Open access peer-reviewed chapter

Raspberry and Blueberry Viruses

Written By

Melike Yurtmen

Submitted: 20 April 2023 Reviewed: 07 May 2023 Published: 05 September 2023

DOI: 10.5772/intechopen.1001860

From the Edited Volume

Edible Berries - New Insights

Nesibe Ebru Yaşa Kafkas and Hüseyin Çelik

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Abstract

Berry fruits are nutrient-rich foods and proved to be beneficial for human health. High nutraceutical properties of these fruits, in particular, blueberries and raspberries, such with exceptionally high antioxidant levels, fiber, and a low natural sugar content have an important criterion for the marketable value as well. Thus, they are defined as functional foods. Naturally, rapid increases in their production and consumption rates during recent years, therefore, make sense. In the cultivation of these berry crops, satisfactory yields and quality of the produce posed a threat by certain pests in the world. Blueberries and raspberries are also infected with viruses that have been identified as new viruses on top of existing ones as a result of expanding cultivation areas around the world. Incurable plant pathogenic viruses cause major damage to the members of blueberry and raspberry as if serious yield losses and longevity of plantings. This chapter is intended to compile knowledge of pathogenic plant viruses that infect blueberry and raspberry plants. Herein, a review of geographic distribution, importance, symptoms, transmission, detection, and management of these berry viruses are provided for the readers.

Keywords

  • pathogenic plant viruses
  • Vaccinium
  • Rubus
  • blueberry
  • raspberry
  • management strategies

1. Introduction

Blueberry and raspberry production is increased worldwide toward consumer demand over the last decades. Accordingly, cultivation of these fruit crops expanded to new areas in the world. Hereby, viruses infecting plants which prevent their growth and production increased in number significantly year by year since the beginning of this millennium. Pathogenic plant viruses pose a threat to their producers since no curative treatment exists [1]. However, not all viruses cause serious damage to plants, but some are widespread and destructive. Major losses in terms of quantity and quality of the crop are caused by these destructive viruses. Besides, members of the blueberry and raspberry plants are known to be hosting a wide range of pathogenic viruses which, especially when present as mixed infections, most probably cause severe symptoms and greatly affect the yield and viability of the plant. These viruses impact their growers by inducing weak stand establishment and fruit quality, reduced yield, and plant decline. However, symptoms caused by viral diseases in plants vary from being completely asymptomatic to dying of the plant. This symptomatic range is affected by several factors for instance weather conditions, the growing methods, and the age and type of the cultivars. At the beginning of all, to understand what the virus is, how it spreads, and how it is determined and controlled is utmost important to manage diseases induced by viruses. Considering all these aspects, knowledge of pathogenic plant viruses infecting blueberry and raspberry plants in particular is reviewed in terms of their geographic distribution, importance, symptoms, transmission, detection, and management strategies in this chapter.

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2. Understanding plant viruses

Plant pathogenic viruses are highly infectious, submicroscopic, and obligate intercellular parasites with a DNA or RNA core. The nucleic acid is the infectious part of the virus surrounded by a protein coat to be able to replicate within the living cells, and the protein coat is the protective part of the particle. They are too small to be seen with the human eye, but they can be observed with electron microscopes. Their taxonomic classification is based on chemical compounds as well as morphologic, biologic, pathologic, and molecular features. The given names, which are in English, are taken from the plant that they infect, the unique symptoms they cause, and the agent that causes them.

Plant pathogenic viruses are immobile agents and need to be spread from infected to healthy plants or plantations via several means of transmission. Their transmission can be divided into two types and are called as vertical transmission and horizontal transmission.

Vertical transmission occurs when the progeny of an infected parent plant inherits the virus through seeds or pollen, as well as vegetative propagation. Horizontal transmission occurs between generations via fungi, invertebrate vectors (nematodes, insects, and mites), human pruning shears and tools, and other types of direct, external contamination [2, 3].

Aphids, whiteflies, thrips, and leafhoppers are the most important plant virus vectors because they have piercing–sucking mouth parts that allow the insects to reach and feed on the contents of plant cells. Among these, aphids and whiteflies are the most capable of transmitting virus species.

The virus is spread by sap-sucking insects in two ways: persistent transmission and non-persistent transmission. The time an insect takes to acquire and transmit a virus determines the differences.

Pathogenic plant viruses are classified into two types based on their spread distance from their origin. The transfer of contaminated propagation material allows viral infections to spread over long distances. The viral diseases can spread locally (short-distance movement) by pollen from infected plants or by direct contact by vectors such as nematodes, aphids, thrips, soil-borne fungi, and leafhoppers.

When a pathogenic virus enters a region or country, its host range determines its spread. The majority of plant viruses, on the other hand, have a diverse spectrum of alternate hosts.

Initially, to spot virus-induced host plant problems, it is necessary to understand what a healthy plant looks like! Some plants have characteristics or habits that, at certain phases of development, can be misinterpreted as disease symptoms. Plants can also develop virus-like symptoms in reaction to adverse weather conditions, soil mineral/nutrient imbalances, infection by non-viral pathogens, insect/mite/nematode pest damage, air pollution, pesticides, and other factors.

A virus’s pathogenic potential is revealed by its capacity to infect one or more plant species and create observable symptoms. Plant symptoms are frequently used to define a viral-etiology disease and to locate infected plants in order to control the disease. When symptoms are specific to a disorder, visual inspection is usually straightforward. Many factors, such as virus strain, host plant cultivar/variety, infection period, and habitat, may influence the symptoms shown. Some viruses may provide no obvious signs or asymptomatic disease. Furthermore, different viruses can generate the same symptoms in the same host, or different strains of the same virus can cause different symptoms in the same host.

Plant viruses create significant economic losses and threaten sustainable agriculture. There are no antiviral chemicals available to heal plants once they have been infected by a viral pathogen. Control strategies that are effective can considerably reduce or prevent the disease from arising. In this step, virus identification is a required initial step in the management of a virus-caused disease. Plant viruses can be difficult to detect since the typical symptoms are similar to herbicide injury, air pollution damage, mineral deficiencies, and other plant diseases, or more than one virus infection. As a result, identifying viral infection is frequently required.

A critical component of every crop management system is the early and accurate detection of plant diseases. When it is determined that a virus is the cause of a disease, a set of tests are required to determine its identity. Even though identifying a virus or virus complex involves one or more other diagnostic techniques, symptom assessments play a significant part in the diagnostic process.

Understanding the biology of the virus such as virus properties, host range, vector, and inoculum sources is required for effective disease management. It is difficult to eliminate pathogens without harming the host plant due to their nature. As a result, the majority of management techniques for plant viruses are aimed at preventing plant infection.

This page discusses blueberry and raspberry viral infections in light of this understanding.

