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Host Plant Resistance and the Spread of Plant Viruses1
GEORGE
Department
of Entomology,
G. KENNEDY"
North Carolina State University, Raleigh 27607
ABSTRACT
Crop cuitivars resistant to insect vectors of plant viruses are likely to alter the population size, activity, and probing and feeding behavior of the vector, thereby influencing
the pattern of virus spread. The effect of a vector resistant cuitivar on virus spread will
depend upon the type of resistance (nonpreference,
antibiosis, or tolerance),
the level of
resistance, the relative importance
of primary and secondary virus spread, the length of
the acquisition,
inoculation,
retention, and latent periods of the virus, and the efrect of
virus infection on vector resistance in the plant. Each combination
of these factors may
result in a different effect on virus spread; the possibilities are discussed.
Because of the
complexities
involved, a thorough
understanding
of the ecology of virus spread, the
biology of vector resistance, and the ecology of the vector arc essential to predict the
effect of vector resistance on virus spread.
virus spread by Aphis craccivora Koch (Evans ]954).
Although no more resistant to rosette virus than other
cultivars,
Mwitunde
often escapes infection
in the
field at least in part because A. craccivora
breeds
more slowly on it than on other cultivars and is eliminated more rapidly by natural enemies. Other factors
may also be involved since aphids reared on Mwitunde have a reduced ability to transmit the virus.
Resistance
in red clover to A cyrthosiphon
pisli/ll
(Harr.)
has been associated with reduced infection
by the clover virus complex present in Minnesota
(Wilcoxon
and Peterson
1960).
]n the field, the
aphid resistant cultivar had less than 10% virus infection, while adjacent plots of a susceptible cultivar
had greater than 90%.
Both cultivars were equally
susceptible to mechanical
inoculation
of the viruses.
The authors concluded that breeding red clover for
resistance to aphids may be a more successful
approach than trying to breed for resistance to virus
diseases.
Thomas and Martin (] 97]) found that non preference by the beet leafhopper,
Circuli/er
f(!llellu'\"
(Baker) was responsible
for a portion of the resistance in certain tomato cultivars to infection by curly
top virus. Vector non preference
accounted
for 2123 % of the resistance of certain tomato cultivars to
infection.
The major portion of resistance to curly
top, however, could not be attributed to vector preference.
A somewhat similar situation was observed
by Linn (1940) who concluded that variation in the
incidence of aster yellows in commercia] plantings of
lettuce cultivars was probably due to differential feeding preferences
of the leafhopper
vector.
Insect resistance in rice has been related to reduced
spread of several virus diseases (Pathak 1970).
For
example, the rice cultivar IR-8 is susceptible to Tungro virus but highly resistant to its vector, the leafhopper Nepl10tettix impicficeps Ishihara.
In the field,
cultivars susceptible
to the vector develop about 4
times as much Tungro virus infection as IR-8. Simi]arly, resistance in IR-8 to the delphacid,
Sogatodes
orizico/a (Muir)
results in a reduction
in the incidence of hoja blanca disease.
Finally, 'Mudgo' rice
is highly resistant
to the plant hopper
vector of
Research on host plant resistance
to insects has
expanded
tremendously
in the last decade and numerous recent comprehensive
reviews on resistance
and its role in pest management
arc available (e.g.,
Maxwell et al. ] 972, Pathak
1970, Stoner
1970,
Luginbill
1969, Gallun et al. 1975, Kogan 1975).
Very limited consideration
has been given to the potential value to plant disease control of resistance to
an insect vector of a plant pathogen.
Painter (] 951 )
recognized the potential value of such resistance in
disease control
as did Holmes
(1954),
Swenson
(1968),
Pathak (1970), Roane (1973), and Adams
( 1975).
There are, however,
relatively
few documented instances in which resistance
to an insect
vector has contributed
to disease control.
Resistance in red raspberry to the aphid AmphoropllOra agathonica
Hottes approaches
complete
immunity (Daubeny
] 966, Kennedy et al. ] 973) and
has been considered
responsible
for the field resistance of certain cuitivars to the common
raspberry
mosaic virus (RMV)
complex.
The cultivar 'Lloyd
George' is immune to A. agatllonica and only rarely
shows symptoms of RMV in the field (Harris ]935).
When artificially infected with RMV by grafting, the
leaves show symptoms (Schwartze and Huber 1937).
