Preferred name: Citrus leprosis disease
Taxonomic position: Viruses and viroids: Viruses (unclassified)
Common names in English: citrus leprosis, leprosis of citrus
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: CILV00

Citrus leprosis disease has been reported from a range of citrus species, with sweet orange (Citrus sinensis) reported as the most susceptible host. The gradual discovery of the viruses associated with this disease causes uncertainty about the identity of the viruses involved in older reports. Consequently, information on the natural host range of individual viruses is frequently limited. Many of them have however been shown to be able to experimentally infect a larger range of plants than their known natural host range, which suggests that the natural host range may in many cases be broader than currently known.

Only a few non-rutaceous species were reported as naturally infected by one or another of the seven causal viruses (EFSA, 2017). However, for OFV, the orchid strains (OFV-Orc1 and Orc2) are able to infect a very broad range of orchid species as well as a range of non-orchid hosts (Kondo et al., 2003). While isolates of these two strains have also been reported from citrus, there is no record to date of isolates of the citrus strains (OFV-Cit1 and Cit2) naturally infecting orchids.

CiLV-C host range includes various citrus species with sweet orange (Citrus sinensis) being the most affected. Other reported hosts include sour orange (C. aurantium), rough lemon (C. jambhiri), Citron (C. medica), Cleopatra mandarin (C. reshni), mandarin (C. reticulata), Grapefruit (C. paradisi), sweet lime (C. limettioides), Key lime (C. aurantiifolia), Rangpur lime (C. limonia), and hybrids such as Tangelo (C. reticulata x C. x paradisi) or Citrange (C. sinensis x Poncirus trifoliata). Lemon (C. limon) is considered as practically immune (Bastianel et al., 2010). CiLV-C has also been observed in natural infection in Commelina benghalensis and Swinglea glutinosa and has been experimentally transmitted to plants of more than 25 families (León et al., 2008; Nunes et al., 2012; Garita et al., 2014; Freitas-Astúa et al., 2018; Chabi-Jesus et al., 2021).

CiLV-C2 has only been reported so far from C. sinensis and a few other non-citrus hosts including S. glutinosa, Dieffenbachia spp., Hibiscus spp. (including H. rosa-sinensis) and passionfruit (Passiflora edulis) (Melzer et al., 2013; Roy et al., 2015a, Olmedo-Velarde et al., 2022; Padmanabhan et al., 2023).

In Hawaii, HGSV-2 mainly infects hibiscus plants (Hibiscus arnottianus, H. tiliaceus) but has also been found in natural infection in a few C. sinensis, C. reticulata and C. volkameriana (Volkamerian lemon) plants (Melzer et al., 2012; Roy et al., 2015a)

In addition to infecting orchids (Kondo et al., 2003) and a range of other non-citrus hosts, the orchid strains of OFV (OFV-Orc1 and OFV-Orc2) have been respectively reported in South Africa from C. sinensis (Cook et al., 2019) and in the USA (Hawaï) from C. reticulata and C. jambhiri (Olmedo-Velarde et al., 2021). The citrus strains of OFV (Cit1 and Cit2) have respectively been reported so far from C. sinensis, C. aurantiifolia, C. aurantium, C. limetta, C. latifolia, C. limon, C. paradisi and C. reticulata (Cit1) (Cruz-Jaramillo et al., 2014; Roy et al., 2015a, b) and from C. aurantium and C. sinensis (Cit2) (Roy et al., 2020).

CiLV-N sensu novo has so far only been reported in natural infection in C. sinensis. It was not identified in mandarin (C. reticulata) or in Key lime (C. aurantifolia) growing near infected C. sinensis suggesting that mandarin and Key lime may not be part of its host range (Ramos-González et al., 2017). It has also been observed in mixed natural infection with CiLV-C2 in S. glutinosa and in Dieffenbachia sp. (Roy et al., 2015a).

CiCSV has been reported so far from only three natural hosts: C. sinensis, Agave desmettiana and H. tiliaceus (Chabi-Jesus et al., 2018, 2019).

The most recently described virus, CiBSV has only been reported so far from C. sinensis (Chabi-Jesus et al., 2023).

