Proc. Fla. State Hort. Soc. 123:156–159. 2010.
Incidence and Spread of Strawberry necrotic shock virus
(SNSV) on Strawberries in Florida
Catalina Moyer, Vance M. Whitaker, and Natalia A. Peres*
University of Florida, IFAS, Gulf Coast Research and Education Center, 14625 CR 672,
Wimauma, FL 33598
Additional index words. Tobacco streak virus (TSV), enzyme-linked immunosorbent assay, ELISA
Strawberry necrotic shock virus (SNSV), formerly considered as a strain of Tobacco streak virus (TSV), is one of the
many viruses reported in strawberries. Viral diseases have not been an issue thus far for strawberries grown in Florida,
probably because most viruses are symptomless on commercial cultivars. However, at the end of the 2008–09 strawberry season, serological tests confirmed the presence of SNSV in research fields at the University of Florida Gulf Coast
Research and Education Center (UF-GCREC) and in some commercial strawberry farms. The presence of SNSV was
investigated during the 2009–10 strawberry season. Seven cultivars from 11 nursery sources were tested for SNSV by
enzyme-linked immunosorbent assay. Leaf samples were collected three times during the season from research plots
at the UF-GCREC and from a grower’s field in the Plant City area. The first sample was taken at the beginning of the
season to determine if plants came infected from the nursery. In both fields, SNSV was identified on ‘Florida Radiance’
originating from nine nurseries. ‘Florida Elyana’ was also virus-positive in the UF-GCREC research plots. To determine
if the virus was spreading throughout the fields, second and third samples were collected at the middle and end of the
season. SNSV was detected on ‘Strawberry Festival’ at the end of the season and additional plants of ‘Florida Radiance’
were also virus-positive, suggesting that the virus had spread somewhat within the fields. During the 2009–10 season,
temperatures were unusually low, which may have prevented a more rapid and extensive spread of SNSV.
Virus diseases are not typically a problem for strawberries grown
in Florida. Most strawberry viruses produce no visible symptoms
in commercially grown cultivars, but reduction of yield and runner production have been reported (Converse, 1987; Johnson et
al., 1984), with the severity of the loss depending on the type
and number of viruses involved (Martin and Tzanetakis, 2006).
Strawberry necrotic shock disease was first reported in strawberries in the 1950s (Jorgensen, 1957), and for many years this
disease was thought to be caused by a strain of Tobacco streak
virus (TSV). Tzanetakis et al. (2004) found that strawberry necrotic
shock disease was caused by a different virus and not by a strain
of TSV. The name Strawberry necrotic shock virus (SNSV) was
then suggested for this virus instead of TSV.
SNSV has been reported in strawberries grown in the U.S.,
Australia, and Israel (Converse, 1987; Spiegel and Cohen, 1985).
In 1998, SNSV was found in the eastern U.S. A virus survey of
commercially grown strawberry plants in Maryland detected
SNSV as well as other viruses. Moreover, plants of the UF cultivar Sweet Charlie shipped from Florida were positive for SNSV
(Hokanson et al., 2000).
SNSV is spread through seed and pollen and by thrips (Johnson et al., 1984; Kaiser et al., 1982). According to Sdoodee and
Teakle (1993), there is a virus-vector-pollen host relationship
in that transmission of SNSV occurs when feeding thrips cause
wounds on plant tissues, allowing the infective pollen grains to
enter and infect.
SNSV has a wide host range, and hosts such as bean, clover,
tomato, and weed species, among others, can serve as sources of
inoculum (Cupertino et al., 1984; Klose et al., 1996). The most
practical way to minimize the risk of infection is to use clean plant
*Corresponding author; phone: (813) 633-4133; email: [email protected]
156
material (i.e., tissue-cultured and virus-tested) and to follow best
management practices for insect and weed control (Biswas et al.,
2007; Martin and Tzanetakis, 2006).
