Breeding For Resistance To Whitefly-Transmited Geminivirus PDF

Ann. appl. Biol.
(2002), 140:109-127
Printed in Great Britain
109
Breeding for resistance to whitefly-transmitted geminiviruses

By MOSHE LAPIDOT1* and MICHAEL FRIEDMANN2
1
Department of Virology, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250,
Israel
2
Department of Plant Genetics, Agricultural Research Organization, The Volcani Center, Bet Dagan
50250, Israel
(Accepted 11 March 2002; Received 27 December 2001)
Summary
Geminiviruses comprise a large and diverse family of viruses that infect a wide range of important
monocotyledonous and dicotyledonous crop species and cause significant yield losses. The family
Geminiviridae is divided into three genera, one of which is Begomovirus. Species of this genus are
transmitted by the whitefly Bemisia tabaci in a persistent, circulative manner and infect dicotyledonous
plants. Severe population outbreaks of B. tabaci are usually accompanied by a high incidence of
begomoviruses. During the last two decades, there has been a worldwide spread of the B biotype of B.
tabaci, accompanied by the emergence of whitefly-transmitted geminiviruses. Control measures in
infected regions are based mainly on limitation of vector populations, using chemicals or physical
barriers. However, under conditions of severe whitefly attack, none of these control measures has
sufficed to prevent virus spread. Thus, the best way to reduce geminivirus damage is by breeding
crops resistant or tolerant to the virus, either by classical breeding or by genetic engineering. A number
of begomoviruses have been the subject of much investigation, due to their severe economic impact.
This review considers the most severe viral diseases of four major crops (tomato, bean, cassava and
cotton). The approaches taken to breed for resistance to these viral diseases should provide a perspective
of the issues involved in breeding for begomovirus resistance in crop plants.
Key words: Geminivirus, resistance, breeding, cassava, bean, tomato, cotton, Bemisia tabaci
Introduction
Geminiviruses are a large and diverse family of
viruses that infect a wide range of important crop
species, including both monocotyledonous and
dicotyledonous plants, and cause significant yield
loses. These viruses are characterised by the
geminate morphology of the capsid and by circular
single-stranded DNA (ssDNA) genomes. The family
Geminiviridae is divided into three genera, based
on genome structure, plant host and insect vector
(Fauquet et al., 2000). Species of the genus
Mastrevirus (Maize streak virus as type member)
are transmitted by leafhoppers (Homoptera:
Cicadellidae), have a monopartite genome, and
generally infect monocotyledonous plants. Species
of Curtovirus (Beet curly top virus, BCTV, as type
member) are also transmitted by leafhoppers, have
a monopartite genome, but with a different genetic
organisation from that of the mastreviruses, and
infect dicotyledonous plants. Species of
Begomovirus (Bean golden mosaic virus, BGMV, as
type member) are transmitted by the whitefly
Bemisia tabaci (Gennadius) and infect
dicotyledonous plants. Most begomoviruses of the
Old World and all New World begomoviruses
*Corresponding Author E-mail: lapidotm@netvision.net.il
2002 Association of Applied Biologists
have bipartite genomes (A and B components);

however, some Old World begomoviruses,
including Tomato yellow leaf curl virus (TYLCV)
have a monopartite genome. All begomoviruses are
transmitted by their whitefly vector in a persistent,
circulative manner. That is, once the vector feeds
on an infected host plant and acquires the virus,
transmission of the virus can then occur within hours,
and may continue for the life span of the vector
(Cohen & Harpaz, 1964). However, as shown for
TYLCV, transmission efficiency declines with time
(Cohen & Harpaz, 1964).
Control measures in infected regions have
traditionally emphasised vector control (Cohen &
Antignus, 1994; Polston & Anderson, 1997; Hilje
et al., 2001; Palumbo et al., 2001), mainly by
pesticides or physical barriers. Chemical control
methods have been only partially effective, since
whitefly populations can reach very high numbers,
leading to intensive pesticide use (sometimes twice
daily) in attempts to eliminate the vector before it
transmits the virus. Furthermore, there are concerns
that the vector may develop pesticide resistance and
the intense application of pesticides may have
deleterious effects on the environment (Pico et al.,
1996; Palumbo et al., 2001). Physical barriers such
110
MOSHE LAPIDOT & MICHAEL FRIEDMANN
as fine-mesh screens have been used in the

Mediterranean Basin to protect crops (Cohen &
Antignus, 1994). Recently, UV-absorbing plastic
sheets and screens have been shown to inhibit
penetration of whiteflies into greenhouses (Antignus
et al., 1996; Antignus et al., 2001b). Furthermore,
filtration of UV light was shown to hinder the
whiteflies dispersal activity, and consequently
reduce virus spread (Antignus et al., 2001a).
However, adoption of physical barriers adds to
production costs and these screens create problems
of shading, overheating and poor ventilation.
Therefore, the best way to reduce geminivirus
damage is by breeding crops resistant or tolerant to
the virus (Cohen & Antignus, 1994; Pico et al., 1996;
Morales, 2001). Apart from virus transmission,
whiteflies cause extensive damage to crops through
excessive sap removal, excretion of honeydew that
promotes growth of sooty mould fungi, and by
inducing systemic disorders (Byrne & Bellows,
1991). For progress in the development of host plant
resistance to whiteflies see Bellotti & Arias (2001).
Breeding for resistance to begomoviruses, which
is the subject of this review, presents particular
challenges. This review will outline strategies that
must be considered when attempting to breed for
resistance. Since many of the viruses are not
transmitted mechanically, in most cases protocols
must be developed to utilise infective whiteflies to
inoculate target plants with the virus. As a part of
inoculation protocols, symptom severity scales need
to be developed for each disease. Susceptible
controls included in the screen should ideally
become totally infected and show the highest
symptom severity. Once efficient inoculation
protocols have been developed, the crop can be
screened to search for resistant genotypes. The
starting material should consist of available cultivars
and lines of the commercial species, and then
progress to related species based on ease of interspecies crossability. In fact, in many cases, sources
of resistance must be identified in wild species of
the crops in question, and protocols must be defined
to evaluate the levels of resistance observed after
inoculation with the virus. The inheritance of
resistance to begomoviruses has been studied for
many years and several sources of resistance have
been shown to be multigenic. Strategies to map the
genes and develop molecular markers should
facilitate the development of tools to sustain breeding
programmes and allow development of resistance
to multiple viruses.
A prevalent problem in breeding for resistance to
geminiviruses has been the lack (until recently) of
consistency in viral nomenclature different viruses
have the same name, names of viruses keep
changing, acronyms that look like they imply strains
actually signify very different viruses, etc. (Fauquet
et al., 2000). The recent finding that recombination

between species of geminiviruses happens relatively
frequently adds to the already complex situation
(Padidam et al., 1999; Fauquet et al., 2000). This
has caused confusion for breeders and researchers,
making communication difficult, slowing progress,
and causing incorrect assumptions. Moreover,
breeders may not understand the subtle but important
distinctions in nomenclature, which may lead to
mistakes. Recently, new guidelines for concise
nomenclature of geminiviruses have been proposed,
which upon implementation should clarify the
confusion (Fauquet et al., 2000). It is also
recommended, whenever embarking on a
geminivirus resistance breeding project, to use
molecular tools (such as cloning and sequencing) to
accurately define the virus(es) in question.
A number of begomoviruses have been the subject
of extensive study due to their severe economic
impact. This review considers the most severe
geminiviral diseases affecting four major crops
(tomato, bean, cassava and cotton). The approaches
taken to breed for resistance to these viral diseases
should indicate the issues involved in breeding for
begomovirus resistance in crop plants. It should be
noted, however, that in many regions there are
commonly multiple infections of individual plants
with several different viruses or even several
different begomoviruses, so that breeding for
resistance to a single virus may not provide a full
solution to compound begomovirus infections.
Definition of resistance
A prevalent problem associated with breeding for
viral resistance is the lack of standard terminology
used by different researchers. Plant breeders do not
always agree with plant pathologists in regards to
the definition of resistance. Breeders are mainly
interested in improving the performance of a plant
variety under field conditions. Thus, yield and fruit
quality are paramount. In contrast, plant pathologists
place an emphasis on the fate of the virus in the plant.
One of the more problematic terms is whether a plant
in question is resistant to the pathogen itself, or to
the effect of the pathogen symptoms of the disease.
The following definitions of resistance are used in
this review. A host plant is resistant if it can suppress
the multiplication of a virus, and consequently
suppress the development of disease symptoms.
Regardless of the mechanism of resistance (the host
may be resistant to establishment of infection, viral
replication or viral spread within the plant), the final
outcome is the same less virus accumulates in the
resistant host. Resistance can range from very high
(up to immunity in which case no virus
accumulates in the plant rendering it, in fact, a nonhost), to moderate, or low. However, even for low
resistance, the resistant plant will accumulate less
virus than the susceptible host, and will express

milder disease symptoms. Tolerance is a unique
instance where in response to virus infection, the
host expresses negligible or mild disease symptoms,
but supports normal levels of virus multiplication.
Thus, the plant rather than being resistant to the virus,
tolerates the pathogen and despite its presence
expresses mild symptoms and produces a good yield
(Cooper & Jones, 1983; Walkey, 1985).
Breeding for Begomovirus Resistance in
Tomato (Lycopersicon esculentum L.)
Several different begomoviruses, depending on the
geographical areas of cultivation, affect tomatoes
grown in tropical and subtropical regions. One of
the most widespread and economically important
viruses is Tomato yellow leaf curl virus (TYLCV),
which in the Mediterranean Basin affects the crop
mainly during the summer and autumn seasons.
Yield losses due to the virus often reach 100% (Pico
et al., 1996). A disease resembling that now known
to be caused by TYLCV was first reported in 1939
in the Jordan valley, in what later became the state
of Israel, and was associated with outbreaks of
whiteflies (Avidov, 1946). Nearly 20 years later,
farmers started large-scale cultivation of cotton in
the Jordan and Bet Shean valleys, which probably
supported the establishment of large whitefly
populations, close to tomato fields. Indeed in 1959,
concomitant with a heavy infestation of whiteflies,
a disease of uncertain etiology destroyed the entire
tomato crop in the area (Cohen & Harpaz, 1964).
Diseased plants were sampled, and it was found that
the disease was transmitted by whiteflies, hence the
identification of the disease agent as a virus. At first
the virus was identified (erroneously) as Tomato
yellow top virus, which is transmitted by aphids.
Later, it became apparent that a new virus, termed
TYLCV, was the causal agent (Cohen et al., 1961;
Cohen et al., 1963; Cohen & Harpaz, 1964). It took
another 20 years before the geminate particle was
observed by electron microscopy (Russo et al.,
1980). Only in 1988 was TYLCV first isolated
(Czosnek et al., 1988), and shortly after it was shown
to be a monopartite geminivirus (Navot et al., 1991).
Following comparisons of TYLCV isolates from
distinct geographical regions, it became apparent that
the name TYLCV has been given to a heterogeneous
complex of begomoviruses (Moriones & NavasCastillo, 2000). Most of the isolates have a
monopartite genome, as does the type member,
although in one instance (Thailand isolate) a bipartite
genome has been demonstrated (Rochester et al.,
1994). During the last two decades, there has been
a worldwide spread of the B biotype of B. tabaci
accompanied by the emergence of whiteflytransmitted geminiviruses, including TYLCV
111
(Bedford et al., 1994; Polston & Anderson, 1997;

