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336
Insect transmission of plant viruses: a constraint on virus variability
Alison G Power
Genetic diversity in viruses is shaped by high rates of
recombination and is constrained by host defenses and the
requirements of transmission. Recent studies of insecttransmitted plant viruses demonstrate highly conserved
molecular motifs in viral genomes that regulate the specificity of
insect transmission. In contrast, advances in our understanding
of host plant response to virus infection reveal some
generalized patterns of host defense to a diversity of viruses.
Addresses
Department of Ecology and Evolutionary Biology, Corson Hall,
Cornell University, Ithaca, New York 14853, USA;
e-mail: agp4@cornell.edu
can lose fitness through Muller’s ratchet, there are no experimental examples of declining RNA-virus fitness in the plant
literature. However, Fraile et al. [11] suggest that Muller’s
ratchet may be partially responsible for the displacement of
tobacco mosaic tobamovirus by tobacco mild green mosaic
tobamovirus in Australian Nicotiana glauca over the past century. In an interesting comparison of the genetic diversity of
geminiviruses infecting sexual and asexual populations of
the host plant Eupatorium, Ooi and Yahara [12] found lower
overall infection rates but greater virus genetic diversity in
the sexual host populations, suggesting that the viruses had
evolved in response to host genetic diversity despite the
potential for evolutionary bottlenecks.
Current Opinion in Plant Biology 2000, 3:336–340
1369-5266/00/$ — see front matter
© 2000 Elsevier Science Ltd. All rights reserved.
Abbreviations
HC
helper component
PTGS
post-transcriptional gene silencing
TYLCV tomato yellow leaf curl geminivirus
Introduction
Plant viruses are known for their remarkable genetic diversity, both within and between species. Among RNA plant
viruses, genetic diversity arises from error-prone replication mechanisms that result in high mutation rates, as well
as from recombination and reassortment. The evidence for
virus recombination among RNA viruses comes from both
experimental systems and virus molecular phylogenies [1–3,4•]. In DNA viruses, recombination also appears
to be common, and some diversity may reflect a lack of
postreplication repair [1]. Recent phylogenetic analyses
indicate that recombination has been particularly important in the evolution of some DNA viruses, particularly the
pareretroviruses [5] and the geminiviruses [6,7,8•,9•]. Yet
patterns of specificity in insect transmission and evidence
from molecular studies indicate that the high genetic
diversity generated by mutation and recombination are significantly constrained by the requirements of insect
transmission. This review summarizes recent studies of
transmission specificity, with special emphasis on advances
in geminivirus and potyvirus research. A brief, selective
overview of recent research on host defenses against viral
invasion is also provided.
How do plants defend themselves against the evolutionary
potential of invading viruses? A variety of defense responses
have been reviewed recently (e.g. [13]), but one of the most
exciting areas of current research is post-transcriptional gene
silencing (PTGS). Recent work on PTGS in plants has provided evidence that this mechanism functions as a general
defense against virus invasion. Viral invasion can induce
gene silencing and provide cross-protection against secondary virus infection [14•,15,16]. At the same time,
suppression of gene silencing is a general strategy used by a
broad range of DNA and RNA plant viruses. Successful virus
infection results from a virus’ ability to prevent PTGS-mediated degradation of its genome, either by directly
incapacitating the plant’s PTGS response or by moving
through the plant more quickly than the PTGS response or
both [17••]. The virus-encoded proteins responsible for suppressing PTGS are known in at least two cases: the helper
component (HC) proteinase of potyviruses [18–21] and the
2b protein of cucumoviruses ([19,21,22•,23]).
Experiments with a diversity of unrelated viruses that
infect a single host plant, Nicotiana benthamiana, found that
many viruses suppressed the gene-silencing defenses of
this plant [24••]. Moreover, in situ analysis of the response
of pea embryonic tissue to virus infection has demonstrated a common pattern of host gene regulation in response
to infection by viruses from four different virus families [25 ••]. These results support the notion of a
generalized host response to viral invasion that might facilitate the adaptation of viruses to multiple hosts.
