. reticulata parent (Bastianel et al., 2006b). The resistance (or tolerance) of Murcott to leprosis is known from previous studies that have ascertained by biological (Boaretto et al., 1994; Rodrigues, 1995) and molecular (Bastianel et al., 2004; Nicolini et al., 2008) methods that Murcott has low CiLV titres. It was not possible to detect the presence of the virus by RT-PCR in any of the field samples collected in this study, despite of the endemic character of the disease in neighbouring sweet orange plantings. This is probably

4 017_JPP_179RP_ :29 Pagina Mandarin and hybrids response to CiLV Journal of Plant Pathology (2008), 90 (2), Fig. 1. Typical local lesions induced by leprosis (cytoplasmic type) in the leaves of (A) Lee tangelo (A), Osceola tangelo (B), Sicilia orange (C), Vermelha orange (D), Clementine Caçula 2 (E), Cravo mandarins (F), Clementine Caçula 2 fruits (G) and Mogi das Cruzes mandarin (H). due to low level of target RNA in the mandarin grove, due to the natural resistance observed in these species and their hybrids. Since Murcott is one of the main citrus genotypes grown in Brazil for fresh fruit consumption and exhibits resistance to leprosis and citrus variegated chlorosis (CVC, caused by Xylella fastidiosa), one of the other main citrus diseases in the country, it has been widely used in breeding programs (Oliveira et al., 2002). In fact, all information available on the genetic inheritance of resistance to leprosis has been obtained by Bastianel et al. (2006b) using Murcott tangor. These authors assessed the incidence and severity of leprosis in a population resulting from a cross between Murcott (highly resistant) and Pêra sweet orange (highly susceptible) infested with viruliferous B. phoenicis, concluding that inheritance of resistance to leprosis is probably controlled by few genes present in Murcott (Bastianel et al., 2006b). Differential behaviour towards leprosis amongst citrus varieties, even among the susceptible ones, has been reported by some authors (Roessing and Salibe, 1967; Rodrigues et al., 2000, 2003) and may be a reaction either to the virus or to the vector (Rodrigues, 2000). However, in our study mites were observed on all genotypes assessed, indicating that the variation in symptoms was due to differential responses to CiLV. It is known that lemons [Citrus limon (L.) Osbeck], limes [C. aurantifolia (Christmann) Swingle], mandarins (various species), grapefruit [C. paradisi (McFad.) Hooker] and some tangors (hybrids between sweet or-