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3. Viruses infecting blueberry (Vaccinium corymposum L.; V. augustifolium Ait. and V. ashei Reade)

3.1 Blueberry fruit drop associated virus (BFDaV)

The virus is a member of the genus Vaccinivirus in the family Caulimoviridae. BFDaV has a DNA genome and can detect through polymerase chain reaction (PCR). The only host of BFDaV is blueberry (Vaccinium corymbosum). As a disease, fruit dropping of blueberry was first detected in Canada (British Colombia) in the late 1990s. The virus was then observed in the USA in 2012. Young leaves show the red coloration of the veins, and the corolla of the flowers exhibits red striping while blooming. These symptoms stay only in the blooming period, and then, the plants appear as if normal. More symptoms are described as aborting the fruits (3–5 mm in diameter) around 100% in infected bushes nearly 3 weeks before harvest. Therefore, during the harvest, infected blueberry plants look taller compared to healthy ones [4].

3.2 Blueberry latent spherical virus (BLSV)

In Japan, Blueberry latent spherical virus (BLSV) was isolated from an asymptomatic highbush blueberry. It is a Nepovirus [5]. It can detect by reverse transcription-PCR (RT-PCR). The virus was reported as present in blueberries but with no symptom expression. Thus, the virus infections call as latent in blueberry trees. BLSV epidemiology and mode of transmission have not been determined yet.

3.3 Blueberry latent virus (BBLV)

Blueberry latent virus is present in the USA, Canada, and Japan. It is symptomless and does not have negative effects in mixed infections. As a result, the virus’s prevalence is of minor concern. It is transmissible by pollen and seed. Taxonomically, it belongs to the genus Amalgavirus and is possible to detect by RT-PCR [6].

3.4 Blueberry leaf mottle virus (BLMoV)

Blueberry leaf mottle virus is reported from blueberry and its hybrids from Canada and USA. It spreads by seeds and pollen—1.5% of blueberry seedlings from a contaminated bush [7]. Although it is a Nepovirus, no means of nematode transmission has yet been identified. It occurs naturally in highbush blueberry (V. corymbosum) and its hybrids with a grapevine (Vitis vinifera, Vitis labrusca).

The highbush blueberry cultivars ‘Jersey’ and ‘Rubel’ are affected negatively by this virus disease. The onset of symptoms is monitored after 4 years of the latent period from the initial infection. Stem dieback and stunting are developing symptoms of infected bushes. Malformed and mottled leaves caused by the shortening internodes appear as if piled on top of one another. Pale yellow-green leaves are smaller than the ones on uninfected bushes. Nearly no yield is harvested [8]. Virus presence was reported in wild species of blueberries. Detection of the virus by ELISA and/or RT-PCR is available.

3.5 Blueberry red ringspot virus (BRRSV)

Red ringspot disease has been described by Hutchinson [9], and Hutchinson & Varney [10]. It is then assigned to the Soymovirus genus with a DNA genome in the family Caulimovididae. Highbush blueberry (V. corymbosum L.) is the host, and symptom expressions are observed on leaves, stems, and fruits [11]. The virus is present in the USA, Japan, the Czech Republic, Slovenia, and Poland [12, 13, 14, 15, 16]. It is a dsDNA virus and is available to diagnose by PCR [17, 18]. It is found in nature only in Vaccinium spp. The only known mode of transmission is vegetative propagation.

Very characteristic red ring spots are observed on at least one older stem. Mature leaves have 2 to 6 mm diameter pale green-centered reddish-brown circular markings. In mid to late summer, these symptoms appear on the upper surface of the leaf. This is a diagnostic symptom, but sometimes rings are visualized on both sides of the leaf in some cultivars. Red-stemmed or dark cultivars may have masked on matured stems [19].

Reddish rings appear on green fruits and hide as they ripen. Small, deformed, and late-ripening berry fruits are distinguishing symptoms of BRRSV.

3.6 Blueberry shoestring virus (BlSSV)

Blueberry shoestring virus (BSSV) belongs to the genus Sobemovirus, an RNA-containing virus, transmissible by aphids. The only known host of BlSSV is blueberries. It is present in the USA and Canada [20, 21]. The disease can be diagnosed by enzyme-linked immunosorbent assay (ELISA) and RT-PCR. After 4 years of latent period, symptoms are recorded. The spread of the virus in an infected blueberry area occurs horizontally from one bush to another [22]. Elongated (0.2–1.2 cm) reddish stripes that disappear by the growing season are the most distinct symptom on the stems. Flower breaks, strap-like, narrow, and curled leaves are also observed. A significant reduction in the yield of infected bushes has been reported [21, 22, 23, 24]. Disease resistance is known for ‘Blueray’ and ‘Atlantic’ cultivars of blueberries [25]. BSSV is cited under the most common highbush blueberry (V. corymbosum) viruses. Yield losses may reach up to 25% of infected bushes [15]. In 1981, a $3 million yield loss caused by BlSSV has been recorded in the USA. One of the most significant economic damages to highbush blueberries is caused by BlSSV [14]. Mechanical inoculation of the virus on blueberry seedlings or rooted softwood cuttings is possible [20].

3.7 Blueberry virus A (BVA)

BVA was first reported in Japan in the ‘Spartan’ highbush blueberry cultivar. The presence of the virus is known in Canada and the USA. Blueberry virus A has a latent infection in blueberries [26, 27]. It is assigned to the family Closteroviridae, but not yet to a genus. Detection is available by RT-PCR [26]. BVA has no specific symptom expression in single infections. Therefore, no data is available on the economic damage to the blueberry industry.

3.8 Blueberry mosaic associated virus (BlMaV)

The mosaic disease of blueberries has been recorded in the 1950s and is suspected to be a virus since it was transmitted by grafting [23]. It was reported not only from mosaic-affected blueberries but also from symptomless plants.

Yellow, yellow to green, and pink coloring, mosaic and mottling of the leaves, late ripening with low quality of the fruits, and reduction in yield are the symptoms induced by BlMaV [23, 28]. BlMaV as a member of the family Ophioviridae was detected in tested plants with symptoms [29]. The presence of the virus is reported in North and South America, Asia, Europe, New Zealand, and South Africa [27, 30, 31]. Blueberry mosaic spreads slowly in the field by unknown means. This disease is of relatively little concern.

3.9 Blueberry necrotic ring blotch virus (BNRBV)

The virus (BNRBV) was reported first with necrotic ring blotch symptoms in highbush blueberries in the USA in 2006 [27]. It is a new genus, Blunervirus, with an RNA genome [32, 33]. Detection of the virus is available by RT-PCR. IBlueberries infected with the virus displayed distinct necrotic rings with green cores, but when the rings joined. Earlier defoliation can be observed on severely infected bushes that are confused with Septoria leaf spot disease. BNRBV, unlike BRRV, infects all the leaf surfaces without any stem symptoms.

