**8. Virus diseases on strawberry plants**

Over 30 viruses and virus-like diseases distressing the genus, Fragaria has been reported. Some of these viruses have different races within themselves. Strawberry varieties can cause symptoms of different severity for each race, or these disease

### *Pests, Diseases, Nematodes, and Weeds Management on Strawberries DOI: http://dx.doi.org/10.5772/intechopen.103925*

agents can be found asymptomatically in plants. While many viruses do not show obvious symptoms in commercial strawberry cultivars, frequently observed symptoms can be observed as plant stunting, crop and yield loss, and dieback. The viruses seen in strawberries can be found in mixed infections, causing reductions in yield and fruit quality, thereby reducing the market value of the product. The most reliable method used to detect the presence of strawberry viruses is the classical molecular and biological method. It is the use of classical clone grafting, aphid transport, and PCR methods on indicator plants of *F. vesca* and *F. virginiana* clones. However, since symptom outputs take 14–21 days in this method, the use of indexing after less time-consuming and reliable methods such as Enzyme-Linked Immunosorbent Assay (ELISA) and Polymerase Chain Reaction-Polymerase Chain Reaction (PCR) helps to obtain more reliable results [127, 128]. Strawberry viruses can be transmitted by aphids, nematodes, and some other vectors, while aphids are the most important vectors. Strawberry aphids known to infect the plants by being carried by *Chaetosiphon fragaefolii* viruses are [129] *Strawberry crinkle cytorhabdovirus* (ScRV), *Strawberry mottle virus* (SMoV), *Tomato ringspot virus* (ToRSV), *Strawberry vein banding virus* (SVBV), *Strawberry pseudo mild yellow edge virus* (SPMYEV), *Raspberry ringspot virus* (RpRSV), *Arabis mosaic virus* (ArMV), *Strawberry latent ringspot virus* (SLRSV), *Strawberry latent C virus* (STLCV), *Tomato black ring virus* (TBRV), and *Strawberry mild yellow edge virus* (SMYEV), which are known to infect the plant by being transmitted by some nematode species, and whiteflies [127, 130–132]. Among the aphid-borne viruses, SCrV, SMOV, SVBV, and SMYEV are the utmost significant viral diseases observed in strawberry production areas [133–135].

*Strawberry crinkle cytorhabdovirus* (ScRV); The family Rhabdoviridae is included in the genus Cytorhabdovirus. They are positive-sense ssRNA viruses [136]. *Strawberry latent virus*, strains A (mild form), and B and *Strawberry vein chlorosis virus* are synonyms. It is one of the most harmful strawberry viruses worldwide. Severe strains in susceptible varieties cause leaflets to be uneven in size, distorted and wrinkled, resulting in the formation of small irregularly shaped chlorotic spots on the veins. It is on the EPPO quarantine list. The presence of the agent has been reported in Asia, Africa, America, Oceania, and many European Union member countries [132, 137].

SCrV has a limited host variety within the Fragaria species. In addition to cultivated strawberries such as *F. x ananassa*, its presence has also been determined in wild species such as *F. vesca*, *F. virginiana,* and *F. chiloensis* [138]. Nicotiana glutinosa has been reported as experimentally transduced hosts in *Physalis floridana* [139]. SCrV is locally transmitted by the strawberry aphid *Chaetosiphon fragaefolii*. It has been reported that the shoot tip meristem culture method, following the application of temperature (38°C) in obtaining SCrV-free plants, increases the percentage of success in obtaining a virus-free plant [140].

*Strawberry mottle virus* (SMoV), *Strawberry mottle virus* (SMoV) from the Secoviridae family, is also called *Strawberry mottle sadwavirus*. The presence of the agent has been reported in Asia, America, Oceania, and many European Union member countries. It is one of the most common viruses in many areas of strawberry cultivation in the world. There are many breeds of SMoV; weak breeds are observed as asymptomatic, while strong breeds can cause yield losses of up to 30% Strawberry aphid, *Chaetosiphon fragaefolii*, is the main vector for SMoV, while *Chaetosiphon jacobi* and *C. minor* can also transmit the virus; *C. gossypii* can also carry SMoV. The transport of SMoV occurs semi-persistently within a few minutes during the feeding period [141]. *Fragaria vesca* and *F. virginiana* clones show symptoms at different rates after inoculation with inoculation due to their sensitivity to the agent. While symptom development is observed in *F. vesca* 7–10 days after infection, this period might be lengthier in mild and moderate breeds. In indicator plants, the symptoms are barely noticeable on the leaves, or the leaves may be slightly mottled, severely stunted, and deformations leading to plant death can be observed. In the control of the agent, the use of certified virus-free plants, the fight against aphids, the isolation of infected production areas is important. Since SMoV is one of the most sensitive to temperature among strawberry viruses, it is possible to obtain virus-free plants with the combination of thermotherapy and meristem culture. It has been reported that 2–3 weeks of thermotherapy is sufficient to obtain SMoV-free plants [127].