Transmission by vectors
Virus diversity and host defense
The genetic diversity generated by high mutation rates
and frequent recombination allows the rapid evolution of
viruses in response to host defenses. The small size of the
virus population that invades a new host may, however, result
in bottlenecks that cause lower viral fitness over successive
transfers (i.e. Muller’s ratchet [10]). Although a few studies
with phages or animal viruses have shown that RNA viruses
The evolution of viruses that rely on a vector to move
between hosts is constrained not only by adaptation to
hosts and host defenses, but also by the requirements of
vector compatibility. Unlike animal viruses, many of which
can depend upon host movement for direct transmission to
new hosts, most plant viruses are transmitted by vectors,
the majority by insects. All transmission requires some
specificity between virus and vector, though the degree of
Insect transmission of plant viruses Power
337
Table 1
Plant virus genera organized according to transmission mode by insects.
Nonpersistent
Noncirculative
Semipersistent
Noncirculative
Persistent
Circulative
Persistent
Propagative
Alfamovirus
Carlavirus
Cucumovirus
Fabavirus
Machlomovirus
Macluravirus
Potexvirus
Potyvirus
Badnavirus
Caulimovirus
Closterovirus
Sequivirus
Trichovirus
Waikavirus
Begomovirus
Curtovirus
Mastrevirus
Enamovirus
Luteovirus
Polerovirus
Enamovirus
Nanavirus
Umbravirus
Bromovirus
Carmovirus
Comovirus
Sobemovirus
Tymovirus
Tospovirus
Marafivirus
Phytoreovirus
Fijivirus
Oryzavirus
Phytorhabdovirus
Cytorhabdovirus
Nucleorhabdovirus
Tenuivirus
Genera not transmitted by insects are not listed. Data from [8•,26•,29,55].
specificity varies dramatically among viruses. We are
beginning to recognize that even those viruses that are
simply carried on the mouthparts of vectors, and appear to
have the least specific relations with their vectors, still
depend on a complex interaction between viral proteins
and vector-associated compounds [26•]. Thus, the diversity of virus populations is constrained by the need to retain
specific interactions with their vectors.
In a number of well known examples, expansion of the host
range of insect vectors has been shown to increase the host
range of the viruses that these vectors transmit (e.g. [8•,27]),
which implies that virus distribution is constrained more by
the specificity of virus–vector relations than by the specificity of virus–host-plant relations. A recent quantitative
comparison of specificity in virus–host and virus–vector relations among over 400 vector-borne plant viruses
demonstrated that these viruses have much more specific
relations with their vectors than with their hosts [28].
Whereas many viruses have a very narrow range of vectors
but a large host range, no viruses have a narrow range of host
plants if they have many vector species. The host range of
the vector largely determines the host range of the virus,
suggesting that viruses can adapt to new hosts fairly readily.
These patterns indicate that most viruses are able to take
advantage of a relatively narrow set of vectors. Indeed,
Nault [29] suggests that transmission mode is a stable
evolutionary trait for virus genera. The transmission
modes of insect-vectored plant viruses have been categorized according to the intimacy of their association with
the vector. Stylet-borne viruses are carried on the mouthparts of the vectors and are known as ‘nonpersistent’
because they are lost once a vector has fed on a host.
Foregut-borne viruses appear to enter the foregut of the
vector and are ‘semi-persistent’ in their vectors.
Circulative ‘persistent’ viruses pass through the insect
gut into the hemolymph and then into the salivary glands
via highly specific transport mechanisms and can be
transmitted over a long period. Propagative viruses are
circulative viruses that replicate in the insect vector as
well as in the plant host, and their relations with vectors
are highly specific.
Although some genera of viruses can be transmitted by
insects from more than one family, no virus species is capable of being transmitted by insects from more than one
family. Furthermore, there are no documented examples of
different members of a virus genus having different insect
transmission modes, for example, one species of virus being
transmitted in a stylet-borne manner and another being
transmitted in a circulative mode (though some stylet-borne
viruses may also be seed-transmitted). This specificity of
transmission mode appears to be a consistent evolutionary
constraint, such that virus genera can be assigned to a particular insect transmission mode (Table 1). The consistency
of transmission mode within a virus genus and the generally greater specificity of vector relations compared to host
relations suggest that selection imposed by a requirement
for efficient vectors may be more severe than that imposed
by host plant defenses. Recent work with geminiviruses and
potyviruses, which differ significantly in their genetics and
ecology, illustrates how transmission constrains virus evolution despite the high genetic diversity of viruses.
