Preferred name: Sadwavirus citri
Taxonomic position: Viruses and viroids: Riboviria: Orthornavirae: Pisuviricota: Pisoniviricetes: Picornavirales: Secoviridae: Sadwavirus
Other scientific names: Citrus mosaic virus, Natsudaidai dwarf virus, Navel orange infectious mottling virus, SDV, Satsuma dwarf nepovirus, Satsuma dwarf sadwavirus, Satsuma dwarf virus
Common names in English: Oleocellosis-like symptoms of Satsuma orange, Summer orange dwarf, dwarf disease of satsuma
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Notes on taxonomy and nomenclature EPPO Categorization: A2 list
EU Categorization: A1 Quarantine pest (Annex II A)
view more categorizations online...
EPPO Code: SDV000

The principal host is satsuma (Citrus unshiu), on which the symptoms have most commonly been observed. However, SDV may naturally infect a range of Citrus species in the family Rutaceae, generally inducing symptoms. Viburnum odoratissimum (China laurestine, sweet viburnum), a woody plant used as hedge in satsuma orchards in Japan, and Daphniphyllum teijsmannii, are the only two non-rutaceous natural hosts identified so far (Koizumi et al., 1988; Nakazono-Nagaoka et al., 2014) and are symptomless hosts. The virus has been experimentally transmitted by grafting to a very broad range of Citrus species and their hybrids (Miyakawa, 1969, Tanaka & Yamada, 1972; Iwanami et al., 1993) so that most Citrus species are considered as susceptible. It is thought that this will also be the case for related Rutaceae species (Fortunella spp., and Poncirus spp.) (Miyakawa, 1969; Tanaka, 1972; Iwanami et al., 1993a; Iwanami, 2010). Some susceptible Citrus (Citrus latifolia, C. medica, Citrus reticulata x C. paradisi cv. Orlando) may not develop obvious symptoms. Several non-Citrus rutaceous species were also found to be susceptible to SDV (Iwanami et al., 1993a; Miyakawa, 1969).

The literature is somewhat confusing, with sometimes contradictory reports, when it comes to herbaceous, non-rutaceous experimental hosts of SDV identified upon artificial mechanical inoculation. Causes for these discrepancies may include the use of different viral isolates, co-infection with other viral agents, the use of different varieties/genotypes of herbaceous hosts or differences in experimental inoculation conditions. In particular, SDV strains may vary in their experimental herbaceous host range, but most isolates are able to systemically infect Sesamum indicum and Physalis floridana (Iwanami et al., 1993a). The majority of these experimental hosts have been reported in the Fabaceae family, including Phaseolus vulgaris and Vigna unguiculata. Outside of this family, two Nicotiana species (N. clevelandii, N. tabacum), Chenopodium quinoa and Gomphrena globosa have been reported as hosts (Tanaka & Imada, 1974).

Host list: Citrus natsudaidai, Citrus tamurana, Citrus trifoliata, Citrus x aurantium var. sinensis, Citrus x aurantium var. unshiu, Citrus x tangelo, Daphniphyllum teijsmannii, Viburnum odoratissimum

Satsuma dwarf virus is present in China, Iran, Japan and the Korean peninsula. It has a restricted distribution in Turkey where it is presumed to have been introduced with budwood imported from the Far East (Onelge and Cınar, 2010). One report from Peru (IOCV website, 2017) has been retracted its author (Iwanami, 2010).

EPPO Region: Türkiye
Asia: China (Sichuan, Zhejiang), Iran, Japan (Honshu, Kyushu, Shikoku), Korea Dem. People's Republic, Korea, Republic

SDV is transmitted by grafting (Ushiyama, 1981), but also mechanically under artificial conditions (Tanaka & Imada, 1974; Usugi and Saito, 1979; Iwanami, 2010). Mechanical transmission does not seem to play a role in the natural spread of the virus (EFSA, 2017 and references therein). Field observations suggest that the disease is slowly transmitted from tree to tree, presumably through soil. Although no vector has been identified so far, involvement of fungi or nematodes cannot be excluded (EFSA, 2017). It is thought that V. odoratissimum and D. teijsmannii may act as a reservoir for infection (Koizumi et al.,1988; Nakazono-Nagaoka et al., 2014). Seed transmission, reported experimentally in Phaseolus vulgaris (kidney bean) (at a rate of 8.6%), was not observed in Citrus or in Sesamum indicum (white sesame) (EFSA, 2017 and references therein). Considering the natural spread pattern in the field, pollen transmission is considered unlikely (EFSA, 2017).

Symptoms

On Citrus, SDV typically causes dwarfing and small boat or spoon-shaped leaves. General symptoms are enations, multiple flushing, stunting or dwarfing, reduction in number and size of leaves and shoots, shortened internodes, and small-sized fruits with thick peel. Fruit production can be seriously reduced both in quality and yield (Iwanami and Koizumi, 2000).