*Strawberry vein banding caulimovirus* (SVBV); the virus exists merely in Fragaria spp. Its chief host *is Fragaria vesca*. It can also infect commercial strawberry cultivars, but symptoms are commonly merely seeming when strawberry exists at the same time as the latent *C 'rhabdovirus'* [137]. The agent exists in some countries in Asia, Europe, America and Oceania, and *M. persicae, Macrosiphum rosae, Amphorophora rubi*, *Chaetosiphon fragaefolii, Aulacorthum solani, C. tetrarhodum, C. thomasi, C. jacobi, A. rubifolii, M. ornatus, Aphis idaei*, *Acyrthosiphon pelargonii* have been reported to be vectors of the agent. The most effective vector of these species is *Chaetosiphon* spp. While the virus can be transmitted to indicator plants by inoculation and *Cuscuta subinclusa*, it cannot be transmitted mechanically. Depending on the indicator plant, contamination occurs within 2–5 weeks. Symptoms appear as epinastie on the midrib and petiole on the youngest leaf. Some or all the affected leaves show varying lengths of yellowish vein banding along the main vein. The second and third leaves formed after the commencement of symptoms show more severe symptoms. In the diagnosis of the agent, the UC-12 clone of *F. vesca* and the UC-12 clone of *F. virginiana* are used as the most effective indicators for detecting SVBV. In routine serological testing, the agent is diagnosed using an antiserum specific for SVBV [129].

*Strawberry latent C 'rhabdovirus'* (STLCV); The agent reported to be in the Rhabdoviridae family has not been defined morphologically. Its presence has been reported in America and Canada [137]. While the agent is usually asymptomatic in cultivated strawberries, in case of mixed infection with other viruses, it can cause moderate to severe leaf deformation such as excessive stunting, curling of leaves, or severe symptoms observed in other viruses with weakening of the plant. In some indicator clones of STLCV *F. vesca*, it can cause severe epinasty and shrinkage in newly formed leaves and petioles, while mild and transient symptoms are observed in other clones. Determination of the presence of the agent can be accomplished by inoculating the agent into clones of *F. vesca* or *F. virginiana* [129]. It has been reported that in the USA, no other virus component in a complex form cause severe stunting in a short time as this factor in cultured strawberries [142].

Strawberry mild yellow edge disease: It has been determined to be caused by a virus complex called *Strawberry mild yellow edge luteovirus* (race or syn; *Soybean dwarf luteovirus*) and *Strawberry mild yellow edge-associated potexvirus* [143]. By itself, it is not the principal pest for most cultivars, but solitary infection rarely occurs. The agent is only Fragaria spp. There are types. While some clones of wild species *F. chiloensis, F. vesca,* and *F. virginiana* show symptoms in nature, *F. ovalis* can carry the agent without symptoms. Many strawberry cultivars are also asymptomatic carriers of the agent. It has been reported that the so-*called Strawberry mild yellow edge-associated 'potexvirus*' virus was experimentally transferred to *Chenopodium murale* and *C. quinoa* but did not remain in the plants for a long time [144].

#### *Pests, Diseases, Nematodes, and Weeds Management on Strawberries DOI: http://dx.doi.org/10.5772/intechopen.103925*

This disease can be seen in many countries where the strawberry plant is grown. These are Australia, Europe, Israel, Japan, South Africa, and Northwest America. There are different views on economic losses due to the existence of different strains of the virus. However, because of many studies, it has been reported that product loss is between 0 and 30%. It is asymptomatic in cultivated strawberry cultivars [145]. In natural conditions, these two viruses in strawberries have been reported to be spread by the strawberry aphid *Chaetosiphon fragaefolii*. The spread of the disease can also occur with vectors or material spread from tissue culture. There is no information about propagation by seed. It has been reported that the complex of the disease with other pathogens such as *Strawberry crinkle rhabdovirus, Strawberry veinbanding caulimovirus*, *Strawberry mottle agent* [137] can cause serious losses in plant growth, fruit quality, and yield [145]. The control of the virus can be achieved with the use of thermotherapy or meristem culture and certified virus-free production material. Control of vectors is also an important factor in the prevention of disease agents [127, 145].

Viruses Carried by Nematodes; *Arabis mosaic nepovirus* (ArMV); the agent in the Nepovirus genus of the Comoviridae family is also called *Raspberry yellow dwarf virus.* ArMV is an RNA virus with a wide host range. The presence of the agent has been reported in Asia, Africa, America, Oceania, and many European Union member countries [146, 147]. ArMV is an RNA virus with a wide host range. It was observed that 93 species from 28 different families were infected by mechanical inoculation [148]. The main hosts are strawberry, hops, raspberry (*Rubus idaeus*), *Sambucus nigra, Rheum* spp., and *Vitis* spp. The virus has also been reported in sugar beet, celery, gladiolus, horseradish, and lettuce. Several further wild and cultivated species are reported as hosts. ArMV is transmitted by seed by nematodes over short distances [149]. *Xiphinema diversicaudatum* was suspected to carry hop strains of ArMV [150].