Transmission constraints on geminivirus variation
The geminiviruses are unipartite or bipartite single-stranded DNA viruses that are divided into three genera
(i.e. Begomovirus, Curtovirus and Mastrevirus). They are
transmitted by whiteflies, leafhoppers and treehoppers in a
persistent, circulative manner. There is one report that a
Begomovirus (tomato yellow leaf curl geminivirus [TYLCV])
may propagate within its whitefly vectors [30], but this
possibility is yet to be definitively established [26•,29].
Additional lines of evidence for the propagation of TYLCV
within whiteflies are provided by several studies carried
338
Biotic interactions
out by Czosnek and colleagues, which suggest that transovarial transmission of the virus from female whiteflies to
their offspring [31] and sexual transmission of the virus
among whiteflies [32] take place. Several authors have suggested that propagative viruses originated with insect hosts
and adapted secondarily to plants [33,34]. This hypothesis
is based on the fact that propagative viruses rarely cause
disease in their vectors and can be transmitted in the
germline from parent to offspring in insects but not in
plants. Thus, it could be argued that the observation that
vector whitefly longevity and fecundity are reduced by carrying TYLCV is evidence against the propagation of this
virus in whiteflies [35]. In any case, transovarial transmission and sexual transmission among vectors, with or
without propagation within vectors, would seem to impose
significant constraints on virus variability.
Although geminiviruses are typically transmitted by a single species of vector, many have large host ranges. The
range of diseases incited by begomoviruses has increased
dramatically over the past decade, largely because of the
introduction of the Old World B-biotype Bemesia tabaci
whitefly into the Americas. Recent phylogenetic analyses
using mitochondrial DNA [36•] support earlier genetic,
biochemical and behavioral evidence that has been used to
seperate whiteflies according to geographic origin, and provide evidence that B. tabaci is a highly cryptic group of
sister species [37]. B-biotype B. tabaci have an unusually
broad host range and can transmit begomoviruses among
host plants that did not previously share insect vectors [37]. The introduction of this new vector to the New
World has apparently provided the opportunity for preexisting viruses to be transmitted to a variety of crops from
their original hosts, which include wild plants. In addition,
the high frequency of mixed infections of begomoviruses
owing to broad vector–host range undoubtedly provides
opportunities for the emergence of new viruses arising
from recombination among strains or species [6,7].
Recent molecular analyses of the whitefly-transmitted
begomoviruses indicate striking levels of genetic diversity
within virus species [38,39•]. Populations of cotton leaf
curl geminivirus are extremely genetically diverse.
Nevertheless, no genetic differentiation has been detected
between isolates from different host plant species or different geographic locations within Pakistan [39•]. The
regions of the genome encoding the coat protein are, however, much less variable than the regions encoding the
replication protein. Nucleotide diversity values for the coat
protein, which determines vector transmission specificity
[40,41], are similar to those of other highly conserved virus
proteins [39•]. These data suggest that the genetic variability of the virus is constrained by the requirements of
maintaining effective whitefly transmission.
A number of recent studies support the hypothesis that
whitefly-transmitted begomoviruses have evolved along
three separate branches of differing geographic origin, a
pattern that mirrors whitefly genetic variation [42–45].
Phylogenetic analyses of begomovirus coat protein
sequences divide these viruses into three groups, from the
Americas, Asia/Australia, and Africa/Mediterranean/Middle
East. It is striking that no relationships based on common
host plants have been detected. For example, a begomovirus infecting tobacco in the New World is much more
similar to other New World begomoviruses than to begomoviruses infecting tobacco in Zimbabwe [45]. This
geographically associated genetic variation appears to
reflect the spatial isolation of the three virus groups combined with their ready adaptation to a diversity of host
plants. It also appears to reflect geographically related
selection pressure exerted by whitefly vectors as a given
begomovirus is transmitted more efficiently by a whitefly
biotype from the same region than by a whitefly biotype
from a different region [46]. In surveys of the tomato yellow
leaf curl virus in Spain, the displacement of one strain by
another appeared to be driven largely by the higher efficiency of transmission of the displacing strain by local
whitefly biotypes [47], although the availability of reservoir
hosts may also have influenced virus success. There was no
competitive advantage for either strain within the host
plant, which suggests that virus–host interactions did not
drive displacement.
Transmission constraints on potyvirus variation
Potyviruses are single-stranded RNA viruses that are characterized by their nonpersistent stylet-borne transmission by
aphids. Potyviruses appear to have evolved a novel strategy
for overcoming the bottleneck of insect transmission by
encoding a ‘helper component’, a non-structural protein that
is produced by the infected plant. HCs aid the virus in binding to the aphid mouthparts, thereby facilitating transmission.
