2751
J. pen. Virol. (1989), 70, 2751-2757. Printed in Great Britain
Key words: transport protein/tobamovirus/complementation
Plant Virus Transport Function: Complementation by Helper Viruses Is
Non-specific
By S. I. M A L Y S H E N K O ,
O. A. K O N D A K O V A ,
J. G. A T A B E K O V *
M. E. T A L I A N S K Y
AND
Department o f Virology, Moscow State University, Moscow 119899, U.S.S.R.
(Accepted 26 M a y 1989)
SUMMARY
The possibility of complementation of the cell-to-cell spread (within the inoculated
leaf) between different related and unrelated plant viruses has been studied. Various
tobamoviruses (tobacco mosaic, sunn-hemp mosaic, cucumber green mottle mosaic
viruses and 'tobamovirus from orchids') can facilitate each other's replication in nonpermissive hosts or at a temperature non-permissive for transport of one of the virus
partners, probably by complementation of transport functions. Complementation of
movement also occurred between some, but not all unrelated viruses tested. The
complementation in transport function seems to be non-specific: it can occur between
viruses even if their putative transport proteins significantly differ in structure.
Consequently these viruses were classified tentatively into different 'transport groups'.
INTRODUCTION
Systemic spread (transport) of plant virus infection from cell to cell is controlled to some
extent by a specific virus-encoded protein(s) termed the transport protein(s), TP(s) (for reviews,
see Atabekov & Dorokhov, 1984; Hull, t989).
Virus-encoded transport function is one of the factors that control virus host range (Taliansky
et al., 1982 b; Malyshenko et al., 1987, 1988); plant species may be resistant to a virus because the
latter cannot express its transport function. As a result the virus replicates only in the initially
infected cells (or in the isolated protoplasts) of the resistant plants. In other words, blockage of
transport function is phenomenologically equivalent to resistance of a plant to a virus. However
this type of resistance can be overcome and, thus, a non-host plant can become infected with a
virus because another virus that can normally spread in this plant (a helper virus) complements
the transport function of a dependent transport-deficient virus. Complementation in transport
function is accomplished not only by related but also by unrelated viruses (Taliansky et al.,
1982a, b; Carr & Kim, 1983; Atabekov et al., 1984; Barker, 1987, 1989; Malyshenko et al., 1987,
1988; Fuentes & Hamilton, 1988), suggesting that TP of a helper virus is likely to have some
general effect on cellular physiology, and this ultimately results in cell-to-cell viral movement.
The purpose of the present work was to supplement the experimental data on systemic spread
complementation first between different viruses within the tobamovirus group and second
between unrelated viruses from different groups.
METHODS
Viruses. Sunn-hemp mosaic tobamovirus (SHMV) was supplied by Dr R. D. Woods and propagated in
Phaseotus vutgaris L. var. Triumph; tobacco mosaic tobamovirus (TMV) (strain vulgare) was obtained from Dr
H. G. Wittmann and propagated either in Nicotiana tabacum L. var Samsun or Lycopersicon esculentum L. var.
Mayak; TMV temperature-sensitive (ts) mutant Lsl defective in transport function was supplied by Dr N.
Oshima; red clover mottle comovirus (RCMV) (Ukrainian strain) was obtained from Dr L. G. Lapchic and
propagated in Vigna unguiculata L. plants; arabis mosaic nepovirus (ArMV) was obtained from Dr B. D. Harrison
and propagated in Chenopodium quinoa; barley stripe mosaic hordeivirus (BSMV) (Norwich strain) was supplied
by Dr L. C. Lane and propagated in Hordeum vulgare L. ; alfalfa mosaic ilarvirus (AIMV) was obtained from Dr L.