3.10 Blueberry scorch virus (BlScV)

In the 1980s, it is found in blueberries in the USA. No symptoms occur on tolerant cultivars. However, necrosis on flowers and young leaves is observed on sensitive cultivars. Die-back of twigs has also been recorded. The degree of blighting severity determines the size of the bearing fruits. Twig die-back allows lateral buds to develop and form branches later in the season below the point of necrosis. The productivity of infected plants that show symptoms declines year by year, and finally, the plants die [34]. BlScV can cause a serious economic impact due to loss of yield and premature death of plants. Aphid vector spreads the virus in nature [34]. The virus belongs to the Carlavirus genus with an RNA genome. Diagnostic techniques based on ELISA and RT-PCR are also available for virus detection [35].

3.11 Blueberry green mosaic-associated virus (BGMaV)

The virus was discovered first in 2006 as a novel Vitivirus from a blueberry plan showing green mosaic symptoms [27]. It is named as ‘blueberry green mosaic-associated virus’ (BGMaV). It has an RNA genome, and its vector is unknown [36, 37]. Green-centered necrotic rings can also be confused with the ones induced by fungal pathogens in blueberries [27]. It is detectable by RT-PCR and presents only in the USA [27].

3.12 Blueberry shock virus (BlShV)

Shock symptoms of blueberries have been reported first in 1987 in the USA and then correlated with Blueberry Scorch Virus. It is an Ilarvirus and is transmitted by pollen. BlShV moves by wind and bees during pollination [38]. Diagnosis of the virus is available by ELISA or RT-PCR.

After the initial infection, symptom expressions take up to 2 years. Bushes demonstrate a ‘shock reaction’ the year after infection, with flowers and foliage blighting in early spring. Sudden dieback of young vegetative shoots and flowers, necrosis and blighting in flowers, defoliation, and lack of fruit set are the symptoms observed. Plants may not show symptoms in spring growth following the first symptom expression. Partially blighted bushes show symptoms the year after although they were symptomless wood the year before. Infected blueberries normally bring into flowers after 1–3 years and bear fruits as if normal although they are still infected and the source of inoculum [34, 38, 39, 40].

3.13 Peach rosette mosaic virus (PRMV)

Rosette mosaic disease of peaches was discovered as the virus in the 1970s. It is then reported from grapes and blueberries [41, 42, 43]. Symptoms observed in blueberries are distorted, malformed, and uneven distribution of bushes in the plant. Yield losses due to the PRMV infection in blueberries are not known. The presence of PRMV is recorded in Canada and USA. It is an RNA virus and is classified as a Nepovirus with soil-borne nature [44, 45, 46]. Virus detection is available by ELISA and RT-PCR.

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4. Viruses infecting raspberry (Rubus idaeus L. and Rubus occidentalis L.)

4.1 Apple mosaic virus (ApMV)

ApMV is in the Ilarvirus genus with an RNA genome and has a wide variety of host plants in the Rosaceae family worldwide [47]. It spreads by pollen. The presence of ApMV is detected in R. idaeus R. occidentalis and R. ursinusin [48, 49, 50]. The virus is symptomless in Rubus. However, some R. idaeus plants in Germany showed symptoms of yellow mottling and/or line patterns [48]. Virus detection is available by ELISA and RT-PCR.

4.2 Arabis mosaic virus (ArMV)

ArMV was discovered for the first time in the 1940s [51]. The virus infects about 100 plant species from roughly 30 families, producing considerable losses in the majority of them [52, 53]. It is a Nepovirus that is spread by nematode vectors [54, 55]. ARMV can be detected using ELISA and RT-PCR. Raspberry cultivars have genetic resistance to ArMV [56].

4.3 Black raspberry necrosis virus (BRNV)

The virus was first detected in black raspberry (R. occidentalis L.) in 1955 [57] by inducing latent or mild symptoms in red raspberry (R. idaeus L.) cultivars and severe cane tip necrosis in black raspberry [58]. It belongs to the Secoviridae family with an unassigned genus. Its transmission in nature occurs by the raspberry aphids and is distributed worldwide where raspberries are produced [59]. RT-PCR is available for virus detection. Rubus is the genus hosting BRNV with its wild and cultivated species. Although BRNV is symptomless in several commercial species, it is still on the list of the most important viral pathogens of Rubus spp. Some BRNV-infected red raspberry cultivars show chlorotic spots and venial chlorotic mottle in leaves, but most of them are symptomless carriers of the virus. Symptoms caused by the virus can be listed as leaf chlorosis, mottling, and puckering. Infected plants do not yield fruits within 3–4 years [60]. Shorter and thinner canes and smaller fruits are also induced by the virus in sensitive cultivars. Yield loss caused by the virus decreases up to 30% in sensitive cultivars [61].

4.4 Cherry rasp leaf virus (CRLV)

CRLV is a type member of the Cheravirus genus [62]. It is spread by the nematode. RT-PCR can be used to diagnose the virus. The virus is found naturally in North America. Rubus has only been identified in a few red raspberries shipped from Canada to Scotland [63]. There is no information concerning the economic importance of the virus in commercial Rubus crops.

4.5 Cucumber mosaic virus (CMV)

CMV occurs worldwide in many different plant species [64], including Rubus spp. The virus is a member of the Cucumovirus genus with an RNA genome and is transmitted by many aphid species in nature [65]. CMV is also seed transmitted in several of its hosts [64], but not in raspberry seedlings. Detection of the virus is available by ELISA and RT-PCR. It is reported in Rubus only from Britain and Eastern Russia. The first report of the virus is from a few plants of R. idaeus L. cv. ‘Lloyd George’ in Scotland [66]. The second record of the virus comes from Scotland [67] and the Soviet Far East [68]. The virus is symptomless in cultivated brambles [67]. It has mild foliar symptoms in red raspberries although it is lethal in R. phoenicolasius Maxim [66, 67, 68]. Some raspberry cultivars show chlorotic mottling and blotching while red raspberry cv. ‘Lloyd George’ has pale green blotching of the leaves with no apparent effect on plant vigor or fruiting [66]. Foliar chlorotic ringspot symptoms are recorded by the single CMV infection of red raspberry with no obvious degeneration in vigor. Small leaves with bright chlorotic mottling were another symptom detected in infected raspberries (cv. ‘Visluha’) [68]. However, infected R. phoenicolasius plantsshow chlorotic blotch and line patterns in leaves which become bright yellow in summer, decline in vigor, and death of the plants in 3–4 years [67].

4.6 Raspberry bushy dwarf virus (RBDV)

RBDV belongs to the Idaeovirus genus with an RNA genome. It is a pollen and seed-borne virus [69]. Laboratory tests are available by ELISA and RT-PCR. The virus infects many Rubus species and cultivars worldwide. There are resistance-breaking (RB) isolates of the virus infecting raspberry cvs (Glen Clova, Malling Admiral, Malling Delight, Malling Jewel, Willamette, Haida) which are known to be immune to the common strain of RBDV [70, 71]. The RB isolates are recorded from Europe. Pollen-borne nature of the virus causes drupelet abortion thus crumbly fruit forms in some red raspberry cultivars. RBDV infection alone is symptomless in red raspberry cultivars. However, crumbly fruit disease can be observed in mixed infections. Mixed infection of RBDV with BRNV induces dwarfing and shoot proliferation in red raspberries, a typical bushy dwarf condition. The origin of virus name is derived from mixed infection of the plants with RBDV and BRNV [72].