Viral infections of commercial cultivars may not result in visible symptoms; thus detection and diagnosis of viral infections in
strawberries can be achieved by biological assays such as graft
or sap inoculations of strawberry species that exhibit obvious
symptoms (Martin, 2004). When susceptible indicator strawberry plants (Fragaria vesca) are grafted to a host infected with
SNSV, a temporary but severe necrotic reaction may appear in
new leaves. The symptoms then fade and the new growth appears
normal and healthy (Frazier et al., 1962; Martin and Tzanetakis,
2006). Viruses are often detected using serological tests such as
enzyme-linked immunosorbent assay (ELISA) and molecularbased methods such as reverse transcription polymerase chain
reaction (RT-PCR).
At the end of the 2008-09 strawberry season, serological tests
detected SNSV on ‘Strawberry Festival’, ‘Sweet Charlie’, ‘Florida
Radiance’, and ‘Florida Elyana’ grown in UF-GCREC research
plots. During the 2009–10 strawberry season, SNSV was of
particular interest in Florida since the virus had been detected in
nursery stock of the cultivar Florida Radiance. Information was
not available regarding infection of other cultivars used by Florida
growers. Thus, the incidence of SNSV on strawberry cultivars
grown in Florida and the spread of the virus throughout the field
during this season was investigated.
Materials and Methods
Leaf samples from strawberry plants were collected during the
2009–10 strawberry season from November to April. Transplants
were shipped to Florida in late Sept. 2009 from 11 nurseries
Proc. Fla. State Hort. Soc. 123: 2010.
located in the U.S. and Canada. Leaf samples were collected
from strawberry plants at two locations in Florida; UF-GCREC
in Wimauma and at a grower’s field in Dover. Plants in the fields
were selected arbitrarily and marked. For each selected plant, three
young and fully expanded leaflets were collected and pooled to
make a single sample. Plants from seven cultivars were evaluated
at UF-GCREC: ‘Strawberry Festival’, ‘Florida Radiance’, ‘Sweet
Charlie’, ‘Camarosa’, ‘Treasure’, ‘Florida Elyana’, and ‘Camino
Real’. In the grower’s field, ‘Strawberry Festival’, ‘Florida Radiance’, and ‘Treasure’ were tested.
Leaf samples were taken at three separate times throughout
the season. The first set of samples was collected at the beginning
of the season (between November and December) to determine
if plants were already infected upon arrival from the nurseries.
The second sample (between January and February) and third
sample (April) were taken to determine if the virus had spread
throughout the strawberry fields.
A total of 101 plants were sampled from UF-GCREC research
fields across the three time points. After the first sampling, the
number of plants tested for ‘Strawberry Festival’ and ‘Treasure’
was reduced and the number of plants tested for ‘Florida Radiance’
was increased. In the grower’s field, the total number of plants
sampled varied over time (70, 68, and 55 plants, respectively).
At the beginning of the survey, selected plants were marked at
each location. Subsequent samples were taken from previously
marked plants, but when plants were found to be diseased or
dead, a new plant, close to the missing one, was then selected and
marked. For the last sample period, ‘Treasure’ had been removed
from the grower’s field and all samples were missing for that time.
Each sample was tested for SNSV by triple antibody sandwich
enzyme-linked immunosorbent assay (ELISA) (Agdia, Inc.,
Elkhart, IN). ELISA results were evaluated by visual inspection and confirmed by measuring absorbance at 405 nm with an
ELISA plate reader (Multiskan Plus Thermo Fisher Scientific
Inc., Waltham, MA).
Results
At the beginning of the season, ‘Florida Radiance’ at UFGCREC was positive for SNSV in three of the four nursery sources.
Also, ‘Florida Elyana’ was positive from the one nursery source
tested (Table 1). In the grower’s field, ‘Florida Radiance’ was
the only cultivar that was positive for SNSV across all nursery
sources (Table 2).
Table 1. Incidence of Strawberry necrotic shock virus in strawberry plants from eight nurseries and seven cultivars grown at the University of
Florida Gulf Coast Research and Education Center during the 2009–10 strawberry season.
