The Virus Disease Situation of Citrus in Cyprus—A Brief Review
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Fifteenth IOCV Conference, 2002—Short Communications The Virus Disease Situation of Citrus in Cyprus—A Brief Review A. Kyriakou, Th. Kapari-Isaia, and N. Ioannou ABSTRACT. Virus and virus-like diseases of citrus in Cyprus are related to the history of cit- rus on the island. Citron, lemon and sour orange were introduced to the island before the 14th century, whereas mandarin and orange were introduced in the 19th century. There are indications that all of the above citrus species came from neighboring countries of the Asian Continent. In the first half of the 20th century several citrus varieties were introduced from South Africa and Israel. In the last 50 yr, virus-free material of several varieties was introduced from California. As a result, citrus grown in Cyprus is affected by the same virus and virus-like diseases which affect citrus in neighboring countries, and by Citrus tristeza virus (CTV) which was most probably intro- duced with the South African material. The main virus and virus-like diseases of citrus identified so far on the island are: CTV, Citrus psorosis virus (CPsV), Citrus variegation virus (CVV), citrus impietratura, stubborn, Citrus exocortis viroid (CEVd), Citrus cachexia viroid (CCaVd) and three other citrus viroids with 284, 305 and 318 nucleotides, respectively. After CTV was detected on the island, a program was initiated for the control of the disease through systematic surveys, uproot- ing of infected trees against compensation to the growers, and production and distribution of virus-free material. Survey results from 744 groves with 406,500 trees from five districts showed a CTV incidence of 4.5% and a disease prevalence of 22%. Nearly all infected trees in four of the five districts were eradicated. In the fifth district, however, CTV infection was high (18.3%) and eradication was not considered feasible. In addition to CTV control, the CTV Program has in gen- eral benefited citriculture in Cyprus as it paved the way for the establishment of a Citrus Certifi- cation Program. The virus disease situation of cit- derived respectively from the San- rus in an area is often associated skrit “Nagrunga” and the Arabic with the history of citrus cultiva- “Leimun”. However, in the Greek tion. For this reason an account of Cypriot dialect, sour orange is called the history of citrus on the island “Kitromilia” (citron apple tree), indi- will be briefly outlined. All informa- cating that citron was already tion for citrus in Cyprus before the present, and lemon is “Oxinia” (from 1930s has been derived from Genna- “oxino” = acidic). Products and dius’ Botanical Dictionary (4). byproducts of these two fruits have The actual time of introduction of been traditionally used in several citrus in Cyprus is not well known, ways in cookery and confectionery. but from early accounts of the pres- Mandarins and oranges were intro- ence of citrus in the Eastern Mediter- duced much later in the second half ranean region, it is gathered that of the 19th century. The local manda- citron was present in Cyprus not rin and Jaffa orange were among the later than the first century A.D, and earliest introductions. In the 1930s was probably introduced as early as citrus budwood of several varieties, the second century B.C. Sour orange, including Marsh seedless grapefruit, which is the main rootstock used on Valencia and Washington Navel, the island to the present, and lemon, were introduced from South Africa. were introduced later, most probably In 1939 Valencias were introduced from Palestine, before the 14th cen- from Israel. In the 1960s nucellar tury. There is a historical account of virus-free material of several variet- the presence of a garden of sour ies was introduced from Willits & orange trees in 1468. It is worth not- Newcomb Inc., California, and in the ing that in Greece, sour orange and 1980s virus-free material of red-flesh lemon are known by the universal grapefruit and Ortanique was intro- names “Naranja” (Greek “Neranja”) duced from California and Florida. and Lemon (Greek “Lemonia”), In the last decade several varieties 427 428 Fifteenth IOCV Conference, 2002—Short Communications were introduced from California and depending on the time of year that Spain. Citrus, which originated from graft-inoculation was performed. material present on the island before Symptoms usually appeared in the 1960s, will be here designated as spring and autumn during one to ‘old-line’. two weeks and they disappeared to The first plant pathologist to work reappear on the new growth the fol- on virus diseases of citrus in Cyprus lowing spring and/or autumn. Iso- was Dr. A. Papasolomontos in the lates from the above trees reacted 1960s, who, by field symptomatology positively in ELISA tests using anti- and biological indexing, noted several sera provided by Prof. R. G. Milne, virus and virus-like diseases, includ- University of Turin, Italy (Rabbit ing psorosis, impietratura, stubborn