4.7 Raspberry latent virus (RpLV)

The virus is not yet assigned taxonomically. It is an aphid-borne virüs with an RNA genome and is detectable by RT-PCR [56]. It was identified from a red raspberry cv. Glen Prosen with leaf spot symptoms and therefore was named before as raspberry leaf spot virus in 1988 [73]. A typical symptom induced by the virus is the formation of a few, stunted canes which are very prone to autumn fruiting.

4.8 Raspberry leaf blotch virus (RLBV)

RLBV as a member of the Emaravirus genus with an RNA genome is readily diagnosed by RT-PCR. It has been originally described in the red raspberry cv. Glen Ample in Scotland and Serbia [74]. It is responsible for leaf blotch disorder which was found before in Tayberry and correlated with the infestation of plants with the raspberry leaf and bud mite, Phyllocoptes gracilis [75]. This virus causes symptoms such as yellow and light green leaf blotches and patches, distortion of leaf margins, and leaf twisting. However, these symptoms were associated with the feeding damage of mites which is widespread in Europe and North America.

4.9 Raspberry leaf curl virus (RpLCV)

RpLCV is reported first in the 1920s [76] and has hosts limited by the genus Rubus. The virus so far is not yet characterized. It is an aphid-borne virus. No laboratory diagnostic tool is available for the virus. The presence of the virus is reported only in the United States and Canada. Infected red raspberries show severe symptoms of curled, distorted, and chlorotic leaves in the following growing season right after infection. Shoots with extreme shortening of the internodes are dwarfed. Crumbly, seedy or small fruits are set in infected plants and naturally, plant yield is severely reduced. Since the virus spread is very slow in the field, there is no significant loss in terms of economic value [56, 77].

4.10 Raspberry leaf mottle virus (RLMV)

The virus is an aphid-borne Closterovirus with an RNA genome and is readily detectable by RT-PCR. It was first identified in 1924 as producing ‘raspberry mosaic disease’ (RMD). RLMV is a widespread virus in Europe and North America. It has a latent infection in most of the red raspberry cultivars although some diagnostic symptoms are induced in a few of them. It is the member of a disease complex inducing mosaic disease in raspberries along with rubus yellow net virus (RYNV) and black raspberry necrosis virus (BRNV). Additionally, RLMV is responsible for producing “raspberry crumbly fruit” syndromes together with the raspberry latent virus (RpLV) and raspberry bushy dwarf virus (RBDV) in a disease complex [56].

4.11 Raspberry ringspot virus (RpRSV)

RpRSV is a Nepovirus with an RNA genome transmissible by pollen, seed, and nematode [78]. Laboratory tests are available by ELISA and RT-PCR. It was first described in the 1950s as the causal agent of the raspberry leaf curl disease [79]. The virus is present in Europe and has a very wide range of host plants belonging to at least 14 families [80]. The virus resistance has been reported in red raspberries [56].

4.12 Raspberry vein chlorosis virus (RVCV)

The virus as a member of the Rhabdovirus genus with an RNA genome has an aphid vector [81] and is detectable by RT-PCR. RVCV was first described in 1952 and is widespread in New Zealand, the UK, and Europe, causing stunted cane growth and reduced vigor thereby reducing yield in particular with mixed infection. A notable symptom caused by the virus is characteristic chlorosis of the minor leaf veins in field-grown red raspberry plants.

4.13 Rubus yellow net virus (RYNV)

RYNV is an aphid-transmitted Badnavirus with a DNA genome and is detectable by PCR [82]. RYNV is a member of a disease complex inducing mosaic disease in raspberries along with raspberry leaf mottle virus (RLMV) and black raspberry necrosis virus (BRNV). The virus infects all the cultivars of red raspberries and most of the cultivars and hybrids of blackberries in North America and Europe [61]. It is symptomless in all red raspberries and although veinal chlorotic mottle or line-pattern symptoms may be observed in some of them. Yield losses of 30–75% in the first year and up to 15% in following years have been documented as a result of the combined infection with the black raspberry necrosis virus [83]. The rapid spread of the virus is correlated with the vector aphid population [56].

4.14 Sowbane mosaic virus (SoMV)

It is a pollen and seed-borne virus with an RNA genome belonging to the genus Sobemovirus. Laboratory tests are available by ELISA and RT-PCR. It was named first as Rubus chlorotic mottle virus (RuCMV) but then classified as Rubus strain of sowbane mosaic virus (SoMV-R). It was found recently in Scotland, in red raspberries and wild blackberries (Rubus fruticosus) [84]. Rubus strain of the virus is not seed transmitted. It is widespread [85]. Identical symptoms produced by SoMV-R are the reverse curling of the tip leaves in R. idaeus ‘Gaia’ temporarily and diffuse chlorotic spots in blackberry leaves.

4.15 Tomato black ring virus (TBRV)

It is transmitted by pollen, seed, and nematode and belongs to the genus Nepovirus with an RNA genome. Laboratory diagnosis of the virus is available by ELISA and RT-PCR. It is described in 1946 [25, 86] and has a very large host range including Rubus spp. It is present in Europe, Japan, India, and Saudi Arabia. The virus together with RpRSV in mixed infection causes diseases named raspberry leaf curl or raspberry ring spot based on the cultivar. The virus’s host range is as broad as that of other nematode-transmitted viruses. Resistance to TBRV has been identified in blackberry and raspberry cultivars [56].

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5. Common viruses infecting blueberry and raspberry

5.1 Cherry leaf roll virus (CLRV)

The virus is a member of the Nepovirus genus with an RNA genome and is detectable by ELISA and RT_PCR [87]. It is a pollen and seed-borne virus and is transmissible by nematodes. It was found in blackberies first in England [88]. It was reported as sometimes being lethal in Rubus armeniacus ‘Himalaya Giant’. The second record came from cultivated red raspberries in New Zealand showing vigor depression and severe leaf symptoms [89]. The virus is reported with a wide natural host range around the world [90]. Chlorotic mottling and line patterning in leaves are produced in the blackberry cv. Himalaya Giant by CLRV. CLRV-infected red raspberry cultivars have stunted and deformed leaves with severe chlorotic mottle and ring and line patterns.

