Robert R. Martin and Ioannis E. Tzanetakis USDA-ARS Horticultural Crops Research Laboratory, Corvallis, OR and Oregon State University, Corvallis

Commercial strawberry (Fragaria × symptoms in clones of F. vesca and F. berry latent C virus (SLCV). SCV, ananassa Duchesne), which originated in virginiana plants induced when graft in- SMYEV, SMoV, and SVBV have been Europe around 1750, is a hybrid between oculated with various viruses (18). Since considered the four most economically F. virginiana Duchesne from North Amer- the last review on strawberry viruses (81), important viruses of strawberry in the ma- ica and F. chiloensis (L.) Duchesne from significant progress has been made in the jority of production areas (8,81). These South America. Today F. × ananassa is molecular characterization of the aphid- viruses are generally less important in grown worldwide for the red fruit that is borne viruses, the identification and char- annual cropping systems, because the consumed fresh or used in jam, yogurt, ice acterization of several whitefly-borne vi- plants are not grown in the field as long cream, and baked goods (12). White and ruses, and the molecular characterization and there is less opportunity to get multi- red-fruited F. chiloensis, known for its of viruses associated with several of the ple infections, which are required for intense fragrance and flavor, is cultivated “graft transmissible virus-like diseases” of symptom expression in most cultivars of F. in parts of South America; whereas another strawberry. Prior to 1998, molecular data × ananassa. Nevertheless, it is important, species, F. vesca L. ‘Alpine’ strawberry, is existed only for Strawberry mild yellow even in annual production systems, to con- grown on small farms in parts of Europe. edge virus (SMYEV) (9,35). Currently, trol the aphid vectors (primarily Chaetosi- Strawberries are propagated vegetatively molecular-based reverse transcription– phon fragaefolii) in order to reduce virus and are subject to infection by viruses polymerase chain reaction (RT-PCR) de- infections. With the increase in whitefly- during plant propagation and fruit produc- tection methods are available for most of transmitted viruses in Mediterranean and tion stages. Reports of initial detections, the viruses known to infect strawberry. The subtropical climates, aphid control be- symptoms, severities, and/or vectors for goals of this paper are to review symptoms comes more critical, as mixed infections of more than 30 viruses, virus-like diseases, induced by the viruses, describe advances the aphid- and whitefly-transmitted viruses and phytoplasmas affecting Fragaria spp. in the detection of strawberry viruses, and may lead to significant yield losses. It is have been reviewed (8,81). Photographs of demonstrate the application of these tests also critical to keep plants virus-free dur- the symptoms caused by strawberry vi- for characterizing the cause of recent out- ing the propagation phase, where plants ruses have been published in those reports breaks of a decline disorder in strawberry are grown for increase in the field for sev- and will not be duplicated here. Only vi- in the western United States and Canada. eral years. Breeders have been effective at ruses will be considered in this article, This disorder, in which plants develop a developing tolerance, and most strawberry because excellent work has been published reddish coloration of the leaves, the roots cultivars grown today do not exhibit symp- on phytoplasmas in strawberry (1,29, appear to stop growing, the plants get pro- toms when infected with a single aphid- or 37,115). The names, acronyms, vectors, gressively weaker and in some cases die whitefly-transmitted virus. However, under classification, and laboratory-based meth- (Fig. 1), has been observed in a number of field conditions, these viruses often occur ods available for detection of the viruses cultivars in California. A similar decline in complexes that may result in foliar discussed below are summarized in Table 1. also has been observed in Oregon, Wash- symptoms and plant decline. These four Initially, many of the virus diseases of ington, and British Columbia in cultivars major aphid-transmitted viruses have been strawberry were described based upon such as ‘Totem’, ‘Rainier’, ‘Puget Reli- studied in greatest detail and can be sepa- ance’, and ‘Puget Beauty’ (Fig. 2). rated in the laboratory using serial trans- missions by the common strawberry aphid Aphid-Transmitted Viruses (C. fragaefolii) onto indicator plants (81). Corresponding author: Robert R. Martin E-mail: [email protected] Seven aphid-transmitted viruses are re- Precautions should be taken when carrying ported in strawberry: Strawberry crinkle out these experiments, since there may be virus (SCV), SMYEV, Strawberry mottle considerable differences in transmission DOI: 10.1094/PD-90-0384 virus (SMoV), Strawberry vein banding efficiency among virus isolates and a sin- This article is in the public domain and not copy- virus (SVBV), Strawberry pseudo mild gle colony of C. fragaefolii or between rightable. It may be freely reprinted with custom- ary crediting of the source. The American Phyto- yellow edge virus (SPMYEV), Strawberry several colonies of C. fragaefolii and a pathological Society, 2006. chlorotic fleck virus (SCFV), and Straw- single virus isolate. Laboratory tests, either

384 Plant Disease / Vol. 90 No. 4 RT-PCR or ELISA, are available for each increased (42). Under cooler temperatures, Chile (31). Conflicting reports on the eco- of these viruses, with the exception of transmission efficiency decreases (42). nomic impact of SMYEV probably result SLCV. This longer latent period may explain the from differences in virus strains, cultivars Strawberry crinkle virus (SCV). SCV lack of SCV in many cooler strawberry evaluated, the likelihood that mixed infec- was first reported in Oregon in 1932 (113) production areas. tions often occur in the field resulting in and in Great Britain in 1934 (62). In both The entire nucleotide sequence of SCV synergistic effects with SMYEV, and envi- cases, mild and severe forms of the virus has been determined, and it shows signifi- ronmental conditions in the different stud- were reported, suggesting that there were cant homology to the cytorhabdoviruses ies. Reported yield losses have ranged probably mixed infections. SCV occurs in Northern cereal mosaic virus and Lettuce from 0 to 30%. SMYEV is vectored effi- strawberry in areas where the strawberry necrotic yellows virus (74). It has a single- ciently in a persistent manner by aphids in aphid is found, and is one of the most stranded minus-sense RNA genome of the genus Chaetosiphon. Therefore, in damaging viruses of strawberry. All spe- 14,547 nucleotides that contains seven areas where these aphids do not occur, the cies of Fragaria are susceptible to SCV. open reading frames in the complementary use of virus-free planting material will be Great losses result from mixed infections RNA. RT-PCR and real-time RT-PCR de- an effective management strategy. There is of SCV with pallidosis virus and/or one or tection assays for SCV have been reported no known resistance to SMYEV in the more of the other aphid-borne viruses. by several groups (57,65,89). Using RT- genus Fragaria, but most cultivars grown However, severe strains of SCV can cause PCR assays, it was found that all ‘Totem’ today are tolerant to infection with this disease symptoms on infected cultivars and plants with decline symptoms in British virus by itself. Sensitive cultivars such as reduce yield and fruit size. Sensitive F. Columbia (B.C.), Canada, and Washing- ‘Hood’, ‘Puget Beauty’, and ‘Marshall’ vesca clones are reliable indicators for ton, USA, were infected with SCV as well develop dwarfing, marginal chlorosis, leaf SCV infection, and symptoms include: as with SMoV and SMYEV. Many of the distortion, and small fruit, whereas tolerant deformed leaves and distorted petioles, asymptomatic plants in the same fields cultivars such as ‘Totem’ and ‘Sumas’ do leaflets with chlorotic spots that are often were infected with SMoV and SMYEV. not show symptoms if infected doubly by uneven in size, distorted, and crinkled, Previously, only the latter two viruses and SMYEV and SMoV or SVBV. However, distorted petioles, and size reduction of SVBV had been detected in B.C. (81). The infection by severe strains of three or more leaves. In addition, necrotic lesions on occurrence of SCV in B.C. may be due to of these viruses leads to a decline of these runners, petioles, and petals often appear the existence of new strains of SCV, new cultivars. on indicators. SCV can be transmitted biotypes of the aphid vector, warmer tem- Symptoms of SMYEV are similar on F. mechanically from strawberry to Nicotiana peratures that allow a shorter latent period vesca ‘UC-4’, ‘UC-5’, and ‘Alpine’ seed- occidentalis P1 and then to Physalis pu- and thus more efficient transmission of the lings, while ‘UC-6’ is usually symptom- bescens (41). SCV caused local lesions virus, resistance to chemicals used for less. Symptoms first appear 8 to 10 days and systemic symptoms on N. occidentalis aphid control, or a combination of these after inoculation with severe strains; P1 and systemic symptoms on P. pubes- factors. whereas mild strains may induce delayed cens, which was used for purification and Strawberry mild yellow edge virus or no symptoms. The use of F. vesca characterization of the virus. (SMYEV). Strawberry mild yellow edge ‘EMC’, which is infected with the latent A The virus is transmitted in a replicative disease (SMYED) was first reported in strain of SCV, may increase sensitivity to persistent manner by aphids in the genus California in 1922 (33) and in Europe in very mild strains of SMYEV. Initial symp- Chaetosiphon. In C. fragaefolii, the major 1933 (27), and it is one of the most wide- toms on standard, healthy indicators in- aphid vector, SCV has a latent period of 10 spread virus diseases of cultivated straw- clude epinasty of the newly emerging to 19 days under optimal conditions; at berry. It also occurs in F. chiloensis in leaves together with small chlorotic flecks. cooler temperatures the latent period is areas remote from cultivated strawberry in As the symptoms develop, the chlorosis

