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Journal of General Virology (2007), 88, 1034–1040
DOI 10.1099/vir.0.82653-0
Synergistic pathogenicity of a phloem-limited
begomovirus and tobamoviruses, despite negative
Diana Pohl and Christina Wege
Christina Wege
[email protected]
Universität Stuttgart, Institute of Biology, Department of Molecular Biology and Plant Virology,
Pfaffenwaldring 57, D-70550 Stuttgart, Germany
Received 19 October 2006
Accepted 28 November 2006
In contrast to previous observations on phloem-limited geminiviruses supported in movement
and accumulation by RNA viruses such as cucumo- and tobamoviruses, tissue infiltration by
Abutilon mosaic virus (AbMV) was enhanced by neither Tobacco mosaic virus nor Tomato
mosaic virus (ToMV) in two different hosts, Nicotiana benthamiana and tomato. Both
tobamoviruses exerted a negative effect on the DNA virus, resulting in a decrease in AbMV
accumulation and significantly reduced infectivity in N. benthamiana. Despite these unexpected
molecular observations, a striking synergistic enhancement in pathogenicity occurred with
respect to stunting and necrosis. In situ hybridization revealed that this was not due to any
alteration of tissue infiltration by AbMV, which also remained limited to the phloem in the mixed
infections. Transgenically expressed ToMV 30K movement protein was not able to induce
phloem escape of AbMV in tomato plants and did not lead to any obvious change in begomovirus
Significant proportions of crop and ornamental plants
from all over the world have been shown to be infected by
two or more distinct viruses (Lesemann & Winter, 2002).
This contrasts with relatively scarce analyses of the
molecular and ecological consequences of mixed infections
with unrelated viruses (reviewed by Hull, 2002). Recent
experiments have revealed that symptom induction,
accumulation and movement by the single-stranded (ss)
DNA-containing begomovirus Abutilon mosaic virus
(AbMV) in the economically important family Geminiviridae
(Stanley et al., 2005) are enhanced strongly by the
positive-sense (+) ssRNA virus Cucumber mosaic virus
(CMV) (Wege & Siegmund, 2007). Tobacco mosaic virus
(TMV) and related (+)ssRNA tobamoviruses (Lewandowski, 2005) comprise one of the few further genera
analysed in more detail with regard to interactions with
simultaneously inoculated viruses. Most of the coinfection and complementation assays have focused on
entire or partial genomes of other (+)ssRNA viruses
(Atabekov et al., 1999; Bendahmane et al., 1995; Cooper
et al., 1996; De Jong & Ahlquist, 1992; Hacker & Fowler,
2000; Hamilton & Nichols, 1977; Malyshenko et al., 1989;
Martin et al., 2004; Ryabov et al., 1999; Solovyev et al.,
1996; Taliansky et al., 1992). The experiments revealed a
range of observations, from unilateral suppression of virus
A supplementary figure and table showing typical symptoms and
phenotypes of N. benthamiana plants of different infection status are
available in JGV Online.
accumulation (Bendahmane et al., 1995) via spread
recovery (Malyshenko et al., 1989) to enhancement, some
of them including symptom synergism. Only a few
analyses have addressed the interplay of tobamoviruses
with DNA viruses. Two reports have focused on
interactions with geminiviruses (Carr & Kim, 1983;
Sunter et al., 2001), which cause devastating epidemics
in crops such as cassava and legumes and in members of
the Solanaceae (Legg & Fauquet, 2004; Mansoor et al.,
2003; Rybicki & Pietersen, 1999). These two publications
presented data in which at least one of the viruses was
supported by another unrelated virus: Carr & Kim (1983)
showed by electron microscopy that co-infection with a
tobamovirus leads to release of the otherwise phloemlimited begomovirus Bean golden mosaic virus (BGMV)
into mesophyll parenchyma of beans, and Sunter et al.
(2001) showed that transgenically delivered (A)C2
proteins of the begomovirus Tomato golden mosaic virus
(TGMV) or the curtovirus Beet curly top virus (BCTV)
increased the rate of TMV infection in Nicotiana species
(‘enhanced-susceptibility’ phenotype).
On the basis of these prior examples, we wanted to
determine whether positive tobamovirus–geminivirus
interactions were typical of the interactions between these
two genera, examining co-infections of TMV or Tomato
mosaic virus (ToMV) with the phloem-limited AbMV
(Horns & Jeske, 1991; Jeske, 2000; Wege et al., 2000, 2001).
We aimed to correlate effects on the symptoms’ phenotype
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Begomo-/tobamoviral interference
with molecular observations on virus accumulation and
with viral tissue tropism at the cellular level. Furthermore,
we analysed the influence of the tobamoviral 30K movement protein on AbMV, as the 30K protein was shown to
have a capacity to support the spread of unrelated viruses
(Giesman-Cookmeyer et al., 1995).