	Viruses causing the Leprosis disease
Rutaceous host plants	CiLV-C	CiLV-C2	HGSV-2	OFV (citrus strains)	CiLV-N sensu novo	CiCSV	CiBSV
Citrus aurantiifolia	X			X
C. aurantium	X			X
C. deliciosa
C. jambhiri	X			X
C. latifolia				X
C limettioides	X
C. limetta				X
C. limon				X
C. limonia	X
C. medica	X
C. paradisi	X			X
C. reshni	X
C. reticulata	X		X	X
C. sinensis	X	X	X	X	X	X	X
C. suhuiensis	X
C. volkameriana	X		X
C. reticulata x C. paradisi	X
C. clementina x C. reticulata	X
C. reticulata x C. sinensis	X
C. sinensis x P. trifoliata	X
Swinglea glutinosa	X	X			X
Non rutaceous host plants
Agave desmettiana						X
Commelina benghalensis	X
Dieffenbachia spp.		X			X
Hibiscus arnottianus			X
H. rosa-sinensis		X
H. tiliaceus			X			X
Passiflora edulis		X

Host list: Agave desmettiana, Citrus hybrids, Citrus medica, Citrus reshni, Citrus reticulata, Citrus x aurantiifolia, Citrus x aurantium var. deliciosa, Citrus x aurantium var. paradisi, Citrus x aurantium var. sinensis, Citrus x aurantium, Citrus x latifolia, Citrus x limon var. limetta, Citrus x limon var. limettioides, Citrus x limon, Citrus x limonia var. jambhiri, Citrus x limonia var. volkameriana, Citrus x limonia, Commelina benghalensis, Dieffenbachia sp., Hibiscus arnottianus, Hibiscus rosa-sinensis, Hibiscus tiliaceus, Passiflora edulis, Swinglea glutinosa

Citrus leprosis disease has been reported from South, Central and North America (including Hawaii) and South Africa. Due to the gradual discovery of the causal agents and to the uncertainties about which viruses are involved in older reports, there are significant uncertainties about the distribution of individual viruses.

CiLV-C is by far the most widespread virus associated with citrus leprosis disease. It has been reported from South America (Argentina, Bolivia, Brazil (Acre, Amazonas, Bahia, Ceara, Distrito Federal, Espirito Santo, Goias, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Para, Parana, Piaui, Rio de Janeiro, Rio Grande do Sul, Rondonia, Roraima, Santa Catarina, Sao Paulo, Sergipe, Tocantins), Colombia, Paraguay, Uruguay, Venezuela), Central America and the Carribean (Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, Panama) and North America (Mexico).

CiLV-C2 has been reported from Colombia (Roy et al., 2013a, Padmanabhan et al., 2023) and, in non-citrus hosts (H. rosa-sinensis, P. edulis) from Hawaii and Florida (USA) (Melzer et al., 2013; Roy et al., 2018; Olmedo-Velarde et al., 2022).

HGSV-2 has so far only been reported from Hawaii (USA).

OFV. The orchid strains (Orc1 and Orc2) of OFV have been reported from a range of countries but have only been reported from Citrus spp. in South Africa (Cook et al., 2019) and in Hawaii (Olmedo-Velarde et al. 2021). The citrus strains (Cit1 and Cit2) of OFV have been described in several countries of the Americas (Brazil, Colombia, Mexico, Panama) (Cruz-Jaramillo et al., 2014; EFSA PLH Panel, 2017; Roy et al., 2013b, 2015a, 2020).

CiLV-N sensu novo has so far only been detected in Brazil in the State of São Paulo (Ramos-González et al., 2017)

CiCSV has so far only been reported from Brazil (State of Piaui) (Chabi-Jesus et al., 2018).

CiBSV has so far only been reported from Brazil (States of Rio Grande do Sul and Santa Catarina) (Chabi-Jesus et al., 2023).

Africa: South Africa
North America: Mexico, United States of America (Hawaii)
Central America and Caribbean: Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, Panama
South America: Argentina, Bolivia, Brazil (Acre, Amazonas, Bahia, Ceara, Distrito Federal, Espirito Santo, Goias, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Para, Parana, Piaui, Rio de Janeiro, Rio Grande do Sul, Rondonia, Roraima, Santa Catarina, Sao Paulo, Sergipe, Tocantins), Colombia, Paraguay, Uruguay, Venezuela

Unlike most viruses, the leprosis-causing viruses are unable to spread systemically in their hosts and only cause localized lesions corresponding to the replication and local spread of the viruses by cell-to-cell movement, close to an inoculation point (Bastianel et al., 2010; Roy et al., 2015a; Dietzgen et al., 2018; Freitas-Astúa et al., 2018). All leprosis viruses are transmitted by false spider mites of the genus Brevipalpus (Tenuipalpidae) (Rodriges & Childers, 2013, Roy et al., 2015a; Beltran-Beltran et al., 2020). These mites feed on young plant tissues (leaves, twigs, fruits etc.) and, if viruliferous, transmit the virus when wounding the plants with their stylets (Ferreira et al., 2020). The virus will then replicate in the inoculated cell and spread to neighbouring cells in a gradual process. Disease symptoms are limited to the patches of infected plant tissues resulting from this localized, non-systemic spread of the virus. Plant tissues outside these infection sites are unaffected but when a large population of viruliferous mites is present, the entire tree canopy can show symptoms, mimicking a systemic infection (EFSA, 2017). Symptom development can take a few weeks after inoculation with most of the symptoms appearing between 3 and 4 weeks post inoculation (Chiavetto et al., 1984; Tassi et al., 2017).