Palmer & Rybicki, 1998; Moriones & NavasCastillo, 2000). TYLCV has been long known in
the Middle East, North and Central Africa, Southeast
Asia, and has later continued to spread to southern
Europe where severe outbreaks have been reported
(Czosnek & Laterrot, 1997; Nakhla & Maxwell,
1998). The virus has also been identified in the
Caribbean (Polston & Anderson, 1997), Mexico
(Ascencio-Ibanez et al., 1999), and in the
Southeastern USA (Polston et al., 1999; Valverde et
al., 2001).
There have been strenuous, prolonged efforts to
breed cultivars resistant to this damaging virus. An
important step in the efforts to breed for TYLCVresistant cultivars has been the development of an
appropriate virus inoculation and screening method
to assess TYLCV resistance (Lapidot et al., 1997).
In essence, 10-day-old seedlings are exposed to large
numbers of viruliferous whiteflies, which upon
feeding on the plants, transfer the virus practically
with 100% efficiency (all susceptible controls
become infected with TYLCV) (Lapidot et al.,
1997). In fact, natural field exposure infection has
been shown to be largely inefficient, as many plants
escape infection, even under heavy inoculation
pressure (Fig. 1). It was shown that only 50% of
susceptible tomato plants were infected during the
first month after planting them in an infected field.
Moreover, despite high whitefly populations and
available inoculum, 90 days after transplanting 10%
of the susceptible plants still escaped infection
(Vidavsky et al., 1998). Thus, it was concluded that
selection of tomato plants based solely on the
absence of symptoms in an infested field could be
misleading (Vidavsky et al., 1998) (Fig. 1).
Furthermore, natural field inoculation led to milder
infection compared to artificial inoculation, probably
due to late and unsynchronised infection (Pico et
al., 1998). In order to search for new sources of
resistance by inoculation of wild species of tomato,
it was necessary to carry out individual inoculations
in cages, since otherwise accessions of some wild
species could escape infection as a consequence of
non-preference by whiteflies (Pico et al., 1998). To
analyse segregating populations for TYLCV
resistance, a symptom severity rating system was
developed, ranging from 0 for plants showing no
visible symptoms, to 4 for plants showing very
severe plant stunting, yellowing, pronounced
cupping and curling of leaves, and cessation of plant
growth (Fig. 2) (Friedmann et al., 1998). However,
the most relevant evaluation of resistance is the effect
of infection on total yield and yield components, as
compared to equivalent non-infected plants (Lapidot
et al., 1997). Usually, tests comparing different
varieties are carried out under field inoculation, and
no comparison is made to the full yield potential of
112
Fig. 1. Field inoculation of susceptible tomato plants with Tomato yellow leaf curl virus (TYLCV). Tomato plants
susceptible to TYLCV (cv. 5656) were transplanted to the field in September 2001, in an area abundant with whiteflies.
The picture was taken 80 days following transplanting. I = Infected; H = Healthy.
Fig. 2. Tomato yellow leaf curl virus (TYLCV) symptom severity rating in segregating F2 populations. Young (10day-old) tomato seedlings from an F2 population segregating for resistance were inoculated with TYLCV using
viruliferous whiteflies. Symptom development was evaluated 30 days after inoculation according to the following
scale: (0) no visible symptoms, inoculated plants show the same growth and development as non-inoculated plants;
(1) very slight yellowing of leaflet margins on apical leaf; (2) some yellowing and minor curling of leaflet ends; (3)
a wide range of leaf yellowing, curling and cupping, with some reduction in size, yet plants continue to develop; (4)
very severe plant stunting and yellowing, and pronounced cupping and curling; plant growth stops.
uninfected plants; information which is necessary

for determining the effect of TYLCV infection on
the yield. Nevertheless, even such imperfect tests
can only be carried out on the most promising new
varieties, as they are lengthy and costly.
One of the major obstacles in the development of
TYLCV-resistance is the assessment of the resistance
level displayed by the plant. Plant age at the time of
infection, inoculation pressure and growth conditions
all have a major effect on the severity of symptoms
induced by the virus (Pico et al., 1998; Lapidot et
al., 2000). Thus, to facilitate the assessment of the
level of resistance to TYLCV in resistant tomato
plants, a panel of differential hosts has been
developed to allow comparative scoring (Lapidot et
al., 2001). The panel comprises seven homozygous
tomato genotypes that exhibit different levels of
TYLCV resistance, ranging from fully susceptible
to highly resistant, based on symptom severity and
virus content. It has been shown that when these
plants are inoculated with TYLCV under different
environmental conditions, although the score of each
individual resistant genotype changes, its ranking
on the scale does not. Thus, to evaluate disease
resistance of a given (test) tomato genotype, the test
genotype is inoculated alongside the panel of
differential hosts, and within four weeks its level of
resistance can be determined relative to its position
on the resistance scale (Lapidot et al., 2001).
Since all cultivars of tomato (Lycopersicon
esculentum) are extremely susceptible to TYLCV,
wild Lycopersicon species have been screened for
their response to the virus (reviewed in Laterrot,
1992; Pico et al., 1996, 1999; Pilowsky & Cohen,
2000). Thus, breeding programmes have been based
on the transfer of resistance genes from accessions
of wild origin into the cultivated tomato. Progress
in breeding for TYLCV resistance has been slow,
primarily because of the complex genetics of the
resistance, and the need to set up a reliable screen
for resistance to the virus, which is dependent on
the availability of viruliferous whiteflies (see above)
(Lapidot et al., 1997; Vidavsky et al., 1998). The
first commercial resistant cultivar, TY20, carrying
resistance derived from L. peruvianum, showed
delay in both symptoms and accumulation of viral
DNA (Pilowsky & Cohen, 1990; Rom et al., 1993).
Thereafter, advanced breeding lines with high levels
of resistance from L. peruvianum (Lapidot et al.,
1997; Friedmann et al., 1998), L. chilense (Zamir et
al., 1994; Scott et al., 1996) L. pimpinellifolium and
L. peruvianum (Vidavsky et al., 1998) and L.
hirsutum (Vidavsky & Czosnek, 1998; Hanson et
al., 2000) have been developed by different breeding
teams and are being used extensively to breed high
quality F1 hybrids. In addition, a number of resistant
F 1 hybrids have been released for commercial
production by several seed companies (Pico et al.,
1998). The tomato line H24 has shown excellent
resistance to strains of TYLCV from Taiwan and
113
south India (Kallo & Banerjee, 1990; Hanson et al.,

2000).
The genetics of resistance to TYLCV has been
studied for a number of the resistant breeding lines
mentioned above. In most cases, the sources of
resistance to TYLCV appear to be controlled by
multiple genes (reviewed in Pico et al., 1996, 1999).
Line TY172, which exhibited the highest level of
resistance in a field trial in which yield components
were evaluated for various resistant cultivars and
lines (Lapidot et al., 1997; Friedmann et al., 1998),
is derived from L. peruvianum (Friedmann et al.,
1998). It is a symptomless carrier of TYLCV, in
which the virus titer is very low. Attempts to produce
disease symptoms on TY172 plants by grafting with
a susceptible infected donor were unsuccessful.
Even when exposed continuously to very high levels
of virus, line TY172 did not develop disease
symptoms (Friedmann et al., 1998). The resistance
in line TY172 is controlled by at least three
interacting genes (Friedmann et al., 1998). The
highly resistant line 902 is derived from a cross
between two L. hirsutum accessions resistant to
TYLCV, followed by crossing to L. esculentum and
selfing resistant symptomless individuals (Vidavsky
& Czosnek, 1998). In addition, an advanced
breeding line (F 8 generation) derived from L.
pimpenellifolium hirsute and a line derived from
L. chilense that underwent four backcrosses to L.
esculentum exhibit strong resistance as evidenced
by symptomless scores (Vidavsky et al., 1998). The
resistance in L. hirsutum appears to be controlled
by two to three additive recessive genes (Vidavsky
& Czosnek, 1998) and that of L. pimpinellifolium
by one major gene (Vidavsky et al., 1998). The L.
chilense LA1969 source is controlled by a major
gene termed TY-1 and at least two more modifier
genes (Zamir et al., 1994) and a number of
commercial hybrids have been released carrying this
resistance. The hirsutum source used in the AVRDC
(Asian Vegetable Research and Development
Center) breeding programme is controlled by two
genes acting epistatically (Hanson et al., 2000).
Wild tomato species have also been screened to
identify sources of resistance to other begomoviruses
affecting tomato worldwide. Several wild species
accessions were shown to have varying degrees of
resistance to a Venezuelan strain of Tomato yellow
mosaic virus (ToYMV) which causes severe losses
to tomato crops in Venezuela (Piven et al., 1995).
This virus is transmitted both mechanically and by
whiteflies. Interestingly, different accessions of wild
species showed varying resistance to the virus,
depending on the inoculation method utilised (Piven
et al., 1995). The L. chilense accession LA1969,
which is a good source of resistance to TYLCV
(Zakay et al., 1991), as well as to the Taiwan strain
of TYLCV (Chiang et al., 1984) was found to be
highly resistant to ToYMV (Piven et al., 1995).
However, it developed symptoms when inoculated
114
mechanically, suggesting either avoidance of

transmission, or inhibition of initial entry of the virus
into plant cells as a mechanism of resistance (Piven
et al., 1995). Breeding lines (F5 generation) derived
from a cross with L. peruvianum were reported as
having nonspecific immunity to several pathogens,
including Tomato yellow top virus (TYTV) and Beet
curly top virus (BCTV) (Thomas & Mink, 1998).
Tomato mottle virus (ToMoV) is an important
geminivirus affecting tomato in Florida (Polston et
al., 1993). There is an ongoing programme at the
University of Florida to introgress ToMoV resistance
from accessions of L. chilense, a species difficult to
use for gene transfer due to interspecific crossability
barriers. In segregating populations from crosses to
tomato, there was a high number of susceptible
progeny, suggesting a multigenic control of
resistance for all the L. chilense accessions studied
(Scott et al., 1996). Several of the lines also had
effective TYLCV resistance.
Recently, a number of TYLCV-resistant tomato
lines exhibited resistance to unrelated
begomoviruses in a field trial in Guatemala (Mejia
et al., 2001). Preliminary results showed the lines
to have decreased symptoms and higher yields than
a susceptible control. The resistant lines showed
differential levels of infection with three
begomoviruses known to be present in the area of
the trial, Tomato severe leaf curl virus, Tomato
golden mottle virus and Pepper golden mosaic virus
(Mejia et al., 2001).
Currently, inoculation protocols exist for TYLCV,
which together with highly resistant breeding lines
derived from different wild species, are already
resulting in the commercial release of resistant
cultivars suitable for production in regions where
TYLCV is a major constraint. There is the additional
issue of adaptability of a given resistant variety to
the growing conditions of a particular region it is
likely that local breeding programmes will need to
incorporate the resistance from the cultivars being
released into locally adapted cultivars. Such
breeding programmes would benefit greatly from
molecular markers linked to the resistance genes.
In addition, molecular markers to the different
sources of resistance will be required in order to
allow the pyramiding of these genes. Further work
is needed to ascertain whether the TYLCV-resistant
cultivars will be resistant to other economically
important begomoviruses.
Breeding for Begomovirus Resistance in
Common Bean (Phaseolus vulgaris)
The common bean (Phaseolus vulgaris) is a major
crop that is severely affected by begomoviruses.
Bean golden mosaic has become the most serious
viral disease of common bean throughout Latin
America and the Caribbean, and has caused severe