In Europe, Lloyd George is an excellent host for the
RMV vector, A. rubi (Kltb.),
and RMV symptoms
arc commonly observed in the field (Harris 1935).
Wilcox and Beckwith (1933) observed a negative
correlation
between the spread of false-blossom
virus
and the relative suitability of cranberry
cultivars as
hosts for the leafhopper
vector, Scleroracus
vaccinii
(Van. D.).
They suggested that field resistance to
false-blossom
virus actually consisted
of resistance
to the vector. This was further supported,
although
not proven, by the agreement
between laboratory
host preference tests with S. vaccinii and field resistance to false-blossom
(Wilcox] 95] ).
A somewhat
more complex relationship
exists in
the field resistance of 'Mwitunde'
peanut to rosette
1 Paper no. 4962 of the Journal
Series of the North Carolina
State Vniv. Agric. Exp. Stn., Raleigh, NC. Received for publication April 2, 1976.
o Asst. Prof. of Entomology.
827
828
Vol. 5, no. 5
ENVIRON M ENTAL ENTOMOLOGY
grassy stunt virus, Nilaparvata lungens (Stat). Mudgo
is susceptible to grassy stunt, but generally escapes
infection in the field because of its resistance to the
vector.
Resistance to an insect vector need not result in a
reduction of disease spread. During a year of high
aphid infestation, Russell (1965) observed no difference between virus incidence in inbred sugar beet
lines resistant and susceptible to the aphid vector.
Baerecke (1958) found spread of leaf roll virus was
greater in aphid resistant potato cultivars than in susceptible cultivars. This was attributed to the greater
activity of aphids between plants of less than optimum host status. Kennedy (1950) recognized this
possibility when he emphasized that both abundance
and activity of winged aphids as well as their ability
to transmit the virus are more important influences
on virus spread than their ability to thrive on the
crop. This is apparent from the fact that aphids will
spread some viruses to plants they do not colonize.
For example, the most important vector of watermelon mosaic virus (= cantaloupe mosaic) in cantaloupe in the southwestern U.S., Myzus persicae
(Sulz.), does not colonize cantaloupe (Dickson 1949,
Dickson et a!. 1949), and cucumber mosaic virus
spread in gladiolus is the result of transient rather
than colonizing aphids (Swenson and Nelson 1959).
Kennedy et at. (1959) discussed the general relationship between host plant suitability and spread of
a nonpersistent virus by an aphid vector; they concluded that the behavior of winged aphids will favor
the spread of nonpersistent viruses among moderate
or borderline hosts more than among better hosts.
This conclusion, however, does not necessarily apply
to persistent (cf. Orlob 1961) or semipersistent viruses which differ from nonpersistent viruses in their
transmission characteristics
(d. Sylvester 1969).
Thus, while the possibility of a vector resistant cultivar increasing the severity of a disease problem is
serious and must be recognized, there are a sufficient
number of examples in which vector resistance has
reduced virus spread to indicate its potential value.
An understanding of the ways in which vector resistance can impact upon disease spread may help to
minimize the use of vector resistance in those instances where it will increase disease spread. This
paper represents an attempt to analyze the relationship between vector resistance and disease spread.
The complexities of this relationship have made desirable the abundant use of references and illustrative
examples; however, no attempt is made to provide a
comprehensive review of the available literature on
virus spread.
General Considerations
Some aspects of the biology and ecology of the
most important insect vectors of plant pathogens,
aphids and leafhoppers, have been reviewed elsewhere (van Emden et a!. 1969, Swenson 1968, Kring
1972, Kennedy and Fosbrooke 1973, DeLong 1971)
as has the general subject of insect transmission of
plant pathogens (Carter 1973, Maramorosch 1969).
The present discussion will be restricted to the spread
of plant viruses, although the interactions discussed
may apply to other pathogens as well.
The effect of a vector resistant cultivar on the
spread of a plant virus will depend upon the type of
resistance (nonpreference, antibiosis or tolerance)
(d. Painter 1951), the level of resistance, the relative
importance of primary and secondary virus spread,
the precise virus-vector relationship (i.e., length of
acquisition, inoculation, retention and latent periods),
and the effect of virus infection on vector resistance
in the plant. Each combination of these factors may
result in a different effect on virus spread. Present
discussions concentrate on the potential responses of
individual insects to resistant plants and their effects
on virus sprcad. It is, however, recognized that virus
spread in the field results from activity of a large
number of individuals, and that all individuals need
not respond in the manner specifically described below for the net effect of the resistance on virus spread
to approach that described. Throughout this discussion, it is assumed that vector resistant and susceptible plants are equally susceptible to the virus. In
actuality, this need not be true and differential virus
susceptibility may profoundly influence patterns of
virus spread in vector resistant and susceptible plants.