polyclonal A322 for trapping the and tristeza. (9, 10, and pers.comm.). virus and monoclonal 13C5 for Economides (2) reported the first detection), and using the protocol for record of exocortis on old-line Marsh TAS ELISA described by Alioto et al. seedless grapefruit. (1). Positive response was obtained The present report, however, will with eight samples from the field focus on the findings of a survey for and three samples from the glass- virus and virus-like diseases which house, all with symptoms. has been conducted by the Agricul- Variegation. Variegation symp- tural Research Institute since 1986. toms have been observed on several This survey was made in the context trees of Jaffa and Valencia orange of a program for the production and and also on the local Lapithou distribution of clean citrus material. lemon, but repeated attempts to The main method used was the con- transmit the symptoms to indicators ventional biological indexing tech- of Citrus variegation virus (CVV), nique by the use of plant indicators including Eureka lemon and Etrog which were imported either from citron, were unsuccessful. Two iso- Willits & Newcomb or from the Uni- lates from Ortanique, however, with versity of California, Riverside. severe variegation symptoms (87- Indexing was performed in a glass- 127 and 87-128), which consisted of house with temperatures 16-33°C. tree stunting, leaf distortion and Other techniques have also been fruit reduction and malformation, used and these will be reported were transmitted by grafting and where appropriate here below. Mea- caused variegation symptoms to sures which have been taken for the Eureka lemon, Etrog citron and control of some of these diseases will Ortanique. They also caused varie- be also outlined. gation symptoms in several other The main diseases which have plant indicators, including Madam been diagnosed since 1986 are the Vinous and Pineapple sweet orange, following: Mexican lime, Citrus excelsa, Rough Citrus Psorosis. Classical pso- lemon and Ortanique. They were rosis symptoms of bark scaling have also transmitted mechanically to been noticed in the field on several Petunia hybrida and Eureka lemon trees of old-line Valencia and Jaffa and from this plant they were trans- orange, Marsh seedless grapefruit mitted by grafting back to Orta- and Clementine. Samples from 15 nique, thus confirming Koch’s Valencia, 11 Jaffa, four grapefruit postulates and indicating the and five Clementine trees, respec- involvement of an infectious and tively, were indexed in the glass- transmissible agent, which may be house on seedlings of Madam Vinous CVV. However, when all above and/or Pineapple sweet orange, and infected plants were tested three Dweet tangor. Characteristic symp- times by ELISA, using antibodies toms appeared on all the indicators 6 against CVV provided by Unité de weeks to 6 mo post-inoculation, Controle des Plants, Direction de Fifteenth IOCV Conference, 2002—Short Communications 429 Domaines Agricoles of Morocco, symptoms in the field, as over 95% of there was no reaction. It is possible citrus trees are on sour orange root- that the Cypriot isolates of CVV are stock which is tolerant to viroids. different from the Moroccan isolates. Cachexia. This disease has been Impietratura. This disease was observed mainly on old-line Clemen- first reported by Papasolomontos tines, but also on some local manda- (12) and affects some old-line grape- rins and on Ortanique. Trees of fruit plantings, but was also found these varieties with the characteris- in some Jaffa, Valencia and acidless tic field symptoms have indexed oranges. Usual symptoms consist of positive for cachexia on Parson’s gumming of the fruit albedo, hard- special mandarin budded on Rough ening of the fruit and reduction of lemon or Volkamer lemon. In 1994 fruit size. It has been observed that cachexia viroid was also identified symptoms of impietratura are more by electrophoresis and was found serious on young trees, and that present in the local lemon and in symptoms on trees over 12-yr old Valencia and Jaffa oranges. are less conspicuous and inconsis- Stubborn. The disease has been tent from year to year. However, two noted in Cyprus since 1956 by isolates of the disease from Valencia Economides (pers. comm.), but was caused consistently severe fruit known to growers even earlier with symptoms and intense psorosis-like the local name “psintrophyllia” (=lit- symptoms on leaves of sweet orange tle leaf). The causal agent of stub- in the field and the glasshouse. The born, Spiroplasma citri, was problem needs further investigation. isolated in culture from Valencia Citrus Exocortis and Related and Washington navel orange trees Viroids. Exocortis disease was first with typical disease symptoms in reported in Cyprus by Economides 1987 (Bové, Saillard, Foss and Kyri- (2) during a scion-rootstock trial, in akou, unpublished data). which old-line Marsh seedless grape- A study conducted at the experi- fruit was budded on Morton and mental station of the Agricultural Troyer citrange.