5.2 Strawberry latent ringspot virus (SLRSV)

It is an RNA virus and not yet assigned species in the Secoviridae family [91]. The virus is detectable by ELISA and RT-PCR. SLRSV has a very wide host range including more than 125 plant species belonging to 27 families and is transmissible by nematodes, pollen, and seed [92]. Yellowing and stunting in blackberry and raspberry are the symptoms observed. The virus is reported from Rubus plants only in Europe. Blackberry and raspberry cultivars have the sources of resistance to SLRSV [56].

5.3 Tobacco ringspot virus (TRSV)

TRSV is a member of the genus Nepovirus with an RNA genome [93, 94]. Laboratory analyses are available by ELISA and RT-PCR. It is a pollen and seed-borne virus transmitted by nematodes. TRSV has a worldwide distribution. It was identified first in 1917 [95]. The presence of the virus in Rubus is reported in the USA, from wild blackberries [96]. TRSV in single infections produces mild or no symptoms. However, severe symptoms are produced when co-infection occurs with other viruses. The only resistant cultivar to the common strain of the virus is reported as ‘Jersey’.

5.4 Tomato ringspot virus (ToRSV)

The virus is classified in the Nepovirus genus and has an RNA genome. It is transmitted by nematodes and is detectable by ELISA and by RT-PCR. The first isolation of the virus in Rubus was in 1938 in Canada [56]. The virus has a wide host range from 35 families [97]. In raspberry production, the virus can induce a serious problem. Blackberries can be infected by ToRSV as well [98, 99]. In raspberries, canes were partially or completely killed 3 years after becoming infected within 10–80% [100]. Infected raspberry plants have no symptoms in the first year. Meanwhile, following spring, some of the primocanes exhibit yellow rings, line patterns, or vein chlorosis in the leaves which may be called shock reactions although the symptoms are infrequent in the following years. The disease’s red raspberry symptoms vary according on the cultivar, the length of the infection, and the stage of growth of the plants. Fruiting canes are delayed, with varied degrees of chlorosis on the leaves and a large proportion of deformed or crumbly fruit, as well as an overall fall in vigor as output decreases [101].

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6. Management of virus diseases

There are a few alternatives for reducing the impact of plant virus diseases [102], but no anti-viral cure that block or interfere with virus infection have been identified. It is, therefore, plant virus disease management strategies based on conventional and non-conventional methods. In conventional methods, pest control, cultural control, development of virus-free/virus-tested plants, quarantine regulations, and breeding programs are employed.

Pathogen resistance is being employed in non-conventional ways. Coat protein, movement protein, replicase, satellite RNA, and antisense RNA all contribute in pathogen-derived resistance.

Insecticides are used to suppress viral vector populations.

Monitoring for virus-like symptoms, removing and burning of infected plants, and identifying alternate and reservoir hosts are all cultural techniques. Plants that show signs of infection should be inspected on a regular basis and removed. Remove weeds and plant debris that may harbor the disease. They should not be buried or composted.

The distribution of healthy plant material is a key step in preventing the spread of harmful viral infections that might accompany plant germplasm mobility. Alternative hosts act as virus reservoirs and cultural controls, as well as having a substantial impact on epidemiology.

Blueberry and raspberry plants are vegetatively multiplied perennial crops. One of the greatest ways for reducing the disease effect generated by pathogenic plant viruses is to establish orchards using virus-tested stock that is devoid of targeted viruses [1]. Apical meristem culture and/or chemotherapy/thermotherapy are used to generate virus-free/virus-tested category plants.

Quarantine regulations is a must to be followed during plant material import and export. Plant quarantine is a bio-security tool used to restrict the introduction and spread of economically relevant pests of plants or plant products that are not yet present in an area or are present but are not extensively distributed and are under official control [103104]. Consumer demand for these fruits has led to a rise in global output in recent years. Viral infections are easily spread since these crops are typically propagated and disseminated as vegetative cuttings.

Traditional breeding is used to create virus-tolerant/resistant cultivars; however, it is a time-consuming process that is not always practical or available.

The key ingredients in deciding which control measures to use and whether to use them alone or in combination with others are thorough epidemiological knowledge of the pathosystem in question, as well as solid information on the selectivity, mode of action, effectiveness, and reliability of each measure, as well as how to respond. To be adopted, control systems must be ecologically and socially sustainable, resilient, low-cost, and consistent with ordinary farming operations.

Virus epidemics in cultivated plants provide a global challenge to achieving acceptable yields and product quality. To confront this challenge, a more sophisticated and broad set of host resistance, cultural (phytosanitary and agronomic), chemical, biological, and legislative control techniques are becoming accessible. Knowing which elements limit viral epidemics in natural plant communities and primitive subsistence farming systems has aided in their evolution.

In Brief:

  1. It is strongly advised to use certified, micro-propagated, virus-tested, and if possible, disease-free stock to establish nursery blocks and commercial plantings.

  2. To control nematode-transmissible viruses, pre-plant soil testing for the presence of nematodes is advised, followed by pre-plant fumigation with an approved nematicide if vector nematodes are identified.

  3. To eliminate new, latent infections, remove diseased plants as well as symptomless plants beyond the symptomatic plants in each direction.

  4. Chemicals used to manage the vector, such as those targeting the mite or insect, may aid in reducing losses due by virus infection.

  5. Weed removal to reduce possible in-season and overwintering viral reservoirs.

  6. When available, choose resistant or tolerant cultivars or get transplants from a trustworthy supplier.

  7. Disinfect all tools and machinery before and after use (one part bleach to four parts water).

Tobacco should not be used near vulnerable plants, especially in greenhouses. Cigarettes and other tobacco products may be contaminated and spread disease.