Van Vloten-Doting and propagated in N. tabacum vat. Samsun; the Russian isolate of brome mosaic bromovirus
0000-8880 © 1989 SGM
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S. I. MALYSHENKO AND OTHERS
(BMV), cucumber green mottle mosaic tobamovirus (CGMMV), tobacco rattle tobravirus (TRV), cucumber
mosaic cucumovirus (CMV) and potatoXpotexvirus (PVX) were propagated in Triticum vulgare L., Cucumis
sativus L., N. tabacum var. Samsun, C. sativus and Datura stramonium L., respectively. The virus isolated by us
from Cattleya bowringianaand identified serologicallyand morphologicallyas a tobamovirus was also used. Since
its identity with Odontoglossum ringspot tobamovirus has not been proved this virus will be referred to as
"tobamovirusfrom orchids'. The viruses were purified as described previously (Atabekov et al., 1970; Novikov &
Atabekov, 1970).
Complementation experiments. Leaves of the plant species normally resistant to the helper-dependent (nonspreading) virus were mechanically inoculated with the helper virus capable of spreading systemically in this
plant. For example, the followingplants were used as normally resistant to the corresponding viruses: N. tabacum,
resistant to TMV Lsl at the non-permissive temperature (33 °C) and to CGMMV, BSMV and RCMV at ambient
temperature (24 °C); C. sativus, resistant to TMV vulgare, tobamovirus from orchids, SHMV and RCMV; C.
bowringiana, resistant to CGMMV; H. vulgate, resistant to PVX (see Tables 1 and 2). Control plants were mockinoculated (buffer-rubbed). Two to 4 days later the leaves were superinoculated with the helper-dependent virus.
The doubly inoculated leaves were harvested after 3 to 7 days and used for the determination of the amount of the
helper-dependent virus accumulated. Three or four plants were used for each test. The harvested leaves were
treated with antiserum to the helper-dependent virus to remove surface virus. After 15 min, antiserum was
removed by washing the leaves with water. Then the leaves were homogenized in 0.01 M-phosphatebuffer pH 7-2,
containing 0.05~ Tween-20. Concentration of the viruses in the extracts was determined by the ELISA double
antibody sandwich method (Clark & Adams, 1977) using serial dilutions as concentration standards. When two
antigenically related tobamoviruses were tested in the mixture the antisera were absorbed with the heterologous
virus prior to reaction. Linearity of absorbance with virus concentration was obtained within a range of 60 to
1000 ng virus/ml. Therefore, only the results of those complementation experiments in which all of the doubly
infected plants accumulated the helper-dependent virus at concentrations higher than 60 ng per 1 g of leaf tissue
were regarded as positive and are presented below (1 g of leaf tissue was usually homogenized in 1 ml of buffer).
Isolation ofprotoplasts. Protoplasts were isolated as described by Malyshenko et al. (1985, 1987).
RESULTS
Effect o f double tobamovirus infection on the accumulation o f the helper-dependent tobamovirus in
non-host plants
The possibility of the helper-dependent systemic spread of a transport-deficient tobamovirus
in the presence of another tobamovirus (helper) within the doubly inoculated leaf of a plant
resistant to one of the virus partners was examined. Different tobamoviruses were used either as
a dependent or as a helper virus in different virus-host combinations (Table 1). For example,
T M V (vulgare) served as the helper for C G M M V in N. tabacum var. Samsun (systemic host for
TMV), whereas C G M M V served as a helper for T M V in C. sativus (systemic host for
C G M M V ) . Also, SHMV was used as the helper for C G M M V in N. tabacum (systemic host for
SHMV) as well as for T M V Lsl (ts in transport) at the non-permissive temperature (33 °C)
(Table 1).
All the tobamoviruses tested, including T M V vulgare, T M V Lsl (at 33 °C), C G M M V ,
SHMV and tobamovirus from orchids, in different combinations in different plants were
capable of increasing each other's concentration. This effect cannot be explained by increased
survival of the dependent virus inoculum on the surface of inoculated leaves preinfected by the
helper virus. Indeed, the determination of the dependent virus by ELISA 1 day after
superinoculation has shown that the treatment of leaves with antisera (as described in Methods)
removed virtually all the virus from the leaf surface (i.e. to a level below the sensitivity of the
method, ~< 10 ng virus/ml) in the different combinations of tobamoviruses tested (data not
shown). The only exception was the combination of tobamovirus from orchids plus C G M M V in
orchid plants, in which C G M M V could not be removed completely from the leaf surface of C.
bowringiana with antisera. For this reason, the epidermis was totally removed from the doubly
inoculated leaves of C. bowringiana before their homogenization. Thus it was shown that
tobamovirus from orchids facilitates the accumulation of the dependent virus ( C G M M V ) in the
mesophyll cells of the non-host plant.