In symptoms and tissue distribution, AbMV resembles
important tomato begomoviruses such as Tomato yellow
leaf curl virus (Morilla et al., 2004). Its interactions with
tobamoviruses were studied in Nicotiana benthamiana
Domin and in Lycopersicon esculentum Mill. ‘Moneymaker’
under controlled greenhouse conditions. Homozygous
ToMV 30K movement protein-expressing tomato plants
(cv. ‘Craigella GCR26’; Weber & Pfitzner, 1998; Weber
et al., 1992) and non-transgenic controls were included in
the experiments. Symptom development was quantified
by optical rating and plant height measurements. Viral
DNA or RNA accumulation was analysed by blots of
total nucleic acid preparations from individual leaves of
defined size and position on the plants (AbMV- or
tobamovirus-specific probes). Whereas TMV and ToMV
infected all leaf-cell types readily, exiting from the phloem
in systemically invaded sink leaves (Cheng et al., 2000),
tissue specificity of AbMV was determined by in situ
hybridization (Morilla et al., 2004; Zhang et al., 2001).
In total, 284 N. benthamiana plants in four independent
experiments were agroinfected with AbMV DNA A and B
by stem pricking (Evans & Jeske, 1993; Frischmuth et al.,
1993; Klinkenberg et al., 1989) or mock-inoculated using
water or DNA B inoculum. Four to six days postagroinoculation, they were superinoculated mechanically
with TMV vulgare strain, ToMV (Meshi et al., 1986) virion
preparations or buffer as a control onto two adjacent leaves
above and below the agroinoculation site [60–70 (except
for ToMV; n516) plants per virus combination]. In
preliminary experiments, simultaneous inoculation was
also tested. With L. esculentum ‘Moneymaker’, the
inoculation scheme of 126 plants (20–25 per combination,
three experiments) was almost identical to that of N.
benthamiana: stem agroinoculation was directed into
cotyledon axils of seedlings with not yet unfolded primary
leaves, which, after expansion, were inoculated mechanically with tobamovirus or buffer 5–7 days later. With
ToMV 30K-expressing or non-transgenic control L.
esculentum ‘Craigella’, two experiments were carried out
(at least five plants each were mock- or AbMV-inoculated).
In both host species, 2–3 weeks post-agroinfection, mixed
infections had produced combinations of symptoms
typical for either of the viruses with additional new
phenotypic alterations (Fig. 1a; supplementary data in
JGV Online). In N. benthamiana, AbMV or tobamoviruses
alone caused mainly leaf symptoms, from leaf-blade
curvatures to curling and chlorotic patches; the tobamoviruses also caused necrotic lesions on leaves and stem
stunting, both more pronounced with ToMV than with
TMV (data not shown). The combination of either
tobamovirus with AbMV clearly enhanced stunting and
the overall amount of necrosis. The rapid progress of
symptoms obstructed exact height measurements, as
doubly infected plants soon shrivelled from wilting and
necrosis. Optical rating, however, showed a growth slowdown or arrest a few days post-tobamovirus superinoculation (p.i.) and indicated a synergism for the necrotic
phenotype (not shown). Simultaneous agro- and mechanical inoculation of AbMV into stems and of tobamovirus
onto pre-existing leaves led to even more rapid disease
development. As it frequently impeded unfolding of
systemically co-invaded leaves, which we aimed to analyse,
it was not used throughout the evaluated experiments.
In tomato, leaf symptoms were similar to those in N.
benthamiana except that in no case did necrosis occur, and
not only green, but also yellow, mosaic developed, which
was enhanced in the virus combinations. Most prominent,
however, was a transient influence of double infection on
plant height: none of the viruses alone induced significant
stunting, but both viral combinations did (Fig. 1a). All sets
of doubly infected tomato plants were stunted significantly
compared with the singly infected ones up to about 25 days
p.i. (i.e. 30–32 days after agroinoculation with AbMV,
validated by t-test and Kruskal–Wallis analysis of variance
on ranks). One to two weeks later, growth recovered. Thus,
a truly synergistic, but transient, disease was produced
whenever AbMV and either TMV or ToMV systemically
co-infected a tomato plant, as was observed for N.
benthamiana by the enhanced necrosis.