damage to snap bean production in Florida (Blair et
al., 1995; Bianchini, 1999; Singh et al., 2000b;
Morales, 2001; Morales & Anderson, 2001). Disease
symptoms include plant dwarfing and malformation,
leaf chlorosis, abortion of flowers and pods, pod
malformation, and reduction of seed yield and
quality (Morales & Niessen, 1988; Bianchini, 1999).
The causal agent of bean golden mosaic is Bean
golden mosaic virus (BGMV). Studies of BGMV
from different geographical regions revealed a
number of strains of the virus, which form two
groups, BGMV type I and II (Faria & Maxwell,
1999; Garrido-Ramirez et al., 2000; Morales &
Anderson, 2001). Type I BGMV isolates are found
in South America and are not sap-transmissible,
whereas type II isolates are found in Central
America, the Caribbean Basin and Florida, and are
sap-transmissible. The nomenclature of BGMV was
revised recently, and type II BGMVs were renamed
Bean golden yellow mosaic virus (BGYMV)
(Fauquet et al., 2000).
Bean is also attacked by TYLCV, which has led
to increased infection of both bean and tomato crops
in Spain, in regions where they are inter-cropped
(Navas-Castillo et al., 1999; Sanchez-Campos et al.,
1999). Resistance to TYLCV has been observed in
commercial varieties, but the inheritance has not yet
been evaluated (Lapidot, 2002).
A protocol for inoculation of bean with BGYMV
by viruliferous whiteflies has been described,
resulting in 100% infection of susceptible parental
lines and uniform timing of symptom expression
(Velez et al., 1998). Likewise, protocols for
mechanical inoculation have been developed
(Morales & Niessen, 1988). In analysing segregating
material for resistance to BGYMV, several symptom
severity ratings have been described (Morales &
Singh, 1993; Bianchini, 1999). A strong effect of
plant age on the incidence of infection was found
when bean plants were inoculated mechanically with
BGYMV. Infection rates dropped from 100%
infection in 7-day-old plants, to 0% infection in 12day-old plants (Morales & Niessen, 1988).
Similarly, the success rate of TYLCV infection by
whiteflies was highly dependent on bean plant age.
When 14-day-old susceptible bean plants were
inoculated, nearly total infection was achieved but,
when 12- or 26-day-old plants of the same variety
were inoculated, the infection rates were only 40%
and 34%, respectively (Lapidot, 2002). Thus the
same phenomenon occurred in both studies a
distinct dependence of infection success rates on
bean plant age.
There have been extensive programmes to search
for sources of resistance and develop bean cultivars
highly resistant to BGYMV. Several sources of
resistance have been identified and utilised to breed
resistant varieties. There are two major groups of

common bean germplasm, the Middle American and
the Andean groups, which apparently were
domesticated separately, from different wild bean
populations. Each group is divided into three races.
For the Middle American group, Durango, Jalisco
and Mesoamerica races are characterised by small
and medium seeded black, small red, pink, white
and pinto types. For the Andean group, the Chile,
Nueva Granada and Peru races are characterised by
medium and large seeded kidney bean, red mottled
and snap bean types. Members of the group can be
intercrossed, yet genetic barriers exist in some cases,
necessitating the use of bridging lines (Morales &
Singh, 1991).
The Mesoamerica race includes the landraces
Porrillo Sintetico and Turrialba 1 which are resistant
to infection by BGYMV, showing delayed chlorosis.
These have been used as the source of resistance for
many of the cultivars that have been released
(Bianchini, 1999; Singh et al., 2000a). However,
under severe disease pressure, the resistance breaks
down, leading to leaf chlorosis and yield losses
(Singh et al., 2000b). The Durango race also
contains landraces with resistance to BGYMV, such
as Garrapato which possesses the gene bgm (or
bgm1), which confers partial resistance, and differs
from the resistance derived from Porrillo Sintetico
(Urrea et al., 1996; Singh et al., 2000b). The
combination of both sources of resistance led to the
development of the highly resistant breeding line
A429 (Velez et al., 1998; Singh et al., 2000c). This
line expresses very attenuated symptoms upon
infection, but lacks the desirable horticultural
characteristics required for release commercially
(Velez et al., 1998). The Nueva Granada race also
possesses resistance to BGYMV, such as the line
Royal Red, carrying the resistance gene bgm2.
This line resists pod deformation caused by
BGYMV, but is susceptible to leaf chlorosis
(Morales & Niessen, 1988). These two recessive
genes, bgm and bgm2 are non-allelic (Velez et al.,
1998).
The genetics of resistance to BGYMV was studied
in a 8 8 complete diallel cross (Morales & Singh,
1991). The parents and hybrids were inoculated
mechanically with BGYMV under greenhouse
conditions, and different symptoms were scored on
a scale of 1 (symptomless) to 9 (most severe
symptoms). Resistances from the classic sources
Porrillo Sintetico and Royal Red were shown to be
largely additive (Morales & Singh, 1991). In another
study using recombinant inbred lines derived from
a cross between a genotype belonging to the
Mesoamerica strain and a genotype of the Durango
strain, several lines showed transgressive values for
resistance or susceptibility as compared to the parent
lines. This indicated that the genes controlling
115
BGYMV resistance in the parent lines were different

and complementary (Morales & Singh, 1993). A
recombinant inbred population derived from the
cross of Dorado (resistant) and XAN176
(susceptible) was used together with random
amplified polymorphic DNA (RAPD) markers to
identify two quantitative trait loci (QTLs) linked to
resistance to BGYMV (Miklas et al., 1996). The
two QTLs had a cumulative additive effect that
explained 60% of the phenotypic variation for
resistance.
As mentioned already, although resistant cultivars
have been developed from single sources of
resistance, they are not adequate under heavy
inoculum pressure. Recent studies have shown that
by pyramiding resistance genes derived from
different races in P. vulgaris, highly resistant lines
may be developed (Urrea et al., 1996; Velez et al.,
1998; Singh et al., 2000a,b). For instance, the highly
resistant line DOR 303 resulted from a combination
of the Mesoamerica strain Porrillo Sintetico with the
New Granada line Royal Red, (Velez et al., 1998).
Other promising breeding lines were developed, such
as line 9236-6, whose resistance was derived from
the previously developed line A429, which showed
resistance to chlorosis due to the single recessive
gene bgm. Likewise, line 9245-94, whose resistance
was derived from DOR303, was shown to carry the
recessive gene controlling resistance to chlorosis,
bgm2 (Velez et al., 1998). In addition, sources of
resistance are found in the secondary gene pool of
common bean (P. constaricensis, P. coccineus, P.
polyanthus). Highly resistant lines have been
developed from interspecific crosses between P.
vulgaris and P. coccineus showing mild and delayed
symptom expression and higher yields upon
BGYMV infection than the susceptible controls,
even under increased virus incidence (Bianchini,
1999; Singh et al., 2000b).
The identification of different sources of resistance
to BGYMV, together with the development of
molecular markers to some of the sources, should
facilitate the release of highly resistant cultivars
based on the combination of resistance genes.
Breeding for Resistance to Begomoviruses in
Cassava (Manihot esculenta)
Cassava (Manihot esculenta) is a staple food in
many parts of the developing world, and especially
in Sub-Saharan Africa where it is severely affected
by begomoviruses. This crop presents a challenge
for breeding for begomovirus resistance, due to its
perennial habit and propagation by vegetative
cuttings rather than by seeds. Consequently, the
incidence of the disease increases during successive
cycles of cultivation, and new crops are affected if
diseased cuttings are used for propagation.
116
Therefore, this has a direct bearing on the breeders

evaluation of the level of resistance that is apparent
in a given field. Cassava mosaic disease (CMD) is
wide spread throughout Sub-Saharan Africa, South
India and Sri Lanka and is the most important factor
limiting cassava yields in many locations (Fauquet
& Fargette, 1990; Fargette et al., 1996; Thresh et
al., 1998b; Legg, 1999; Legg & Thresh, 2000). The
disease is caused by a number of begomoviruses,
occurring singly or together (Thresh et al., 1998c;
Fondong et al., 2000b; Berry & Rey, 2001; Pita et
al., 2001a). Currently, four distinct begomoviruses
have been found associated with CMD in Africa:
African cassava mosaic virus (ACMV), East African
cassava mosaic virus (EACMV) (Swanson &
Harrison, 1994), an ACMV-EACMV recombinant
virus which has been referred to as either Ugandan
variant virus (UgV) or as EACMV-Ug (Deng et al.,
1997; Zhou et al., 1997) and South African cassava
mosaic virus (SACMV) (Berrie et al., 1998). For a
recent review on the diversity of African cassava
begomoviruses see Pita et al. (2001a).
Cassava yields in Africa are much lower than their
full yield potential (5-10 tons ha-1 compared with
80 tons ha-1), mainly due to insect pests and diseases
and the use of infertile soils (Fauquet & Fargette,
1990). In fact, CMD can cause yield losses of up to
95%, (Legg, 1999), and annual losses have been
estimated at 30% (Fargette et al., 1996). The
incidence of the disease coincides with the whitefly
populations and with the rainfall cycle of the year
(Legg & Thresh, 2000). Since cuttings used
routinely to propagate the crop can also transmit
CMD, sanitation and selection of healthy cuttings
are an important component of control of the disease
(Thresh & Otim-Nape, 1994; Gibson & Otim-Nape,
1997; Thresh et al., 1998a; Fondong et al., 2000a).
The symptoms of CMD are affected by
temperature, being suppressed above 35C (Hahn
et al., 1980; Fondong et al., 2000a). This has a direct
bearing on screening for resistance. Consequently,
field screening is carried out in areas with high
inoculum pressure and where the average
temperature is relatively low (below 30C). A
symptom severity rating ranging from 0 (no
symptoms) to 5 (severe mosaic and distortion of the
entire leaf), has been defined and used in several
breeding programmes including those of IITA
(International Institute of Tropical Agriculture,
Ibadan, Nigeria), where there has been a longstanding programme to breed CMD resistant cassava
cultivars (Hahn et al., 1980, 1989; Fargette et al.,
1996).
The evaluation of resistance to CMD is
complicated by the fact that cuttings taken from
infected plants may grow into symptomless plants,
this being more prevalent in resistant cultivars
(Gibson & Otim-Nape, 1997; Thresh et al., 1998b).
This is a result of the virus not becoming fully

