Crop Protection 128 (2020) 104995

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Crop Protection
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Short communication

The recent association of a DNA betasatellite with Tomato yellow leaf curl
virus in Israel – A new threat to tomato production
Dana Gelbart a, Lea Chen a, Tamar Alon b, Svetlana Dobrinin b, Ilan Levin a, Moshe Lapidot a, *
a
Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel
b
Extension Service, Ministry of Agriculture and Rural Development, Rishon LeZion, Israel

A R T I C L E I N F O A B S T R A C T

Keywords: During November 2016, tomato yellow leaf curl virus (TYLCV)-resistant F1 hybrid indeterminate tomato plants
TYLCV cv. Diagrama, grown in a commercial greenhouse in Revaya, Israel, expressed severe symptoms of tomato yellow
Betasatellite leaf curl disease (TYLCD). Samples were collected from symptomatic tomato plants, and using TYLCV-specific
Tomato
PCR primers, it was confirmed that these plants were indeed infected with TYLCV. Using the universal betasa­
Resistance
tellite primer pair B01/B02, followed by cloning and sequencing, it was found that the plants were also infected
Ty-1
with a betasatellite. The satellite sequence was deposited in NCBI (GeneBank Acc. No. MK456609). Phylogenetic
analysis revealed that the closest similarity, with 96% nucleotide identity, was to cotton leaf curl Gezira beta­
satellite (CLCuGB). Sampling symptomatic tomato plants in major growing areas in Israel revealed that CLCuGB
is disseminated throughout the country. To the best of our knowledge, this is the first identification of a beta­
satellite, associated with TYLCV, in tomato plants in Israel.

Viruses belonging to the genus Begomovirus, family Geminiviridae, are
transmitted by whiteflies of the Bemisia tabaci complex in a persistent
manner, and cause significant damages to many crop plants. During the
late 1950’s, a new disease was detected in tomato plants in Israel. It was
found that the disease was caused by a new virus, which was named
tomato yellow leaf curl virus (TYLCV). TYLCV has a genome composed
of a single circular ssDNA molecule, nearly 2.8 kb in size (Navot et al.,
1991). TYLCV has a relatively small host range, and is mainly known
due to its devastating effect on tomato (Solanum lycopersicum) produc­
tion world-wide (Navas-Castillo et al., 2011; Lapidot et al., 2014; Lap­
idot and Levin, 2017). TYLCV-induced disease symptoms include
upward cupping and chlorosis of tomato leaves, combined with signif­
icant plant stunting and reduction of plant yield (Cohen and Harpaz,
1964; Lapidot et al., 1997). With time it became clear that tomato yel­
low leaf curl disease (TYLCD) is induced by more than ten different
begomovirus species (Moriones and Navas-Castillo, 2001; Nav­
as-Castillo et al., 2011). Two different strains of TYLCV are prevalent in
Israel, TYLCV-IL (the type strain of the species) and TYLCV-Mld (Anti­
gnus and Cohen, 1994; Anfoka et al., 2008).
The populations of the whitefly vector of TYLCV tend to reach very
high numbers, which makes TYLCV-management a challenge. Most so­
lutions are aimed at reduction of insect numbers, by using insecticides or
physical barriers such as 50-mesh nets. Still, breeding tomatoes for
resistance to TYLCV, although slow and tedious, is highly desirable as
genetic resistance is the best strategy to combat viral-induced damages.
Most efforts have been concentrated on screening wild tomato species
for resistance to the virus, since all genotypes of cultivated tomato tested
were found susceptible to TYLCV. Hence, resistant loci discovered in
wild Solanum species were introgressed into S. lycopersicum. Among
these are: Ty-1, Ty-3, Ty-4 and Ty-6 that were introgressed from
S. chilense accessions, Ty-2 from S. habrochaites, and ty-5 presumably
from S. peruvianum (Lapidot and Levin, 2017).
Commercial tomato cultivars resistant to TYLCV are readily avail­
able. Following TYLCV-infection, most show some degree of disease
symptoms, as well as some yield loss (Lapidot et al., 1997, 2014;
Vidavsky et al., 2008). As Ty-1 was the first TYLCV-resistant locus
identified, and it is dominantly inherited (Zamir et al., 1994), many
breeding programs have utilized it. As a result, many commercial tomato
hybrids resistant to TYLCV carry Ty-1 either alone or in combination
with other resistance genes.
Three types of DNA satellites, alphasatellites betasatellites and del­
tasatellites, have been associated with monopartite begomoviruses
(Briddon and Stanley, 2006; Zhou, 2013; Lozano et al., 2016). Betasa­
tellites are circular ssDNAs, approximately 1,350 nt in size, that utilize