Nevertheless, the general virus-vector-plant interactions outlined below will remain influential in determining the ultimate degree of virus spread.
NOllpreference
Resistance
The effect of a feeding non preference on primary
virus spread (i.e., introduction of a virus into a field
from a source outside the field) will depend upon
the rapidity with which the vector recognizes the resistant plant as a nonhost relative in the inoculation
and retention times of the virus. Several possibilities
exist. If the nonpreference is extreme and the vector
does not probe the plant for the inoculation threshold
period, then the virus will not be transmitted; primary
virus spread will be eliminated. This is most likely to
occur with persistent viruses for which there is typically a positive correlation between the inoculation
access period and the probability of transmission
(Sylvester 1969) and which usually are not transmitted during brief probes. Most persistent viruses
must be inoculated into the phloem and typically require probes of 15 min or longer for inoculation
(Watson and Plumb 1972). In addition, this may
occur with some of the semipersistent viruses for
which there is also a positive correlation between
the duration of the inoculation feeding period and
the probability of transmission (Sylvester 1969). It
is unlikely in the case of nonpersistent viruses which
can be transmitted by probes of only a few seconds
duration, unless the resistant plant is recognized as
unsuitable before the vector probes the plant. This
can occur; Mueller (1956 cited by Broadbent 1964)
reported that brown lettuce varieties had only % as
many aphids alight on them and were less frequently
infected with lettuce mosaic virus than green varieties.
With a more moderate non preference in which the
October 1976
KENNEDY:
RESISTANCE AND VIRUS SPREAD
vector must probe the plant for a considerable period
before recognizing it as unsuitable (e.g., Pathak 1971,
Kennedy and Schaefers 1974, 1975), primary spread
wilIlikely not be eliminated. Should tlie duration of
the vector's test probe exceed both the inoculation
and retention times of the virus, the plant wilI become infected with the virus, but the vector will lose
its infectivity. The resulting pattern of primary spread
would be the same as observed in a planting of a
susceptible cultivar. This is most likely to prevail
among the nonpersistent viruses which have brief
retention times (Sylvester 1969) and is less likely
with semipersistent viruses which are retained for
varying periods ranging from hours to days (Sylvester 1969, Swenson 1968). This situation typicalIy
wilI not prevail for persistent viruses which are retained by the vector for many days (Sylvester 1969).
Alternatively, the level of nonpreference may be such
that the vector probes sufficiently long to inoculate
the plant with the virus, but recognizes the plant as
an unsuitable host before it has lost its infectivity.
If the vector then moved to another nearby plant in
search of a suitable host and repeated the procedure
one or more times, the resulting primary spread
could exceed that typically observed in susceptible
cultivars. Those persistent and semipersistent viruses
having relatively short inoculation periods, are most
likely to fall in this category. Despite their very brief
retention times, nonpersistent viruses may also faIl
into this category if the vector probes the plant only
briefly before recognizing it as a nonhost (d. Kennedy et al. 1959).
The overall magnitude of the resistance operating
as a nonpreference will influence the degree of primary spread. If the resistance borders on total immunity as in the case of resistance in red raspberry
to the aphid vector of raspberry mosaic (Kennedy
and Schaefers 1974), then all of the above situations
are possible. The one that prevails will depend on
the probing behavior of the aphid on the immune
plant and the inoculation and retention times of the
viruses involved. If the resistance is less than total
immunity then primary spread wiII probably not be
eliminated, although it may be increased, decreased
or unaffected.
The effect of a nonpreference on secondary virus
spread will be influenced by many factors including
the magnitude of the resistance, the relative importance of transient and resident vector populations in
secondary spread, the acquisition, inoculation and retention times of the virus and the effect of the virus
on the resistance. In the case of aphids, the relative
roles of alatae and apterae in secondary virus spread
have not been completely resolved (d. Swenson
1968). Most evidence suggests that alate aphids occupy a significant role in the secondary spread of
both nonpersistent and persistent viruses (Broadbent
and Martini 1959).