The CiMV strain is characterized by the particular symptoms it causes on fruits. On satsumas, these are green blotches or ring-shaped spots on the rind at colour break and delayed colouring of the spotted area. Fruit symptoms also appear on lemons, but not typically on oranges, although fruit quality is reduced on this host. However, some isolates do not induce symptoms on fruits of satsuma (Iwanami et al., 1993a), while others have been associated with specific symptoms, i.e. CiMV with dapples on rinds of satsuma mandarin fruits, NDV with mottling and curling of new leaves of Citrus natsudaidai, NIMV with chlorotic spots on navel oranges, and HV with brown growth rings on hyuganatsu (Citrus tamurana). Severity of symptoms has also been correlated with low temperature environmental conditions (Kitajima et al., 1972).

Some host plants are known to be symptomless (e.g. V. odoratissimum and D. teijsmannii).

Morphology

SDV is an isometric virus approximately 26 nm in diameter, with particles containing two capsid proteins with a molecular weight of about 42 and 22-23 kilodaltons (Iwanami et al., 1993b). The virions encapsulate the two genomic RNAs (RNA1 and RNA2) of respectively about 7.0 kb and 5.4 kb. Both RNAs have a poly(A) sequence at their 3' end. For more information on characteristics of SDV, see Usugi and Saito (1977, 1979).

Detection and inspection methods

Visual inspection may allow the detection of symptoms but is not considered reliable enough since symptoms are not highly specific and are not always obvious in infected plants. 

White sesame is the best herbaceous indicator plant for detecting SDV through biological assays based on mechanical inoculation of homogenates from Citrus plants (EPPO, 1998; Tanaka et al., 1965). Blackeye cowpea, 'Satisfaction' kidney bean and Physalis floridana can also be effectively used as indicators (Tanaka and Kishi, 1963; Tanaka et al., 1965). Bioassays can also rely on graft inoculation of Citrus indicator seedlings [Citrus natsudaidai, citron (C. medica), sour lemon (C. limon), Dweet tangor, mandarin (C. reticulata) or satsuma (C. unshiu)] (EPPO, 1998) however the possible interference of citrus tristeza virus, if present in the plants to be tested, must be considered (Roistacher, 2004). SDV, including the CiMV strain, can be detected by ELISA using polyclonal antibodies produced against SDV and extracts from young tender leaves from the spring flush (Usugi & Tsuchizaki, 1982; Koizuimi et al., 1988). ELISA is extremely helpful in large-scale detection. However, it should not be used as the only method for the testing of mother trees because it sometimes gives false negative results, in particular with some strains of SDV. ELISA can be used in conjunction with mechanical transmission to white sesame or with other method(s) to ensure that important budwood or mother trees are free from SDV. ELISA with monoclonal antibodies can be used to distinguish the CiMV strain from other SDV strains (Nozu et al., 1986). Reliable molecular tests, based on reverse-transcriptase polymerase chain reaction (RT-PCR) (Iwamani, 2010), multiplex RT-PCR (Hyun et al., 2017), QuantiGene Plex-Luminex-based test (Dang et al., 2016) are available to detect SDV alone or in mixed infections.

Movement and trade of contaminated propagation materials is considered the most significant mode of spread since SDV is readily transmitted by grafting. SDV may also move locally, probably through soil with the possible contribution of unidentified vector(s) (Isoda & Gyoutoku, 1990). In international trade, SDV is most likely to be carried in infected propagation material, but soil should also be considered as a potential pathway.

Economic impact

Trees of satsuma mandarin infected by SDV are generally stunted, with reduced yield. Fruits on trees severely affected by the CiMV strain are of poor quality and low commercial value. Detailed data on yield losses caused by SDV are not available. However, a field infection rate of 31% has been reported in Turkey (Çınar and Önelge, 2010), showing the potential for severe impact on satsuma mandarin and some other Citrus cultivations. 

Control

The most efficient control strategy appears to be the development and use of SDV-free propagation material, as described in EPPO Standard PM 4/12 Pathogen-tested citrus trees and rootstocks (EPPO, 1998). No control measures are known in the field, besides the destruction of infected plants. Though field observation suggests the transmission of SDV through soil, soil fumigation is not effective to control disease progression in Citrus groves (Isoda et al., 1991).

Phytosanitary risk

The virus typically infects and has its main impact in satsumas (C. unshiu) compared to other Citrus. Satsumas are not widely grown in the EPPO region. In Turkey, where satsumas are grown in the Aegean region, the virus has only been reported on this species and does not appear to have spread to other Citrus species, or to other regions of Turkey, or elsewhere in the EPPO region. Even if no vector is known, SDV natural infection has already been reported from other Citrus species elsewhere in the world, in particular for CiMV, NIMV, NDV and HV; most Citrus species have been experimentally shown to be susceptible. There are no ecoclimatic constraints for SDV affecting establishment, except those affecting its hosts; and Citrus cultivation occurs widely in the Mediterranean part of Europe (EFSA, 2017). It was therefore considered justified by EPPO to prevent further spread of SDV and, in particular, introduction of new strains from the Far East.