Table 1. Strawberry viruses, names, acronyms, natural modes of transmission, genera, and means of laboratory detectiona Mode of Laboratory Virus name Acronym transmission Genus detectionb Apple mosaic ApMV Pollen, seed Ilarvirus ELISA, RT-PCR Arabis mosaic ArMV Nematode, seed Nepovirus ELISA, RT-PCR Beet pseudo-yellows BPYV Whitefly Crinivirus RT-PCR Fragaria chiloensis cryptic FClCV Unknown Unknown RT-PCR Fragaria chiloensis latent FClLV Pollen, seed Ilarvirus ELISA, RT-PCR Raspberry ringspot RpRSV Nematode, seed Nepovirus ELISA, RT-PCR Strawberry chlorotic fleck StCFV Aphid Closterovirus RT-PCR Strawberry crinkle SCV Aphid Cytorhabdovirus RT-PCR Strawberry feather leaf NA Unknown Unknown NA Strawberry latent StLV Unknown Cripavirus RT-PCR Strawberry latent C SLCV Aphid Nucleorhabdovirus NA Strawberry latent ringspot SLRSV Nematode, seed Sadwavirus ELISA, RT-PCR Strawberry mild yellow edge SMYEV Aphid Potexvirus ELISA, RT-PCR Strawberry mottle SMoV Aphid Sadwavirus RT-PCR Strawberry necrotic shock SNSV Thrips, pollen, seed Ilarvirus ELISA, RT-PCR Strawberry pallidosis associated SPaV Whitefly Crinivirus RT-PCR Strawberry pseudo mild yellow edge SPMYEV Aphid Carlavirus ELISA Strawberry vein banding SVBV Aphid Caulimovirus PCR Tobacco necrosis TNV Oomycete Necrovirus ELISA, RT-PCR Tomato black ring TBRV Nematode, seed Nepovirus ELISA, RT-PCR Tomato ringspot ToRSV Nematode, seed Nepovirus ELISA, RT-PCR a NA = not available, indicates the virus disease has been described in the literature but that the authors are unaware of a known isolate of the virus currently maintained in a collection. b Detection methods listed do not include sap inoculation, graft transmission, or vector transmission to indicator plants.

Plant Disease / April 2006 385 Fig. 1. Decline symptoms in strawberry plants near Watsonville, CA, U.S.A.: A, production field showing reddening, uneven growth, and decline associated with infection by multiple strawberry viruses in ‘Ventana’; B, several plants of ‘Ventana’ at various stages of decline; C, close-up of ‘Camarosa’ strawberry plant that exhibits reddening, stunted and distorted leaves, and small fruit.

Fig. 2. Symptoms of decline in ‘Totem’ strawberry in British Columbia, Canada showing: A, vein reddening; B, leaf distortion, vein reddening, and lesions on petioles all associated with multiple virus infection.

386 Plant Disease / Vol. 90 No. 4 increases and gradually becomes necrotic. and the presence of other viruses, only low incidence in strawberry fields, but Interveinal necrosis follows, and eventu- tolerant cultivars can be grown without under extreme aphid pressure, the inci- ally the entire leaf collapses. New leaves extensive use of insecticides for vector dence can approach 100% in third-year continue to emerge and go through the control. Because SMoV is transmitted by fields (92). SVBV is vectored primarily by same cycle of symptom development. A. gossypii, this virus can be common in Chaetosiphon spp. in a semipersistent Eight to 12 weeks after infection with areas where the strawberry aphid does not manner. It also can be transmitted by severe strains of SMYEV, leaves that de- occur, although it should not be a problem aphids in five other genera, but their effi- veloped prior to infection appear healthy, a because most cultivars are tolerant to in- ciency of transmission is low. It is likely ring of dead leaves exists and the younger fection by SMoV alone. that Chaetosiphon spp. are the most impor- leaves exhibit the range of symptoms de- Both F. ve sc a and F. virginiana clones tant vectors of SVBV in the field; however, scribed above. The lack of symptoms on are sensitive indicators for SMoV and in situations where other less efficient grafted ‘UC-6’ plants is helpful in identify- produce a range of symptoms following vectors reach high populations, they could ing SMYEV. inoculation by leaflet grafting or aphid have an important impact on the epidemi- SMYEV was the first strawberry virus transmission. F. vesca ‘Alpine’ and clone ology of the disease. In areas where Chae- cloned and sequenced (31). It is a member ‘UC-5’ are the most frequently used indi- tosiphon spp. are not found, control with of the genus Potexvirus in the family Flex- cator plants for SMoV. Symptoms usually virus-free planting stock usually provides iviridae, and has a single-stranded posi- appear on F. vesca plants 7 to 10 days excellent control of this virus. SVBV was tive-sense RNA containing 5,966 nucleo- following inoculation, but may take longer reported to reduce runner production, tides excluding the 3′ poly A-tail, that has for mild isolates. Symptoms on indicator yield, and fruit quality in the United States five open reading frames. Using a full- clones range from barely discernible, to in commercial fields of ‘Marshall’, ‘Ti- length infectious clone of SMYEV, it was mild leaf mottle, to severe stunting and oga’, and more recently in ‘Carlsbad’. shown that this potexvirus was capable of distortion, to plant death. The use of serial Symptoms also developed in SVBV- causing SMYED in indicator plants (43) transmissions by aphid vectors has shown infected ‘Gaviota’, ‘Cuesta’, ‘Pacifica’, (Fig. 3). This was surprising, because it that individual plants from the field often and ‘Selva’. However, in most cultivars has long been known that field isolates of carry a range of SMoV isolates, probably grown currently, SVBV is symptomless. the causal agent of SMYED are transmit- an indication of mixed infections with Mixed infections of SVBV with SCV or ted in a persistent manner by the straw- SMYEV or SVBV. Strawberry latent C virus led to more se- berry aphid, and it was anticipated that the The complete nucleotide sequence of vere losses; whereas interactions with causal agent would be a luteovirus. The SMoV has been determined (88), and the SMoV, SMYEV, or Strawberry pallidosis potexvirus is not aphid-transmissible from sequence suggests SMoV is a member of associated virus(es) result in a mild disease symptomatic plants inoculated with the the Sadwavirus genus in the family Se- (46). infectious clone, which suggests that there quiviridae. It has a bipartite genome with F. vesca and F. virginiana indicator may be a helper virus that provides aphid single-stranded positive-sense RNAs of clones all develop symptoms when in- transmission in the field. Some evidence of 7,036 and 5,619 nucleotides, respectively, fected with SVBV; ‘UC-6’ and ‘UC-12’ a luteovirus associated with SMYED ex- excluding the poly-A tail. Nucleotide se- are the most sensitive of the two indicator ists, including the presence of isometric quence identity in a 327-base region of the species. The intensity of symptom devel- particles (47) and size and pattern of large coat protein gene varied by as much opment varies depending on the virus iso- dsRNA (80). However, attempts to identify as 25% among 16 geographically diverse late and the indicator used. Three types of a luteovirus or other helper virus in plants isolates of SMoV (87). Based on con- symptoms are known to be caused by dif- infected with SMYEV have not been suc- served nucleotide sequence in the 3′ non- ferent strains of SVBV: (i) vein banding, cessful. SMYEV has been purified and coding region, primers have been devel- (ii) leaf curl, and (iii) necrosis. Vein band- used to produce monoclonal antibodies oped that allowed detection of these same ing symptoms, seen as chlorotic banding that can be used to detect a range of iso- 16 isolates with a single primer pair, a along the primary and secondary veins, are lates from geographically diverse areas good tool for general detection (87). most intense in the first few leaves that (69). SMYEV can be detected readily by Strawberry vein banding virus (SVBV). develop after grafting. Leaves that develop RT-PCR or ELISA (69,89) and has been SVBV is the least common of the four later may show discontinuous streaks detected in all sources of SMYED charac- major aphid-transmitted viruses of straw- along the veins, mild chlorosis along the terized by symptoms on indicator plants. berry and was first described in 1955 (16). veins, or no symptoms. The vein banding Strawberry mottle virus (SMoV). SVBV usually occurs sporadically and at a symptoms tend to be more severe with SMoV was first recognized as a distinct virus in 1946 when it was separated from “mild yellow edge” based on the differ- ence in aphid transmission properties (67). It is the most common virus of strawberry and occurs naturally in the genus Fragaria wherever strawberries are grown. Numer- ous strains of SMoV exist, and most are symptomless in strawberry cultivars, but severe strains may reduce vigor and yield by up to 30% (22). In nature, SMoV is vectored in a semi-persistent manner by the aphids Chaetosiphon sp. and Aphis gossypii. The virus can be acquired and transmitted with feeding times of a few minutes. In areas where Chaetosiphon spp. are the major vectors, the potential for simultaneous transmission of the other aphid-borne viruses of strawberry may Fig. 3. Fragaria vesca inoculated with full-length clone of Strawberry mild yellow edge result in a greater impact on yield. In areas virus (SMYEV) (left) and uninoculated (right), demonstrating that the strawberry mild with high populations of the aphid vectors yellow edge potexvirus is capable of causing typical symptoms of the disease.