For N. benthamiana, this coincided with an unexpected
reduction in susceptibility for AbMV by about 25 % when
TMV was superinoculated [Table 1; with ToMV, 12 %
fewer plants became infected, but the low number (16) did
not suffice for statistical evaluation]. In N. benthamiana
tissue explants, replicative forms of AbMV can be detected
regularly as soon as 48 h post-agroinoculation (unpublished data). Therefore, it seems probable that tobamovirus
inoculation into a different but nearby site of the plant, i.e.
an adjacent leaf, resulted in a reduced efficiency of systemic
infection by the geminivirus after its initial onset of
replication. This may be due to an impeded multiplication
or movement, but was not analysed in more detail. It might
be speculated that RNA virus-mediated protection against
a DNA virus could be triggered by the activation of host
non-specific antiviral defences by the tobamovirus, resulting in begomovirus abortion in a subset of the plants
[putatively involved systemic signalling pathways were
reviewed by Beckers & Spoel (2006)]. Any similar RNA
virus-induced protection against systemic AbMV infection
was, however, absent in tomato.
To find out whether synergistic symptom enhancement
was correlated with alterations of the begomo- and/or
tobamovirus titre(s), blot hybridization experiments were
carried out. Total nucleic acids were extracted from
systemically infected (or control) leaves, or pinnate leaflets
in the case of tomato, of all plants at different time points
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D. Pohl and C. Wege
Fig. 1. Symptoms and AbMV tissue tropism in tomato plants of different infection status. (a) Phenotype (19 days p.i.). (b–e) In
situ hybridization revealing AbMV DNA (dark signals) limitation to vascular tissues in plants that were (b) mock-inoculated, (c)
singly AbMV-infected, (d) TMV-co-infected, (e) ToMV 30K MP-expressing. X, Xylem; eP/iP, external/internal phloem; PalPar/
SpPar, palisade/spongy parenchyma. Differential interference contrast. Bars, 100 mm (b, d, e); 50 mm (c).
(Wege & Siegmund, 2007). Young (not yet completely
expanded) and mature, fully expanded leaves were
compared (length of young versus mature leaves: N.
benthamiana, up to 10 versus 15–20 mm; tomato, 50–80
versus about 200 mm). Samples containing equal amounts
of plant genomic DNA were tested for relative levels of
AbMV DNA and tobamovirus RNA in parallel on Southern
or Northern blots, respectively (Fig. 2). Ethidium bromide
Table 1. TMV-mediated reduction in susceptibility of N. benthamiana for AbMV
Data are infection rate [no. infected/no. inoculated plants (%)] determined 15 days p.i. or later. TMV inoculation was carried out 4–6 days p.i. with
AbMV. The plants’ infection status was determined by blot-hybridization analyses.
Infection by AbMV
Mean (±SD)
Infection by TMV
*t-test: for a,0.05, AbMV infectivity is reduced significantly in comparison with singly AbMV-infected plants; Perror50.038.
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Journal of General Virology 88
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Begomo-/tobamoviral interference
Fig. 2. (a) Southern (left panels) and Northern (right panels) blots indicating viral nucleic acid accumulation in N. benthamiana leaves. 1–24, Samples from
individual plants 8/15 days p.i. (odd/even numbers). Equivalent amounts of plant genomic DNA were loaded (15 ng per sample; asterisks indicate
exceptional unevenly loaded lanes). Viral nucleic acid forms are indicated. (b) Median signal intensities (si) reflecting viral nucleic acid titres in singly or
doubly infected plants during progression of infection (four independent experiments, eight blots; ToMV-specific values following a similar course were
excluded for reasons of clarity). Asterisk pairs indicate significant differences (a,0.05, Mann–Whitney rank sum test). (c) AbMV DNA in ToMV 30Kexpressing and non-transgenic tomato (28 days p.i.).
D. Pohl and C. Wege
staining of the corresponding agarose gels confirmed equal
loading, and dilution series of AbMV- and TMV-derived
hybridization standards confirmed reproducible band
intensities between different blots, following probe detection via chemiluminescence and film exposure. All individual hybridization signals in equally loaded lanes were
quantified (mean pixel intensities of identical areas;
SigmaScan Pro, v. 5.0.0; SPSS Inc.) and used for statistical
verification of differences in virus accumulation.
Typically, 75–100 % of the individual samples of same
leaf age, time point of inoculation and infection status
contained very similar levels of the respective viral nucleic
acids. In N. benthamiana, accumulation of the begomovirus was repressed until at least 8 days p.i. upon coinfection with a tobamovirus (Fig. 2a, b). After a transient
enhancement of AbMV DNA accumulation throughout the
following week, it again declined, to remain reduced significantly compared with the single infections, from 18 days
p.i. until the end of data collection (27 days p.i.) in both
young and mature leaves. Calibration blots (Wege &
Siegmund, 2007) allowed for the estimation that the
diminished AbMV-specific hybridization signals at 18 days
p.i. reflected viral DNA levels reduced by a factor of 10 (in
young leaves) to 15 (in mature leaves). Contrasting with
these observations, tobamoviral RNA titres in doubly
infected plants in the early stages (8 days p.i.) were either
indistinguishable from those in the single infections (TMV)
or reduced (ToMV; Fig. 2a) but, after a period
of suppression or delay, reached a peak of maximum
accumulation between 16 and 18 days p.i. even more
rapidly than in singly infected plants. Henceforth, they
did not differ significantly from titres in single infections
(Fig. 2b). All virus titres underwent an almost steady
decline after 18 days p.i., reflecting the effects of ageing of
the plants and necrogenesis.