Several recent studies [48,49] have shown that the HC regulates the specificity and efficiency of potyvirus transmission.
In some systems, HC encoded by one virus may enable the
transmission of a different virus, although homologous
virus–HC combinations appear to be required for high transmission efficiency [49]. Pirone and Blanc [50] have argued
that the ability of a given HC to facilitate transmission of
more than one virus (i.e. heterologous as well as homologous
combinations) makes viruses that use helper-assisted transmission less prone to severe evolutionary bottlenecks than
stylet-borne viruses that rely only on direct virus binding.
The exact mechanism by which HC aids in virus binding is
still controversial, but recent studies [51,52] support the
‘bridge hypothesis’; that is, that the HC acts as a bifunctional molecule of which one domain binds to the virus coat
protein and the other binds to the vector mouthparts. The
amino-terminal region of the viral coat protein must interact
with the HC for successful transmission to occur, and the particular molecular motifs are typically highly conserved in
potyviruses [49,51,53]. In potato A potyvirus, a single aminoacid substitution controls aphid transmission and virus
accumulation in the plant, suggesting that there is a mechanistic relationship between these two traits; this relationship
Insect transmission of plant viruses Power
does not appear to hold for other potyviruses [54]. In general, the pattern of highly conserved motifs that are responsible
for insect transmissibility suggests that the requirements of
vector transmission exert significant selection pressure that
limits the diversity of coat protein sequences.
Conclusions
Recent molecular studies of geminiviruses and potyviruses,
and of patterns of virus transmission by insects, suggest
that insect transmission imposes significant constraints on
the evolution of plant viruses. The accelerating pace of
molecular studies of viruses will undoubtedly add to our
understanding of the genetic regulation of transmission
specificity. In addition, evolutionary explanations for this
specificity should be explored. Obviously, transmission is
an essential part of virus life history. Yet, it is not obvious
why it should be significantly more difficult for a virus to
increase its range of efficient vectors than to increase its
host range. Future research should address this question.
Acknowledgements
Financial support from the United States Department of Agriculture is
gratefully acknowledged.
References and recommended reading
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Insect transmission of plant viruses: a constraint on virus variability
Alison G Power
Genetic diversity in viruses is shaped by high rates of
recombination and is constrained by host defenses and the
requirements of transmission. Recent studies of insecttransmitted plant viruses demonstrate highly conserved
molecular motifs in viral genomes that regulate the specificity of
insect transmission. In contrast, advances in our understanding
of host plant response to virus infection reveal some
generalized patterns of host defense to a diversity of viruses.
Addresses
Department of Ecology and Evolutionary Biology, Corson Hall,
Cornell University, Ithaca, New York 14853, USA;
e-mail: agp4@cornell.edu
can lose fitness through Muller’s ratchet, there are no experimental examples of declining RNA-virus fitness in the plant
literature. However, Fraile et al. [11] suggest that Muller’s
ratchet may be partially responsible for the displacement of
tobacco mosaic tobamovirus by tobacco mild green mosaic
tobamovirus in Australian Nicotiana glauca over the past century. In an interesting comparison of the genetic diversity of
geminiviruses infecting sexual and asexual populations of
the host plant Eupatorium, Ooi and Yahara [12] found lower
overall infection rates but greater virus genetic diversity in
the sexual host populations, suggesting that the viruses had
evolved in response to host genetic diversity despite the
potential for evolutionary bottlenecks.
Current Opinion in Plant Biology 2000, 3:336–340
1369-5266/00/$ — see front matter
© 2000 Elsevier Science Ltd. All rights reserved.
Abbreviations
HC
helper component
PTGS
post-transcriptional gene silencing
TYLCV tomato yellow leaf curl geminivirus
Introduction
Plant viruses are known for their remarkable genetic diversity, both within and between species. Among RNA plant
viruses, genetic diversity arises from error-prone replication mechanisms that result in high mutation rates, as well
as from recombination and reassortment. The evidence for
virus recombination among RNA viruses comes from both
experimental systems and virus molecular phylogenies [1–3,4•]. In DNA viruses, recombination also appears
to be common, and some diversity may reflect a lack of
postreplication repair [1]. Recent phylogenetic analyses
indicate that recombination has been particularly important in the evolution of some DNA viruses, particularly the
pareretroviruses [5] and the geminiviruses [6,7,8•,9•]. Yet
patterns of specificity in insect transmission and evidence
from molecular studies indicate that the high genetic
diversity generated by mutation and recombination are significantly constrained by the requirements of insect
transmission. This review summarizes recent studies of
transmission specificity, with special emphasis on advances
in geminivirus and potyvirus research. A brief, selective
overview of recent research on host defenses against viral
invasion is also provided.