systemic in highly resistant cultivars, and where the
virus titer is also low. This leads to a slower spread
of the virus, and thus, some cuttings, although taken
from infected plants, may grow into healthy plants,
a phenomenon termed reversion. Therefore,
reversion is important in reducing the incidence of
infection in the cassava stocks used for propagation
(Gibson & Otim-Nape, 1997; Fondong et al., 2000a).
Moreover, symptomless cuttings may arise as a result
of exposure to high temperatures. Likewise, selection
of cuttings from healthy rather than infected plants
for propagation also affects the spread of the virus.
Thus, in addition to the primary infection due to
whitefly inoculation, there is also a secondary spread
due to propagation from cuttings. This affects the
incidence of the disease when monitored over a
period of several years. Mathematical simulations
to assess the interactions of the different parameters
affecting CMD epidemics have been developed
(Fargette & Vie, 1995), and have shown that host
resistance, in combination with reversion and cutting
selection, can potentially reduce the incidence of
disease significantly. Resistant cultivars therefore
not only suffer less yield loss than susceptible plants,
but also are less likely to become heavily infected,
even after many years of successive cropping, as
long as their use is combined with selection of
healthy cuttings and expression of reversion.
No adequate level of resistance to CMD was found
in the cultivated cassava species Manihot esculenta.
Therefore, resistance was introgressed from other
related Manihot species by interspecific crosses
(Hahn et al., 1980), including the ceara rubber M.
glaziovii (Fargette et al., 1996; Fregene et al., 2000).
The generation of resistant germplasm dates back
to the 1930s in Eastern Africa and Madagascar
(Jennings, 1994; Cours et al., 1997; Fregene et al.,
2000; Morales, 2001). The material generated by
Storey in the 1930s (Storey, 1936) has been a major
source of resistance for breeding programmes. An
epidemic in Madagascar in the 1930s almost
eliminated the cultivation of cassava and led to the
generation and deployment of resistant varieties
generated from inter-specific crosses (Cours et al.,
1997). This, in combination with utilising CMDfree cuttings for propagation and roguing of diseased
plants, has helped to maintain a low incidence of
CMD. However, the varieties developed in
Madagascar showed a lower level of resistance under
high inoculum pressure in the Ivory Coast (Cours et
al., 1997). Since cassava originated in Latin
America, there are several related species there with
potential for resistance to the virus (Fargette et al.,
1996). Backcrosses to the cultivated cassava are
needed, in order to increase the yield potential, both
of the tuberous roots (major carbohydrate source)
and of the leaves (used as a vegetable) (Jennings,
1994). In fact, a number of inter-specific hybrids

have been developed which show good resistance
and have been used in breeding programmes (Hahn
et al., 1989; Fargette et al., 1996). Resistance from
the interspecific cross in cassava has been reported
to be recessive, polygenic and additive with a
heritability of about 60% (Hahn et al., 1980, 1989).
Lines with improved resistance have been developed
both at IITA and at CIAT (Centro Internacional de
Agricultura Tropical, Cali, Colombia), these retain
the desirable horticultural traits and quality of the
cassava products. Studies are beginning to emerge
comparing the resistance of newly released CMDresistant cassava lines. The components of resistance
to CMD were compared over a number of years for
several cassava cultivars (Fargette et al., 1996).
Significant correlations were found between
symptom intensity, disease incidence and virus titre.
Interestingly, a close relationship between disease
incidence and yield reduction was not found when
the yield was compared between infected and healthy
plants of five selected cultivars (Fargette et al.,
1996). This has a direct bearing on the efficacy of
breeding programmes based on screening material
according to disease symptoms and incidence.
Therefore, the authors suggested that yield
assessments should be included early in breeding
programmes, in order to complement screens for
symptom intensity, which are highly variable.
However, it seems that a larger sample of cultivars
should be assayed for yield loss under infection in
order to test this lack of correlation. Nevertheless,
the authors concluded that the use of highly resistant
germplasm showing a high field resistance,
combined with the selection of healthy cuttings for
propagation, should limit the impact of CMD to a
large extent (Fargette et al., 1996).
A number of cultivars were assessed for resistance
to CMD in multi-location trials in Uganda, where
there is a severe ongoing epidemic (Otim-Nape et
al., 1998). This is in part due to the intercropping of
resistant and susceptible varieties, exposing the
former to high inoculum pressures (Thresh et al.,
1998b; Morales, 2001). There were considerable
differences in the rate of spread of the disease among
different sites in the country as well as large
differences in the extent of field infection of
susceptible genotypes. Nevertheless, a number of
improved genotypes showed considerable resistance
to infection and have been released for use in Uganda
(Otim-Nape et al., 1998). Recently, several
genotypes from the IITA germplasm collection were
assessed for resistance to CMD and other major
diseases affecting cassava in Africa, under natural
infestation conditions (Fokunang et al., 2000). CMD
incidence and severity reached a peak 3 months after
infection, with the severity being high in 80% of the
genotypes. In addition, the severity of the disease
117
was negatively correlated with tuberous root number

and weight.
Breeding for begomovirus resistance in cassava
requires the standardisation of inoculation protocols
that will address the phenomenon of reversion, so
as to assess properly the resistance level of the
material being screened. The development of
molecular markers linked to resistance genes would
be extremely valuable, as it would allow screening
of symptomless propagation material to ascertain it
comes from a resistant source.
Breeding for Resistance to Begomoviruses in
Cotton (Gossypum hirsutum L.)
The two most prominent whitefly-transmitted
diseases of cotton are cotton leaf crumple disease,
and cotton leaf curl disease. Since high incidences
of both diseases are associated with high whitefly
populations, begomoviruses have been a major
candidate as the causal agents of the disease. Indeed,
Cotton leaf crumple virus (CLCrV), a bipartite
begomovirus (Nadeem et al., 1997), was found to
be associated with the crumple disease (Brown &
Nelson, 1984; Briddon & Markham, 2000). Cotton
crumple disease mainly affects cotton in the southern
USA, and causes relatively mild symptoms since it
usually appears late in the cotton growing season.
This may explain why breeding cotton for resistance
to CLCrV is progressing rather slowly. It has been
shown that the resistance of Cedix, a highly resistant
cotton cultivar to CLCrV from El Salvador, is
controlled by two dominant and supplementary
genes, which must occur together in order to confer
full resistance (Wilson & Brown, 1991). Resistant
lines, however, appear to have relatively low yields
and this has complicated the development of elite,
resistant cultivars. Recently, more efforts were made
to find resistance in upland cotton to CLCrV
(Natwick et al., 2000). In this study, the researchers
developed a rating system for disease symptom
severity, molecular tools for disease evaluation, and
most importantly, confirmed that cotton leaf crumple
disease is indeed induced by CLCrV. However, due
to a lack of an alternative inoculation system,
Natwick et al. (2000) have had to rely on field
infection, which hinders progress.
In the last decade cotton leaf curl disease (CLCuD)
has become the major limiting factor of cotton
production in Pakistan (Briddon & Markham, 2000).
Recently, the disease spread to India (Briddon &
Markham, 2000). Due to the severity of the disease,
and the widespread presence of whitefly populations,
the 1993 Pakistan cotton crop was declared a disaster
(Brown, 1996). Since whiteflies transmit the disease,
and the symptoms were indicative of geminivirus
infection, a begomovirus was sought as the causal
agent of the disease. Indeed, in 1993 a monopartite
118
begomovirus was found in CLCuD-infected cotton

plants, and named Cotton leaf curl virus (CLCuV)
(Mansoor et al., 1993). However, full-length
infectious clones of CLCuV were unable to induce
the characteristic symptoms of CLCuD in cotton.
Thus, other factors involved in inducing CLCuD
were sought. In 1999, Mansoor and co-workers
(Mansoor et al., 1999) found a smaller ssDNA
molecule (termed DNA 1) that was associated with
CLCuD. DNA 1 could self-replicate in plant cells
but required CLCuV for spread in plants and for
insect transmission. However, it was found that
DNA 1 plays no part in inducing disease symptoms.
Only recently, an additional small (c. 1350
nucleotides) ssDNA molecule (termed DNA b) was
isolated from CLCuD-infected cotton plants
(Briddon et al., 2001). DNA b requires CLCuV for
replication and encapsidation, and when coinoculated with CLCuV to cotton plants, induces
symptoms typical of CLCuD. Thus, the
begomovirus (CLCuV) DNA b complex represents
the infectious unit responsible for CLCuD (Briddon
et al., 2001).
Although resistant cotton cultivars are required,
and despite considerable efforts, progress in breeding
cotton for resistance to CLCuD has been slow,
mainly since breeders have had to rely on field
inoculation, and until very recently were unable to
identify the disease-inducing agent. Nevertheless,
resistant cotton cultivars have been developed in
Pakistan, and some show high resistance and/or even
seem to be immune. However, these cultivars have
narrow adaptability to different growth conditions,
and yield less than uninfected susceptible cultivars
(Briddon et al., 2000; Rahman et al., 2001). The
authors suggest that the highly resistant cultivars
could be grown together with better-adapted tolerant
cultivars, and thus diminish the spread of the disease
while reaching acceptable yields. It was also found
that the Pakistan native cotton (Desi, Gossypium
arboreum) is resistant to the virus, but the majority
of cotton cultivated in Pakistan is Gossypium
hirsutum (Briddon et al., 2000; Rahman et al., 2001).
This may indicate that the disease is not new to the
Pakistan area, and that the wide use of susceptible
hirsutum cultivars contributed to the current
epidemics. Support of this suggestion comes from
the finding that the most popular cotton varieties
used in the last decade in Pakistan are highly
susceptible to the disease (Briddon et al., 2000). In
breeding for resistance, a strong environmental
interaction with genotypes has been shown to
confound the results. The level of resistance
exhibited by different lines was affected by the year
of the trials, perhaps as a result of differences in the
incidence of the virus present in each year (Rahman
et al., 2001).
In order to select for resistant genotypes it would
therefore be advisable to develop protocols of