References

  1. 1. Gergerich RC, Welliver RA, Gettys S, Osterbauer NK, Kamenidou S, Martin RR, et al. Safeguarding fruit crops in the age of agricultural globalization. Plant Disease. 2015;99:176-187
  2. 2. Singh S, Awasthi LP, Jangre A. Transmission of plant viruses in fields through various vectors. In: Awasthi LP, editor. Applied Plant Virology. Cambridge, MA, USA: Academic Press; 2020. pp. 313-334
  3. 3. Lefeuvre P, Martin DP, Elena SF, Shepherd DN, Roumagnac P, Varsani A. Evolution and ecology of plant viruses. Nature Reviews. Microbiology. 2019;17:632-644
  4. 4. Diaz-Lara A, Martin RR. Blueberry fruit drop-associated virus: A new member of the family Caulimoviridae isolated from blueberry exhibiting fruit drop symptoms. Plant Disease. 2016;100:2211-2214
  5. 5. Isogai M, Tatuto N, Ujiie C, Watanabe M, Yoshikawa N. Identification and characterization of blueberry latent spherical virus, a new member of subgroup C in the genus Nepovirus. Archives of Virology. 2012;157:297-303
  6. 6. Saad N, Olmstead JW, Jones JB, Varsani A, Harmon PF. Known and new emerging viruses infecting blueberry. Plants. 2021;10:2172. DOI: 10.3390/plants10102172
  7. 7. Childress AM, Ramsdell DC. Detection of blueberry leaf mottle virus in highbush blueberry pollen and seed. Phytopathology. 1986;76:1333-1337
  8. 8. Ramsdell DC, Stace-Smith R. Blueberry leaf mottle, a new disease of highbush blueberry. Acta Horticulturae No. 95. In: II International Symposium on Small Fruit Virus Diseases, Budapest (Hungary). 3 July 1979. pp. 37-48
  9. 9. Hutchinson MT. Can you recognize the symptoms of stunt disease? Proceedings of the Nineteenth Annual Blueberry Open House. 1950;19:9-11
  10. 10. Hutchinson MT, Vamey EH. Ringspot: A virus disease of cultivated blueberry. Plant Disease Reporter. 1954;38:260-263
  11. 11. Gillett JM. Physical and chemical properties of blueberry red ringspot virus. [M.S. thesis], Michigan State University, East Lansing, MI, USA. 1988
  12. 12. Isogai K, Ishii M, Umemoto S, Watanabe M, Yoshikawa N. First report of blueberry red ringspot disease caused by blueberry red ringspot virus in Japan. Journal of General Plant Pathology. 2009;75:140-143
  13. 13. Cho IS, Chung BN, Cho JD, Choi GS. First report of blueberry red ringspot virus infecting highbush blueberry in Korea. Plant Disease. 2012;96:1074
  14. 14. Kalinowska E, Paduch-Cichal E, Chodorska M, Sala-Rejczak K. First report of blueberry red ringspot virus in highbush blueberry in Poland. Journal of Plant Pathology. 2011;93:S4.73
  15. 15. Pleško IM, Marn MV, Koron D. Detection of blueberry red ringspot virus in highbush blueberry cv. 'Coville' in Slovenia. Julius-Kuhn-Archives. 2010;427:204-205
  16. 16. Přibylová J, Špak J, Kubelková D, Petrzik K. First report of blueberry red ringspot virus in highbush blueberry in the Czech Republic. Plant Disease. 2010;94:1071
  17. 17. Glasheen BM, Polashock JJ, Lawrence DM, Gillett JM, Ramsdell DC, Vorsa N, et al. Cloning, sequencing, and promoter identification of blueberry red ringspot virus, a member of the family Caulimoviridae with similarities to the “soybean chlorotic mottle-like” genus. Archives of Virology. 2002;147:2169-2186
  18. 18. Polashock JJ, Ehlenfeldt MK. Molecular detection and discrimination of blueberry red ringspot virus strains causing disease in cultivated blueberry and cranberry. Plant Disease. 2009;93:727-733
  19. 19. Cline WO, Ballington JR, Polashock JJ. Blueberry red ringspot observations and findings in North Carolina. Acta Horticulturae. 2009;810:305-312
  20. 20. Ramsdell DC. Physical and chemical properties of blueberry shoestring virus. Phytopathology. 1979;69:1087-1091
  21. 21. Lesney M, Ramsdell D. Purification and some properties of blueberry shoestring virus. Acta Horticulturae. 1976;66:105-109
  22. 22. Caruso FL, Ramsdell DC. Compendium of Blueberry and Cranberry Diseases; American Phytopathological Society: St. MN, USA: Paul; 1995
  23. 23. Varney EH. Mosaic and shoestring virus diseases of cultivated blueberry in New Jersey. Phytopathology. 1957;47:307-309
  24. 24. Martin RR, Bristow PR. Scorch. In: Caruso FL, Ramsdell DC, editors. Compendium of Blueberry and Cranberry Diseases. St. Paul, MN, USA: American Phytopathological Society; 1995. pp. 51-52
  25. 25. Murant AF. Tomato black ring virus. In: CMI/AAB Descriptions of Plant Viruses No. 38. Wellesbourne, UK: Association of Applied Biologists; 1970
  26. 26. Isogai M, Muramatu S, Watanabe M, Yoshikawa N. Complete nucleotide sequence and latency of a novel blueberry-infecting closterovirus. Journal of General Plant Pathology. 2013;79:123-127
  27. 27. Martin RR, Polashock JJ, Tzanetakis IE. New and emerging viruses of blueberry and cranberry. Viruses. 2012;4:2831-2852
  28. 28. Ramsdell D, Stretch AW. Blueberry mosaic. In: Converse RH, editor. Virus Diseases of Small Fruits. Washington, DC, USA: US Department of Agriculture, Agriculture Handbook No. 631; US Government Printing Office; 1987. pp. 119-120
  29. 29. Thekke-Veetil T, Ho T, Keller KE, Martin RR, Tzanetakis IE. A new ophiovirus is associated with blueberry mosaic disease. Virus Research. 2014;189:92-96
  30. 30. Martin R, Tzanetakis I, Caruso F, Polashock J. Emerging and reemerging virus diseases of blueberry and cranberry. Acta Horticulturae. 2009;810:299-304
  31. 31. Isogai M, Matsuhashi Y, Suzuki K, Yashima S, Watanabe M, Yoshikawa N. Occurrence of blueberry mosaic associated virus in highbush blueberry trees with blueberry mosaic disease in Japan. Journal of General Plant Pathology. 2016;82:177-179
  32. 32. Quito-Avila DF, Brannen PM, Cline WO, Harmon PF, Martin RR. Genetic characterization of blueberry necrotic ring blotch virus, a novel RNA virus with unique genetic features. The Journal of General Virology. 2013;94:1426-1434
  33. 33. Melzer MJ, Freitas-Astúa J, Rodriguez JCV, Roy A, Wei G. Create one new family Kitaviridae comprising three previously unassigned genera, Cilevirus, Blunervirus and Higrevirus. 2018;002. Available from: https://talk.ictvonline.org/ictv/proposals/2018.002P.A.Kitaviridae.zip. [Accessed: 04 July, 2023]
  34. 34. Bristow PR, Martin RR, Windom GE. Transmission, field spread, cultivar response, and impact on yield in highbush blueberry infected with blueberry scorch virus. Phytopathology. 2000;90:474-479