Plant Disease / April 2006 387 isolates from the western United States open reading frame (46,56,89). A second and an antiserum developed (110). compared with those from the eastern virus may be associated with vein banding SPMYEV can be detected by ELISA or United States. Symptoms of necrosis may in Europe, because some isolates do not immuno-dot blots directly from strawberry develop on mature leaves. The net veins hybridize with a cDNA clone of SVBV of tissue (109). Sequence information is not may become necrotic, followed by necro- a North American isolate (56). available for this virus or for Strawberry sis of the interveinal tissues. During Strawberry pseudo mild yellow edge vi- latent C (see below); therefore, these vi- chronic infections, premature discoloration rus (SPMYEV). SPMYEV was first re- ruses cannot be detected by RT-PCR or often appears on older leaves. In the ported in 1966 from the eastern United other nucleic acid based tests at this time. United States, the necrosis symptom is States and also has been reported from Strawberry chlorotic fleck virus more common with eastern than with Japan (17,112). It is not clear how wide- (StCFV). Strawberry chlorotic fleck dis- western strains. The vein banding symp- spread it is in Japan, where it was isolated ease was identified in the 1960s in Louisi- tom is diagnostic; whereas leaf curl and from commercial strawberry plantings ana (32), and was named for the symptoms necrosis may be induced by other disease (111). There is only one report from the observed on F. vesca and F. virginiana agents. Symptoms may be more severe in United States, in which it was isolated in indicators. The disease had a significant combination with SCV or be masked in Minnesota from the indicator clone ‘M-1’ impact on plant growth and fruit yield in combination with SMoV or by high levels of F. virginiana. SPMYEV is transmitted ‘Headliner’ in Louisiana (32). The causal of nitrogen in the potting medium. in a semi-persistent manner by Chaetosi- agent of the disease was transmitted by Natural infections of SVBV are known phon sp. and A. gossypii. The disease is of Aphis gossypii, the cotton aphid (32). The only in species of Fragaria, but it has been no known economic significance in the National Clonal Germplasm Repository transmitted to Sanguisorba minor experi- United States, and its importance in Japan (NCGR) in Corvallis, OR, maintains the mentally. No symptoms have been de- is unknown. only known isolate of strawberry chlorotic tected in infected clones of F. chiloensis Infected strawberry cultivars are symp- fleck. Using standard procedures for infected singly with SVBV. In mixed in- tomless. Graft-inoculated F. ve sc a indica- dsRNA extraction, cloning, and sequenc- fections with SCV, SMYEV, and SMoV, tor clones as well as F. virginiana ‘UC-12’ ing, this plant was found to be infected some clones of F. chiloensis show decline develop symptoms of SPMYEV; whereas with a new virus in the genus Closterovi- symptoms (Fig. 4). inoculated F. virginiana ‘UC-10’ and ‘UC- rus in the family Closteroviridae and the SVBV is a member of the Caulimovirus 11’ remain symptomless. F. virginiana two criniviruses associated with strawberry genus in the family Caulimoviridae. Parti- clone ‘UC-12’ develops yellow to reddish pallidosis disease (described in more detail cles 40 to 50 nm in diameter have been coloration with necrotic areas in older in the whitefly transmitted viruses section). isolated, and cytoplasmic inclusion bodies leaves. All F. ve sc a clones show mottled This new closterovirus has similarities in typical of caulimoviruses have been ob- discoloration (yellow to red) followed by genome organization and sequence to Cit- served in leaf tissues of infected plants. premature necrosis. The symptoms of rus tristeza virus (I. E. Tzanetakis and R. The genome of SVBV is a double-stranded SPMYEV can be confused with mild R. Martin, unpublished results) and other circular molecule of DNA about 7,800 bp strains of SMYEV. In such cases, leaflet aphid-transmitted members of the Clos- in size, and it has been cloned (86) and grafting onto F. vesca ‘UC-6’ can be used terovirus genus. Studies are underway in sequenced (63). SVBV has recently been to differentiate the two viruses. our laboratory to separate these three vi- verified as the causal agent of the typical SPMYEV is a member of the Carlavirus ruses and verify aphid transmission of this North American vein banding disease (45). genus in the family Flexiviridae and is closterovirus with strawberry and cotton The coat protein of the virus is highly con- serologically related to Carnation latent aphids, respectively, and determine if this served, and SVBV can be detected readily virus, the type member of the genus. The new virus is associated with the symptoms by PCR using primers in the coat protein virus has been purified from strawberry observed in chlorotic fleck infected F. vesca plants. An RT-PCR has been devel- oped in our laboratory for this new clos- terovirus, and the incidence of the virus in commercial fields and its role in strawberry decline are currently under investigation. Strawberry latent C virus (SLCV). Strawberry latent C (SLC) is a poorly de- scribed disease, first reported in 1942 (28). Electron microscopy studies on infected material have identified a nucleorhabdovi- rus associated with the disease (111), which was designated as Strawberry latent C virus (SLCV). The disease has been reported from eastern North America, and studies have verified that the causal agent can be transmitted by grafting and several aphid species (8). A wide range of symp- toms has been attributed to SLCV, al- though it is difficult to rule out the possi- bility that some isolates may be due to mixed infections with other viruses. The importance of the virus is mainly due to synergism with other strawberry viruses. Grafting and aphid transmission to indica- tor plants are the only available methods today to detect SLC disease. Sensitive F. Fig. 4. Fragaria vesca exhibiting peacock pattern symptoms and downward curling of vesca clones such as ‘EMC’ and ‘UC-5’ leaves. The leaves shown are from a plant infected with Apple mosaic, Beet pseudo develop symptoms that include epinasty yellows, and Strawberry pallidosis associated viruses. and dwarfing; however, verification of