* Corresponding author.
E-mail address: lapidotm@volcani.agri.gov.il (M. Lapidot).

https://doi.org/10.1016/j.cropro.2019.104995
Received 30 June 2019; Received in revised form 24 October 2019; Accepted 26 October 2019
Available online 31 October 2019
0261-2194/© 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
D. Gelbart et al. Crop Protection 128 (2020) 104995

Fig. 1. Cv. Diagrama tomato plants showing tomato yellow leaf curl disease symptoms, Revaya, November 2016. (A) General view of the greenhouse; (B) Close-up on
a plant showing disease symptoms.

monopartite begomoviruses as helper viruses, contribute to the induc­

Table 1
tion of disease symptoms and are prevalent mainly in eastern Asia.
Satellites accessions with more than 90% nucleotide sequence identity to the
Betasatellites rely on the helper begomoviruses for replication, encap­
satellite sequence identified in Revaya, November 2016.
sidation and spread within the host. By definition, betasatellites share no
Satellite Accession Genome size Nucleotide
sequence similarity with the helper virus other than the begomoviral
No. (nt.) identity (%)
conserved hairpin structure that serves as the origin of viral DNA
replication (Laufs et al., 1995; Zhou, 2013). Betasatellites code for a Cotton leaf curl Gezira KT099177 1324 95.8
betasatellite isolate IsSq-
single multifunctional βC1 protein, which is involved in enhancement of C112
disease symptoms and suppression of both transcriptional and post Cotton leaf curl Gezira satDNA AF397215 1305 94.3
transcriptional gene silencing (Saunders et al., 2004; Cui et al., 2005; 10a
Yang et al., 2011; Amin et al., 2011; Zhou, 2013). Okra yellow vein disease AJ316039 1307 93.9
associated sequencea
During November 2016, F1 hybrid TYLCV-resistant indeterminate
Cotton leaf curl Gezira KU095847 1310 93.8
tomato plants cv. Diagrama (Nunhems, The Netherlands), grown betasatellite isolate IsSq1
commercially in greenhouses in Revaya (approximately 30 Km south of Cotton leaf curl Gezira satDNA KJ396939 1320 93.4
the Sea of Galilee, Israel), unexpectedly displayed severe TYLCD 10 isolate Homraa
symptoms (Fig. 1). Leaf samples were collected from 18 symptomatic Cotton leaf curl Gezira satDNA JX649952 1339 92.6
10 isolate Ammana
tomato plants from two different greenhouses and total nucleic acid
Cotton leaf curl Gezira satDNA AF397217 1350 90.4
were extracted from each (Dellaporta et al., 1983). Using PCR primer 3a
pair specific to TYLCV, TYC1F and TYC1R (Lapidot, 2002), all the tested a
Orginally termed OkLC betasatellite, but later recognized as cotton leaf curl
plants were confirmed to be infected with TYLCV. To discriminate be­
Gezira betasatellite (Briddon et al., 2008).
tween TYLCV-IL and TYLCV-Mld, PCR primer pairs TY78R and IL2629F
for TYLCV-IL, and TY78R and Mld2277F for TYLCV-Mld were used ac­
OkLCB identified in Egypt and by 93.9% to OkLCB from Jordan [Orig­
cording to Belabess et al. (2015). It was determined that eleven plants
inally termed OkLCB but later recognized as CLCuGB (Briddon et al.,
were infected with TYLCV-IL while seven plants were infected with
2008)] (Table 1). Interestingly, CLCuGB isolate IsSq-C112 was identified
TYLCV-Mld (we have also cloned and fully sequenced two clones of each
in whiteflies collected from squash plants in Israel in 2011. The collec­
TYLCV-IL and Mld. The full sequences were as expected of both TYLCV
tion was from a squash field just outside Kafr Manda, approximately
strains). However, due to the unexpected severity of disease symptoms
50 Km North-West of Revaya. This identification was part of a
expressed by the TYLCV-resistant plants and to the earlier identification
vector-enabled metagenomics study of begomovirus-associated satellite
of a betasatellite associated with TYLCV in Jordan (a neighboring
DNAs analyzing whiteflies collected in different locations around the
country whose border is about 10 Km east from Revaya) (Anfoka et al.,
world, Israel being one of them (Rosario et al., 2016). This shows that
2014), the samples were also tested for the presence of betasatellites
this betasatellite is present in Israel for at least eight years.
using the universal primer pair, B01 and B02 (Briddon et al., 2002).
Plants containing both TYLCV-Mld and satellite served as source
While all 18 plants tested positive for TYLCV, ten tested positive for a
plants for inoculation of F1 hybrid Diagrama test plants using whiteflies.
betasatellite DNA (six plants were determined to be co-infected with
Adult whiteflies were allowed a 48 h acquisition access period (AAP) on
TYLCV-Mld, four with TYLCV-IL and one with both viral strains). The
tomato source plants infected either with TYLCV-Mld or with TYLCV-
amplification products from four plants (two co-infected with
Mld and CLCuGB isolate Revaya. Following the AAP, the whiteflies
TYLCV-Mld and two co-infected with TYLCV-IL) were cloned into the
were allowed a 48 h inoculation access period on 12 TYLCV-resistant
plasmid pGEM-T Easy (Promega, USA) and sequenced. All four se­
‘Diagrama’ test plants. To remove the whiteflies the test plants were
quences (one from each plant), 1329 nt in size, were found to be iden­
treated with imidacloprid (Confidor, Bayer, Leverkusen, Germany), kept
tical and deposited as a single accession in NCBI sequence database
in an insect-proof greenhouse at 26–32 � C and monitored for TYLCD
(https://www.ncbi.nlm.nih.gov/genbank/, accession number
symptoms. The inoculation experiment was repeated twice, at two
MK456609). Phylogenetic analysis revealed that the closest sequence
different dates. Using a Ty-1 specific molecular marker (P19) (Verlaan
similarity, with 95.8% nucleotide identity, was to cotton leaf curl Gezira
et al., 2013), it was determined that all the Diagrama F1 hybrid plants
betasatellite (CLCuGB) isolate IsSq-C112, followed by 94.3% identity to
contain the TYLCV-resistant locus Ty-1 in a heterozygous state. While