How do plants defend themselves against the evolutionary
potential of invading viruses? A variety of defense responses
have been reviewed recently (e.g. [13]), but one of the most
exciting areas of current research is post-transcriptional gene
silencing (PTGS). Recent work on PTGS in plants has provided evidence that this mechanism functions as a general
defense against virus invasion. Viral invasion can induce
gene silencing and provide cross-protection against secondary virus infection [14•,15,16]. At the same time,
suppression of gene silencing is a general strategy used by a
broad range of DNA and RNA plant viruses. Successful virus
infection results from a virus’ ability to prevent PTGS-mediated degradation of its genome, either by directly
incapacitating the plant’s PTGS response or by moving
through the plant more quickly than the PTGS response or
both [17••]. The virus-encoded proteins responsible for suppressing PTGS are known in at least two cases: the helper
component (HC) proteinase of potyviruses [18–21] and the
2b protein of cucumoviruses ([19,21,22•,23]).
Experiments with a diversity of unrelated viruses that
infect a single host plant, Nicotiana benthamiana, found that
many viruses suppressed the gene-silencing defenses of
this plant [24••]. Moreover, in situ analysis of the response
of pea embryonic tissue to virus infection has demonstrated a common pattern of host gene regulation in response
to infection by viruses from four different virus families [25 ••]. These results support the notion of a
generalized host response to viral invasion that might facilitate the adaptation of viruses to multiple hosts.
Transmission by vectors
Virus diversity and host defense
The genetic diversity generated by high mutation rates
and frequent recombination allows the rapid evolution of
viruses in response to host defenses. The small size of the
virus population that invades a new host may, however, result
in bottlenecks that cause lower viral fitness over successive
transfers (i.e. Muller’s ratchet [10]). Although a few studies
with phages or animal viruses have shown that RNA viruses
The evolution of viruses that rely on a vector to move
between hosts is constrained not only by adaptation to
hosts and host defenses, but also by the requirements of
vector compatibility. Unlike animal viruses, many of which
can depend upon host movement for direct transmission to
new hosts, most plant viruses are transmitted by vectors,
the majority by insects. All transmission requires some
specificity between virus and vector, though the degree of
Insect transmission of plant viruses Power
337
Table 1
Plant virus genera organized according to transmission mode by insects.
Nonpersistent
Noncirculative
Semipersistent
Noncirculative
Persistent
Circulative
Persistent
Propagative
Alfamovirus
Carlavirus
Cucumovirus
Fabavirus
Machlomovirus
Macluravirus
Potexvirus
Potyvirus
Badnavirus
Caulimovirus
Closterovirus
Sequivirus
Trichovirus
Waikavirus
Begomovirus
Curtovirus
Mastrevirus
Enamovirus
Luteovirus
Polerovirus
Enamovirus
Nanavirus
Umbravirus
Bromovirus
Carmovirus
Comovirus
Sobemovirus
Tymovirus
Tospovirus
Marafivirus
Phytoreovirus
Fijivirus
Oryzavirus
Phytorhabdovirus
Cytorhabdovirus
Nucleorhabdovirus
Tenuivirus
Genera not transmitted by insects are not listed. Data from [8•,26•,29,55].
specificity varies dramatically among viruses. We are
beginning to recognize that even those viruses that are
simply carried on the mouthparts of vectors, and appear to
have the least specific relations with their vectors, still
depend on a complex interaction between viral proteins
and vector-associated compounds [26•]. Thus, the diversity of virus populations is constrained by the need to retain
specific interactions with their vectors.
In a number of well known examples, expansion of the host
range of insect vectors has been shown to increase the host
range of the viruses that these vectors transmit (e.g. [8•,27]),
which implies that virus distribution is constrained more by
the specificity of virus–vector relations than by the specificity of virus–host-plant relations. A recent quantitative
comparison of specificity in virus–host and virus–vector relations among over 400 vector-borne plant viruses
demonstrated that these viruses have much more specific
relations with their vectors than with their hosts [28].