388 Plant Disease / Vol. 90 No. 4 SLC disease also requires grafting on ‘UC- Strawberry pallidosis associated virus the widest host range of all criniviruses 4’, which shows no symptoms when graft- (SPaV). SPaV is latent in most commer- (109), and new hosts continue to be identi- inoculated with SLCV; whereas it develops cial cultivars grown today and in the F. fied (97,108). The virus is vectored by the symptoms when inoculated with nine other vesca indicator clones. Infected F. v i rg i n - greenhouse whitefly and has been an viruses that infect strawberry. To our iana ‘UC-10’ and ‘UC-11’ develop small emerging problem in temperate regions knowledge, there is not a reference isolate chlorotic leaves; runners may be short- worldwide because of the expanding range of SLCV available in North America to use ened; and it has been reported that severe of the vector (107). The increased range for further characterization. strains can be lethal. In our studies with and high fecundity of the greenhouse pallidosis, we never encountered strains whitefly suggest that the incidence of Whitefly-Transmitted Viruses that were lethal to indicator plants. It is BPYV and SPaV in strawberry production Whitefly-transmitted viruses are an possible that these strains reported in the may increase in the future. emerging problem in world agriculture, past were actually mixed infections of Two isolates of BPYV have been se- due to migration and naturalization of the pallidosis and one or more other straw- quenced completely, one from cucumber whitefly vectors and movement of plant berry viruses. (then referred to as Cucumber yellows germ plasm. Members of the Crinivirus Sap transmission to 24 plant species was virus) (30) and the other from strawberry genus of the Closteroviridae family com- unsuccessful in our laboratory. Studies (96). The genome organization of the prise one of the predominant groups of with the whitefly vectors of criniviruses BPYV isolate from cucumber is similar to whitefly-transmitted viruses that have indicated that Trialeurodes vaporariorum, that of SPaV, but there are significant dif- emerged in the last decade (72,107,109). the greenhouse whitefly, is a vector of the ferences between the two BPYV isolates. Closteroviruses have long filamentous virus (94). The host range of SPaV, as in The differences include the presence of an particles of 700–2,000 × 11–12 nm and the case of most criniviruses, is narrow, additional open reading frame in the 3′ end comprise the group of plant viruses with including members of Fragaria and related of RNA 1 of the strawberry isolate as well the largest positive-sense single-stranded genera and a few weed species (91). The as an insertion in the middle of the replica- RNA genomes. Criniviruses have bipartite virus has been found in the major straw- tion-related polyprotein. The differences or tripartite genomes and are transmitted in berry production areas of the United may be host- or geography-dependent, but a semi-persistent manner by whiteflies States, and studies are currently in pro- additional data is needed to determine the belonging to the Trialeurodes or Bemisia gress in our laboratory to determine if the origin of the diversity. Both molecular and genera. Until recently, there were no virus occurs in other states in the United immunological tests have been developed criniviruses identified in strawberry or any States and in other countries. for BPYV, but as in the case of SPaV, the of the other small fruit crops. Modern mo- Anecdotal reports suggested that the low titer of the virus makes immunological lecular techniques have allowed identifica- pallidosis agent may be pollen-borne (10). tests for BPYV less suitable for routine tion of new criniviruses in crops not However, more than 400 and 170 plants detection. known to be infected by members of the were tested for seed and pollen transmis- group (50,76), because the inefficient sap sion, respectively, and all the plants tested Nematode-Transmitted Viruses transmission of all the known members of negative for SPaV, suggesting that the Five nematode-transmitted viruses are the genus did not allow their identification virus either is not pollen- or seed-borne, or known to infect strawberry. Four belong to with the limited tools of the past. Two if it is, that transmission occurs at very low the genus Nepovirus, in the family Co- closely related criniviruses have now been levels (91). Alternatively, the pallidosis moviridae; whereas one, Strawberry latent associated with pallidosis disease of isolates used in the previous transmission ringspot virus (SLRSV), is a possible strawberry: the newly identified Straw- studies may have been infected with member of the genus Sadwavirus in the berry pallidosis associated crinivirus BPYV, the second virus associated with family Sequiviridae. Nepoviruses and (SPaV) (93) and Beet pseudo-yellows virus pallidosis disease, or the plants used for SLRSV have spherical (icosahedral) parti- (BPYV) (104). these studies may have been contaminated cles of ~28 to 30 nm in diameter and are Strawberry pallidosis disease. Straw- by the greenhouse whitefly, which was not efficiently transmitted by members of the berry pallidosis was identified in the 1950s known as a virus vector at the time. nematode genera Xiphinema and Longi- in both Australia and the United States SPaV is considered to be the major dorus as well as via pollen and seed. The (20). The disease was thought to be in- agent associated with pallidosis in United strawberry nematode-transmitted viruses digenous to North America because the States because more than 97% of the have wide host ranges and can cause sig- plants in Australia originated in the United plants identified as pallidosis positive by nificant losses in the crop (6,21,44,54,83), States (20). Pallidosis (pale or pallid ap- grafting were infected with the virus (93). especially when present in mixed infec- pearance) is a disease caused by graft- The complete sequence of the virus has tions with other viruses. Many of these transmittable agent(s), causing symptoms been determined (103). SPaV has a bipar- viruses are quite diverse at the nucleotide that include marginal leaf chlorosis and tite genome, similar to that of other level, possibly a result of their adaptation stunting on F. virginiana clones (‘UC-10’ criniviruses. Both molecular and immu- to a diversity of hosts (38). This genetic and ‘UC-11’); whereas F. vesca plants nological detection tests for SPaV have diversity makes detection based on RT- remain asymptomatic. Pallidosis may also been developed, but the low titer of the PCR a challenging task, as oligonucleotide cause root and runner reduction (10). An- virus, especially during summer, makes primers may not detect all strains. Antisera ecdotally, the major effect on strawberry antibody-based detection unreliable. Labo- are available for each of these viruses, and production is due to the synergistic effects ratory detection by RT-PCR correlates well detection by ELISA is possible, but again of the pallidosis agent(s) with other straw- with symptom development in indicator strain diversity can be a problem with this berry viruses. Symptoms are masked dur- plants. assay. ing the summer months unless plants are Beet pseudo-yellows virus (BPYV). The use of methyl bromide and other heavily shaded. Tzanetakis et al. (93) tested 38 strawberry soil fumigants in most strawberry produc- Pallidosis was considered a rarity until a plants that were pallidosis positive by ing areas has reduced the importance of survey in Maryland, USA, demonstrated grafting for the identification of the the nematode-borne viruses in strawberry. that the disease was the most widespread agent(s). All but one of these plants tested However, the restrictions on methyl bro- of the graft-transmittable strawberry dis- positive for SPaV by RT-PCR. DsRNA mide and pressure to reduce use of other eases in that state, with more than 70% of cloned from this single plant negative for chemical fumigants may result in a re- the plants tested being infected with the SPaV revealed that it was infected with emergence of these diseases in the future. causal agent(s) (48). BPYV. BPYV, a crinivirus like SPaV, has Because the vectors of these viruses have

Plant Disease / April 2006 389 been controlled, the diseases they cause recently, SLRSV was thought to be primar- the former USSR (58). Most cultivars do have been very rare since 1975. As a re- ily a European virus. However, it was iden- not exhibit symptoms when infected only sult, the reaction of strawberry cultivars tified recently in strawberry in California with ArMV; however, in some cultivars grown today to these viruses is largely in the United States and in British Colum- ArMV infection can cause a chlorotic leaf unknown. This brief review will focus on bia, Canada, and in mint samples from mottle and mild to severe stunting or death the data obtained recently on nematode Nebraska, Ohio, and Maryland in the of plants in the field. In the United King- transmitted viruses. Extended reviews of United States (49,66). Strawberry plants in dom, ArMV and SLRSV are commonly the biological properties of the viruses in the United States that were infected with found in mixed infections where they oc- strawberry can be found elsewhere (8). SLRSV were either symptomless, or when cur due to their common vector, although Tomato ringspot virus (ToRSV). symptomatic, were infected with at least ArMV has not been observed in strawberry ToRSV was first identified in F. chiloensis one additional virus. SLRSV has been plants infected with SLRSV in the United along the California coast in 1961 (21). reported in North America previously, but States (I. E. Tzanetakis and R. R. Martin, The virus has a host range that includes there was no evidence that it had estab- unpublished data). Most F. vesca indicator plants in 35 families of both dicotyledo- lished or become widespread (2). clones are symptomless when infected nous and monocotyledonous plants (83). It SLRSV has a host range that exceeds with ArMV. can be a serious problem in raspberry pro- 125 plant species belonging to 27 families ArMV is a member of subgroup A of the duction in the Pacific Northwest of the of both monocots and dicots, and it is Nepovirus genus and is transmitted in na- United States, but has not been a serious transmitted by nematodes of the genus ture mainly by Xiphinema diversicauda- problem in strawberry, although it has Xiphinema (60). SLRSV is listed as a tum, although there are reports of other been reported in strawberry (7). This may member of the genus Sadwavirus (51); Xiphinema species that can transmit the be due to several factors, such as the short however, the taxonomic status of this virus virus (90). The efficiency of transmission period of time that strawberry plants are in is in flux and may change in the near fu- by the vectors is highly strain-dependent the field combined with the use of soil ture now that the complete sequence has (4). The complete nucleotide sequence of fumigants (68). In some cultivars, such as been determined (102). Phylogenetic ArMV (105,106) confirmed the close rela- ‘Olympus’ or ‘Puget Beauty’, ToRSV in- analysis of the RNA-dependent RNA po- tionship of ArMV with Grapevine fanleaf fection can have a dramatic effect on plant lymerase and helicase motifs indicate that virus (GFLV), another member of sub- growth and yield, although this is not SLRSV is closely related to Apple spheri- group A. common. ToRSV causes severe necrosis in cal latent virus and Cherry rasp leaf virus, Raspberry ringspot virus (RpRSV). F. virginiana clones ‘UC-10’ or ‘UC-11’ members of the Cheravirus genus; RpRSV was first identified in the 1950s as that can result in death of the plant. In F. whereas analysis of the coat protein se- the putative causal agent of the raspberry vesca, the symptoms are generally a mild quence shows it is also related to the Sad- leaf curl disease (6). The virus has been mosaic and sometimes a reddish discolora- wavirus genus and the Comoviridae fam- found throughout Europe but in strawberry tion of the young petioles and leaves, al- ily. Unlike the nepoviruses, which encode has been found only in the United King- though symptoms are not distinctive and a single coat protein, SLRSV has two coat dom and the former USSR (61). The F. fluctuate depending on environmental proteins, a feature found in the Sadwavirus vesca indicator clones initially show a conditions. genus. It is likely that the status of the yellow blotching, but the symptoms fade. The genome of ToRSV is typical of viruses in the Sequiviridae family will In some strawberry cultivars, leaves de- nepoviruses and picorna-like plant viruses. change as more sequence information velop yellow blotching, ring spots, crin- The genome is divided between two becomes available. kling, stunting, and eventually plants may monocistronic genomic RNA molecules Because of the previous quarantine die. The symptoms on susceptible cultivars that encode polyproteins that are processed status of SLRSV, detection of the virus include chlorosis, blotches, and crinkling, to mature proteins by a cysteine protease was not included in virus surveys until while in the second season, plant recovery encoded by RNA 1 (70). As in the case of recently. The wide host range of the virus may be observed. all nepoviruses, the 5′ ends have a ge- and its wide geographical distribution in RpRSV also belongs to subgroup A of nome-linked virus protein (VPg), while mint in the United States suggest it should the Nepovirus genus and is transmitted by ToRSV has a very long untranslated region be included in strawberry certification members of the genus Longidorus, at the 3′ terminus of the genomic mole- programs and possibly in other vegeta- whereas there is a report of RpRSV trans- cules ending with a poly adenosine tail. tively propagated crop certification pro- mission by members of the genera RNA 2 encodes the movement and coat grams. On the other hand, the ornamental Paratrichodorus and Xiphinema (90). proteins of the virus (71). The virus be- mint that was found infected with SLRSV RpRSV infects dicotyledonous and mono- longs to subgroup C of the Nepovirus ge- is widely distributed and probably has cotyledonous plants belonging to 14 fami- nus and is transmitted by Xiphinema spp. been in the ornamental trade in the United lies (61). The virus sequence (13) reveals ToRSV can be detected serologically with States for many years. Alternate vectors for shared characteristics with members of the ELISA and by RT-PCR; however, there are SLRSV should be further investigated, subgroup GFLV and Tobacco ringspot significant strain differences, and one must based on its unusual sequence compared virus as well as the comovirus Cowpea take care to ensure that an appropriate test with the nepoviruses. SLRSV also can be severe mosaic virus; this indicates the is used. The virus can also be easily de- pollen and seed-borne, thus care should be uniqueness of the virus and a possible tected by mechanical transmission to taken by strawberry breeders that the virus insight into the evolution of the Comoviri- Chenopodium quinoa and Nicotiana cleve- is not introduced into their programs via dae. landii, which avoids the potential problem germ plasm. Tomato black ring virus (TBRV). of strain variation in detection. Arabis mosaic virus (ArMV). ArMV TBRV was identified in 1946 (59) and is Strawberry latent ringspot virus was first described in the 1940s (79). It widespread in Europe. In Europe, the virus (SLRSV). SLRSV often is found in asso- infects almost 100 plant species belonging is often found together with RpRSV be- ciation with Arabis mosaic virus (ArMV) to more than 28 families, causing signifi- cause they are both vectored by the nema- in Europe, where both viruses are transmit- cant losses in many crops (58). The virus tode Longidorus elongatus, although ted by the same nematode vector, Xiphi- was reported to be widespread in straw- TBRV tends to spread more slowly in the nema diversicaudatum (5). The symptoms berry prior to the introduction of chemical field than RpRSV, possibly reflecting dif- on strawberry plants are unknown because control of the nematode vector. It has also ferences in efficiency of transmission. plants showing symptoms in field situa- been reported to occur in strawberry in Symptoms in F. vesca indicator clones tions also were infected with ArMV. Until Germany, Hungary, Ireland, Poland, and may vary from being asymptomatic to leaf