artificial inoculation using whiteflies carrying all the
components of CLCuV. These studies should be done
under strong inoculation pressure and consistent
environmental conditions.
Development of Molecular Markers Linked to
Resistance to Begomoviruses
It would greatly facilitate the development of
resistant germplasm if molecular markers, based on
polymorphism of DNA sequences, linked to
resistance genes were identified to aid in the selection
process during the breeding efforts. Without
molecular markers, breeding for viral resistance is
limited to a phenotypic screen of the resistant plants,
i.e., selecting plants solely on the basis of the
presence or absence of symptoms or on symptom
severity. Since the begomoviruses are transmitted
by whiteflies, the inoculations and screening are
limited to the warmer seasons of the year. Moreover,
the use of field inoculation, even in an area of very
high activity of viruliferous whiteflies, is inefficient
and can be misleading (Vidavsky et al., 1998) (Fig.
1). Thus, the use of molecular markers should
enhance the efficiency and reliability of methods for
screening for resistance, and should reduce the costs
associated with classical breeding for resistance
(Kelly, 1995; Chague et al., 1997). Identifying
molecular markers linked to each source of
resistance will enable the study and understanding
of the genetic components that influence viral
resistance. The mapping of resistance genes from
different sources will indicate which genes may be
common to different sources, and which may be
distinct. This will be of great value in determining
how to combine different sources of resistance in
breeding programmes.
Lander and Botstein (1989) suggested that by
using molecular markers strategically positioned
throughout the genome, QTLs could be identified,
mapped, and analysed. Using L. chilense as the
resistance donor, Zamir et al. (1994) mapped the
TYLCV-resistance gene, TY-1, to chromosome 6.
Two more resistance modifier genes were mapped
to chromosomes 3 and 7 (Zamir et al., 1994).
Another TYLCV-resistance gene, originating from
L. pimpinellifolium and accounting for 27.7% of the
resistance, has been mapped by using RAPD PCRbased markers to chromosome 6, but to a locus
different from TY-1 (Chague et al., 1997). Recently,
Tomato leaf curl Taiwan virus (ToLCTWV, termed
by the authors as TYLCV Taiwan isolate) resistance
originating from the wild tomato species L. hirsutum
was mapped to chromosomes 8 and 11 (Hanson et
al., 2000). By marker-assisted selection, the
introgression on chromosome 11 was shown to
confer resistance to both ToLCTWV and Tomato leaf
curl Bangalore virus (ToLCBV; Hanson et al., 2000).

It is likely that combining genes from different
sources of resistance can lead to superior levels of
resistance to begomoviruses. For instance, Pilowsky
et al. (1997) developed the highly TYLCV- resistant
TY172 and TY197 lines by combining lines that
expressed moderate levels of resistance to TYLCV.
Thus, combining resistances derived from different
wild tomato species, such as L. hirsutum, L. chilense,
L. peruvianum and L. pimpinellifolium, could result
in breeding lines expressing high and stable levels
of resistance to TYLCV (Vidavsky et al., 1998).
Molecular markers linked to each source of
resistance would greatly simplify the process of
combining different genes into breeding material.
A codominant RAPD marker tightly linked to the
bgm (or bgm1) gene from the common bean
Garrapato resistant source was developed by
applying bulked segregant analysis (Urrea et al.,
1996). The marker R2 570/530 was then identified in
lines likely to contain the bgm gene. The marker
was also used to confirm that the resistant source
DOR303 contains a resistance gene distinct from
the bgm gene (Velez et al., 1998). Recently, highly
resistant lines that combine different sources of
resistance to BGYMV have been released and shown
to contain both the R2 570/530 marker as well as a
sequence characterised amplified region (SCAR)
marker SW12 700 linked to a gene derived from the
Porrillo Sintetico resistance (Singh et al., 2000b).
Therefore, incorporation of molecular markers
linked to different resistance genes allows for the
pyramiding of resistances into breeding lines and
cultivars, which greatly enhances the resistance to
the virus. Markers enable breeders to identify which
resistances have been bred into highly resistant lines,
whose main source of resistance would otherwise
remain unknown (Bianchini, 1999).
A concerted effort is being made at CIAT and other
institutes to establish a molecular genetics platform
for cassava, which should facilitate and lead to the
generation of molecular markers linked to CMD
resistance (Fregene et al., 2001). This platform
includes the generation of a molecular genetic map
of cassava constructed with molecular markers such
as restriction fragment length polymorphism
(RFLP), RAPDs, microsatellites, and isozymes,
initially estimated to cover approximately 60% of
the cassava genome (Fregene et al., 1997). Since
the generation of the map, markers have been
continuously added to it, especially simple sequence
repeat (SSRs) and expressed sequence tags (ESTs)
(Fregene et al., 2001). Amplified fragment length
polymorphism (AFLP) markers were used to screen
CMD-resistant and susceptible cassava accessions
and the resulting band patterns allowed the clustering
of the accessions into groups based on geographical
location and/or CMD resistance (Fregene et al.,
119
2000). Although a particular AFLP marker linked

to CMD resistance was not reported, the molecular
genetic map being generated should lead to the
development of molecular markers linked to CMD
resistance from different accessions.
Pathogen-Derived Resistance of Begomoviruses
The breakthrough in recombinant DNA
technology and the establishment of transformation
and regeneration systems for plants has enabled the
use of a genetic engineering approach for breeding.
The concept of pathogen-derived resistance (PDR)
was proposed by Sanford & Johnston (1985), who
suggested engineering resistance by transforming a
susceptible plant with gene sequences derived from
the pathogen itself. It was suggested that the
expression of certain key gene products of a
pathogen by the plant either in an inappropriate form
or amount, or at an inappropriate time during the
infection cycle could disturb infection by the
invading pathogen (Sanford & Johnson, 1985). The
first manifestation of PDR was provided by the
demonstration that transgenic tobacco plants
expressing the tobacco mosaic virus (TMV) capsid
protein (CP) were resistant to infection with TMV
(Powell Able et al., 1986). Subsequently, there have
been several successful attempts to generate virus
resistance in transgenic plants based on this concept
through the expression of virus-derived genes or
genome fragments (Lomonossoff, 1995; Baulcombe,
1996).
A number of PDR strategies have been
investigated for the control of begomoviruses
(Frischmuth & Stanley, 1993). These can be arranged
into five categories: a) capsid protein-mediated
resistance, b) movement protein-mediated
resistance, c) defective interfering (DI) viral DNA,
d) genes in antisense orientation, e) truncated or
mutated replicase (Rep) (C1 or AC1) gene. The first
two approaches involve expression of viral capsid
or movement proteins in order to inhibit viral
proliferation. The last three categories, despite
differences in transgene construct used, all aim to
inhibit viral replication by disrupting the activity of
the Rep gene. This is not surprising, since the Rep
gene encodes the only viral protein that is
indispensable for geminiviral DNA replication
(Brough et al., 1988; Elmer et al., 1988; Etessami et
al., 1991).
Capsid protein-mediated resistance
Capsid protein-mediated resistance (CPMR) has
been used extensively and successfully to induce
resistance to many RNA viruses (Fitchen & Beachy,
1993). The first attempt to use CPMR for
begomoviruses was by Kunik et al. (1994). Primary
(R0) transgenic plants of an interspecific tomato
120
hybrid transformed with the TYLCV CP gene (V1)

showed a delay in symptom development and a
recovery from viral infection with time. The
resistance was manifested only by expression of the
transgenic protein, since transgenic plants expressing
the CP gene only at the RNA level showed no
resistance to viral infection (Kunik et al., 1994).
Sinisterra et al. (1999) transformed tobacco plants
with a modified CP gene (30 nucleotides were
deleted from the 5 end) of ToMoV. Inoculated plants
varied in response from susceptibility to immunity.
The transformed plants expressed the transgene
transcript, but the transgene product could not be
detected. However, there was a positive correlation
between the presence of the transgene and resistance,
although the correlation was not 100%. Moreover,
in some cases the presence of the transgene gave
rise to infected plants that expressed unusual
symptoms. The authors concluded that the resistance
could be due to a RNA-mediated mechanism
(Sinisterra et al., 1999).
The above reports are the only ones demonstrating
successful resistance mediated by begomovirus CP.
Azzam et al. (1996) have expressed the CP of
BGYMV in transgenic beans. However, the
transformed plants were susceptible to the virus and
exhibited severe symptoms similar to those of nontransgenic plants. The transformed plants expressed
the transgene transcript but not the viral CP, which
may account for the lack of resistance. However,
transgenic Nicotiana benthamiana plants that
expressed the CP of ACMV also failed to express
any level of resistance (Azzam et al., 1996;
Frischmuth & Stanley, 1998). With TMV (an RNA
tobamovirus), it has been demonstrated that CPMR
affects early stages of viral penetration into cells,
probably at the stage of viral disassembly (Fitchen
& Beachy, 1993). While TMV is transmitted
mechanically to leaf mesophyl cells, begomoviruses
are transmitted by whiteflies into the phloem.
Moreover, while TMV and other RNA viruses
replicate in the cytoplasm of infected cells,
begomoviruses replicate in the cell nucleus. These
differences may explain why CPMR has not proven
successful for begomoviruses.
Movement protein-mediated resistance
The expression of non-functional movement
proteins (MP) in transgenic plants has been tested
successfully as a PDR strategy for plant RNA viruses
(Lapidot et al., 1993; Malyshenko et al., 1993; Beck
et al., 1994). In general, the transgenic plants showed
mediocre levels of resistance, which was expressed
mainly as delayed and attenuated symptoms of
infection, against the virus from which the transgene
was derived. However, the resistance was mediated
against a wide range of different viruses (i.e., widespectrum resistance), unlike CPMR (Cooper et al.,
1995).
Two movement proteins, BC1 and BV1, both
encoded by DNA B of bipartite begomoviruses, are
required for viral infectivity and systemic infection
(Sanderfoot & Lazarowitz, 1996). The BC1 MP
mediates viral cell-to-cell movement by increasing
plasmodesmatal size exclusion limits, whereas the
BV1 MP functions as a nuclear shuttle (Noueiry et
al., 1994; Sanderfoot & Lazarowitz, 1996). The first
suggestion that expression of a non-functional BC1
MP by transgenic plants may induce inhibition of
begomovirus movement came from the work of von
Arnim & Stanley (1992), who tested if BC1 MP from
one virus (Tomato golden mosaic virus; TGMV)
could support movement of another virus (ACMV).
To do this, the ACMV AV1 gene (which encodes the
viral CP) was replaced by TGMV BC1 gene. This
recombinant construct was used to inoculate N.
benthamiana plants, together with ACMV B DNA.
The TGMV BC1 MP not only did not supplement
ACMV movement, it actually inhibited it (von Arnim
& Stanley, 1992). Indeed, transgenic tobacco plants
expressing a mutated form of the BC1 gene of
ToMoV showed resistance to this virus as well as to
Cabbage leaf curl virus (CabLCV) (Duan et al.,
1997b). The tobacco plants were transformed with
the wild type form of BC1, which resulted in
transgenic plants expressing viral disease-like
phenotypes. One of the transgenic plant lines had
an asymptomatic phenotype. In this line, the BC1
transgene underwent a spontaneous mutation,
potentially resulting in the production of a protein
from which the 119 C-terminal amino acids were
deleted and 26 amino acids derived from an
unidentified origin were incorporated (Duan et al.,
1997a).
Recently, transgenic tomato plants expressing the
BV1 or BC1 MPs from Bean dwarf mosaic virus
(BDMV) were generated (Hou et al., 2000). The
transgenic plants expressing the BV1 MP appeared
normal, whereas plants expressing the BC1 MP
showed viral disease-like symptoms, although
BDMV induces only a symptomless infection in
tomato. One BC1 transgenic line did not show any
disease-like symptoms. This line expressed a
truncated BC1 protein, following a spontaneous
mutation, which resulted in a deletion in the 3 region
of the gene. Transgenic R0 plants, expressing either
BV1 or BC1, showed a significant delay in the onset
of infection following inoculation with ToMoV. R1
progeny plants also showed a delay in ToMoV
infection, but to lesser extent than the R0 plants (Hou
et al., 2000). These results demonstrate that
begomovirus MPs, similar to RNA viruses MPs, can
be used for development of PDR. However, to date,
the level of resistance induced by begomovirus MPs
is not sufficient for commercial use.
Inhibition of viral replication