  35. 35. Wegener LA, Punja Z, Martin R, Bernardy M, MacDonald L. Epidemiology and identification of strains of blueberry scorch virus on highbush blueberry in British Columbia, Canada. Canadian Journal of Plant Pathology. 2006;28:250-262
  36. 36. Thekke-Veetil T, Ho T. Molecular characterization of a new vitivirus discovered in a blueberry plant with green mosaic symptoms. Archives of Virology. 2019;164:2609-2611
  37. 37. Thekke-Veetil T, Ho T, Polashock J, Tzanetakis I. Blueberry green mosaic symptoms are associated with the presence of a new vitivirus. In: Phytopathological. Vol. 106, No. 12. USA: Amer Phytopathological Soc.; 30 December 2016. p. 126
  38. 38. Bristow PR, Windom GE, Martin RR. Recovery of plants infected with blueberry shock ilarvirus (BlShV). Acta Horticulturae. 2002;574:85-89. DOI: 10.17660/ActaHortic.2002.574.10
  39. 39. MacDonald SG, Martin RR, Bristow PR. Characterization of an ilarvirus associated with a necrotic shock reaction in blueberry. Phytopathology. 1991;81:210-214
  40. 40. Schilder A. Blueberry Shock Virus, Pest Alert Factsheet. East Lansing, MI, USA: Michigan State University Extension; 2009
  41. 41. Ramsdell D, Gillett J. Peach rosette mosaic virus in highbush blueberry. Plant Disease. 1981;65:757-758
  42. 42. Dias HF, Cation D. The characterization of a virus responsible for peach rosette mosaic and grape decline in Michigan. Canadian Journal of Botany. 1976;54:1228-1239
  43. 43. Ramsdell D, Myers R. Peach rosette mosaic virus, symptomatology, and nematodes associated with grapevine degeneration in Michigan. Phytopathology. 1974;64:1174-1178
  44. 44. Lammers AH, Allison RF, Ramsdell DC. Cloning and sequencing of peach rosette mosaic virus RNA1. Virus Research. 1999;65:57-73
  45. 45. Allen W, Schagen JV, Ebsary B. Comparative transmission of the peach rosette mosaic virus by Ontario populations of Longidorus diadecturus and Xiphinema americanum (Nematoda: Longidoridae). Canadian Journal of Plant Pathology. 1984;6:29-32
  46. 46. Sanfaçon H, Iwanami T, Karasev A, Van der Vlugt R, Wellink J, Wetzel T, et al. Family Secoviridae. In: Virus Taxonomy. Amsterdam, The Netherlands: Elsevier; 2011. pp. 881-900
  47. 47. Fulton RW. Apple Mosaic Virus. CMI/AAB Descriptions of Plant Viruses No. 83. Wellesbourne, UK: Association of Applied Biologists; 1972
  48. 48. Baumann G, Casper R, Converse RH. The occurrence of apple mosaic virus in red and black raspberry and in blackberry cultivars. In: ISHS Acta Horticulturae No. 129.1. III International Symposium on Small Fruit Virus Diseases. Vancouver, B.C., Canada; 1982. pp. 13-20. DOI: 10.17660/ActaHortic.1982.129.3
  49. 49. Baumann G. Virus infection in cropping and nursery plantations of raspberry and blackberry. I.Aphid-transmitted viruses. Erwerbsobstbau. 1984;26:188-192
  50. 50. Converse RH, Casper R. A member of the apple mosaic virus group occurring in Rubus. In: Acta Horticulturae No. 44. 1975. p. 63
  51. 51. Smith KM, Markham R. Two new viruses affecting tobacco and other plants. Phytopathology. 1944;34:324-329
  52. 52. Mossop DW, Fry PR, Young BR. New plant disease records in New Zealand: Arabis mosaic virus in celery, lettuce and Chinese cabbage; tomato spotted wilt virus in celery. New Zealand Journal of Agricultural Research. 1983;26:257-259
  53. 53. Murant AF. Arabis mosaic virus. CMI/AAB Descriptions of Plant Viruses No. 16. Wellesbourne, UK: Association of Applied Biologists; 1970
  54. 54. Brown DJF. The transmission of two strains of Arabis mosaic virus by populations of Xiphinema diversicaudatum (Nematoda: Dorylaimoidea) from ten countries. Revue de Nématologie. 1986;9:83-87
  55. 55. Trudgill DL, Brown DJF, McNamara DG. Methods and criteria for assessing the transmission of plant viruses by longidorid nematodes. Revue de Nématologie. 1983;6:133-141
  56. 56. Stace-Smith R. Virus and virus-like diseases of Rubus (raspberry and blackberry). In: Converse RH, editor. Virus Diseases of Small Fruits. Washington, D.C: U.S. Government Printing Office; 1987
  57. 57. Stace-Smith R. Studies on Rubus virus diseases in British Columbia. II. Black raspberry necrosis. Canadian Journal of Botany. 1955;33:314-322
  58. 58. Martin RR, MacFarlane S, Sabanadzovic S, et al. Viruses and virus diseases of Rubus. Plant Disease. 2013;97:168-182
  59. 59. Jones AT, Wood GA. The virus status of raspberries (Rubus idaeus L.) in New Zealand. N.Z. Journal of Agricultural Research. 1979;22:173-182
  60. 60. Halgren A, Tzanetakis IE, Martin RR. Identification, characterization, and detection of black raspberry necrosis virus. Phytopathology. 2007;97(1):44-50. DOI: 10.1094/phyto-97-0044 Available from: https://www.dpvweb.net/dpv/showdpv/?dpvno=333
  61. 61. Stace-Smith R, Jones A. Black raspberry necrosis. In: Converse RH, editor. Virus Diseases of Small Fruits. Washington: US Government Printing Office; 1987
  62. 62. Thompson JR, Perry KL, De Jong W. A new potato virus in a new lineage of picorna-like viruses. Archives of Virology. 2004;149:2141-2154
  63. 63. Jones AT, Badenoch S. New virus in raspberry from Canada. In: Scottish Horticultural Research Institute Annual Report for 1980. Dundee Scotland; 1981. p. 100
  64. 64. Francki RIB, Mossop DW, Hatta T. Cucumber mosaic virus. In: Descriptions of Plant Viruses No. 213. Kew, Surrey, England: Commonwealth Mycological Institute and the Association of Applied Biologists; 1979. p. 6
  65. 65. Kennedy JS, Day MF, Eastop VF. A conspectus of aphids as vectors of plant viruses. Commonwealth Institute of Entomology. London: Eastern Press Ltd.; 1962. p. 114
  66. 66. Harrison BD. Cucumber mosaic virus in raspberry. Plant Pathology. 1958;7:109-111
  67. 67. Jones AT. An isolate of cucumber mosaic virus from Rubus phoenicolasius maxim. Plant Pathology. 1976;25:137-140
  68. 68. Gordejchuk OG, Krylov AV, Krylova NV, Samonina IN. Virus diseases of berry crops in the soviet Far East. I. Identification of some mechanically transmitted viruses, detected in Primorye territory. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, Abteilung II. 1977;132:686-707
  69. 69. Derrick KS, Beretta MJ, Barthe GA. Detection of an Idaeovirus in citrus by subtraction hybridization. (Abstr.). Phytopathology. 2005;95:S24