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2753
Table 1. Enhancement of dependent tobamovirus accumulation in the non-host plants by the helper
tobamovirus
Amountof dependent
References proposing
Inoculated
virus accumulated
plant resistant (ng/gplant tissues)t dependent virus replication
Non-spreading
in protoplasts of
(helper-dependent) to dependent ~
~--~
resistant plants
tobamovirus
virus
Expt. 1 Expt.2
lnoculum*
A
r
Helper virus
used for
preinfection
TMV vulgare
MI:~
CGMMV
MI
SHMV
MI
SHMV
MI
CGMMV
CGMMV
TMV
TMV
CGMMV
CGMMV
TMV Lsl (ts)
TMV Lsl (ts)
N. tabacum
var. Samsun
C. sativus
N. tabacum
var. Samsun
N. tabacum
var. Samsun
(33 °C) §
L. esculentum
TMV
SHMV
MI
SHMV
var. Mayak
C. sativus
CGMMV
SHMV
MI
SHMV
CGMMV
Tobamovirusfrom orchids C. sativus
MI
Tobamovirusfrom orchids
C. bowringiana
Tobamovirusfrom orchids¶
CGMMV
MI
CGMMV
140
~< 10
100
~<10
140
~< 10
100
~< 10
200 Sugimura& Ushiyama(1975)
~<10
Coutts & Wood (1976)
80
~< 10
180 Sugimura& Ushiyama(1975)
~< 10
Nishiguchiet aL (1978)
120
~<10
120
~< 10
80
~<10
140
~< 10
150
~<10
160
~<10
120
~ 10
80
~< 10
100
~<10
yrll
NT
NT
NT
* The leaves of the plants were preinoculated with the helper tobamovirus at a concentration of 20 ktg/ml and
superinoculated 3 days later with dependent virus at a concentration of 50 to 100 I.tg/ml.
t Detected by ELISA 5 days after superinfection.
:~MI, Mock inoculation.
§ 33 °C, non-permissive temperature for Lsl transport. All other experiments were performed at 25 °C.
IIyr, Not tested.
¶ In this combination virus was detected in leaf tissues, stripped of the epidermis,
Effect of double infection on the accumulation o f unrelated helper-dependent virus
In the next series of experiments several combinations of viruses belonging to different
taxonomic groups were used in double inoculation tests. It was shown by ELISA that in all
combinations tested (Table 2) treatment of the leaves with antisera removed practically all the
dependent virus inoculum from the surface (data not shown). On the other hand the facilitation
of accumulation of the dependent virus by the helper occurred in various combinations as shown
in Table 2. Thus, accumulation of R C M V comovirus was efficiently complemented by T M V
tobamovirus; that of R C M V was increased also by A r M V nepovirus, C M V cucumovirus and
PVX potexvirus; accumulation of BSMV hordeivirus was enhanced by T M V tobamovirus; that
of T M V was enhanced by ArMV nepovirus, T R V tobravirus and R C M V comovirus;
accumulation of PVX potexvirus was enhanced by BMV bromovirus and BSMV hordeivirus;
that of BMV bromovirus was enhanced by A1MV ilarvirus (Table 2). In all these cases the
resistance of a plant that was a non-host for a dependent virus was evidently overcome in the
presence of a helper virus in doubly inoculated leaves.
It should be mentioned that in several combinations of helper and dependent viruses the
increase in accumulation of the dependent virus did not occur. The accumulation of the
dependent virus was not substantially different between singly and doubly infected leaves for the
following combinations: T R V and R C M V in tobacco, BSMV and T R V in wheat, T R V and
BSMV in tobacco, and BSMV and A1MV in wheat (Table 2).