Defective interfering (DI) resistance
The first demonstration of PDR for geminiviruses
was the expression of a defective interfering DNA
B of ACMV in transgenic N. benthamiana plants
(Stanley, 1990). Symptom severity and viral
replication were reduced following inoculation with
ACMV. No difference in disease severity or in viral
replication was observed following inoculation with
TGMV, or with BCTV (Stanley, 1990).
Antisense resistance
Antisense sequences of the Rep gene of TGMV
strongly reduced symptom development and viral
replication in transgenic tobacco plants (Day et al.,
1991). When these plants were inoculated with other
geminiviruses, a four-fold reduction in BCTV, but
not ACMV DNA accumulation was found (Bejarano
et al., 1994). Bendahmane & Gronenborn (1997)
obtained almost complete suppression of TYLCV
replication and disease symptoms in several lines
of transgenic N. benthamiana plants expressing
TYLCV Rep (C1) in the antisense orientation.
Although a strict correlation between transgene
transcript level and degree of resistance was not
shown, plants with elevated levels of transcript
consistently exhibited a higher degree of virus
resistance. Incorporation of a hammerhead
ribozyme to the Rep antisense construct did not
improve the resistance level displayed by the
antisense construct alone (Bendahmane &
Gronenborn, 1997).
Aragao et al. (1998) transformed beans with a
construct containing antisense copies of the Rep and
BC1 genes of BGMV (Brazilian isolate). Four lines
of transgenic plants (R4 generation) were challenged
with BGMV. Plants of two lines showed both
delayed and attenuated viral symptoms. Plants of
the other two lines developed typical BGMV
symptoms. No correlation was found between
transgene RNA level and resistance (Aragao et al.,
1998).
Truncated or mutated Rep gene
N. benthamiana plants were transformed with the
ACMV AC1 gene (Hong & Stanley, 1996). Although
the AC1 RNA transcript was detected in the
transgenic plants, the plants were unable to
complement the infection of an ACMV AC1 mutant.
Those plants which showed some level of resistance
to ACMV were either asymptomatic or produced
delayed and attenuated symptoms, and accumulated
less viral DNA. None of the lines showed resistance
to the related geminiviruses TGMV and BCTV,
demonstrating the virus-specific nature of the
resistance (Hong & Stanley, 1996).
Resistance to Tomato yellow leaf curl Sardinia
virus (TYLCSV), accompanied by a substantial
121
reduction in viral replication, was demonstrated in

transgenic N. benthamiana plants expressing the
TYLCSV Rep gene which had a truncated 3 end.
The Rep protein was predicted to comprise only the
first 210 amino acids (Noris et al., 1996). However,
resistance was eventually overcome, and the
inheritance was not Mendelian. Brunetti et al. (1997)
transformed tomato plants with the same construct
and found that 1) accumulation of high levels of the
truncated Rep protein was required for resistance,
2) high accumulation of the transgene product
resulted in plants with a curled phenotype, and 3)
the resistance did not extend to an unrelated
geminivirus. Recently, it was shown that the
resistant plants were susceptible to inoculation with
a related strain of TYLCSV (TYLCSV-ES) (Brunetti
et al., 1997). It was shown that the truncated Rep
acts as a trans-dominant-negative mutant, inhibiting
(but not abolishing) transcription of the Rep gene of
the invading virus, and consequently, inhibiting viral
replication. Moreover, the C4 ORF, which is located
within the truncated Rep gene coding sequence, does
not participate in resistance induction (Brunetti et
al., 2001).
An analysis of mutations in the putative NTPbinding site of the Rep gene of BGYMV
demonstrated that the NTP-binding domain is
required for replication (Hanson et al., 1995). Thus,
the authors proposed that mutations in this motif
might serve as dominant negative mutations for
PDR and that they would interfere with viral
replication. Sangare et al. (1999) mutated the Rep
of ACMV altering the putative NTP-binding site,
and transformed transgenic N. benthamiana plants
with this mutant. When transgenic plants expressing
the mutated Rep were inoculated with ACMV, a
delay in symptom appearance occurred and
symptom attenuation was seen. The resistant plants
also accumulated less viral DNA than control plants.
It was found that a high level of expression of the
mutated Rep gene was essential for development of
resistance (Sangare et al., 1999), as noted for
transgenic tomato plants expressing a truncated Rep
of TYLCSV (Brunetti et al., 1997).
Resistance to ToMoV in both tobacco and inbred
tomato lines has been generated using a full length
Rep gene of ToMoV (Polston et al., 1998). The Rep
gene provided stable resistance, was not associated
with an altered phenotype, and was successfully
passed through five generations of tomato.
Following inoculation, no evidence of viral
replication could be found in transformed plants,
suggesting this transgene can confer very high levels
of resistance to ToMoV. Resistance and horticultural
qualities of T4 generation plants were evaluated in
the field for three production seasons. Yields of
transformed plants were found to be equivalent to
the untransformed parents in the absence of ToMoV
122
and greatly superior in the presence of ToMoV.

Polston & Hiebert (2001) transformed inbred
tomato genotypes with a truncated Rep gene of
TYLCV (containing approximately 40% of the
gene). The truncated Rep conferred a very high level
of resistance to TYLCV (Florida isolate) T 1
generation plants were symptomless following
inoculation and virus DNA was undetectable. T2
generation plants were inoculated in the greenhouse
and later transplanted to the field. The plants
remained symptomless under field conditions, and
the phenotype of the transformed plants was normal
(Polston & Hiebert, 2001; Polston et al., 2001).
Transgenic tobacco plants transformed with the same
construct were immune to TYLCV, but were
susceptible to CabLCV and to ToMoV. The authors
concluded that the truncated Rep appears to confer
immunity to TYLCV in tobacco and tomato, but the
resistance appears to be narrow spectrum (Polston
et al., 2001).
Transient assay for resistance
One of the major drawbacks of using transgenic
plants for testing viral constructs for PDR is the
amount of time and effort required for plant
transformation and regeneration. Thus, transient
expression assays have been developed, by cotransformation of suspension cells or protoplasts
with intact virus and the viral gene product in
question. This transient expression assay allows the
rapid screening of many potential dominant mutants,
by studying the effect of the different viral products
and/or mutants on viral replication. Indeed, the
transient expression of intact or truncated ACMV
Rep gene product caused a marked reduction in the
ACMV DNA replication in tobacco protoplasts
(Hong & Stanley, 1996). Hanson & Maxwell (1999)
used a transient expression assay in tobacco
suspension cells to demonstrate that several different
BGMV and BGYMV Rep gene mutants, with
mutations in the NTP-binding or DNA-nicking
domains, were potent trans-inhibitors of geminivirus
replication. Moreover, these mutants inhibited the
replication of different BGMV and BGYMV isolates
as well as replication of BDMV (Hanson & Maxwell,
1999).
Recently, transient expression of the Tomato leaf
curl New Delhi virus (ToLCNDV) truncated Rep
(capable of producing the N-terminal 160 amino
acids) was found to inhibit viral DNA accumulation
in tobacco protoplasts and in N. benthamiana plants
(Chatterji et al., 2001). In vivo assays, conducted
by co-bombarding N. benthamiana plants with
infectious clones of ACMV, Pepper huasteco yellow
vein virus and Potato yellow mosaic virus, indicated
inhibition of replication of heterologous viral DNA
by the truncated Rep of ToLCNDV. The authors
postulated the potential of using Rep proteins with
mutations in the oligomerisation and DNA binding

domain (both mapped to the first 160 amino acids)
to interfere with viral DNA replication (Chatterji et
al., 2001).
It seems that the most promising PDR approach
is the transformation of susceptible plants with
mutated (especially truncated) forms of the viral Rep
gene. However in some instances, the transgenically
expressed Rep induced undesirable phenotypes.
Progress is being made in the assessment of this
approach as commercial cultivars (as opposed to
test plants such N. benthamiana) have recently
been tested in field experiments (Polston & Hiebert,
2001).
Concluding Remarks
Similar approaches to the breeding for resistance
to begomoviruses have been taken for a number of
major crops. In general, protocols have been defined
for inoculation with the identified casual agent of
the disease, ideally under controlled conditions. In
most cases resistance has been transferred from
related species and efforts are being made to develop
molecular markers for the sources of resistance. The
release of resistant cultivars is already ongoing, with
variable levels of success.
However, new viruses and strains of the
begomovirus group keep on emerging. This is
mainly a result of changes in cultivation habits, the
continuing world-wide spread of different biotypes
of whiteflies, and the relatively high frequency of
recombination among geminiviruses (Padidam et al.,
1999; Pita et al., 2001b). Another major challenge
is that often two or more viruses co-infect a crop.
These new challenges necessitate the development
of plants that express multi-viral resistance. One
approach will be the identification and/or
development of resistance sources with a widespectrum of resistance, i.e., resistance against
multiple viruses. Another approach to achieve multivirus resistance will be by combining genes
conferring resistances to different viruses, that is,
pyramiding resistance genes. This poses to the
breeder two major problems: how to distinguish
between the different resistance genes to be
combined, and a need to continuously develop novel
sources of resistance to the new emerging viruses.
Molecular markers linked to resistance genes can
be instrumental in achieving the pyramiding of
resistance genes, as it will allow identification of
resistance genes. It will also circumvent the problem
of phenotypic selection of plants infected with a
number of viruses, which could mask the effects of
certain resistance genes.
The combination of classical breeding with PDR
can create an unlimited pool of resistance genes;
since the genome of the new viruses that are able to
infect the crop will serve as a source of resistance