390 Plant Disease / Vol. 90 No. 4 blotching. Symptoms often diminish after once the virus is established. detected in hundreds of samples tested in the first season, as in the case of RpRSV. Strawberry necrotic shock virus 2004. This difference is unexplained at this Symptoms in strawberry cultivars are simi- (SNSV). SNSV was first identified in the time. The complete nucleotide sequence of lar to those caused by RpRSV. 1950s (19) and was named after the symp- FClLV has been determined (98), revealing TBRV belongs to subgroup B of the toms observed on F. vesca clones when unique features in the genome organization Nepovirus genus. The host range of the grafted with infected material. Grafted of the virus. Some ilarviruses encode a virus is as wide as those of the other nema- plants develop symptoms 6 to 14 days after gene involved in suppression of RNA inter- tode-transmitted viruses. The complete grafting, and some isolates cause a severe ference or gene silencing in RNA 2. FClLV nucleotide sequence of the virus has been necrotic reaction in newly formed leaves. lacks the suppressor of gene silencing but determined and confirms a close relation- After the initial severe reaction that devel- has an open reading frame in RNA 2 that ship of TBRV with Grapevine chrome ops on 1 to 3 young leaves, the subsequent shares homology to eukaryotic receptors, mosaic virus and Cycas necrotic stunt leaves appear normal, and no further whose function in this virus is unknown. virus (39). symptoms develop. SNSV is seed- FClLV also has an open reading frame transmitted up to 35%. The virus can have downstream from the coat protein gene in Oomycete-Transmitted Virus a significant impact on strawberry produc- RNA 3 that is not present in any other Tobacco necrosis virus (TNV). The tion, reducing yield by up to 15% and ilarviruses that have been sequenced. Phy- symptoms of TNV that are usually ob- runner production by up to 75% (36). logenetic analysis places FClLV with served on strawberry indicator plants are Early studies indicated that SNSV, which Prune dwarf virus in subgroup 4 of the similar to those caused by SMYE and also infected Rubus species, was a strain of genus and also reveals a close relationship SPMYE viruses. TNV has been associated Tobacco streak virus (TSV) (40), the type with Prunus necrotic ringspot virus, Apple with dwarfing and leaf and root necrosis in member of the Ilarvirus genus (84). How- mosaic virus, and Alfalfa mosaic virus. indicator clones and commercial cultivars ever, several lines of evidence indicated Apple mosaic virus (ApMV). Straw- (14). Fránová-Honetšlegrová et al. (14,15) that strains from Fragaria and Rubus dif- berry leaf roll disease has been reported in have verified that TNV strain D is able to fered from the type strain of TSV. In im- northeastern North America and Kazakh- replicate in strawberry, while there is no munodiffusion tests, SNSV formed spurs stan (3). In F. virginiana, symptoms in- information on the pathogenicity of TNV with antisera developed against other TSV clude a peacock pattern on the leaves, strain A in strawberry. Information on the strains (24), an indication of differences in whereas a downward rolling is observed incidence of the virus in commercial fields the epitopes between the strains. In addi- on some F. ve sca indicators (Fig. 4). The is limited (81), because detection is prob- tion, SNSV isolates failed to cross-protect only isolate of strawberry leaf roll cur- lematic due to low titer of the virus in the plants from other strains of TSV (26), and rently known is maintained at the National aboveground tissues (R. R. Martin, per- there was no cross-hybridization between Clonal Germplasm Repository in Corval- sonal observation). strawberry and blackberry isolates and lis, OR, and it was used in an attempt to TNV belongs to the genus Necrovirus of non-small-fruit strains of TSV in Northern characterize the strawberry leaf roll dis- the family Tombusviridae, and is transmit- blot analysis (85). ease. This plant exhibited the peacock ted by the oomycete Olpidium brassicae Several attempts to use RT-PCR for de- pattern on the leaves (Fig. 5). After cloning (34). In the past, TNV was considered a tection of TSV in small fruit crops were and sequencing dsRNA extracted from this single species with diverse isolates, but unsuccessful using primers developed source, it was found to be infected with sequence data suggest that there are at against the type isolate of TSV. An isolate three viruses, one of which was ApMV. least two individual TNV species from strawberry was cloned and se- This is the first report of this virus natu- (53,55,114). TNV has icosahedral virions quenced, and analysis of RNA 3 and part rally infecting strawberry (99). The other that are 26 nm in diameter and encapsidate of RNA 2 revealed about 70% nucleotide two viruses identified in this plant were the the monopartite single-stranded positive- sequence identity with TSV (95). This criniviruses SPaV and BPYV. ApMV is a sense genomic RNA. A satellite RNA often indicated that the strawberry ilarvirus be- typical Ilarvirus (77,78) and belongs to is associated with the viruses and results in longed to a different species, distinct from subgroup 3 of the genus. The virus has a a dramatic change in symptoms. TNV is TSV. The coat protein gene from 15 broad host range that exceeds 65 species in persistent in the soil and has a wide host “TSV” isolates from Fragaria and Rubus 19 families (25) and has many diverse range. The virus can be detected by ELISA were sequenced, and analysis indicated strains (11,64). ApMV is one of several and RT-PCR, but due to strain variation, it that all clustered with the strawberry iso- viruses that have been transmitted experi- is important to carry out sap transmission late that was sequenced, which was then mentally to strawberry from tree fruits (23). tests to Chenopodium quinoa to avoid false given its original historic name, SNSV. The association of the virus with symp- negatives with the laboratory-based assays. None of the strawberry and Rubus plants tom development is under examination were found infected with TSV (95), an because the plant infected with leaf roll Viruses with Unknown Vectors indication that TSV may not be a pathogen was also infected with the two criniviruses Ilarviruses. Three ilarviruses are known of Fragaria or Rubus species. associated with pallidosis disease. The lack to infect strawberry: Strawberry necrotic Fragaria chiloensis latent virus of testing for ApMV during virus surveys shock virus, (SNSV), Fragaria chiloensis (FClLV). FClLV was identified in F. means the distribution and impact of this latent virus (FClLV), and Apple mosaic chiloensis plants that originated in Chile virus in strawberry production areas are virus (ApMV). Ilarviruses comprise the (82). F. chiloensis is found along the west unknown. Future testing for ApMV will be largest genus of the Bromoviridae family coast of the Americas except for the trop- included in virus surveys of declining and are positive-sense RNA viruses with ics. Graft indexing for detection of FClLV strawberry plants to determine its inci- tripartite genomes (73). They can be is problematic because it remains symp- dence and impact. transmitted via pollen to maternal tissue tomless in F. chiloensis and strawberry (horizontal transmission, spread within a cultivars, and only causes mild symptoms Unclassified Viruses field or within a generation) and through when grafted onto F. vesca ‘UC-4’. It can of Strawberry seed (vertical transmission, spread from be sap transmitted to Chenopodium quinoa Fragaria chiloensis cryptic virus one generation to the next). Thrips have and Cucumis sativus. (FClCV). During the molecular charac- been reported to transmit some of the ilar- Molecular and immunological tests have terization of FClLV, several cDNA clones viruses (75). Since these viruses can be been developed, and the presence of the corresponding to a novel virus with ho- pollen-transmitted, there is not an effective virus was confirmed along the west coast mology to cryptic viruses and also to plant way to prevent movement within a field of North America in 2003 (92) but was not dsRNA polymerases were identified (100).