Evidence for complementation o f the systemic spread in some combinations o f dependent and
helper viruses
In several combinations mentioned above (Tables 1 and 2) it remained unclear whether the
increase in dependent virus accumulation was based on transport function complementation or
was due to the increased susceptibility of doubly infected cells to the dependent virus. If the
latter were true, the enhanced replication would have occurred only in the initially inoculated
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S. I. M A L Y S H E N K O AND O T H E R S
T a b l e 2. Enhancement o f dependent virus accumulation by unrelated helper viruses
Inoculum*
,
~
Helper virus
used for
preinfection
Non-spreading
(helper-dependent)
virus
TMV tobamovirus
MI :~
RCMV comovirus
MI
TRV tobravirus
MI
RCMV comovirus
RCMV
TMV - Lsl (ts)
TMV- Lsl (ts)
TMV - Lsl (ts)
TMV Lsl (ts)
ArMV nepovirus
MI
ArMV nepovirus
MI
BMV bromovirus
MI
A1MV ilarvirus
MI
CMV cucumovirus
MI
PVX potexvirus
MI
BSMV hordeivirus
MI
TMV tobamovirus
MI
TRV tobravirus
MI
BSMV hordeivirus
MI
TRV tobravirus
MI
BSMV hordeivirus
MI
TMV tobamovirus
TMV
RCMV comovirus
RCMV
PVX potexvirus
PVX
BMV bromovirus
BMV
RCMV comovirus
RCMV
RCMV eomovirus
RCMV
PVX potexvirus
PVX
BSMVhordeivirus
BSMV
RCMV comovirus
RCMV
TRV tobravirus
TRV
BSMV hordeivirus
BSMV
A1MVilarvirus
AIMV
-
Inoculated
plant, resistant
to dependent
virus
N. tabacum
var. Samsun
V. unguiculata
(33 °C)*
N. tabacum
var. Samsun
(33 °C)
C. satit,us
C. satious
H. rulgare
V. unguiculata
N. tabacum
var. Samsun
N. tabacum
var. Samsun
H. trulgare
N. tabacum
var. Samsun
N. tabacum
var. Samsun
T. vulgare
N. tabacum
var. Samsun
T. vulgare
Amount of dependent
virus accumulated
(ng/g of leaf tissues t
r ~ x - - ~
Expt. t
Expt. 2
References proposing
dependent virus replication
in protoplasts of
resistant plants
1500
~< 10
220
~< 10
160
~< 10
1800
~< 10
140
~< 10
320
~< 10
Malyshenko et al. (1988)
110
~< 10
80
,< 10
260
~< 10
< 120
~< 10
120
~< 10
140
~< 10
80
<~ 10
80
< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
380
~< 10
120
~< 10
120
~< 10
-
Coutts & Wood (1976)
NI :~
Nishiguchi et al. (1978)
brr
Malyshenko et al. (1985)
NT
Malyshenko et al. (1988)
-
Malyshenko et al. (1988)
100
~< 10
80
< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
~< 10
Malyshenko et al. (1985)
Our unpublished data
Malyshenko et al. (1988)
NT
Our unpublished data
NT
* The leaves of the plants were preincubated by a helper virus at a concentration of 10 to 50 p.g/ml and 2 to 4 days
later superinoculated with dependent virus at 50 to 100 ~tg/ml.
t Detected by ELISA 4 to 7 days after superinfection.
:~ See footnotes to Table 1.