genes. In addition, resistance genes introgressed
from wild species may complement those transgenic
plants with PDR that provides only partial resistance.
Moreover, viral sequences shared by many
begomoviruses may be utilised for the development
of PDR with a wide-spectrum of resistance.
Acknowledgments
Contribution from the Agricultural Research
Organization, the Volcani Center, Bet Dagan, Israel.
Number 534/01.
We wish to thank our colleagues for their advice
and by making data (published and unpublished)
available: Claude Fauquet, Douglas Maxwell,
Francisco Morales, Meir Pilowsky and Jane Polston.
We are grateful to Shlomo Cohen and Victor Gaba
(Dept. of Virology, Volcani Center) for critically
reviewing this manuscript.
References
Antignus Y, Lapidot M, Cohen S. 2001a. Interference with
UV vision of insects: an IPM tool to impede epidemics of
insect pests and insect associated virus diseases. In Virusinsect-plant interactions, pp. 331-350. Eds K F Harris, O P
Smith and J E Duffus. New York: Academic Press.
Antignus Y, Nestel D, Cohen S, Lapidot M. 2001b. Ultravioletdeficient greenhouse environment affects whitefly attraction
and flight behavior. Environmental Entomology 30:394-399.
Antignus Y, Mor N, Joseph B, Lapidot M, Cohen S. 1996.
Ultraviolet-absorbing plastic sheets protect crops from insect
pests and from virus diseases vectored by insects.
Environmental Entomology 25:919-924.
Aragao F J L, Ribeiro S G, Barros L M G, Brasileiro A C M,
Maxwell D P, Rech E L, Faria J C. 1998. Transgenic beans
(Phaseolus vulgaris L.) engineered to express viral antisense
RNAs show delayed and attenuated symptoms to bean golden
mosaic geminivirus. Molecular Breeding 4:491-499.
Ascencio-Ibanez J T, Diaz-Plaza R, Mendez-Lozano J,
Monsalve-Fonnegra Z I, Arguello-Astorga G R, RiveraBustamante R F. 1999. First report of tomato yellow leaf
curl geminivirus in Yucatan, Mexico. Plant Disease 83:1178.
Avidov H Z. 1946. Tobacco whitefly in Israel. Tel Aviv:
Hassadeh Publishing House (in Hebrew).
Azzam O, Diaz O, Beaver J S, Gilbertson R L, Russell D R,
Maxwell D P. 1996. Transgenic beans with the bean golden
mosaic geminivirus coat protein gene are susceptible to virus
infection. Annual Report of the Bean Improvement
Cooperative 39:276-277.
Baulcombe D C. 1996. Mechanisms of pathogen-derived
resistance to viruses in transgenic plants. Plant Cell 8:18331844.
Beck D L, van Dolleweerd C J, Lough T J, Balmori E, Voot
D M, Andersen M T, OBrien I E W, Forster R L S. 1994.
Disruption of virus movement confers broad-spectrum
resistance against systemic infection by plant viruses with a
triple gene block. Proceedings of the National Academy of
Sciences, USA 91:10310-10314.
Bedford I D, Briddon R W, Brown J K, Rosell R C,
Markham P G. 1994. Geminivirus transmission and
biological characterisation of Bemisia tabaci (Gennadius)
biotypes from different geographic regions. Annals of Applied
Biology 125:311-325.
123
Bejarano E R, Lichtenstein C P. 1994. Expression of TGMV

antisense RNA in transgenic tobacco inhibits replication of
BCTV but not ACMV geminiviruses. Plant Molecular
Biology 24:241-248.
Bellotti A C, Arias B. 2001. Host plant resistance to whiteflies
with emphasis on cassava as a case study. Crop Protection
20:813-824.
Bendahmane M, Gronenborn B. 1997. Engineering resistance
against tomato yellow leaf curl virus (TYLCV) using
antisense RNA. Plant Molecular Biology 33:351-357.
Berrie L C, Palmer K E, Rybicki E P, Rey M E C. 1998.
Molecular characterisation of a distinct South African cassava
infecting geminivirus. Archives of Virology 143:2253-2260.
Berry S, Rey M E C. 2001. Molecular evidence for diverse
populations of cassava-infecting begomoviruses in Southern
Africa. Archives of Virology 146:1795-1802.
Bianchini A. 1999. Resistance to bean golden mosaic virus in
bean genotypes. Plant Disease 83:615-620.
Blair M W, Bassett M J, Abouzid A M, Hiebert E, Polston J
E, McMillan R T Jr, Graves W, Lamberts M. 1995.
Occurrence of bean golden mosaic virus in Florida. Plant
Disease 79:529-533.
Briddon R W, Markham P G. 2000. Cotton leaf curl virus
disease. Virus Research 71:151-159.
Briddon R W, Mansoor S, Bedford I D, Pinner M S,
Markham P G. 2000. Clones of cotton leaf curl geminivirus
induce symptoms atypical of cotton leaf curl disease. Virus
Genes 20:19-26.
Briddon R W, Mansoor S, Bedford I D, Pinner M S,
Saunders K, Stanley J, Zafar Y, Malik K A, Markham P
G. 2001. Identification of DNA components required for
induction of cotton leaf curl disease. Virology 285:234-243.
Brough C L, Hayes R L, Morgan A J, Coutts R H A, Buck K
W. 1988. Effects of mutagenesis in vitro on the ability of
cloned tomato golden mosaic virus DNA to infect Nicotiana
benthamiana plants. Journal of General Virology 69:503-514.
Brown J K. 1996. Distribution and genetic variability of
whitefly-transmitted geminiviruses of cotton,. In Proceedings
Beltwide Cotton Conferences, pp. 275-276. Nashville, TN,
USA: National Cotton Council.
Brown J K, Nelson M R. 1984. Geminate particles associated
with cotton leaf crumple disease in Arizona. Phytopathology
74:987-990.
Brunetti A, Tavazza R, Noris E, Lucioli A, Accotto G P,
Tavazza M. 2001. Transgenically expressed T-Rep of tomato
yellow leaf curl Sardinia virus acts as a trans-dominantnegative mutant, inhibiting viral transcription and replication.
Journal of Virology 75:10573-10581.
Brunetti A, Tavazza M, Noris E, Tavazza R, Caciagli P,
Ancora G, Crespi S, Accotto G P. 1997. High expression of
truncated viral rep protein confers resistance to tomato yellow
leaf curl virus in transgenic tomato plants. Molecular PlantMicrobe Interactions 10:571-579.
Byrne D N, Bellows T S. 1991. Whitefly biology. Annual
Review of Entomology 36:431-457.
Chague V, Mercier J C, Guenard M, Courcel A de, Vedel F.
1997. Identification of RAPD markers linked to a locus
involved in quantitative resistance to TYLCV in tomato by
bulked segregant analysis. Theoretical and Applied Genetics
95:671-677.
Chatterji A, Beachy R N, Fauquet C M. 2001. Expression of
the oligomerization domain of the replication-associated
protein (Rep) of Tomato leaf curl New Delhi virus interferes
with DNA accumulation of heterologous geminiviruses.
Journal of Biological Chemistry 276:25631-25638.
Chiang B T, Maxwell D P, Green S. 1984. Leaf curl virus in
Taiwan. Tomato Leaf Curl Newsletter 5:3.
Cohen S, Antignus Y. 1994. Tomato yellow leaf curl virus, a
whitefly-borne geminivirus of tomatoes. Advances in Disease
and Vector Research 10:259-288.
124
Cohen S, Harpaz I. 1964. Periodic, rather than continual

acquisition of a new tomato virus by its vector, the tobacco
whitefly (Bemisia tabaci Gennadius). Entomologia
experimentalis et Applicata 7:155-166.
Cohen S, Nitzany F E, Harpaz I. 1963. Experiments in the
control of yellowing top virus in tomatoes. Tel Aviv: Hassadeh
Publishing House (in Hebrew) 43:576-578.
Cohen S, Nitzany F E, Vilde T. 1961. The tomato yellow top
virus in Israel. Hassadeh Tel Aviv (in Hebrew). 42:139-140.
Cooper J I, Jones A T. 1983. Responses of plants to viruses:
proposals for the use of terms. Phytopathology 73:127-128.
Cooper B, Lapidot M, Heick Dodds J A, Beachy R N. 1995.
A defective movement protein of TMV in transgenic plants
confers resistance to multiple viruses whereas the functional
analog increases susceptibility. Virology 206:307-313.
Cours G, Fargette D, Otim-Nape G W, Thresh J M. 1997.
The epidemic of cassava mosaic virus disease in Madagascar
in the 1930s-1940s: lessons for the current situation in
Uganda. Tropical Science 37:238-248.
Czosnek H, Laterrot H. 1997. A worldwide survey of tomato
yellow leaf curl viruses. Archives of Virology 142:1391-1406.
Czosnek H, Ber R, Navot N, Zamir D, Antignus Y, Cohen S.
1988. Detection of tomato yellow leaf curl virus in lysates of
plants and insects by hybridization with a viral DNA probe.
Plant Disease 72:949-951.
Day A G, Bejarano E R, Buck K W, Burrell M, Lichtenstein
C P. 1991. Expression of an antisense viral gene in transgenic
tobacco confers resistance to the DNA virus tomato golden
mosaic virus. Proceedings of the National Academy of
Sciences, USA 88:6721-6725.
Deng D, Otim-Nape G W, Sangare A, Ogwal S, Beachy R N,
Fauquet C. 1997. Presence of a new virus closely associated
with cassava mosaic outbreak in Uganda. African Journal of
Root Tuber Crops 2:23-28.
Duan Y P, Powell C A, Purcifull D E, Broglio P, Hiebert E.
1997a. Phenotypic variation in transgenic tobacco expressing
mutated geminivirus movement/pathogenicity (BC1)
proteins. Molecular Plant-Microbe Interactions 10:10651074.
Duan Y P, Powell C A, Webb S E, Purcifull D E, Hiebert E.
1997b. Geminivirus resistance in transgenic tobacco
expressing mutated BC1 protein. Molecular Plant-Microbe
Interactions 10:617-623.
Elmer J S, Brand L, Sunter G, Gardiner W E, Bisaro D M,
Rogers S G. 1988. Genetic analysis of tomato golden mosaic
virus II. The product of the AL1 coding sequence is required
for replication. Nucleic Acids Research 16:7043-7060.
Etessami P, Saunders K, Watts J, Stanley J. 1991. Mutational
analysis of complementary-sense genes of African cassava
mosaic virus DNA A. Journal of General Virology 72:10051012.
Fargette D, Vie K. 1995. Simulation of the effects of host
resistance, reversion, and cutting selection on incidence of
African cassava mosaic virus and yield losses in cassava.
Phytopathology 85:370-375.
Fargette D, Colon L T, Bouveau R, Fauquet C. 1996.
Components of resistance of cassava to African cassava
mosaic virus. European Journal of Plant Pathology 102:645654.
Faria J C, Maxwell D P. 1999. Variability in geminivirus
isolates associated with Phaseolus spp. in Brazil.
Fauquet C, Fargette D. 1990. African cassava mosaic virus:
etiology, epidemiology, and control. Plant Disease 74:404411.
Fauquet C M, Maxwell D P, Gronenborn B, Stanley J. 2000.
Revised proposal for naming geminiviruses. Archives of
Virology 145:1743-1761.
Fitchen J H, Beachy R N. 1993. Genetically engineered
protection against viruses in transgenic plants. Annual Review
of Microbiology 47:739-763.
Fokunang C N, Akem C M, Dixon A G O, Ikotun T. 2000.
Evaluation of a cassava germplasm collection for reaction to
three major diseases and the effect on yield. Genetic
Resources and Crop Evolution 47:63-71.
Fondong V N, Thresh J M, Fauquet C. 2000a. Field
experiments in Cameroon on cassava mosaic virus disease
and the reversion phenomenon in susceptible and resistant
cassava cultivars. International Journal of Pest Management
46:211-217.
Fondong V N, Pita J S, Rey M E C, Kochko A de, Beachy R
N, Fauquet C M. 2000b. Evidence of synergism between
African cassava mosaic virus and a new double-recombinant
geminivirus infecting cassava in Cameroon. Journal of
General Virology 81:287-297.
Fregene M, Bernal A, Duque M, Dixon A, Tohme J. 2000.
AFLP analysis of African cassava (Manihot esculenta Crantz)
germplasm resistant to the cassava mosaic disease (CMD).
Theoretical and Applied Genetics 100:678-685.
Fregene M, Angel F, Gomez R, Rodriguez F, Chavarriaga
P, Roca W, Tohme J, Bonierbale M. 1997. A molecular
genetic map of cassava (Manihot esculenta Crantz).
Theoretical and Applied Genetics 95:431-441.
Fregene M, Okogbenin E, Mba C, Angel F, Suarez M C,
Janneth G, Chavarriaga P, Roca W, Bonierbale M, Tohme
J. 2001. Genome mapping in cassava improvement:
challenges, achievements and opportunities. Euphytica
120:159-165.
Friedmann M, Lapidot M, Cohen S, Pilowsky M. 1998. A
novel source of resistance to tomato yellow leaf curl virus
exhibiting a symptomless reaction to viral infection. Journal
of the American Society for Horticultural Science 123:10041007.
Frischmuth T, Stanley J. 1993. Strategies for the control of
geminivirus diseases. Seminars in Virology 4:329-337.
Frischmuth T, Stanley J. 1998. Recombination between viral
DNA and the transgenic coat protein gene of African cassava
mosaic geminivirus. Journal of General Virology 79:12651271.
Garrido-Ramirez E R, Sudarshana M R, Gilbertson R L.
2000. Bean golden yellow mosaic virus from Chiapas,
Mexico: characterization, pseudorecombination with other
bean-infecting geminiviruses and germ plasm screening.
Gibson R W, Otim-Nape G W. 1997. Factors determining
recovery and reversion in mosaic-affected African cassava
mosaic virus resistant cassava. Annals of Applied Biology
131:259-271.
Hahn S K, Terry E R, Leuschner K. 1980. Breeding cassava
for resistance to cassava mosaic disease. Euphytica 29:673683.
Hahn S K, John C, Isoba G, Ikoutun T. 1989. Resistance
breeding in root and tuber crops at the International Institute
of Tropical Agriculture (IITA), Ibadan, Nigeria. Crop
Protection 8:147-168.
Hanson S F, Maxwell D P. 1999. Trans-dominant inhibition of
geminiviral DNA replication by bean golden mosaic
geminivirus rep gene mutants. Phytopathology 89:480-486.
Hanson S F, Hoogstraten R A, Ahlquist P, Gilbertson R L,
Russell D R, Maxwell D P. 1995. Mutational analysis of a
putative NTP-binding domain in the replication-associated
protein (AC1) of bean golden mosaic geminivirus. Virology
211:1-9.
Hanson P M, Bernacchi D, Green S, Tanksley S D,
Venkataramappa M, Padmaja A S, Chen H, Kuo G, Fang
D, Chen J. 2000. Mapping a wild tomato introgression
associated with tomato yellow leaf curl virus resistance in a
cultivated tomato line. Journal of the American Society for
Horticultural Science 125:15-20.
Hilje L, Costa H S, Stansly P A. 2001. Cultural practices for
managing Bemisia tabaci and associated viral diseases. Crop