5 017_JPP_179RP_ :29 Pagina 311 Journal of Plant Pathology (2008), 90 (2), Bastianel et al. 311 anges and mandarins) show various levels of resistance to CiLV (Roessing and Salibe, 1967; Rodrigues et al., 2003; Bastianel et al., 2006a, 2006b). However, few studies have been made with the objective to compare resistance amongst these genotypes. Our results were based on the assessment of leprosis symptoms in a commercial orchard containing several varieties and hybrids of different species of mandarins, located in a region where CiLV is endemic. This combination of factors, uncommon to find under natural conditions, provided an unique opportunity to study the behaviour of these genotypes against the disease. Broadening our experience on the response of mandarin cultivars and hybrids to leprosis under natural inoculation conditions is relevant for a better understanding of the epidemiology of the disease and its management. ACKNOWLEDGEMENTS We would like to thank the owners of the Esmeralda farm (Mogi Mirim, São Paulo, Brazil), where the work was done. Financial support was from the Fund for Citrus Plant Protection (Fundecitrus), Brazil and FAPESP (Proc. 04/ ). N. Segatti had a scholarship from Fundecitrus. REFERENCES Bastianel M., Freitas-Astua J., Rodrigues V., Arrivabem F., Antonioli-Luizon R., Machado M.A., Resposta do tangor Murcott à inoculação do vírus da leprose dos citros a campo e em casa de vegetação. Laranja 25: Bastianel M., Freitas-Astúa J., Kitajima E.W., Machado M.A., 2006a. The citrus leprosis pathosystem. Summa Phytopathologica 32: Bastianel M., Oliveira A.C., Cristofani M., Guerreiro Filho O., Freitas-Astúa J., Rodrigues V., Astúa-Monge G., Machado M.A., 2006b. Inheritance and heritability of resistance to citrus leprosis. Phytopathology 96: Boaretto M.A.C., Chiavegato L.G., Transmissão da leprose por ácaros Brevipalpus phoenicis (Geijskes, 1939) (Acari: Tenuipalpidae) temporariamente mantidos em hospedeiros intermediários, em condições de laboratório. Científica 22: Colariccio A., Lovisolo O., Chagas C.M., Galetti S.R., Rossetti V., Kitajima E.W., Mechanical transmission and ultrastructural aspects of citrus leprosis virus. Fitopatologia Brasileira 20: Coletta Filho H.D, Machado M.A., Targon M.L.P.N., Moreira M.C.P.Q.D.G., Pompeu J. Jr., Analysis of the genetic diversity among mandarins (Citrus spp.) using RAPD markers. Euphytica 102: Dominguez F.S., Bernal A., Childers C.C., Kitajima E.W., First report of citrus leprosis in Panama. Plant Disease 85: 228. Freitas-Astúa J., Kitajima E.W., Locali E.C., Antonioli-Luizon R., Bastianel M., Machado M.A., Further evidence to support that citrus leprosis virus-cytoplasmic and nuclear types are different viruses. Annual Meeting of the American Phytopathological Society, Caribbean Division, San Jose 2005: 93. Freitas-Astúa J., Nicolini F., Bastianel M., Kitajima E.W., Interações entre o vírus da leprose dos citros e seu vetor Brevipalpus phoenicis. Summa Phytopathologica 34: Kitajima E.W., Müller G.W., Costa A.S., Yuki W., Short, rod-like particles associated with citrus leprosis. Virology 50: Locali E.C., Freitas-Astúa J., Souza A.A., Takita M.A., Astúa- Monge G., Antonioli R., Kitajima E.W., Machado M.A., Development of a molecular tool for the diagnosis of leprosis, a major threat to citrus production in the Americas. Plant Disease 87: Locali-Fabris E.C., Freitas-Astúa J., Souza A.A., Takita M.A., Astúa-Monge G., Antonioli-Luizon R., Rodrigues V., Targon M.L.P.N., Machado M.A., Complete nucleotide sequence, genomic organization and phylogenetic analysis of Citrus leprosis virus cytoplasmic type. Journal of General Virology 87: Machado M.A., Coletta-Filho H.D., Targon M.L.P.N., Pompeu J. Jr., Genetic relationship of Mediterranean mandarins (C. deliciosa Ten.) using RAPD markers. Euphytica 92: Marques J.P.R., Freitas-Astúa J., Kitajima E.W., Appezzatoda-Glória B., Lesões foliares e de ramos de laranjeira-doce causadas pela leprose-dos-citros. Pesquisa Agropecuária Brasileira 42: Nicolini F., Bastianel M., Freitas-Astua J., Kitajima E.W., Kubo K., Antonioli-Luizon R., Schons J., Machado M.A., Evidence suggesting that Brevipalpus phoenicis-citrus leprosis virus interaction may not be of the circulative propagative type. In: 17th Conference of the International Organization of Citrus Virologists Adana 2007: 156. Nicolini F., Bastianel M., Freitas-Astúa J., Antonioli-Luizon R., Schons J., Machado M.A., Quantification of Citrus leprosis virus in its host plants. In: XXXI Congresso Paulista de Fitopatologia, Campinas 2008: 66. Nunes M.A., Transmissão do vírus da leprose dos citros por B. phoenicis (Acari: Tenuipalpidae) para plantas próximas de pomares cítricos. PhD Thesis: Faculdade de Ciências Agrárias e Veterinárias, Jaboticabal, Brazil. Oliveira A.C., Garcia A.N., Cristofani M., Machado M.A., Identification of citrus hybrids through the combination of leaf apex morphology and SSR markers. Euphytica 128: Pascon R.C., Kitajima J.P., Breton M.C., Assumpção L., Greggio C., Zanca A., Okura V.K., Alegria M.C., Camargo M.E., Silva G.G.C., Cardozo J.C., Vallim M.A., Franco S.F., Silva V.H., Jordão Jr H., Oliveira F., Giachetto P.F., Ferrari F., Aguilar-Vildoso C., Franchiscini F.J.B., Silva J.H.I., Arruda P., Ferro J.A., Reinach F., Silva A.C.R., The complete nucleotide sequence and genomic organization of Citrus leprosis-associated virus, cytoplasmatic type (CiLV-C). Virus Genes 32: Pio R.M., Minami K., Figueiredo J.O., Pompeu J. Jr., Caracterização e avaliação de duas novas variedades híbridas de tangerina Clementina. Laranja 21:

6 017_JPP_179RP_ :29 Pagina Mandarin and hybrids response to CiLV Journal of Plant Pathology (2008), 90 (2), Rodrigues J.C.V., Leprose dos citros: cito-histopatologia, transmissibilidade e relação com o vetor Brevipalpus phoenicis Geijskes (Acari: Tenuipalpidae). Dissertation. Universidade de São Paulo, Piracicaba, Brazil. Rodrigues J.C.V., Relações patógeno-vetor-planta no sistema leprose dos citros. PhD thesis. Universidade de São Paulo, Piracicaba, Brazil. Rodrigues J.C.V., Kitajima E.W., Childers C.C., Chagas C.M., Citrus leprosis virus vectored by Brevipalpus phoenicis (Acari: Tenuipalpidae) on citrus in Brazil. Experimental and Applied Acarology 30: Rodrigues J.C.V., Muller G.W., Nogueira N.L., Machado M.A., Yield damage associated to citrus leprosis on sweet-orange varieties. Proceedings of the 9 th Congress of the International Society of Citriculture, Orlando : Roessing C., Salibe A.A., Incidência da leprose em variedades cítricas. Ciência e Cultura 19: 303. Salvo Filho A., Notas sobre o tratamento fitossanitário em citros. Laranja 18: Salva R.A., Massari C.A., Situação do ácaro da leprose no Estado de São Paulo, levantamento Fundecitrus, agosto In: Oliveira C.A.L., Donadio L.C. (eds.) Leprose dos Citros. pp , FUNEP, Jaboticabal, SP, Brazil. Received January 23, 2008 Accepted March 19, 2008

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