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.