Plants infected/plants sampled
Sample #1
Sample # 2
Sample #3
Cultivar Nursery (19 Nov. 2009)
(28 Jan. 2010)
(8 Apr. 2010)
Strawberry Festival 1
2
3
0/10
0/10
0/8
0/10
0/7
0/8
1/10
1/7
0/8
Florida Radiance
1
4
5
8
5/10 1/4
2/4
0/10
5/10
3/8
3/4
0/10
5/10
5/8
2/4
4/10
Sweet Charlie
6
7
0/10
0/10
0/10
0/10
0/10
0/10
Camarosa
2
0/10
0/10
0/10
Treasure
6
1
0/6
0/3
0/5
0/3
0/5
0/3
Florida Elyana
1
3/4
3/4
3/4
Camino Real
1
0/2
0/2
0/2
Table 2. Incidence of Strawberry necrotic shock virus in strawberry plants from seven nurseries and three cultivars in a grower’s field in Dover,
FL during the 2009–10 strawberry season.
Plants infected / plants sampled
Florida Radiance
Strawberry Festival
Treasure
Sample #1
Sample #2
Sample #3
Sample #1
Sample #2
Sample #3
Sample #1
Sample #2
Nursery
(10 Dec. 2009) (11 Feb. 2010) (8 Apr. 2010) (10 Dec. 2009) (11 Feb. 2010) (8 Apr. 2010) (10 Dec. 2009) (11 Feb. 2010)
1
naz
na
na
0/5
0/5
0/5
0/5
0/5
3
na
na
na
0/5
0/5
0/5
na
na
4
2/15
1/13
2/15
na
na
na
na
na
6
1/5
1/5
1/5
na
na
na
0/5
0/5
8
1/5
0/5
1/5
0/5
0/5
0/5
naz
naz
10
1/5
1/5
4/5
0/5
0/5
0/5
0/5
0/5
11
3/5
3/5
3/5
na
na
na
na
na
na = samples not available from this nursery-cultivar.
z
Proc. Fla. State Hort. Soc. 123: 2010.
157
In January and February, ‘Florida Radiance’ and ‘Florida
Elyana’ from UF-GCREC were still the only cultivars that were
virus-positive and the number of infected plants of ‘Florida
Radiance’ had increased slightly (Table 1). Samples of ‘Florida
Radiance’ were virus-positive in the grower’s field, but the virus
was not detected in one sample that was positive in the first
screen (Table 2).
By the end of the season, SNSV had been detected in three
of the seven cultivars (Tables 3 and 4). The last sampling was
conducted during the first week of April at both locations. SNSV
was confirmed on ‘Florida Radiance’ from all nursery sources and
on ‘Florida Elyana’ from the one source. In addition, ‘Strawberry
Festival’ samples from two nursery sources were virus-positive
in the UF-GCREC research field. Six more ‘Florida Radiance’
samples were virus-positive at this time; however, the presence
of the virus was not detected in one sample that had been positive previously (Table 1). Regardless of cultivar and nursery, the
percentage of virus-positive samples increased from 11 at the
beginning of the season to 20 at the end (Table 3 and 4).
Discussion
In this study, ‘Florida Radiance’ and ‘Florida Elyana’ were
found to be SNSV-positive at the first sampling conducted at the
beginning of the 2009–10 strawberry season. All other cultivars
tested were negative for SNSV. Thus, it is likely that the plants
from both of these cultivars came infected from the nursery. In
the UF-GCREC research fields, ‘Strawberry Festival’ plants in
plots adjacent to ‘Florida Radiance’ tested positive by the end of
the season. In the grower’s field, however, despite the presence
of SNSV from the beginning of the season, the virus was not
detected in other cultivars planted in areas near SNSV-infected
‘Florida Radiance’. This indicates that transmission and infec-
Table 3. Incidence of Strawberry necrotic shock virus-positive plants
on seven cultivars during three sampling periods at the University
of Florida Gulf Coast Research and Education Center during the
2009–10 strawberry season.