Appropriate phytosanitary measures to import plants for planting (excluding seeds and pollen) of Citrus, other rutaceous hosts, as well as the natural non rutaceous hosts of SDV into the EPPO region could require that these plants are produced in a pest free area, in a pest free place/site of production (e.g. established according to EPPO Standard PM 5/8 Guidelines on the phytosanitary measure ‘Plants grown under physical isolation’ (EPPO, 2016)), or shown to be free from SDV by appropriate diagnostic methods. A number of EPPO countries already ban the import of Citrus, Fortunella, Poncirus and their hybrids (other than fruits and seeds) (EU, 2019).

SDV already occurs in the EPPO region (i.e. in Turkey). So, within the EPPO region, Citrus planting material should be certified free from SDV (EPPO, 2018).

Ahlawat YS, Chenulu VV, Viswanath SM, Pandey PK & Bhagabati KN (1985) Mosaic disease of citrus in India. Current Science, India 54, 873-874.

Çınar A & Önelge N (2010) Virus and virus-like diseases in turkey citriculture. In Proc. 20 th Conf. IOCV. IOCV, Riverside (CA). pp. 233–236. https://escholarship.org/uc/item/0bn1239x [accessed on 30 March 2022].

Dakshinamurti V & Reddy GS (1975) Mosaic - a transmissible disorder of sweet oranges. Indian Phytopathology 28, 398-399.

Dang T, Ramirez B, Osman F, Bodahi S & Vidalakis G (2016) QuantiGene Plex: A non-PCR, high throughput, multiplex detection assay for citrus pathogens. Abstract of the 20th Conference of the International Organization of Citrus Virologists, Chongqing (CN) https://escholarship.org/uc/item/12c1x3hz [accessed on 30 March 2022].

EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Jaques Miret JA, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Chatzivassiliou E, Winter S, Catara A, Duran-Vila N, Hollo G & Candresse T (2017) Scientific Opinion on the pest categorization of Satsuma dwarf virus. EFSA Journal 15(10), 20 pp. https://doi.org/10.2903/j.efsa.201d7.5032 [accessed on 30 March 2022].

EPPO (1998) Certification schemes. EPPO Standard PM4/12(1) Pathogen-tested citrus trees and rootstocks. EPPO Bulletin (1995) 25, 737-755. Edited as an EPPO Standard in 1998. Available at https://gd.eppo.int/download/standard/91/pm4-012-1-en.pdf [accessed on 30 March 2022].

EPPO (2016) EPPO Standard PM 5/8 Guidelines on the phytosanitary measure ‘Plants grown under complete physical isolation’. EPPO Bulletin 46, 421-423. Available at https://gd.eppo.int/standards/PM5/ [accessed on 30 March 2022].

EU (2019) Commission implementing regulation (EU) 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. Official Journal of the European Union, L 319, 1-279.

Hyun JW, Hwang RY & Jung KE (2017) Development of multiplex PCR for simultaneous detection of citrus viruses and the incidence of citrus viral diseases in late-maturity citrus trees in Jeju Island. The Plant Pathology Journal 33, 307.

Isoda T & Gyoutoku Y (1990) Studies on citrus virus diseases. VII. Propagation of satsuma dwarf virus to adjacent trees in a citrus orchard. Proceedings of the Association for Plant Protection of Kyushu 36, 64-67.

Isoda T, Gyoutoku Y & Yamada K (1991) Studies on citrus virus diseases. VIII. Post-measure of orchard attacked by satsuma dwarf virus. Proceedings of the Association for Plant Protection of Kyushu 37, 55-58.

Ito T, Iwanami T, Ieki H, Shimomura K, Shimizu S & Ito T (2004) A new virus related to Satsuma dwarf virus: nucleotide sequence of the 3’-terminal regions of Hyuganatsu virus RNAs 1 and 2. Archives of Virology 149 1459–1465.

Iwanami T & Ieki H (1996) Nucleotide sequence of the coat protein genes of citrus mosaic virus. Virus research 42(1-2), 181-186.

Iwanami T & Koizumi M (2000) Satsuma dwarf virus group. In Compendium of Citrus Diseases (eds Timmer LV, Gansey SM & Graham JH), pp. 59. APS, St. Paul, MN (US).

Iwanami T (2010) Properties and control of Satsuma dwarf virus. Japan Agricultural Research Quarterly: JARQ 44, 1–6.