Mites acquire the virus by feeding on patches of infected host tissue. Brevipalpus mites transmit all leprosis viruses in a persistent circulative manner and the mites remain viruliferous for an extended period of time. All life stages can acquire and transmit the viruses but viruses are not transmitted transovarially to the progeny (Rodrigues et al., 2003; Bassanezi & Laranjeria, 2007). There are indications that Dichorhaviruses (OFV, CiLV-N, CiCSV, CiBSV) replicate in their mite vectors so that they could have a circulative-replicative mode of transmission (Kondo et al., 2003; Roy et al., 2015a; Chabi-Jesus et al., 2018). However, the ability of cileviruses to replicate in their mite vectors has not been clearly established (Tassi et al., 2017; Chabi-Jesus et al., 2018; Tassi et al., 2022).

The taxonomy of Brevipalpus mites is complex (Navia et al., 2013) and has significantly evolved over time. It should also be noted that transmission experiments involving mites are notoriously complex to perform. The information on virus-vector relationships in the case of leprosis viruses is therefore limited and the vector range of individual viruses might be broader than currently reported.

Within the B. phoenicis sensu lato species complex (Beard et al., 2015), B. yothersi is considered the most important vector of the Cileviruses CiLV-C and CiLV-C2. B. papayensis and B. phoenicis sensu stricto can also transmit CiLV-C, but with lower efficiency (Ramos-González et al., 2016; Nunes et al., 2018; García-Escamilla et al., 2018; Ferreira et al., 2020). The Higrevirus HGSV-2 has been shown to be transmitted by B. azores but the mechanism involved is still poorly documented (Olmedo-Velarde, 2021, 2023).

B. californicus has been shown to be a vector of OFV-Cit1 (García-Escamilla et al., 2018), whereas B. phoenicis sensu stricto transmits CiLV-N sensu novo (Ramos-González et al., 2017). B. yothersi and a possible new related species ("B. aff. yothersi") have been shown to transmit CiCSV (Chabi-Jesus et al., 2018, 2019; Ramos-González et al., 2017), while citrus bright spot virus has been shown to be vectored by B. azores (Chabi-Jesus et al., 2023).

Symptoms

Round to elliptical local lesions are seen on fruits, leaves and twigs. Their severity varies with the species of citrus host and, possibly, the virus involved. Leaf symptoms are usually roundish with a dark-brown central spot about 2-3 mm in diameter, surrounded by a chlorotic halo, in which 1 to 3 brownish rings frequently appear surrounding the central spot. The overall lesion size varies from 10 to 20 mm, though larger lesions may form by the fusion of 2 or more adjacent lesions. On fruits, lesions are 10-20 mm wide necrotic spots, with a necrotic centre. Gum exudation is occasionally observed on the lesion. On green fruits, the lesions are initially yellowish, becoming more brown- or blackish, sometimes depressed and reducing the market value of the fruits. On twigs, lesions are protuberant, cortical, grey, brownish, or sometimes dark-reddish. Lesions may coalesce when present in large numbers, leading to the death of the twig. Superficially lignified tissues such as the main trunk do not show symptoms but the trunk of young seedlings may. In extreme cases, such as those seen in Argentina (where the disease is called lepra explosiva de los cítricos), severe defoliation and fruit fall are observed (Frezzi, 1940; Bitancourt, 1955; Rossetti et al., 1969; Bastianel et al., 2006; Roy et al., 2013a; Moreira et al., 2022).

Citrus leprosis lesions are usually very characteristic, but may sometimes be mistaken for lesions of citrus canker, caused by the bacterium Xanthomonas citri pv. citri (EPPO, 2023) or zonate chlorosis, which is associated with infestation by Brevipalpus mites but shows symptoms that are essentially concentric green and chlorotic rings and do not become necrotic (Catara et al., 2021).