Incidence (%)
Sample #1
Sample #2
Sample #3
Cultivar (19 Nov. 2009) (28 Jan. 2010) (8 Apr. 2010)
Strawberry Festival
0
0
8
Florida Radiance
29
34
50
Sweet Charlie
0
0
0
Camarosa
0
0
0
Treasure
0
0
0
Florida Elyana
75
75
75
Camino Real
0
0
0
Table 4. Incidence of Strawberry necrotic shock virus-positive plants on
three cultivars during three sampling periods in a grower’s field in
Dover, FL during the 2009–10 strawberry season.
Incidence (%)
Sample #1
Sample #2
Sample #3
Cultivar (10 Dec. 2009) (2 Feb. 2010) (8 Apr. 2010)
Florida Radiance
23
18
31
Strawberry Festival
0
0
0
Treasure
0
0
ndz
nd = not determined
z
158
tion by SNSV progressed slowly and occurred only when plants
were in very close proximity as was the case at the UF-GCREC
research plots.
SNSV was detected in higher percentage of plants and more
cultivars at the end of 2008–09 than in the 2009–10 strawberry
season at the UF-GCREC research fields (data not shown). The
hypotheses that the plants were also infected in the nurseries in
2008–09 could not be dismissed since plants were not tested
early in the season. Additionally, other conditions associated
with a more efficient virus transmission may have been present
during 2008–09 season.
It is possible that the colder than normal temperatures and
the overhead irrigation used to prevent freeze damage during
the 2009–10 strawberry season may have prevented more rapid
spread of SNSV as populations of thrips are affected by temperature and precipitation (Morsello et al., 2008). Also, host
plant species, cultivar, relative humidity and light affect thrips
development (Stacey and Fellowes, 2002) and the efficiency and
extent of virus transmission may be affected by the strain of the
virus (Klose et al., 1996).
The inconsistency of SNSV detection in the second and third
sampling was not unexpected. Converse (1978) found that SNSV
was not distributed uniformly in the shoots of blackberry plants.
Furthermore, irregular distribution of SNSV was found in roots
and shoots of strawberry plantlets grown in vitro (Spiegel et al.,
1995). Because SNSV-infected plants do not show virus symptoms, collection of leaves for virus testing is done by selecting
the youngest fully expanded leaves since it is assumed that the
virus will more likely be present in the actively growing parts of
the plant. However, it is possible that young plant tissues may
be free of virus when other plant parts are infected. In addition,
detection capability depends on the amount of virus in the plant
tissue tested and the detection method used.
SNSV has a wide host range and host plant species such as
tomatoes and weeds can serve as sources of inoculum (Cupertino
et al., 1984; Kaiser et al., 1982). At the end of the 2009–10 season,
SNSV was not detected in seven weed species found adjacent to
infected plants or within the same planting hole (data not shown).
In the work of Cupertino et al. (1984), common lambsquarter
(Chenopodium album) was used as an experimental host for
SNSV from naturally infected tomatoes. However, we did not
detect SNSV when we tested this weed in the UF-GCREC field.
C. album may not have been infected since virus dissemination
within the strawberry fields was slow. Nevertheless, host–virus
strain specificity cannot be ignored.
Johnson et al. (1984) reported that SNSV has the potential
to reduce yield by up to 15% and runner production by up to
75%. In this preliminary study, even though SNSV was detected
in more than 20% of the samples tested since the beginning of
the season, it did not cause noticeable reduction in strawberry
growth or yield, nor did it seem to spread significantly during the
2009–10 strawberry season. One could assume that if viruses do
not cause symptoms and/or reduce yield, then there is no need
for concern. However, viruses that seem harmless by themselves
may become problematic in combination with others (Martin
and Tzanetakis, 2006). Plants with these mixed infections may
develop more severe symptoms than those harboring a single viral
pathogen. Therefore, strawberry growers should minimize the
risk of infection and spread by using clean stock plant material
(tissue-cultured and virus-tested). Consequently, nursery fields
should continue to be monitored closely and plants destroyed if
infected material is found.