2
D. Gelbart et al. Crop Protection 128 (2020) 104995

Fig. 2. CLCuGB isolate Revaya associated with

TYLCV-Mld enhances disease symptoms. Fourteen
days old TYLCV-resistant cv. Diagrama plants (A, B)
were inoculated with either TYLCV-Mld (A) or with
TYLCV-Mld and with CLCuGB (B) using whiteflies.
Following inoculation the test plants were treated
with imidacloprid (Confidor, Bayer, Leverkusen,
Germany), kept in an insect-proof greenhouse at
26–32 � C and monitored for symptom development.
Pictures were taken 21 days after inoculation.

Table 2
Identification of Cotton leaf curl Gezira betasatellite in tomato production greenhouses and open fields in Israel between October, 2016 to October 2018.
Location Sampling date (M-Y) Genotype Ty-1 No. of samples

Total Positive for

TYLCV-IL TYLCV-Mld CLCuGB

A. Greenhouse production
Revaya 10–2016 Diagrama þ/ 18 11 7 10
Elifaz 2–2017 Eshkol þ/ 4 0 3 3
Netiv HaAsara 5–2017 Eshkol þ/ 2 1 1 2
Beit Hanan 9–2017 3951 þ/ 7 7 1 7
Yesha 10–2017 Eshkol þ/ 6 5 1 6
Idan 10–2017 Eshkol þ/ 4 2 2 4
Mivtachim 10–2017 Olympicos þ/ 2 1 1 2
Ein Yahav 10–2017 Eshkol þ/ 4 2 2 2
Ranen 7–2018 Bruno þ/ 6 1 5 6
Sde David 10–2018 Toni þ/ 4 1 3 3
Nachla 10–2018 Gila þ/ 4 1 4 4

B. Open field production

Tomer 3–2017 Unknown / 4 2 2 4
Mop Darom 10–2017 Unknown / 4 2 4 3
Givat Yoav 8–2018 Shavit þ/ 8 4 7 6
Afik 8–2018 Shanty þ/ 4 2 4 4

Varieties sampled: Diagrama (Nunhems, The Netherlands); Eshkol (Seminis, USA); Olympicos, Bruno, 3951, Shavit, Shanty (Hazera Seeds, Israel); Toni, Gila (Rimi,
Israel). Presence or absence of Ty-1 was determined using a specific molecular marker (P19) according to Verlaan et al. (2013); þ/ denotes presence of Ty-1 in a
heterozygous state; / denotes plants that do not carry Ty-1.