Only a few differences have been reported in the symptoms induced by the different viruses and these were minor and not sufficient to allow an accurate diagnosis of the virus involved. Cytoplasmic viruses such as CiLV-C are reported to cause larger lesions that tend to be pale green in colour, with one or more concentric gummy ring(s), whereas lesions caused by nuclear viruses such as OFV-Cit1 tend to have a darker centre with orange or bright yellow rings at the periphery (Melzer et al., 2013; Roy et al., 2014).

Morphology

The cytoplasmic viruses (Cilevirus, Higrevirus) have non-enveloped bacilliform particles (50-70 × 110-120 nm) and cause the accumulation of electron-dense cytoplasmic inclusions. The nuclear viruses (Dichorhavirus) have non-enveloped, short rod-like particles (40–50 nm × 100–110 nm) and are associated with the presence of a large electron-lucent inclusion in the nucleus (Kitajima et al., 2003; Freitas-Astúa, 2018).

Detection and inspection methods

Procedures for the inspection of places of production of citrus plants for planting and for the inspection of consignments of citrus fruits are provided in the EPPO Standards PM 3/(in press) (EPPO, 2023) and PM 3/90 (EPPO, 2020) respectively.

In addition to symptom observation and electron microscopy to observe viral particles or cytopathological alterations, leprosis viruses can be detected by mechanical inoculation of herbaceous indicators that react with the production of local lesions such as Chenopodium amaranticolor, C. quinoa, Phaseolus vulgaris and Gomphrena globosa (Colariccio et al., 1995; Garita et al., 2013). However, no indicators have been described for the most recently discovered leprosis viruses such as CiCSV and CiBSV.

Serological detection tests were developed for some of the leprosis viruses but antibodies are not commercially available. For example, polyclonal and monoclonal antibodies were obtained against CiLV-C and CiLV-C2 and used to detect these viruses in ELISA tests or in immunocapture reverse-transcription polymerase chain reaction (RT-PCR) tests (Calegario et al., 2013; Choudhary et al., 2013, 2014, 2017).

The most broadly used technique for the detection of leprosis viruses is RT-PCR. RT-PCR tests based on species-specific primers targeting different genomic regions of the viruses allow the detection of the leprosis viruses in infected plant tissues and also in viruliferous vectors (Locali et al., 2003; Roy et al., 2013a; Melzer et al., 2012, Olmedo-Velarde et al., 2021; Roy et al., 2020; Ramos-Gonzalez et al., 2017; Chabi-Jesus et al., 2018, 2021). RT-PCR-based tests for the simultaneous detection of several viruses causing leprosis have also been developed (Roy et al., 2017; Adducci et al., 2017). It should however be stressed that for the most recently described viruses, few isolates have been sequenced so that the primers designed on these sequences may not capture the whole diversity within these species and may therefore not be suitable to amplify all isolates. A very sensitive one-step real-time RT-PCR is also available for the detection of CiLV-C and allows diagnosis at early infection stages (Choudhary et al., 2015). A Taq-Man RT- real-time PCR test with high sensitivity has also been developed that may allow the quantification of CiLV-C in asymptomatic plants and also in B. yothersi individuals (Arena et al., 2023)

Finally, recent developments in high-throughput sequencing technology allow the detection of all viruses present in a sample, even in the absence of any prior knowledge of the virus(es) present (Olmos et al., 2018). While such approaches are not currently used as routine detection methods, their power for the identification and study of leprosis viruses has already been demonstrated (Padmanabhan et al., 2023).

Leprosis viruses only infect plants locally, each lesion being associated with an inoculation event by a vector mite. The viruses do not move systemically in host plants (Bastianel et al., 2010; Roy et al., 2015a). In the absence of Brevipalpus mite vectors, movement through latently infected plants for planting (which is a common pathway for most plant viruses) is unlikely for leprosis viruses. The same would apply to plants for planting of non-regulated rutaceous and non-rutaceous hosts (in particular for CiLV-C and CiLV-C2, known to naturally infect S. glutinosa, C. benghalensis and Dieffenbachia sp.) and also to fruits of susceptible citrus species as Brevipalpus spp. vector mites are known to be able to acquire the viruses from fruit lesions (Tassi et al., 2017). In practice, the main pathway for movement and dispersal, both locally from plant to plant or long distance between citrus growing areas is with the Brevipalpus vector mites. These colonize most Citrus spp. and many other plant species; according to Oliveira (1986), Brevipalpus mites have been found infesting more than 200 different plant species and several species (B. azores, B. californicus, B. yothersi) vectoring leprosis viruses are known to occur in some countries of the EPPO region.