Plant Disease / April 2006 391 only part of a crown or only on some crowns in a plant with multiple crowns. When grafted onto F. virginiana, symp- toms typical of pallidosis were observed. As far as we are aware, no known refer- ence isolates of this disease are available for development of laboratory tests or characterization of the pathogen. The pos- sibility of a mixed virus infection of sev- eral of the viruses described above causing the disease seems remote, due to the long incubation time that may be required for symptom development in indicator plants and the unique combination of symptoms. Strawberry decline. Since 2000, straw- berry decline disease has been increasing in the Pacific Northwest (PNW), including British Columbia, Washington, and Ore- gon, and also in California. All cultivars can develop symptoms of the disease. Pre- viously, cultivars in the PNW, such as ‘To- tem’ and ‘Puget Reliance’, did not develop symptoms due to virus infections in the field. Analysis of declining plants in this area showed that SCV was present in the Fig. 5. Fragaria chiloensis near Contulmo, Chile, naturally infected with Strawberry symptomatic plants in addition to SMYEV, crinkle virus, Strawberry mottle virus, Strawberry mild yellow edge virus, and Straw- SMoV, and SVBV. In the past, only the berry vein banding virus. latter three viruses were observed in north- ern Washington and British Columbia. A large portion of the RNA polymerase of Clonal Germplasm Repository in Corval- Aphid populations were generally very this novel virus, designated Fragaria lis, and dsRNA was extracted and cloned. high in this area either due to lack of con- chiloensis cryptic virus (FClCV), has been The virus, now designated Strawberry trol efforts, or because aphid control had sequenced, and an RT-PCR detection test latent virus (StLV), may be a link between become ineffective due to development of has been developed. In order to minimize plant and insect viruses (101). The genome resistance to the aphicides that had been the possibility that the dsRNA molecule is organization of StLV appears similar to used for many years. No whiteflies were encoded by the plant genome, multiple members of the Cripavirus genus, Dicis- observed in the strawberry fields in PNW, DNA extractions from plants that tested troviridae family. The members of the and the incidence of BPYV and SPaV was positive for FClCV were carried out and family are devastating insect pathogens less than 5% (92). tested by PCR without a reverse transcrip- with single-stranded, positive-sense RNA In California, where strawberries are tion step. In all cases, no amplicons were genomes that consist of two open reading grown as an annual crop, symptoms of obtain in PCR, while the cryptic virus was frames encoding the viral replicase and decline are generally rare. However, in readily detectable after RT-PCR using coat proteins of the virus. 2002 and 2003, decline symptoms were either total RNA or dsRNA preparations The virus can be purified from straw- common in strawberry fruit production (100). A band of ~1.8 kbp was extracted berry, which proves that it replicates in the fields in California. Declining strawberry from the dsRNA gels and was both cloned plant and that it is a plant virus rather than plants from California were almost always and subjected to RT-PCR. Both tests con- an insect virus found in a plant. The com- infected with one of the whitefly- firmed that this band belonged to this cryp- plete sequence of the virus will determine transmitted criniviruses plus one or more tic virus. More than 20 FClLV-free F. if the virus encodes a movement protein or of the aphid-borne viruses. The prelimi- chiloensis plants were tested for FClCV, if it is translocated in the plant in a manner nary testing done on strawberry plants and several tested positive for the virus, similar to that of other cryptic viruses. A suggests that the whitefly-transmitted vi- indicating that FClLV is not needed for detection protocol for the virus has been ruses are an important component in the replication of this cryptic virus (100). developed, while future plans include stud- decline observed in California, in contrast Strawberry latent virus (StLV). Be- ies on the effect of the virus when found in to the PNW where the aphid-borne viruses fore the identification of SMEYV as the complexes with other strawberry viruses. are primarily responsible. The virus test causal agent of the SMYE disease (43), a Strawberry feather-leaf disease. results are in agreement with observations luteovirus was thought to be associated Strawberry feather-leaf disease was first on vector abundance in strawberry fields in with the disease. Many attempts were reported in Arkansas in 1970, and has the two locations. In California, whiteflies made to isolate and characterize that virus. since been detected in a few plants from were very common on strawberries in Martin and Converse (47) purified a Maryland, Michigan, and Missouri (52). production fields in the south and central spherical virus of 25 nm diameter from No information on the natural transmission coast areas, with several whiteflies com- SMYE diseased plants, but they also iden- of the pathogen is available, but it was monly observed on each leaflet (Fig. 6). tified this virus in SMYE-free plants, in- reported that 1 to 9 months were required Aphids also were present in these areas, cluding several F. vesca seedlings. They for symptom development in indicator but at much lower numbers than observed named the agent ‘cryptic’ virus, because it plants. In F. vesca, symptoms include in the PNW. caused no obvious symptoms on cultivars feather-leaf symptoms that include dwarf- In a visit to Chile in 2004, decline or indicators. ing, narrowed strap-like and somewhat symptoms were observed on F. chiloensis In the effort to develop detection proto- rugose leaf deformations with deeply ser- grown for commercial fruit production cols for all strawberry viruses and graft- rated margins and leaflets that may be near Contulmo, Chile (Fig. 5). Upon test- transmittable diseases, a plant used in the fused at the base. Symptoms may be obvi- ing for viruses, it was found that these previous study was obtained from National ous to obscure and often are exhibited on plants were infected with SCV, SMoV,

392 Plant Disease / Vol. 90 No. 4 SMYEV, and SVBV, but not with SPaV or BPYV. The symptoms were similar to those observed in F. × ananassa cultivars in the PNW that were infected with these four viruses (Fig. 2). Conclusions Over the past 50 years, breeders have been effective at selecting for virus toler- ance in commercial strawberry cultivars, and as a result, very few cultivars grown today exhibit symptoms when infected with a single virus. Due to high aphid numbers and virus spread, cultivars that have become important in the PNW are tolerant to infection with multiple aphid- transmitted viruses. The only exception to this is the cultivar ‘Hood’, which com- mands a premium price for its use in the “high end” ice cream market, and is grown despite its sensitivity to virus infection and requirement for stringent aphid control. Selection for improved virus tolerance will become a priority for breeders as virus complexes become more common in the future due to reduced pesticide use, in- Fig. 6. Strawberry near Watsonville, CA, with greenhouse whiteflies on the under sur- creased resistance to insecticides by vec- face of a leaf. Whiteflies have only recently become important pests of strawberry in California. tors, and increased demand for organically grown fruit. Resistance to aphid- and whitefly-transmitted viruses in strawberry the high infection rates with BPYV and sweet cherry growing in Ontario. Phytopa- has not been reported in the Fragaria germ SPaV. thology 60:1262-1265. 3. Berkeley, G. H., and Plakidas, A. G. 1942. plasm used by breeders, which suggests With the recent advances in virus detec- Strawberry leaf roll, a new disease. Phytopa- that breeding for resistance in not an im- tion, it is now possible to quickly identify thology 32:631-633. mediate option. However, the use of ge- viruses in field plants, whether in single or 4. Brown, D. J. F. 1986. The transmission of netic engineering to produce virus resistant multiple infections. These newly devel- two strains of Arabis mosaic virus by popula- strawberry cultivars should be quite oped tests are being adopted in the certifi- tions of Xiphinema diversicaudatum (Nema- toda: Dorylaimoidea) from ten countries. straightforward. cation programs in the United States. In Rev. Nematol. 9:83-87. Strawberries are vegetatively propa- addition, these technologies are being used 5. Brown, D. J. F., and Trudgill, D. L. 1983. gated, and in most cases, the increase from to monitor nurseries at each stage of mul- Differential transmissibility of arabis mosaic nuclear stock to certified plants that are tiplication to determine if and when vi- and strains of strawberry latent ringspot vi- sold for fruit production takes place in the ruses might be introduced into the plant ruses by three populations of Xiphinema di- versicaudatum (Nematoda: Dorylaimoidea) field, where there is potential for reintro- production scheme. Visual inspection is from Scotland, Italy and France. Rev. Nema- duction of viruses. In the past, efforts dur- very inefficient in nurseries since most of tol. 6:229-238. ing plant production have concentrated on the strawberry viruses do not cause any 6. Cadman, C. H. 1956. Studies on the etiology controlling nematode and aphid vectors. symptoms when they occur in single infec- and mode of spread of Scottish raspberry leaf The nematodes have been controlled effi- tions. Additionally, a coordinated effort is curl disease. J. Hortic. Sci. 31:111-118. 7. Converse, R. H. 1981. Infection of cultivated ciently with methyl bromide and other soil underway to validate the molecular tests strawberries by Tomato ringspot virus. Phy- fumigants, and aphids through the use of that are now available for the detection of topathology 71:1149-1152. insecticides, although development of viruses in strawberries. The tests are being 8. Converse, R. H. 1987. Virus and viruslike resistance to the chemical insecticides has used in several laboratories to determine if diseases of Fragaria (Strawberry). Pages 1- been a problem. With the discovery of they will detect a broad range of virus 100 in: Virus Diseases of Small Fruits. R. H. Converse, ed. U.S. Dep. Agric. Agric. Res. whitefly-transmitted viruses that infect isolates. The development of specific RT- Serv. Agric. Handb. No. 631. strawberry, attention must now be directed PCR tests for almost all of the known 9. Converse, R. H. 1992. Modern approaches to toward the control of whiteflies. The strawberry viruses allows for a re- strawberry virus research. Acta Hortic. greenhouse whitefly has a very broad host evaluation of severe and mild strains re- 308:19-30. range and recently has become naturalized ported in the literature for many of the 10. Converse, R. H., and Volk, E. 1990. Some effects of pallidosis disease on strawberry in the strawberry growing areas of Califor- strawberry viruses, to determine whether growth under greenhouse conditions. Plant nia and the southern United States (107). severe strains are actually mixed infections Dis. 74:814-816. During the 2002 and 2003 growing sea- that were not separated by aphid transmis- 11. Crowle, D. R., Pethybridge, S. J., Leggett, G. sons, incidences of plant infections with sion studies. W., Sherriff, L. J., and Wilson, C. R. 2003. SPaV and BPYV infection reached as high Diversity of the coat protein-coding region among Ilarvirus isolates infecting hop in Aus- as 90% in southern California strawberry Literature Cited tralia. Plant Pathol. 52:655-662. fields, and over 70% in the Watsonville 12. Dale, A., and Luby, J. J., eds. 1990. The area along the central coast of California. 1. Ahrens, U., and Seemüller, E. 1992. Detec- Strawberry into the 21st Century. Timber In mixed infections with several of the tion of DNA of plant pathogenic mycoplas- Press, Portland, OR. aphid-borne viruses, whitefly-transmitted malike organisms by a polymerase chain re- 13. Ebel, R., Schnabel, A., Reustle, G. M., action that amplifies a sequence of the 16S Krczal, G., and Wetzel, T. 2003. Complete viruses caused a serious decline (92) (Fig. rRNA gene. Phytopathology 82:828-832. nucleotide sequence of an isolate of the 1). In field visits in 2003, it was noted that 2. Allen, W. R., Davidson, T. R., and Briscoe, nepovirus raspberry ringspot virus from whiteflies were present on most strawberry M. R. 1970. Properties of a strain of Straw- grapevine. Virus Res. 97:141-144. leaflets (Fig. 6), and this is consistent with berry latent ringspot virus isolated from 14. Fránová-Honetšlegrová, J., Erbenova, M., and