  70. 70. Jones AT, Murant AF, Jennings DL, Wood GA. Association of raspberry bushy dwarf virus with raspberry yellows disease; reaction of Rubus species and cultivars, and the inheritance of resistance. The Annals of Applied Biology. 1982;100:135-147
  71. 71. Knight VH, Barbara DJ. A review of raspberry bushy dwarf virus at HRI-East Malling and the situation on sample of commercial holdings in England in 1995 and 1996. Acta Horticulturae. 1999;505:263-271
  72. 72. Jones AT. The effects of black raspberry necrosis and raspberry bushy dwarf viruses in Lloyd George raspberry and their involvement in raspberry bushy dwarf disease. Journal of Horticultural Sciences. 1979;54:267-272
  73. 73. Jelkmann W, Martin RR. Complementary DNA probes generated from double-stranded RNAs of a Rubus virus provide the potential for rapid in vitro detection. Acta Horticulturae. 1988;236:103-109
  74. 74. McGavin WJ, Mitchell C, Cock PJA, Wright KM, MacFarlane SA. Raspberry leaf blotch virus, a putative new member of the genus Emaravirus, encodes a novel genomic RNA. The Journal of General Virology. 2012;93:430-437
  75. 75. Jones AT, Gordon SC, Jennings DL. A leaf-blotch disorder of tayberry associated with the leaf and bud mite (Phyllocoptes gracilis) and some effects of three aphid-borne viruses. Journal of Horticultural Sciences. 1984;59:523-528
  76. 76. Bennett CW. Further observations and experiments on the curl disease of raspberries. Phytopathology. 1930;20:787-802
  77. 77. Bolton AT. Spread of raspberry leaf curl virus. Canadian Journal of Plant Science. 1970;50:667-671
  78. 78. Ebel R, Schnabel A, Reustle GM, Krczal G, Wetzel T. Complete nucleotide sequence of an isolate of the nepovirus raspberry ringspot virus from grapevine. Virus Research. 2003;97:141-144
  79. 79. Cadman CH. Studies on the etiology and mode of spread of Scottish raspberry leaf curl disease. Journal of Horticultural Sciences. 1956;31:111-118
  80. 80. Murant AF. Raspberry ringspot virus. CMI/AAB Descriptions of Plant Viruses No. 198. Wellesbourne, UK: Association of Applied Biologists; 1978
  81. 81. McGavin WJ, Cock PJA, MacFarlane SA. Partial sequence and RT-PCR diagnostic test for the plant rhabdovirus raspberry vein chlorosis virus. Plant Pathology. 2011;60:462-467
  82. 82. Jones AT, McGavin WJ, Geering ADW, Lockhart BEL. Identification of Rubus yellow net virus as a distinct badnavirus and its detection by PCR in Rubus species and in aphids. The Annals of Applied Biology. 2002;141:1-10
  83. 83. Stace-Smith R, Jones AT. Rubus yellow net virus. In: Converse RH, editor. Virus Diseases of Small Fruits. No. 631. Washington, D.C.: USDA Agriculture Handbook; 1987. pp. 175-178
  84. 84. McGavin WJ, MacFarlane SA. Rubus chlorotic mottle virus, a new sobemovirus infecting raspberry and bramble. Virus Research. 2009;139:10-13
  85. 85. Kado CI. CMI/AAB Descr. In: Plant Viruses – Sowbane Mosaic Virus. No. 64. 1971. p. 4
  86. 86. Madhusudan T, Govindu HC. Identification of virus diseases of tobacco in South India. Indian Journal of Virology. 1985;1:163-173
  87. 87. Von Bargen S, Langer J, Robel J, Rumbou A, Büttner C. Complete nucleotide sequence of cherry leaf role virus (CLRV), a subgroup C nepovirus. Virus Research. 2012;163:678-683
  88. 88. Cropley R, Tomlinson JA. Cherry leaf roll virus. CMI/AAB Descriptions of Plant Viruses No. 80. Wellesbourne, UK: Association of Applied Biologists; 1971
  89. 89. Jones AT, Wood GA. The occurrence of cherry leaf roll virus in red raspberry in New Zealand. Plant Disease Report. 1978;62:835-838
  90. 90. Al-Chaabi S, Ismaeil F. First report of the cherry strain of cherry leaf roll virus on walnut and pecan trees in Syria. Journal of Plant Pathology. 2009;91:502
  91. 91. Sanfaçon H, Iwanami T, Karasev AV, van der Vlugt R, Wellink J, Wetzel T, et al. Secoviridae. In: King AMQ , Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus Taxonomy, 9th Report of the International Committee on Taxonomy of Viruses. San Diego, CA, USA: Academic Press; 2012
  92. 92. Murant AF. CMI/AAB Descr. In: Plant Viruses – Strawberry latent Ringspot Virus. Descript of Plant Viruses 126. Kew, Surrey, England; 1974. 4 p
  93. 93. Rott ME, Tremaine JH, Rochon DM. Nucleotide sequence of tomato ringspot virus RNA 2. The Journal of General Virology. 1991;72:1505-1514
  94. 94. Rott ME, Gilchrist A, Lee L, Rochon D. Nucleotide sequence of tomato ringspot virus RNA 1. The Journal of General Virology. 1995;76:465-473
  95. 95. Fromme FD, Wingard SA, Priode CN. Ringspot of tobacco: An infectious disease of unknown cause. Phytopathology. 1927;17:321-328
  96. 96. Rush MC, Gooding GV, Ellis DV. Wild Rubus spp. as natural hosts for tobacco ringspot virus. Phytopathology. 1968;58:1065
  97. 97. Stace-Smith R. CMI/AAB Descr. In: Plant Viruses - Tomato ringspot virus. Descript of Plant Virus. No. 18. Kew, Surrey, England; 1970. 4 p
  98. 98. Anonymous. EPPO data sheet on quarantine organisms no. 102: Tomato ringspot virus. OEPP/EPPO Bulletin. 1982;12:6
  99. 99. Pinkerton JN, Martin RR. Management of tomato ringspot virus in red raspberry with crop rotation. International Journal of Fruit Science. 2005;5:55-67
  100. 100. Freeman JA, Stace-Smith R. Effects of tomato ringspot virus on plant and fruit development of raspberries. Canadian Journal of Plant Science. 1968;48(1):25-29
  101. 101. Stace-Smith R, Converse RH. Tomato ringspot virus in Rubus. In: Converse RH, editor. Virus Diseases of Small Fruits. Vol. 631. Washington, USA: USDA, Agricultural Handbook; 1987. pp. 223-227
  102. 102. Ellis P, Stace-Smith R, de Villiers G. Identification and geographic distribution of serotypes of potato virus Y. Plant Disease. 1997;81(5):481-484
  103. 103. FAO. Pest risk analysis for quarantine pests, including analysis or environmental risks and living modified organisms. In: Int. Stand. Phytosanit. Meas. Number 11. Rome: Food Agric. Organ; 2004
  104. 104. FAO. Framework for pest risk analysis. In: Int. Stand. Phytosanit. Meas. Number 2. Rome: Food and Agriculture Organization of the United Nations; 2007

Written By

Melike Yurtmen

Submitted: 20 April 2023 Reviewed: 07 May 2023 Published: 05 September 2023