Whereas many viruses have a very narrow range of vectors
but a large host range, no viruses have a narrow range of host
plants if they have many vector species. The host range of
the vector largely determines the host range of the virus,
suggesting that viruses can adapt to new hosts fairly readily.
These patterns indicate that most viruses are able to take
advantage of a relatively narrow set of vectors. Indeed,
Nault [29] suggests that transmission mode is a stable
evolutionary trait for virus genera. The transmission
modes of insect-vectored plant viruses have been categorized according to the intimacy of their association with
the vector. Stylet-borne viruses are carried on the mouthparts of the vectors and are known as ‘nonpersistent’
because they are lost once a vector has fed on a host.
Foregut-borne viruses appear to enter the foregut of the
vector and are ‘semi-persistent’ in their vectors.
Circulative ‘persistent’ viruses pass through the insect
gut into the hemolymph and then into the salivary glands
via highly specific transport mechanisms and can be
transmitted over a long period. Propagative viruses are
circulative viruses that replicate in the insect vector as
well as in the plant host, and their relations with vectors
are highly specific.
Although some genera of viruses can be transmitted by
insects from more than one family, no virus species is capable of being transmitted by insects from more than one
family. Furthermore, there are no documented examples of
different members of a virus genus having different insect
transmission modes, for example, one species of virus being
transmitted in a stylet-borne manner and another being
transmitted in a circulative mode (though some stylet-borne
viruses may also be seed-transmitted). This specificity of
transmission mode appears to be a consistent evolutionary
constraint, such that virus genera can be assigned to a particular insect transmission mode (Table 1). The consistency
of transmission mode within a virus genus and the generally greater specificity of vector relations compared to host
relations suggest that selection imposed by a requirement
for efficient vectors may be more severe than that imposed
by host plant defenses. Recent work with geminiviruses and
potyviruses, which differ significantly in their genetics and
ecology, illustrates how transmission constrains virus evolution despite the high genetic diversity of viruses.
Transmission constraints on geminivirus variation
The geminiviruses are unipartite or bipartite single-stranded DNA viruses that are divided into three genera
(i.e. Begomovirus, Curtovirus and Mastrevirus). They are
transmitted by whiteflies, leafhoppers and treehoppers in a
persistent, circulative manner. There is one report that a
Begomovirus (tomato yellow leaf curl geminivirus [TYLCV])
may propagate within its whitefly vectors [30], but this
possibility is yet to be definitively established [26•,29].
Additional lines of evidence for the propagation of TYLCV
within whiteflies are provided by several studies carried
338
Biotic interactions
out by Czosnek and colleagues, which suggest that transovarial transmission of the virus from female whiteflies to
their offspring [31] and sexual transmission of the virus
among whiteflies [32] take place. Several authors have suggested that propagative viruses originated with insect hosts
and adapted secondarily to plants [33,34]. This hypothesis
is based on the fact that propagative viruses rarely cause
disease in their vectors and can be transmitted in the
germline from parent to offspring in insects but not in
plants. Thus, it could be argued that the observation that
vector whitefly longevity and fecundity are reduced by carrying TYLCV is evidence against the propagation of this
virus in whiteflies [35]. In any case, transovarial transmission and sexual transmission among vectors, with or
without propagation within vectors, would seem to impose
significant constraints on virus variability.
Although geminiviruses are typically transmitted by a single species of vector, many have large host ranges. The
range of diseases incited by begomoviruses has increased
dramatically over the past decade, largely because of the
introduction of the Old World B-biotype Bemesia tabaci
whitefly into the Americas. Recent phylogenetic analyses
using mitochondrial DNA [36•] support earlier genetic,
biochemical and behavioral evidence that has been used to
seperate whiteflies according to geographic origin, and provide evidence that B. tabaci is a highly cryptic group of
sister species [37]. B-biotype B. tabaci have an unusually
broad host range and can transmit begomoviruses among
host plants that did not previously share insect vectors [37]. The introduction of this new vector to the New
World has apparently provided the opportunity for preexisting viruses to be transmitted to a variety of crops from
their original hosts, which include wild plants. In addition,
the high frequency of mixed infections of begomoviruses
owing to broad vector–host range undoubtedly provides
opportunities for the emergence of new viruses arising
from recombination among strains or species [6,7].