T a b l e 3. C o m p l e m e n t a t i o n o f s y s t e m i c spread between related a n d unrelated viruses
Inoculum *
~"
r
Helper virus
used for
preinfection
SHMV
MI *
TMV
MI
BMV
MI
PVX
MI
BSMV
MI
TMV
MI
~
Non-spreading
(helper-dependent)
virus
TMV-Lsl
TMV-Lsl
RCMV
RCMV
PVX
PVX
RCMV
RCMV
PVX
PVX
BSMV
BSMV
Inoculated
plant resistant
to dependent
virus
N. tabacum
var. Samsun
N. tabacum
var. Samsun
H. vulgare
N. tabacum
var. Samsun
H. vulgate
N. tabacum
var. Samson
Amount of dependent
virus accumulated in
mesophyll protoplasts
(ng per 5 x 106
protoplasts) t
360
~< 20
2600
~< 20
240
~< 20
300
~< 20
240
~< 20
I20
~< 20
* See footnotes to Tables 1 and 2.
t Protoplasts were isolated 4 to 7 days after superinfection, incubated for 24 h to allow the accumulation of virus,
and tested by ELISA.
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Non-specificity of transport function
2755
epidermal cells. The situation was clarified for some combinations of the dependent and helper
viruses listed in Tables 1 and 2 by isolation of the mesophyll protoplasts from doubly inoculated
plants, in which the dependent virus was detected by ELISA. It can be seen from Table 3 that in
all combinations tested the mesophyll protoplasts isolated from mixedly infected non-host plants
contained the dependent virus. A high amount of the dependent virus was detected in
protoplasts isolated from tobacco plants and coinoculated with TMV (helper virus) and RCMV
(dependent virus) (Table 3). By immunofluorescent staining it was shown that the proportion of
tobacco protoplasts containing RCMV was as. high as 3 0 ~ (data not shown). In other cases the
amount of helper-dependent virus accumulated in protoplasts was not so high but it
considerably exceeded that which was accumulated in control (Table 3).
Thus, direct detection of helper-dependent virus in mesophyll protoplasts suggests that at
least in the cases listed (Table 3) the complementation of systemic spread of helper-dependent
virus by a helper virus occurred. The same conclusion seems correct for the combination of
tobamovirus from orchids and C G M M V in C. bowringiana, since C G M M V (dependent virus) in
this case was detected in leaves stripped of the epidermis (Table I).
DISCUSSION
The main purpose of this paper was to analyse the degree of specificity of viral transport
function complementation between related viruses and between unrelated viruses. To this end
the experiments on complementation of the systemic spread of the dependent viruses within the
helper virus-inoculated leaf of a non-host plant were performed. In most dependent virus-host
combinations used the resistance of a given plant was evidently based on blocked transport
function of a virus since protoplasts isolated from the resistant plants have been shown to be
susceptible to these viruses (see the references in Tables 1 and 2). TMV ts mutant Lsl was used in
various combinations in this work as the key virus in transport complementation. It was
experimentally proven that the transport gene of Lsl contained a single point mutation making
the 30K transport protein non-functional at 32 to 35 °C (Meshi et al., 1987). Therefore, the
systemic spread of Lsl at 33 °C in the presence of a helper virus meant unequivocally that its
transport function was complemented. Our data suggest that the efficiency of Lsl transport
complementation at the non-permissive temperature (33°C) was similar to that of
complementation of other transport-deficient viruses (Tables 1 to 3). It should be noted however
that the experimental data presented here do not allow a correct quantitative comparison of
complementation efficiencies in different dependent virus-helper and virus-host combinations.
The results of the complementation experiment may depend on numerous factors, e.g.
effectiveness of replication, possible interference between the viruses, concentration of
dependent and helper viruses in the inoculum, interval between preinoeulation and
superinoculation, interval between superinoculation and the virus content determination. The
conditions of complementation were selected in every case to obtain a reliable level of dependent
virus accumulation.
One may argue that the enhancement of dependent virus accumulation was not due to
transport complementation but represented either the increased survival of dependent virus
inoculum on the surface of inoculated leaves preinfected with helper virus or an enhanced
accumulation of the dependent virus that occurred only in the initially infected epidermal cells
but not in mesophyll cells. The first suggestion can be dismissed by the knowledge that the
dependent virus inocula had been totally removed from the surface of the helper viruspreinfected leaves. The second suggestion can be discounted for at least several combinations
listed in Table 3 in which the presence of the dependent viruses was shown directly in mesophyll
cells. It can be proposed that in these cases the helper viruses provided the transport function to
related and unrelated dependent viruses. It appears likely that this explanation was also correct
for other combinations (Tables 1 and 2); however we cannot rule out the possibility that in some
cases this effect was due to the increased susceptibility of the helper virus-preinfected leaves to
infection by the dependent virus.
