The third edition of our blog series Plant virus snapshots focuses on a plant virus from the Closteroviridae virus family, the Tomato chlorosis virus (ToCV). The Tomato chlorosis virus is one of two criniviruses that are transmitted by whiteflies.
What is the Tomato chlorosis virus?
ToCV is a crinivirus found worldwide, but that is especially present in the countries of the Mediterranean basin. 85 plant species belonging to 25 botanical families are natural hosts for the virus. The crinivirus ToCV was first detected in 1989 in greenhouse-grown tomato plants showing a ‘yellow leaf disorder’ syndrome in the US state of Florida. Soon after its identification in the USA, VIRTIGATION researcher Jesús-Navas Castillo from partner CSIC was part of a team of researchers detecting the virus in Spain in 1997. Considering its name, it could be assumed that ToCV only infects tomatoes, but this is actually not the case. This plant virus infects a wide range of cucurbits (e.g. pumpkin) and other vegetables (e.g. eggplant, lettuce, potato or sweet pepper), as well as ornamental crops, weeds and wild plants. Thanks to its whitefly vector (e.g. Bemisia tabaci), this emerging plant virus has spread rapidly around the globe, affecting at least 39 countries and territories. But unlike some other viruses (e.g. tobamoviruses), ToCV cannot be spread by means of mechanical transmission, such as crop working methods or human contact.
Virus structure
The Tomato chlorosis virus is a typical crinivirus, with a bipartite genome of positive-sense single-stranded RNA encapisdated in flexuous virions of 800-850 nm. The ToCV genome consists of two molecules (RNA1 and RNA2). RNA1 and RNA2 contain four and nine open reading frames (ORFs), respectively. RNA1 encodes proteins associated with virus replication and suppression of gene silencing, while RNA2 encodes proteins putatively involved in virus encapsidation, whitefly transmission, membrane association, cell-to-cell movement and the suppression of gene silencing. Both RNAs are needed for infectivity. Although no formal description of strains has been reported by scientists investigating the ToCV virus structure, ToCV isolates are phylogenetically grouped into several supported clusters. Certain genetic differentiation could be related to the host from which ToCV isolates were obtained, which are mainly tomato or pepper plants.
Transmission
ToCV is semi-persistently transmitted by whiteflies of the genera Bemisia. To date, scientists, including VIRTIGATION CSIC investigators Jesús Navas-Castillo and Elvira Fiallo-Olivé, confirmed transmission for MED, MEAM1 and New World of the Bemisia tabaci complex of cryptic species, as well as Trialeurodes (Trialeurodes vaporariorum and Trialeurodes abutiloneus). The transmission efficiency differs among whitefly species, with Bemisia tabaci MED being the most efficient at transmitting ToCV. Researchers also found that the virus can be transmitted by grafting between tomato plants, and from experimentally infected Nicotiana benthamiana (i.e. a close relative of tobacco) plants to tomato. In international trade, ToCV may be carried by infected plants for planting. The high number of natural plant hosts and ready transmission by several whitefly species have facilitatd the emergence of ToCV worldwide. Viruliferous whiteflies could be carried long distances on plants of hosts or non-hosts.
Symptoms
The symptoms of ToCV are similar to those of Tomato infectious chlorosis virus (TICV), another crinivirus. Growers can recognise ToCV by yellowing between the veins of old leaves. About four weeks after infection, the first symptoms appear; the old leaf curls around and feels brittle. Symptoms are often similar to a deficiency disease such as magnesium or nitrogen deficiency. Yellow discoloration in the leaf is characteristic, and is easy to distinguish from the green areas. In later stages of this disease, the leaves develop a chlorotic bronze color. Tomato plants infected by ToCV show an irregular chlorotic mottle that develops first on lower leaves and gradually advances toward the growing point. Interveinal yellow areas on leaves also develop red and brown necrotic flecks. No obvious symptoms develop on tomato fruit and flowers, but ToCV decreases fruit size and numbers due to a loss of photosynthetic area. Significant yield losses occur as a result. Other symptoms include rolling of lower leaves and thickened crispy leaves, while the upper leaf canopy appears normal.
Virus management and control
To date, there are no commercial cultivars of tomato or other host plants resistant or tolerant to ToCV. However, scientists have identified wild tomato materials that react with mild symptoms and/or low viral titers following natural or experimental inoculation with ToCV. Once a plant is infected with a virus like ToCV there is no cure. Therefore, growers should take measures to eradicate sources of inoculum and eliminate the presence of vectors to minimise the risk of further transmission. Hence, control of the whitefly vectors is quintessential to managing and controlling ToCV. These control methods have proven to be efficient in keeping ToCV in check:
- Keep tomato seedlings for transplanting free from infection;
- Eradicate isolated outbreaks in greenhouse-grown tomatoes by destruction of affected hosts and of the vector(s). However, eradication is unlikely for outbreaks in the field in southern Europe;
- Use high-quality greenhouse and nethouse covers to effectively exclude whiteflies;
- Remove weeds surrounding crops, as those may act as reservoirs for ToCV;
- Discard virus infected plants;
- Use predators such as the beetle Delphastus pusillus against the Bemisia tabaci whiteflies;
- Roguing of severely infested plants reduces whitefly populations;
- Finally, employ ToCV-adapted conventional RT-PCR and real-time RT-PCR to detect and identify virus infection;
Current status of Tomato chlorosis virus
ToCV still remains a serious issue for tomato production across the globe. This plant virus can reach up to 100% infection in greenhouses in Southern European countries like Spain (including the Canary Islands) and Italy, thereby causing significant reduction in yield and quality. While there are no exact estimates of yield losses for ToCV, growers worldwide reported severe yield losses due to reduced fruit growth and delayed ripening. he severity of symptoms and damage vary according to the cultivar. VIRTIGATION CSIC researchers Jesús Navas-Castillo and Elvira Fiallo-Olivé also observed synergism in a mixed virus infection of ToCV with Tomato spotted wilt virus (TSWV) synergism, which led to the rapid death of affected plants. In conclusion, the EPPO has recently assessed that ToCV continues to present a significant phytosanitary risk for further spread in the EPPO region, including in Northern Europe and Africa, where the climatic conditions were initially not thought to be conducive to the effective transmission of the virus by its whitefly vectors.