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Heflebower, R. F., and Rouse, R. 2001. Sur- clonal antibodies specific for strawberry mild 29. Harrison, N. A., Legard, D. E., DiBonito, R., vey of strawberry viruses occurring in com- yellow edge potexvirus. Acta Hortic. 385:39- and Richardson, P. A. 1997. Detection and mercial plantings in the state of Maryland, 45. differentiation of phytoplasmas associated USA. Acta Hortic. 551:71-74. 70. Rott, M. E., Gilchrist, A., Lee, L., and Ro- with diseases of strawberry in Florida. Plant 49. Martin, R. R., Tzanetakis, I. E., Barnes, J. E., chon, D. 1995. Nucleotide sequence of to- Dis. 81:230. and Elmhirst, J. F. 2004. First report of mato ringspot virus RNA 1. J. Gen. Virol. 30. Hartono, S., Tomohide, N., Genda, Y., and Strawberry latent ringspot virus in strawberry 76:465-473. Okuda, S. 2003. Nucleotide sequence and in the United States and Canada. Plant Dis. 71. Rott, M. E., Tremaine, J. H., and Rochon, D. genome organization of Cucumber yellows 88:575. M. 1991. Nucleotide sequence of tomato virus, a member of the genus Crinivirus. J 50. Martin, R. R., Tzanetakis, I. E., Gergerich, ringspot virus RNA 2. J. Gen. Virol. 72:1505- Gen. Virol. 84:1007-1012. R., Fernandez, G., and Pesic, Z. 2004. Black- 1514. 31. Hepp, R. F., and Martin, R. R. 1992. Occur- berry yellow vein associated virus: A new 72. Rubio, L., Soong, J., Kao, J., and Falk, B. W. rence of strawberry mild yellow-edge associ- crinivirus found in blackberry. Acta Hortic. 1999. Geographic distribution and molecular ated virus in wild Fragaria chiloensis in 656:137-142. variation of isolates of three whitefly-borne South America. Acta Hortic. 308:57-59. 51. Mayo, M. A. 2005. Changes to virus taxon- closteroviruses of cucurbits: Lettuce infec- 32. Horn, N. L., and Carver, R. G. 1962. Effects omy. Arch. Virol. 150:189-198. tious yellows virus, cucurbit yellow stunting of three viruses in plant production and yields 52. McGrew, J. R. 1970. Strawberry feather-leaf. disorder virus, and beet pseudo-yellows virus. of strawberries. Plant Dis. Rep. 46:762-765. Pages 46-47 in: Virus Diseases of Small Fruit Phytopathology 89:707-711. 33. Horne, W. T. 1922. Strawberry troubles. and Grapevines. N. W. Frazier, ed. Univ. 73. Schneider, W. L., and Allison, R. F. 1995. Calif. Agric. Exp. Stn. Rep. 1921-22:122- Calif. Div. Agric. Sci., Berkeley. The Bromoviruses: Biochemistry, Patho- 123. 53. Meulewaeter, F., Seurinck, J., and Van Em- genicity, Replication and Recombination. 34. Hull, R. 2002. Matthew’s Plant Virology, 4th melo, J. 1990. Genome structure of tobacco Pages 143-155 in: Pathogenesis and Host ed. Academic Press, New York. necrosis virus strain A. Virology 177:699- Specificity in Plant Disease. Vol. III: Viruses 35. Jelkmann, W., Maiss, E., and Martin, R. R. 709. and Viroids. R. P. Singh, U. S. Singh, and K. 1992. The nucleotide sequence and genome 54. Milkus, B. N. 2001. Incidence of four nepovi- Kohmoto, eds. Elsevier Science Inc., New organization of strawberry mild yellow edge- ruses in Missouri vineyards. Am. J. Enol. York. associated potexvirus. J. Gen. Virol. 73:457- Vitic. 52:56-57. 74. Schoen, C. D., Limpens, W., Moller, I., Gro- 479. 55. Molnar, A., Havelda, Z., Dalmay, T., eneveld, L., Klerks, M. M., and Lindner, J. L. 36. Johnson, H. A., Jr., Converse, R. H., Amorao, Szutorisz, H., and Burgyan, J. 1997. Com- 2004. The complete genomic sequence of A., Espejo, J. I., and Frazier, N. W. 1984. plete nucleotide sequence of tobacco necrosis Strawberry crinkle virus, a member of the Seed transmission of Tobacco streak virus in virus strain DH and genes required for RNA Rhabdoviridae. Acta Hortic. 656:45-50. strawberry. Plant Dis. 68:390-392. replication and virus movement. J. Gen. Vi- 75. Sdoodee, R., and Teakle, D. S. 1987. Trans- 37. Jomantiene, R., Davis, R. E., Maas, J., and rol. 78:1235-1239. mission of Tobacco streak virus by Thrips Dally, E. 1998. Classification of new phyto- 56. Mráz, I., Petrzik, K., Šip, M., and Fránová- tabaci: A new method of plant virus transmis- plasmas associated with diseases of straw- Honetšlegrová, J. 1998. Variability in coat sion. Plant Pathol. 36:377-380. berry in Florida based on analysis of 16S protein sequence homology among American 76. Segundo, E., Martin, G., Cuadrado, I. M., and