Proc. Fla. State Hort. Soc. 123: 2010.
Literature Cited
Biswas, M.K., M. Hossain, and R. Islam. 2007. Virus free plantlets
production of strawberry through meristem culture. World J. Agr. Sci.
3 (6):757–763.
Converse, R.H. 1987. Virus and viruslike diseases of Fragaria (strawberry), p. 1–100. In: R.H. Converse (ed.). Virus diseases of small fruits.
U.S. Dept. Agr. Res. Serv. Agr. Hdbk. No.631.
Converse, R.H. 1978. Uneven distribution of tobacco streak virus in
santiam blackberry before and after heat therapy. Phytopathology
68:241–244.
Cupertino, F.P., R.G. Grogan, L.J. Petersen, and K.A. Kimble. 1984.
Tobacco streak virus infection of tomato and some natural weed hosts
in California. Plant Dis. 68:331–333.
Frazier, N.W., P.S. Jorgensen, H.E. Thomas, and H.A. Johnson, Jr.
1962. Necrotic shock—A virus disease of strawberries. Plant Dis.
Rep. 46:547–550.
Hokanson, S.C., R.R. Martin, and J.L. Maas. 2000. First report of tobacco
streak virus in strawberry in the Eastern United States. Plant Dis. 84: 488.
Jorgensen, P.S. 1957. Strawberry virus transmission by insert graft. Plant
Dis. Rep. 41:1009–1010.
Johnson, H.A., Jr., R.H. Converse, A. Amorao, J.I. Espejo, and N.W.
Frazier. 1984. Seed transmission of tobacco streak virus in strawberry.
Plant Dis. 68:390–392.
Kaiser, W.J., S.D. Wyatt, and G.R. Pesho. 1982. Natural hosts and vectors of tobacco streak virus in eastern Washington. Phytopathology
72:1508–1512.
Proc. Fla. State Hort. Soc. 123: 2010.
Klose, M.J., R. Sdoodee, D.S. Teakle, J.R. Milne, R.S. Greber, and G.H.
Walter. 1996. Transmission of three strains of tobacco streak ilarvirus
by different thrips species using virus-infected pollen. Phytopathology
144:281–284.
Martin, R.R. 2004. Recommended procedures for detection of viruses
of small fruit crops. Acta Hort. 656:222–234.
Martin, R.R. and I.E. Tzanetakis. 2006. Characterization and recent
advances in detection of strawberry viruses. Plant Dis. 90:384–396.
Morsello, S.C., R.L. Groves, B.A. Nault, and G.G. Kennedy. 2008.
Temperature and precipitation affect seasonal patterns of dispersing
tobacco thrips, Frankliniella fusca, and onion thrips, Thrips tabaci
(Thysanoptera: Thripidae) caught on sticky traps. Environ. Entomol.
37(1):79–86,
Sdoodee, R. and D.S. Teakle. 1993. Studies on the mechanism of transmission of pollen-associated Tobacco streak ilarvirus virus by Thrips
tabaci. Plant Pathol. 42:88–92.
Spiegel, S. and J. Cohen. 1985. Occurrence of Tobacco streak virus in
strawberries in Israel. Plant Dis. 69:448–449.
Spiegel, S., Y. Tam, R.R. Martin, and M. Ter Borg. 1995. Uneven distribution of tobacco streak virus in strawberry plantlets grown in vitro.
Acta Hort. 385:122–125.
Stacey, D.A. and M.D.E. Fellowes. 2002. Temperature and the development rates of thrips: Evidence for a constraint on local adaptation? Eur.
J. Entomol. 99: 399–404.
Tzanetakis, I.E., I.C. Mackey, and R.R. Martin. 2004. Strawberry necrotic
shock virus is a distinct virus and not a strain of Tobacco streak virus.
Arch. Virol. 149:2001–2011.
159