In the diagnosis of the agent, some indicator plants are used because they produce typical symptoms. *Chenopodium quinoa* and *C. amaranticolor* produce systemic blotches that follow chlorotic local lesions [151]. *Cucumis sativus* may produce chlorotic local lesions and systemic vascular banding or yellow spots in infected cotyledons. *Phaseolus vulgaris* shows symptoms as chlorotic local lesions, systemic necrosis, and deteriorations, *Petunia hybrida* as local chlorotic lesions, tiny necrotic rings, streaks, or vascular opening. However, these symptoms are more pronounced, especially in the hops variant (ArMV-H). ArMV is mostly seen in mixed infection with *Strawberry latent ringspot nepovirus* (SLRSV), which is also a nematode-transmitted agent [137]. Diagnosis of the agent is mostly made by ELISA. The presence of ArMV in a single nematode can also be detected by electron microscopy. Another way to detect ArMV is to use cDNA clones in dot hybridization tests [152, 153]. Distribution of virus-free production material for the control of ArMV with a strict certification program. In areas with infected nematode-vector populations, fallow and/or soil fumigation for at least a year is required, as replanting virus-free material without additional precautions will be ineffective [149].

*Raspberry ringspot nepovirus*; *Raspberry ringspot virus* (RPRSV), which is in the genus Nepovirus of the family Secoviridae, is a single-stranded RNA virus. Asia (Kazakhstan, Uzbekistan) and Europe (France, Serbia, Romania, Germany, Norway, Bulgaria, Italy, Greece, Denmark, Hungary, Ireland, Estonia, Latvia, Czech Republic, Luxembourg, Poland, Austria, Finland, Portugal, Belgium, Russia, Spain, Albania, Switzerland, Turkey, Ukraine, England) have also been reported [147, 154]. However, the main host is *Rubus idaeus, Fragaria* spp., Fragaria x ananassa, some Rubus spp., and Prunus spp. species. *Vitis vinifera* is another important host. Experimentally, It

has also been reported to be transmitted by *Chenopodium giganteum,* Cucurbita spp., Nicotiana, Petunia spp., *Solanum lycopersicum*, *Spinacia oleracea, Vigna unguiculata* species [155]. The agent can be transmitted to some herbaceous plants mechanically and by infected seeds. RpRSV can be transmitted by both species of the nematode genus Longidorus. Scottish and Dutch variants of RpRSV are most effectively transmitted by *L. elongates* [156], while the English variant is transmitted by *L. macrosoma* [157]. Other nematode species (*Xiphinema diversicaudatum* and other Longidorus species) were suspected to carry variants of RpRSV, but transmissions were not considered acceptable [158]. Although the symptoms of RpRSV in strawberries vary according to the season and the breed of the agent, it can usually result in severe stunting and death. In *Fragaria vesca,* seedlings show yellow spots in the first year of infection but no spots after that. While symptoms vary in susceptible varieties, symptoms are less common in summer at high temperatures. RpRSV causes a serious disease that reduces both growth and fruiting and even kills plants. The use of fumigants such as dazomet or dichloropropane-dichloropropene for vector nematodes in raspberry and strawberry production areas provides prevention and control of virus transmission. Rubus spp., Ribes spp., and Fragaria species, the use of healthy certified production material free from RpRSV are one of the best control methods [127, 159, 160].

*Strawberry latent ringspot 'nepovirus'* (SLRSV); SLRSV has a very large host range. The agent, which is mostly found latent in berry fruits such as strawberries and raspberries, can sometimes cause infections resulting in mottling and back-drying [161]. It is found naturally in many berry species as well as in cherries, grapes, plums, peaches, *Sambucus nigra*, asparagus, celery, gladiolus, daffodils, and roses, as well as in many wild species, usually asymptomatic [162]. The presence of the agent has been reported in some countries in Europe, Oceania, North America, and in Israel and Turkey from Asian countries. SLRSV can be mechanically transported to herbaceous plants. It is reported that naturally, both larvae and adults of *Xiphinema diversicaudatum* can carry SLRSV for up to 84 days and up to 70% of seed transmission in several plant species [163]. While the causative agent is usually asymptomatic, varying degrees of mottling and retrograde death can be observed in some strawberry cultivars. Reliable diagnosis is possible with SLRSV specific antisera. *Chenopodium murale*, *C. quinoa*, and *C. amaranticolor* show symptoms as systemic chlorosis, necrotic or chlorotic local lesions, and sometimes pale chlorotic mottling or necrosis. Cucumber shows local lesions in the form of systemic intervascular chlorosis or necrosis or shows no symptoms at all. During the summer, the later leaves are asymptomatic but contain the virus, while in the winter, the symptoms may persist on the newly arrived leaves. *Nicotiana rustica*, *Nicotiana tabacum*, and *Petunia hybrida* are infected without symptoms. The virus can sometimes be found in soil together with *Arabis mosaic nepovirus*, which is also carried by *X. diversicaudatum* [137].