The simplest situation involves a nonpreference
type of immunity in which no vector population develops on the plants and alI secondary spread attributable to the resident vector population is eliminated.
829
Immunity in 'Canby' red raspberry to A. agathonica,
the vector of raspberry mosaic, represents this situation (Kennedy and Schaefers 1974). Secondary
spread by a transient vector population will be related to the vector's probing behavior relative to the
acquisition, inoculation and retention times of the
virus. It will also be influenced by the occurrence
and duration of a latent period for the virus in the
vector. If the transient vector recognizes the virus
infected plant as a nonhost and departs before it has
probed or fed for the acquisition period of the virus,
than secondary spread will not occur. Alternatively,
if the vector probes sufficiently long to acquire the
virus before it recognizes the plant as an unsuitable
host then secondary spread may occur. For nonpersistent and semipersistent viruses which have no latent period in the vector, the amount of secondary
spread will depend upon the proportion of viruliferous vectors moving to other plants in the field as
opposed to leaving the field, and the probing behavior
of the vector relative to the inoculation and retention
times of the virus. The effect of these latter will be
the same as described under primary spread. For
persistent viruses, the duration of the latent period in
the vector relative to the length of time the vector
continues to search the field for a suitable host will
influence secondary spread. Vectors leaving the field
before the latent period has elapsed will not contribute to secondary spread.
When, as is usualIy the case, the resistance is less
than total immunity a resident vector population will
develop and will likely contribute to secondary virus
spread. Since the non preference may result in an
increase in the amount of interplant movement by
members of the resident population, their contribution to secondary spread may be greater than in
plantings of a susceptible cultivar (e.g., Baerecke
1958).
Secondary spread may be profoundly affected if
virus infection results in the loss of resistance to the
vector. Numerous instances are known in which
virus infected plants are more suitable hosts for the
vector than healthy plants (Kennedy 1951). For example, Baker (1960) noted that aphid resistance in
inbred sugar beet lines was lost when the plants were
infected with yellows virus; 3 aphid species were
more fecund and lived longer on virus infected than
on healthy leaves. Arenz (cited in Swenson 1968)"
found reproduction of M. persicae to be greater on \
leaf roll infected plants of a normally aphid-resistant
cultivar than on a healthy susceptible cultivar. This
need not occur, however. Lowe and Strong (1963)
reported that infection by cucumber mosaic virus
reduced the suitability of 3 plant species as hosts
for M. persicae.
Where virus infection resu']ts in a loss of resistance,
the magnitude of that loss and the number of plants
involved (i.e., primary infections) will determine the
size of the resident vector population which develops
and very likely the degree to which it contributes to
secondary spread. The importance of transient vectors in secondary spread will be in part determined
830
ENVIRONMENTAL
by their ability to acquire the virus from an infected
resistant plant.
A ntibiosis Resistance
An antibiosis type of resistance to a vector will
influence virus spread in a manner similar to insecticidal control. The detailed discussions of insecticidal
control of plant virus spread by Broadbent (1957,
.1969) are highly pertinent. In general, an antibiosis
type of immunity, like an effective insecticidal control program, will have little or no effect on primary
virus spread, but will eliminate that portion of secondary spread attributable to resident vector populations. Primary spread and secondary spread by transient vectors would be reduced or eliminated only if
the antibiosis were so effective that it killed the vector or otherwise prevented it from probing for the
requisite virus inoculation and/or acquisition period.
The presence of a dense pubescence of glandular
hairs such as that found in some species of Solanum
(e.g., Gentile and Stoner 1968) might entrap the vector before it could inoculate the plant with the virus.
In most cases, it is unlikely that the vector will be
killed quickly enough to prevent primary spread.
Secondary spread by transient vectors would be prevented if they were killed or incapacitated before
they had the opportunity to acquire the virus, move
to another plant, and infect it with the virus. The
probability of this occurring might be greatest for
persistent viruses which have a latent period.