‘Diagrama’ plants inoculated only with TYLCV-Mld hardly showed any
disease symptoms (Fig. 2), ‘Diagrama’ plants inoculated with
TYLCV-Mld and CLCuGB isolate Revaya developed severe TYLCD
symptoms within 14–21 days (Fig. 2). The inoculated test plants were
tested by PCR for presence of TYLCV-Mld and CLCuGB 28 days after
inoculation. Indeed, all the test plants inoculated only with TYLCV-Mld
were tested positive for the virus and negative for the satellite, while all
the plants inoculated with both TYLCV-Mld and CLCuGB were tested
positive for both. Moreover, a few test plants inoculated with both
TYLCV-Mld and CLCuGB were kept in a greenhouse for 6 months and
monitored for disease development. No change in symptom severity was
detected, and after 180 days the plants were tested again and found
positive for TYLCV-Mld and CLCuGB.
Following the identification of a betasatellite in Revaya, samples
were collected from commercially grown tomato greenhouses and fields
throughout the country (Table 2, Fig. 3). Samples were collected from
plants that exhibited severe TYLCD symptoms. All the sampled symp­
tomatic plants were found positive for either TYLCV-IL or TYLCV-Mld,
most were also coinfected with CLCuGB. As the majority of tomato ge­
notypes grown commercially in Israel are TYLCV-resistant, indeed most
of the sampled plants were determined positive for Ty-1 (Table 2).
Betasatellites from six samples (two from each site) from Idan, Elifaz and
from Givat Yoav (Fig. 3) were cloned and sequenced. All six sequences
were found to be identical to the betasatellite detected earlier in Revaya
(we had an odd nucleotide difference in one sequence, but it may be a
result of the PCR amplification performed prior to cloning).
The association of a betasatellite with TYLCV was reported for the
first time in 2008 from Oman (Khan et al., 2008), but the satellite effect
on disease severity was not clear since no comparison was made to
infection with the virus without the satellite. Recently, Conflon et al.
(2018) studied the effect that CLCuGB (accession No. FN554575) iso­
lated from Okra in Burkina-Faso associated with TYLCV may have upon
disease severity and upon virus accumulation in the infected plant. The
betasatellite was found to increase the disease severity induced by
TYLCV. Moreover, a Ty-1 resistant tomato genotype (Pristyla, Gautier
Semences) infected with both CLCuGB and TYLCV (either Mld or IL)
exhibited mild disease symptoms at the early stages of infection while
later on symptoms became milder and eventually disappeared (Conflon
et al., 2018). However, in our case, following inoculation of Ty-1 plants
with TYLCV-Mld and CLCuGB the plants expressed severe disease
symptoms (see Fig. 2) and showed no recovery for at least 180 days.
Moreover, the presence of the satellite was discovered in relatively
mature (4 months old, see Fig. 1) TYLCV-resistant tomato plants
showing severe symptoms of TYLCD. Thus our results suggest that the
association of CLCuGB with TYLCV compromises Ty-1 resistance.
However, although CLCuGB was associated with either TYLCV-IL or

3
D. Gelbart et al.
Fig. 3. Distribution of CLCuGB associated with TYLCD in tomatoes grown
commercially in greenhouses and open fields in Israel. Samples were collected
from commercially grown tomato greenhouses and fields throughout the
country, from October 2016 to October 2018 as described in Table 2.
TYLCV-Mld in most symptomatic plants sampled in the field, these
plants were not infected by a single viral clone but rather with a mixture
of isolates. Hence, we cannot rule out the possibility that one of these
viral isolates, or a combination of isolates is overcoming the Ty-1
resistance, and not necessarily the betasatellite.
To the best of our knowledge, this is the first identification of a
betasatellite associated with TYLCD in tomato plants in Israel. The sat­
ellite enhances the effect of the disease, possibly compromises the
TYLCV-resistance induced by Ty-1 to a significant extent, and may very
well increase yield loss due to TYLCD. This is of great concern for tomato
growers in the Mediterranean region.
Declaration of competing interest
The authors declare that they have no known competing financial
4
Crop Protection 128 (2020) 104995
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
This work was supported by the Chief Scientist of The Ministry of
Agriculture, Israel (grant number 20-10-0045) within the ERANET-
ARIMNet2 (ref. 302) program.
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