Professional Documents
Culture Documents
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: martinrr@science.oregonstate.edu 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
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.
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.
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-
SPaV. thology 60:1262-1265.
has not been reported in the Fragaria germ
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-
oped tests are being adopted in the certifi- tions of Xiphinema diversicaudatum (Nema-
strawberry cultivars should be quite
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-
ruses might be introduced into the plant ruses by three populations of Xiphinema di-
sold for fruit production takes place in the
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
tions. Additionally, a coordinated effort is curl disease. J. Hortic. Sci. 31:111-118.
The nematodes have been controlled effi-
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-
they will detect a broad range of virus 100 in: Virus Diseases of Small Fruits. R. H.
been a problem. With the discovery of
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.
ported in the literature for many of the 10. Converse, R. H., and Volk, E. 1990. Some
range and recently has become naturalized
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.
Diversity of the coat protein-coding region
SPaV and BPYV infection reached as high
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 Seemller, 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.
malike organisms by a polymerase chain re- 13. Ebel, R., Schnabel, A., Reustle, G. M.,
aphid-borne viruses, whitefly-transmitted 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. Frnov-Honetlegrov, J., Erbenova, M., and