For tomato, no systematic influence of mixed infection was
observed at the level of virus accumulation (not shown).
However, in 15–25 % of the doubly infected (but none of
the singly infected) plants, begomovirus DNA titres were
reduced transiently as in N. benthamiana, up to at least 15
days p.i. Two weeks later, AbMV accumulation had
Even if elevated virus titres can be excluded, a qualitative
change in viral tissue distribution, e.g. the usually phloemlimited geminivirus BGMV dislocated into mesophyll upon
tobamovirus co-infection (Carr & Kim, 1983), might serve
as explanation for an increased pathogenicity. Therefore,
leaf explants from highly symptomatic regions of several
independent singly and doubly infected tomato plants were
paraffin-embedded at 32 days p.i. and subjected to AbMVspecific in situ hybridization. However, the analyses of
about 200 sections (each 2.5 mm in length) from different
typical leaves co-infected with TMV or ToMV did not
indicate an altered tissue tropism: all AbMV-specific
signals were confined to cells associated closely with the
phloem, as with the virus alone (Fig. 1b–d).
To establish whether the tobamovirus 30K movement
protein by itself, in the absence of further viral RNA
elements that might trigger antiviral defence in mesophyll
tissues, might induce phloem escape of AbMV or be the
responsible tobamoviral symptom determinant in the
synergism, ToMV 30K protein-expressing tomato plants
infected with AbMV were analysed for viral DNA content
and tissue specificity. Neither the overall accumulation of
AbMV DNA during the course of infection (Fig. 2c) nor its
tissue tropism (Fig. 1e) was changed in these plants, compared with non-transgenic tomato of the same cultivar.
Hence, the tobamoviral movement protein did not produce
synergistic effects with a geminivirus in the common host.
The symptom-synergism determinants of the DNA and of
the RNA viruses and their putative interacting partners in
the family Solanaceae thus remain to be determined. The
effects of enhanced pathogenicity on the one hand, and RNA
virus-induced reduction of DNA virus accumulation on the
other, differ from the former reports on tobamovirus–
geminivirus interactions, but resemble those described
for Cauliflower mosaic virus [CaMV; double-stranded
(ds)DNA]–ssRNA virus interplay. Hii et al. (2002) detected
symptom synergy of CaMV and the tobamovirus Turnip
vein clearing virus in turnip (Brassica rapa L.), despite no
change in the levels of either virus. Kamei et al. (1969) found
that, in CaMV-preinfected Brassica perviridis Bailey plants
challenged with the potyvirus Turnip mosaic virus, the latter
was suppressed by the dsDNA virus. The negative effect may
have been caused indirectly, due to impaired cellular
functions as a consequence of disease. Similar reasons might
also contribute to the negative interference between
tobamoviruses and AbMV, but are unlikely to explain a
transient suppression of virus accumulation in early stages
of the infections or a reduction in susceptibility.
Molecularly, the most interesting aspect of this study is the
failure of tobamoviruses to enhance AbMV replication and/
or spread against the background of our contrasting findings
for cucumoviruses. The synergism between CMV and AbMV
was shown to involve the CMV 2b silencing-suppressor
protein, which enhanced AbMV titres and numbers of
invaded cells in different solanaceous hosts (Wege & Siegmund, 2007). Therefore, the inability of tobamoviruses to
assist AbMV in the same host species might indicate that
their respective RNA-silencing suppressors, i.e. the 126K or
130K proteins (Ding et al., 2004; Kubota et al., 2003), appear
to be inefficient for AbMV infection, an observation that
merits further investigation. Silencing-suppression activity
has not yet been attributed to any AbMV protein and may
implicate different begomoviral gene products (Bisaro,
2006). Therefore, the results may also suggest that AbMV
differs from the geminiviruses BGMV, BCTV and TGMV in
some of its strategies operating during tissue infiltration, as
has been proposed previously (Zhang et al., 2001). The startling symptom synergism that we observed for the RNA–DNA
virus combinations, which even induced completely new
yellowing and stunting phenotypes, despite decreased virus
accumulation, could be best explained by simultaneous
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Journal of General Virology 88
Begomo-/tobamoviral interference
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