394 Plant Disease / Vol. 90 No. 4 Janssen, D. 2004. A new yellowing disease in the strawberry pallidosis disease. Acta Hortic. families: Nucleotide sequence and evolution Phaseolus vulgaris associated with a white- 656:21-26. of Strawberry latent ringspot virus. Virus fly-transmitted virus. Plant Pathol. 53:517. 95. Tzanetakis, I. E., Mackey, I. C., and Martin Res. In press. 77. Shiel, P. J., Alrefai, R. H., Domier, L. L., R. R. 2004. Strawberry necrotic shock virus 103. Tzanetakis, I. E., Reed, J., and Martin, R. R. Korban, S. S., and Berger, P. H. 1995. The is a distinct virus and not a strain of Tobacco 2005. Nucleotide sequence, genome organi- complete nucleotide sequence of apple mo- streak virus. Arch. Virol. 149:2001-2011. zation and phylogenetic analysis of Straw- saic virus RNA-3. Arch. Virol. 140:1247- 96. Tzanetakis, I. E., and Martin, R. R. 2004. berry pallidosis associated virus, a new mem- 1256. Complete nucleotide sequence of a straw- ber of the genus Crinivirus. Arch. Virol. 78. Shiel, P. J., and Berger, P. H. 2000. The com- berry isolate of Beet pseudo-yellows virus. 150:273-286. plete nucleotide sequence of apple mosaic vi- Virus Genes 28:239-246. 104. Tzanetakis, I. E., Wintermantel, W. M., and rus (ApMV) RNA 1 and RNA 2: ApMV is 97. Tzanetakis, I. E., and Martin, R. R. 2004. Martin, R. R. 2003. First report of Beet more closely related to alfalfa mosaic virus First report of Beet pseudo yellows virus in pseudo yellows virus in strawberry in the than to other Ilarviruses. J. Gen. Virol. blackberry in the United States. Plant Dis. United States: A second crinivirus able to 81:273-278. 88:223. cause pallidosis disease. Plant Dis. 87:1398. 79. Smith, K. M., and Markham, R. 1944. Two 98. Tzanetakis, I. E., and Martin, R. R. 2005. 105. Wetzel, T., Beck, A., Wegener, U., and new viruses affecting tobacco and other New features of the genus Ilarvirus revealed Krczal, G. 2004. Complete nucleotide se- plants. Phytopathology 34:324-329. by the nucleotide sequence of Fragaria quence of the RNA 1 of a grapevine isolate of 80. Spiegel, S. 1987. Double-stranded RNA in chiloensis latent virus. Virus Res. 112:32-37. Arabis mosaic virus. Arch. Virol. 149:989- strawberry plants infected with strawberry 99. Tzanetakis, I. E., and Martin, R. R. 2005. 995. mild yellow-edge virus. Phytopathology First report of strawberry as a natural host of 106. Wetzel, T., Meunier, L., Jaeger, U., Reustle, 77:1492-1494. Apple mosaic virus. Plant Dis. 89:431. G. M., and Krczal, G. 2001. Complete nu- 81. Spiegel, S., and Martin, R. R. 1998. Virus and 100. Tzanetakis, I. E., and Martin, R. R. 2005. cleotide sequences of the RNAs 2 of German viruslike diseases. Pages 62-72 in: Compen- Fragaria chiloensis cryptic virus: A new isolates of grapevine fanleaf and Arabis mo- dium of Strawberry Diseases. J. L. Maas, ed. strawberry virus found in Fragaria chiloensis saic nepoviruses. Virus Res. 75:139-145. American Phytopathological Society, St. plants from Chile. Plant Dis. 89:1241. 107. Wintermantel, W. M. 2004. Emergence of Paul, MN. 101. Tzanetakis, I. E., and Martin, R. R. 2005. greenhouse whitefly (Trialeurodes vaporari- 82. Spiegel, S., Martin, R. R., Leggett, F., ter Strawberry latent virus: A potential link be- orum) transmitted Criniviruses as threats to Borg, M., and Postman, J. 1993. Characteri- tween plant and insect viruses. (Abstr.) Phy- vegetable and fruit production in North zation and geographical distribution of a new topathology 95:S105. America. APSnet feature article, June 2004. ilarvirus from Fragaria chiloensis. Phytopa- 102. Tzanetakis, I. E., Postman, J. D., Gergerich, Online publication. thology 83:991-995. R. C., and Martin, R. R. A virus between 108. Wintermantel, W. M. 2004. Pumpkin (Cucur- 83. Stace-Smith, R. 1970. CMI/AAB Descr. bita maxima and C. pepo), a new host of Beet Plant Viruses – Tomato ringspot virus. No. 18. p. 4. 84. Stace-Smith, R., and Frazier, N. W. 1971. Tobacco streak virus isolated from strawberry infected with necrotic shock. Phytopathology 61:757-758. 85. Stenger, D. C., Mullin, R. H., and Morris, T. J. 1987. Characterization and detection of the Strawberry necrotic shock isolate of Tobacco streak virus. Phytopathology 77:1330-1337. 86. Stenger, D. C., Mullin, R. H., and Morris, T. J. 1988. Isolation, molecular cloning, and de- tection of strawberry vein banding virus DNA. Phytopathology 78:154-159. 87. Thompson, J. R., and Jelkmann, W. 2003. The detection and variation of Strawberry mottle virus. Plant Dis. 87:385-390. 88. Thompson, J. R., Leone, G., Lindner, J. L., Jelkmann, W., and Schoen, C. D. 2002. Char- acterization and complete nucleotide se- quence of Strawberry mottle virus: A tenta- tive member of a new family of bipartite Robert R. Martin Ioannis E. Tzanetakis plant picorna-like viruses. J. Gen. Virol. 83:229-239. Dr. Martin is a research plant pa- Dr. Tzanetakis is postdoctorate fellow 89. Thompson, J. R., Wetzel, S., Klerks, M. M., thologist working with viruses and with Dr. Theo Dreher at Oregon State Vašková, D., Schoen, C. D., Špak, J., and virus diseases of small fruit crops at University, where he is studying trans- Jelkmann, W. 2003. Multiplex detection of the USDA-ARS Horticulture Crops lational enhancers of plant positive- four aphid-borne viruses in Fragaria spp. in Research Laboratory in Corvallis, OR, strand RNA viruses. After receiving his combination with a plant mRNA specific in- where he currently serves as research B.S. in soil science and agricultural ternal control. J. Virol. Methods 111:85-95. leader. He received his B.S. in forestry chemistry from the Agricultural Uni- 90. Trudgill, D. L., Brown, D. J. F., and McNa- and Ph.D. in plant pathology from the versity of Athens in Greece, he was a mara, D. G. 1983. Methods and criteria for University of Wisconsin-Madison. Post- visiting scientist at the International assessing the transmission of plant viruses by doctoral experience working with straw- Center of Agricultural Research in the longidorid nematodes. Rev. Nematol. 6:133- berry viruses was at the USDA-ARS in Dry Areas (I.C.A.R.D.A.), working with 141. Corvallis. He then joined the staff at Dr. K. Makkouk. He received his Ph.D. 91. Tzanetakis, I. E. 2004. Molecular characteri- zation of criniviruses and ilarviruses infecting Agriculture Canada in Vancouver, in molecular and cellular biology from strawberry. Ph.D. diss. Oregon State Univer- British Columbia, where he worked on Oregon State University, where he sity, Corvallis. small fruit viruses and Potato leafroll studied the characterization of crini- 92. Tzanetakis, I. E., Bolda, M., and Martin, R. virus. He returned to the USDA-ARS viruses and ilarviruses in strawberry R. 2004. Identification of viruses in declining laboratory in Corvallis in 1995 and in Dr. Martin’s laboratory. He contin- strawberries along the west coast of North continues working on the characteri- ued working on viruses of small fruit America. (Abstr.) Phytopathology 94:S104. zation, detection, and management of crops as a postdoctorate fellow until 93. Tzanetakis, I. E., Halgren, A. B., Keller, K. viruses of small fruit crops. He holds a leaving to complete a year of manda- E., Hokanson, S. C., Maas, J. L., McCarthy, courtesy appointment in the Depart- tory military service in Greece. P. L., and Martin, R. R. 2004. Identification ment of Botany and Plant Pathology, and detection of a virus associated with Oregon State University. strawberry pallidosis disease. Plant Dis. 88:383-390. 94. Tzanetakis, I. E., Halgren, A. B., Winter- mantel, W. M., Keller, K. E., and Martin, R. R. 2004. Two criniviruses are associated with

Plant Disease / April 2006 395 pseudo yellows virus in California. Plant Dis. 236:59-67. of tobacco necrosis virus: The deduced coat 88:82. 112. Yoshikawa, N., Poolpol, P., and Inouye, T. protein sequence has only moderate homol- 109. Wisler, G. C., Duffus, J. E., Liu, H.-Y., and 1986. Use of dot immunoblotting assay for ogy with those of strain A and strain D. Arch. Li, R. H. 1998. Ecology and epidemiology of rapid detection of strawberry pseudo mild Virol. 132:291-305. whitefly-transmitted closteroviruses. Plant yellow-edge virus. Ann. Phytopathol. Soc. 115. Zreik, L., Danet, J. L., Foissac, X., Gandar, Dis. 82:270-279. Japan 52:728-731. J., Verdin, E., Bové, J. M., Garnier, M., and 110. Yoshikawa, N., and Inouye, T. 1986. Purifica- 113. Zeller, S. M., and Vaughan, E. K. 1932. Nourrisseau, J. G. 2001. Marginal chlorosis tion, characterization and serology of straw- Crinkle disease of strawberry. Phytopathol- of strawberry plants can be induced by two berry pseudo mild yellow-edge virus. Ann. ogy 22:709-713. different phloem-restricted bacteria; The Pro- Phytopathol. Soc. Jpn. 52:643-652. 114. Zhang, L., French, R., and Langenberg, W. G. teobacterium “Candidatus Phlomobacter fra- 111. Yoshikawa, N., and Inouye, T. 1988. Straw- 1993. Molecular cloning and sequencing of gariae” and the stolbur phytoplasma. Acta berry viruses occurring in Japan. Acta Hortic. the coat protein gene of a Nebraskan isolate Hortic. 551:101-106.

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