Recent molecular analyses of the whitefly-transmitted
begomoviruses indicate striking levels of genetic diversity
within virus species [38,39•]. Populations of cotton leaf
curl geminivirus are extremely genetically diverse.
Nevertheless, no genetic differentiation has been detected
between isolates from different host plant species or different geographic locations within Pakistan [39•]. The
regions of the genome encoding the coat protein are, however, much less variable than the regions encoding the
replication protein. Nucleotide diversity values for the coat
protein, which determines vector transmission specificity
[40,41], are similar to those of other highly conserved virus
proteins [39•]. These data suggest that the genetic variability of the virus is constrained by the requirements of
maintaining effective whitefly transmission.
A number of recent studies support the hypothesis that
whitefly-transmitted begomoviruses have evolved along
three separate branches of differing geographic origin, a
pattern that mirrors whitefly genetic variation [42–45].
Phylogenetic analyses of begomovirus coat protein
sequences divide these viruses into three groups, from the
Americas, Asia/Australia, and Africa/Mediterranean/Middle
East. It is striking that no relationships based on common
host plants have been detected. For example, a begomovirus infecting tobacco in the New World is much more
similar to other New World begomoviruses than to begomoviruses infecting tobacco in Zimbabwe [45]. This
geographically associated genetic variation appears to
reflect the spatial isolation of the three virus groups combined with their ready adaptation to a diversity of host
plants. It also appears to reflect geographically related
selection pressure exerted by whitefly vectors as a given
begomovirus is transmitted more efficiently by a whitefly
biotype from the same region than by a whitefly biotype
from a different region [46]. In surveys of the tomato yellow
leaf curl virus in Spain, the displacement of one strain by
another appeared to be driven largely by the higher efficiency of transmission of the displacing strain by local
whitefly biotypes [47], although the availability of reservoir
hosts may also have influenced virus success. There was no
competitive advantage for either strain within the host
plant, which suggests that virus–host interactions did not
drive displacement.
Transmission constraints on potyvirus variation
Potyviruses are single-stranded RNA viruses that are characterized by their nonpersistent stylet-borne transmission by
aphids. Potyviruses appear to have evolved a novel strategy
for overcoming the bottleneck of insect transmission by
encoding a ‘helper component’, a non-structural protein that
is produced by the infected plant. HCs aid the virus in binding to the aphid mouthparts, thereby facilitating transmission.
Several recent studies [48,49] have shown that the HC regulates the specificity and efficiency of potyvirus transmission.
In some systems, HC encoded by one virus may enable the
transmission of a different virus, although homologous
virus–HC combinations appear to be required for high transmission efficiency [49]. Pirone and Blanc [50] have argued
that the ability of a given HC to facilitate transmission of
more than one virus (i.e. heterologous as well as homologous
combinations) makes viruses that use helper-assisted transmission less prone to severe evolutionary bottlenecks than
stylet-borne viruses that rely only on direct virus binding.
The exact mechanism by which HC aids in virus binding is
still controversial, but recent studies [51,52] support the
‘bridge hypothesis’; that is, that the HC acts as a bifunctional molecule of which one domain binds to the virus coat
protein and the other binds to the vector mouthparts. The
amino-terminal region of the viral coat protein must interact
with the HC for successful transmission to occur, and the particular molecular motifs are typically highly conserved in
potyviruses [49,51,53]. In potato A potyvirus, a single aminoacid substitution controls aphid transmission and virus
accumulation in the plant, suggesting that there is a mechanistic relationship between these two traits; this relationship
Insect transmission of plant viruses Power
does not appear to hold for other potyviruses [54]. In general, the pattern of highly conserved motifs that are responsible
for insect transmissibility suggests that the requirements of
vector transmission exert significant selection pressure that
limits the diversity of coat protein sequences.
Conclusions
Recent molecular studies of geminiviruses and potyviruses,
and of patterns of virus transmission by insects, suggest
that insect transmission imposes significant constraints on
the evolution of plant viruses. The accelerating pace of
molecular studies of viruses will undoubtedly add to our
understanding of the genetic regulation of transmission
specificity. In addition, evolutionary explanations for this
specificity should be explored. Obviously, transmission is
an essential part of virus life history. Yet, it is not obvious
why it should be significantly more difficult for a virus to
increase its range of efficient vectors than to increase its
host range. Future research should address this question.
Acknowledgements
Financial support from the United States Department of Agriculture is
gratefully acknowledged.
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