An antibiosis might influence virus spread in other
ways as well. Where resistance results in an alteration of the vectors normal feeding site, the probability of virus transmission could be altered. This is
most likely for persistent viruses which typically are
acquired and inoculated when the vector feeds in the
phloem (Watson and Plumb 1972). McMurtry and
Stanford (1960) and later Nielson and Don (1974)
demonstrated that resistance in alfalfa to Therioaphis
maculata (Buckton) interferes with that aphid's ability to locate the phloem. What effect, if any, this
has on virus transmission is not known. With sugar
beets, the results of Hills et a1. (1969) suggested that
Ivarietal resistance to the semipersistent beet yellows
virus was due to resistance to virus transmission by
M. persicae rather than resistance to virus infection
per se. Haniotakis and Lange (1974) confirmed this
and demonstrated the resistance to transmission was
associated with differences in the aphids probing behavior on resistant plants.
If resistance alters the pattern of alate production
in an aphid population, the degree of virus spread
might be similarly altered as indicated by the corrclation between the abundance of alate aphids and
virus spread (cf. Swenson 1968). Alate production
in aphids is often closely related to the condition of
the host plant (cf. Schaefers 1972); thus it follows
that aphid resistance might alter the normal pattern
of alate production. This occurs on cantaloupe lines
resistant to A phis gossypii Glover (Kennedy and
Kishaba 1976). A, gossypii populations on resistant
plants are not only smaller, but produce a signifi-
Vol. 5, no. 5
ENTOMOLOGY
cantly smaller percentage of alate progeny than populations on susceptible plants. In those cases where
virus infection does not alter this effect of resistance,
virus infected resistant plants are likely to assume a
reduced importance as sources for virus spread. The
effect of reduced alate production on virus spread
would be greatest when most of the crop acreage
consisted of resistant cultivars and the vector had
few important alternate hosts.
As with insecticides, an antibiosis type of immunity
can be expected to provide little reduction in the
spread of nonpersistent viruses (ct. Broadbent 1957).
Greatest reductions can be expected for persistent
viruses. In the more common situation involving a
moderate level of vector resistance, the reduction in
virus spread may be negligible, especially in individual fields. Virus spread will be reduced to the extent
that it is positively correlated with vector abundance.
Widespread cultivation of a moderately resistant cultivar in a crop that is the principal host of a virus
vector, could significantly reduce the vector population over a large area. Any factor consistently reducing a vector population may be expected to have a
similar or greater impact on virus spread (Swenso.n
1968) .
Tolerance
Tolerance to feeding injury by an inscct pest is a
valuable character (Painter 1951), but if that pest is
also the vector of a plant virus, the use of a tolerant
cultivar could prove disastrous. If larger vector
populations are allowed to develop on tolerant than
on susceptible cultivars, there might be a corresponding increase in virus spread. This would be especially true if the tolerant cultivar were widely cultivated over large areas. The danger of increased virus
spread might extend to other crops susceptible to the
same viruses or affected by viruses transmitted by the
vector. The potential problem is illustrated by the
important role of sugar beets in the spread of watermelon mosaic virus (= cantaloupe mosaic) in cantaloupe in the Imperial Valley of California (Dickson
1949, Dickson et al. 1949). There, large M. persicae
populations leaving sugar beet acquire the virus from
various cucurbits and transmit it to cantaloupe, which
the aphid does not colonize.
Concluding Remarks
Resistance to a virus vector is likely to exert a
complex influence on virus spread. Since nonpreference, antibiosis, and tolerance are often combined
into a single resistant cultivar, their relative contribution to the resistance as well as the overall magnitude
of the resistance will influence the effect of resistance
on virus spread. In addition, since observed virus
spread is the result of both primary and secondary
spread, the relative importance of these and the effect
of the resistance on them is important. The complexities involved are such that without a thorough
understanding of the ecology of both the virus and
vector and the biology of vector resistance it would
be impossible to predict, a priori, the effect of vector
October
1976
KENNEDY:
RESISTANCE
resistance on virus spread. Each combination
of virus, vector, and resistance must be considered
separately.
Because resistance
to a vector may result in an
increased level of virus spread, it is incumbent
upon
those breeding for resistance to consider the probable
effects of vector-resistance
on virus spread. In addition, since resistance to one arthropod species may be
associated with altered levels of susceptibility to other
species, the potential impact on virus spread of cross
resistance to a vector species should not be ignored.
Despite these dangers, the potential
for controlling
certain types of virus diseases through vector resistance is considerable.
There exist a sufficient number
of examples wherein vector resistance has contributed
to disease reduction to justify continued efforts in this
area.
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CITED
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832
ENVIRONMENTAL ENTOMOLOGY
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