On their own, Brevipalpus mites are slow moving and have limited dispersal abilities (Alves et al., 2005; EFSA, 2008). They can however be dispersed by wind or passively carried on on packaging, agricultural commodities (e.g. fruit), animals or humans (e.g. on their clothes) (Alves et al., 2005; Bassanezi & Laranjeira, 2007; Childers & Rodrigues, 2011).

Economic impact

While symptoms severity may vary depending on citrus species and, in some cases varieties (Bastianel et al., 2008), leprosis is considered a very important disease in affected areas (Bastianel et al., 2010; Roy et al., 2015a). As the leprosis viruses are not systemic, the number of lesions and thus the impact of the disease are directly linked to the size of mite vector populations. If proper mite control is not undertaken, severe losses in yield may occur, in both quantity and quality, in particular in sweet orange which is the most susceptible species. Fruits with lesions have low commercial value, especially for direct consumption. In severe disease cases, twigs may die, jeopardizing succeeding production while leaf drop will severely affect the tree canopy and result in dieback so that recovery following the adoption of vector control measures may take up to two years (EFSA, 2017). Furthermore, untreated orchards may serve as a source for the mite thus favouring spread of citrus leprosis to other plantations in the area (Bassanezi & Laranjeira, 2007).

Economic and environmental impacts also result from the need for vector control strategies that often rely on heavy use of acaricide sprays. In Brazil, it has been estimated to represent a significant portion of production costs, with 80-100 million USD invested annually in the early 2000s on vector control alone (Bastianel et al., 2010).

Control

Citrus leprosis is mainly controlled by controlling the Brevipalpus vector population using integrated pest management practices targeting the vectors, such as acaricide treatments or, potentially, the use of biological control agents (Argolo, 2020). Other practices that may contribute to control include cultural practices that decrease sources of inoculum and movement of mite vectors such as pruning infected plants (since leprosis viruses are not systemic), using wind break barriers to limit mites dispersal or eliminating alternative host plants. Although some citrus species are less susceptible, there are currently no resistant varieties available for important citrus host species.

Phytosanitary risk

Leprosis viruses can affect many citrus species which are important crops of the southern part of the EPPO region, in particular sweet orange. These viruses cause a severe disease with high economic and environmental impact. There are no known ecoclimatic constraints for leprosis viruses establishment, except those affecting their hosts; and some of the Brevipalpus vector species favouring the establishment and spread of the viruses have been reported in southern EPPO region countries with citrus production (EFSA, 2017). It was therefore considered justified by several EPPO countries to prevent establishment and spread of leprosis viruses.

The import of Citrus L. plants and their hybrids, other than fruits and seeds is regulated/prohibited in many EPPO countries which strongly reduces the risk of introduction of citrus leprosis via this pathway. For example in the EU, their import is prohibited from third countries, by Annex VI of Commission Implementing Regulation (EU) 2019/2072 (EU, 2023).

In other countries, appropriate phytosanitary measures to import plants for planting (excluding seeds and pollen) of citrus hosts that are free from leprosis viruses could require that these plants are produced in a pest free area or in a pest free place/site of production, or shown to be free from the various citrus leprosis viruses by appropriate diagnostic methods. In addition, specific measures targeting the Brevipalpus vector could be required (e.g. acaricide treatments).

Measures specifically addressing the risk with Brevipalpus vector mites on other plant material or as a contaminant would be needed, but the small size of these mites, the variety of commodities that could host viruliferous mites, and the fact some species are already present in some countries of the EPPO region, make the development of such measures complicated.

Addressing other identified pathways such as plants for planting of non-citrus rutaceous and non-rutaceous hosts or fruits of susceptible citrus species could also be considered.

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CABI and EFSA resources used when preparing this datasheet

Lázaro E, Vanaclocha P, Vicent A, Vives MC & Delbianco A (2023) Pest survey card on Citrus leprosis viruses. EFSA Supporting Publication EN-7804. https://doi.org/10.2903/sp.efsa.2023.EN-7804

CABI Datasheet on Citrus leprosis virus C (leprosis of citrus). CABI Compendium. https://doi.org/10.1079/cabicompendium.13449

CABI Datasheet on Citrus leprosis N Dichorhavirus. CABI Compendium. https://doi.org/10.1079/cabicompendium.88562658

This datasheet was extensively revised in 2024 Thierry Candresse (INRAE, France) and Francesco di Serio (CNR, Italy). Their valuable contribution is gratefully acknowledged.

EPPO (2024) Citrus leprosis disease. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-11-21)

This datasheet was first published in 1997 in the second edition of 'Quarantine Pests for Europe', and revised in 2024. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1997) Quarantine Pests for Europe (2^nd edition). CABI, Wallingford (GB).