It should be emphasized that in our experiments the increase of virus accumulation occurred
within the doubly inoculated leaves, but not in other uninoculated leaves i.e. the transport
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s . I . MALYSHENKO AND OTHERS
function complementation was confined to cell-to-cell spread of the dependent virus prior to its
spread to the vascular system.
In four virus combinations no enhanced accumulation of the dependent virus was revealed
(Table 2). Similar negative results were reported by Barker (1989) who examined the influence of
several sap-transmissible viruses on the accumulation of phloem-associated luteoviruses. The
accumulation of luteoviruses was increased in plants coinoculated with different potyviruses,
potexviruses, tobraviruses and carrot mottle virus, but was not substantially affected by
coinfection with nepoviruses, cucumoviruses, ilarviruses and some other viruses (Barker, 1989).
As outlined above the results of the complementation experiment may depend on numerous
factors and the conditions of complementation, which should be selected in every case to obtain
a reliable level of dependent virus accumulation. It is possible that the negative results in some
double-infection experiments mentioned above may be due to non-optimal conditions having
been selected for complementation. On the other hand, it is possible that the transport function
cannot ever be complemented between these viruses.
There are good reasons to suggest that the TPs are encoded in the genomes of various (if not
all) plant viruses. The 30K protein encoded by the TMV genome has been experimentally
demonstrated to be responsible for the cell-to-cell transport function i.e. to act as the TP (Deom
et al., 1987 ; Meshi et al., 1987). Putative TPs were described for several other plant viruses (for
review, see Hull, 1989). Comparison of nucleotide sequences of putative TP genes revealed
significant variability in their structure. No homology was found between the putative viral TPs
of some taxonomically unrelated viruses. The structural diversity between the TPs of plant
viruses probably reflects not only their host specificity but also the possibility of the existence of
several different mechanisms of cell-to-cell transport after infection. Nevertheless, it may be
assumed that the number of such mechanisms should be limited. For the sake of simplicity we
regarded it possible to divide some plant viruses into tentative transport groups based on the
sequence homology between their TPs although the homology may not be very pronounced
(J. G. Atabekov & M. E. Taliansky, unpublished results). A similar division was proposed
recently by Hull (1989). We consider that this approach to be rather speculative at present and
that future studies would possibly bring changes into this classification. The first transport
group can include tobamoviruses, tobraviruses and caulimoviruses. The TPs of comoviruses,
nepoviruses and of some potyviruses have slight homology with the TP of TMV (Meyer et al.,
1986; Domier et al,, 1987). The significance of this similarity is unclear, but these viruses can be
tentatively included into the first group (J. G. Atabekov & M. E. Taliansky, unpublished results)
or into another group (Hull, 1989). The next group consists of tripartite genome viruses such as
BMV (Hull, 1989; J. G. Atabekov & M. E. Taliansky, unpublished results). The last transport
group may be needed to accommodate hordeiviruses, potexviruses and furoviruses, as suggested
by Skryabin et al. (1988).
The results presented here together with literature data have shown that the viruses belonging
to different transport groups can complement each other in transport function. This conclusion
is correct even if we take into account only the results on virus-host combinations for which
complementation in transport function has been shown directly (Table 3) and is in agreement
with the results of previous studies (Tatiansky et al., 1982a, b; Carr & Kim, 1983; Atabekov et
al., 1984; Barker, 1987, 1989; Malyshenko et al., 1987; 1988; Fuentes & Hamilton, 1988). Thus
the phenomenon of transport function complementation is rather non-specific although certain
exceptions can nevertheless be found.
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(Received 23 January 1989)
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