Iwanami T, Koizumi M & Ieki H (1993b) Diversity of properties among satsuma dwarf virus and related viruses. Annals of the Phytopathological Society of Japan 59, 642-650.

Iwanami T, Kondo Y & Karasev AV (1999) Nucleotide sequences and taxonomy of satsuma dwarf virus. Journal of General Virology 80(3), 793-797.

Iwanami T, Kondo Y, Makita Y, Azeyanagi C & Ieki H (1998) The nucleotide sequence of the coat protein genes of satsuma dwarf virus and navel orange infectious mottling virus. Archives of virology 143(2), 405-412.

Iwanami T, Omura M & Ieki H (1993a) Susceptibility of several citrus relatives to Satsuma dwarf virus. In Proc. 12th IOCV (eds Moreno P, da Graca JV & Timmer LW), pp. 352–356, IOCV, Riverside (CA).

Kitajima H, Tanaka H, Yamada S & Kishi K (1972) Influence of temperature on the development of leaf symptoms of satsuma dwarf disease, pp. 76–79, IOCV Proceedings.

Koizumi M, Kano T, Ieki H & Mae H (1988) China laurestine: a symptomless carrier of Satsuma dwarf virus which accelerates natural transmission in fields. In Proc. 10th IOCV (eds Timmer LW, Garnsey SM & Navarro L), pp. 348–352, IOCV, Riverside (CA).

Le Gall O, Sanfaçon H, Ikegami M, Jones T, Karasev A, Lehto K, Wellink J, Wetzel T & Yoshikawa N (2007) Cheravirus and Sadwavirus: two unassigned genera of plant positive-sense single-stranded RNA viruses formerly considered atypical members of the genus Nepovirus (family Comoviridae). Archives of Virology 152, 1767–1774.

Miyakawa T (1969) Susceptibility of Citrus spp. and the other related plants to the Satsuma Dwarf Virus (SDV). Japanese Journal of Phytopathology 35, 224–233.

Nakazono-Nagaoka E, Takemoto S, Fujikawa T, Nakajima K, Uenishi H & Iwanami T (2014) Natural Satsuma dwarf virus infection of two woody plants, Daphniphyllum teijsmannii Zoll. ex Kurz. and Viburnum odoratissimum Ker-Gaul. var. awabuki (K. Koch) Zabel near Citrus Fields. Japan Agricultural Research Quarterly: JARQ 48, 419–424.

Nozu Y, Usugi T & Nishimori K (1986) Production of monoclonal antibodies to satsuma dwarf virus. Annals of the Phytopathological Society of Japan 52, 86-89.

Pant RP & Ahlawat YS (1997) Partial characterisation of citrus mosaic virus. Indian Phytopathology 50(4), 557-564.

Roistacher CN (2004) Diagnosis and management of virus and virus like diseases of citrus. In Diseases of Fruits and Vegetables Volume I, pp. 109–189, Springer (NL).

Tanaka S & Kishi K (1963) Studies on indicator plants for citrus viruses. Mechanical inoculation on leguminous plants with sap from satsuma dwarf tree. Annals of the Phytopathological Society of Japan 28, 262–269.

Tanaka S, Kishi K & Yamada A (1965) Research on the Indicator Plants of Satsuma dwarf and Hassaku dwarf viruses. Proceedings of the IOCV 3(3), 260-267.

Tanaka H (1972) Mechanical transmission of viruses of satsuma dwarf and natsudaidai dwarf from citrus to citrus. Annals of the Phytopathological Society of Japan 38, 156-160.

Tanaka H & Imada J (1974) Mechanical transmission of viruses of satsuma dwarf, citrus mosaic, navel infectious mottling and natsudaidai dwarf to herbaceous plants. In Proceedings of the 6th Conference of the International Organization of Citrus Virologists (eds Weathers & LG Cohen M), pp. 141-145. University of California, Riverside (USA).

Ushiyama K (1981) Studies on satsuma dwarf disease. II. Spread of the disease by topworking satsuma trees with infected scions. Bulletin of the Kanagawa Horticultural Experiment Station 28, 24-30.

Usugi T & Saito Y (1977) Some properties of satsuma dwarf virus. Annals of the Phytopathological Society of Japan 43, 137-144.

Usugi T & Saito Y (1979) Citrus mosaic virus. CMI/AAB Descriptions of Plant Viruses No. 208. Association of Applied Biologists, Wellesbourne (UK).

Usugi T & Tsuchizaki T (1982) Detection of citrus mosaic virus by enzyme-linked immunosorbent assay. Annals of the Phytopathological Society of Japan 48, 330-332.

This datasheet was updated in 2022 by Drs Francesco di Serio and Thierry Candresse. Their valuable contribution is gratefully acknowledged.

EPPO (2024) Sadwavirus citri. 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 2022. 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).