Hong Y, Stanley J. 1996. Virus resistance in Nicotiana
benthamiana conferred by African cassava mosaic virus
replication-associated protein (AC1) transgene. Molecular
Plant-Microbe Interactions 9:219-225.
Hou Y, Sanders R, Ursin V M, Gilbertson R L. 2000.
Transgenic plants expressing geminivirus movement proteins:
abnormal phenotypes and delayed infection by Tomato mottle
virus in transgenic tomatoes expressing the Bean dwarf
mosaic virus BV1 or BC1 proteins. Molecular Plant-Microbe
Interactions 13:297-308.
Jennings D L. 1994. Breeding for resistance to African cassava
mosaic geminivirus in East Africa. Tropical Science 34:110122.
Kallo G, Banerjee M K. 1990. Transfer of tomato leaf curl
virus resistance from Lycopersicon hirsutum f. glabratum to
L. esculentum. Plant Breeding 105:156-159.
Kelly J D. 1995. Use of random amplified polymorphic DNA
markers in breeding for major gene resistance to plant
pathogens. HortScience 30:461-465.
Kunik T, Salomon R, Zamir D, Navot N, Zeidan M,
Michelson I, Gafni Y, Czosnek H. 1994. Transgenic tomato
plants expressing the tomato yellow leaf curl virus capsid
protein are resistant to the virus. Bio-Technology 12:500-504.
Lander E S, Botstein D. 1989. Mapping Mendelian factors
underlying quantitative traits using RFLP linkage maps.
Genetics 121:185-199.
Lapidot M. 2002. Screening common beans (Phaseolus
vulgaris) for resistance to tomato yellow leaf curl virus. Plant
Disease 86:429-432.
Lapidot M, Friedmann M, Pilowsky M, Cohen S. 2001.
Development of a universal scale for evaluation of TYLCVresistance level in tomato plants. Tomato Breeders Round
Table, Antigua, Guatemala.
Lapidot M, Gafny R, Ding B, Wolf S, Lucas W J, Beachy R
N. 1993. A dysfunctional movement protein of tobacco
mosaic virus that partially modifies the plasmodesmata and
limits virus spread in transgenic plants. Plant Journal 4:959970.
Lapidot M, Friedmann M, Lachman O, Yehezkel A, Nahon
S, Cohen S, Pilowsky M. 1997. Comparison of resistance
level to tomato yellow leaf curl virus among commercial
cultivars and breeding lines. Plant Disease 81:1425-1428.
Lapidot M, Goldray O, Ben-Joseph R, Cohen S, Friedmann
M, Shlomo A, Nahon S, Chen L, Pilowsky M. 2000.
Breeding tomatoes for resistance to tomato yellow leaf curl
begomovirus. EPPO Bulletin 30:317-321.
Laterrot H. 1992. Resistance genitors to tomato yellow leaf
curl virus (TYLCV). Tomato Leaf Curl Newsletter 1:2-4.
Legg J P. 1999. Emergence, spread and strategies for controlling
the pandemic of cassava mosaic virus disease in east and
central Africa. Crop Protection 18:627-637.
Legg J P, Thresh J M. 2000. Cassava mosaic virus disease in
East Africa: a dynamic disease in a changing environment.
Virus Research 71:135-149.
Lomonossoff G P. 1995. Pathogen-derived resistance to plant
viruses. Annual Review of Phytopathology 33:323-343.
Malyshenko S I, Kondakova O A, Navarova J K, Kaplan I
B, Taliansky M E, Atabekov J G. 1993. Reduction of tobacco
mosaic virus accumulation in transgenic plants producing
non-functional viral transport proteins. Journal of General
Virology 74:1149-1156.
Mansoor S, Bedford I D, Pinner M S, Stanley J, Markham
P G. 1993. A whitefly-transmitted geminivirus associated with
cotton leaf curl disease in Pakistan. Pakistan Journal of
Botany 25:105-107.
Mansoor S, Khan S H, Bashir A, Saeed M, Zafar Y, Malik
K A, Briddon R, Stanley J, Markham P G. 1999.
Identification of a novel circular single-stranded DNA
125
associated with cotton leaf curl disease in Pakistan. Virology

259:190-199.
Mejia L, Czosnek H, Vidavsky V, Lapidot M, Friedmann
M, Pilowsky M. 2001. Evaluation of tomato germplasm
resistant to TYLCV for resistance to bipartite whitefly
transmitted geminiviruses in Guatemala. APS Caribbean
Division Meeting, La Habana, Cuba.
Miklas P N, Johnson E, Stone V, Beaver J S, Montoya C,
Zapata M. 1996. Selective mapping of QTL conditioning
disease resistance in common bean. Crop Science 36:13441351.
Morales F J. 2001. Conventional breeding for resistance to
Bemisia tabaci-transmitted geminiviruses. Crop Protection
20:825-834.
Morales F J, Anderson P K. 2001. The emergence and
dissemination of whitefly-transmitted geminiviruses in Latin
America. Archives of Virology 146:415-441.
Morales F J, Niessen A I. 1988. Comparative responses of
selected Phaseolus vulgaris germ plasm inoculated artificially
and naturally with bean golden mosaic virus. Plant Disease
72:1020-1023.
Morales F J, Singh S P. 1991. Genetics of resistance to bean
golden mosaic virus in Phaseolus vulgaris L. Euphytica
52:113-117.
Morales F J, Singh S P. 1993. Breeding for resistance to bean
golden mosaic virus in an interracial population of Phaseolus
vulgaris L. Euphytica 67:59-63.
Moriones E, Navas-Castillo J. 2000. Tomato yellow leaf curl
virus, an emerging virus complex causing epidemics
worldwide. Virus Research 71:123-34.
Nadeem A, Weng Z, Nelson M R. 1997. Cotton leaf crumple
virus and cotton leaf curl virus are two distantly related
geminiviruses. Molecular Plant Pathology On-Line http://
www.bspp.org.uk/mppol/1997/0612nadeem/.
Nakhla M K, Maxwell D P. 1998. Epidemiology and
management of tomato yellow leaf curl virus. In Plant Virus
Disease Control, pp. 565-583. Eds A Hadidi, R K Khetarpal
and H Koganezawa. St. Paul: APS Press.
Natwick E T, Cook C, Gilbertson R, Seo Y, Turini T. 2000.
Resistance in upland cotton to the silverleaf whitefly
transmitted cotton leaf crumple disease. Proceedings Beltwide
Cotton Conferences, National Cotton Council, San Antonio,
USA, pp. 164-167.
Navas-Castillo J, Sanchez-Campos S, Diaz J A. 1999. Tomato
yellow leaf virus-Is causes a novel disease of common bean
and severe epidemics in tomato in Spain. Plant Disease 83:2932.
Navot N, Pichersky E, Zeidan M, Zamir D, Czosnek H. 1991.
Tomato yellow leaf curl virus: a whitefly-transmitted
geminivirus with a single genomic component. Virology
185:131-161.
Noris E, Accotto G P, Tavazza R, Brunetti A, Crespi S,
Tavazza M. 1996. Resistance to tomato yellow leaf curl
geminivirus in Nicotiana benthamiana plants transformed
with a truncated viral C1 gene. Virology 224:130-138.
Noueiry A O, Lucas W J, Gilbertson R L. 1994. Two proteins
of a plant DNA virus coordinate nuclear and plasmodesmal
transport. Cell 76:925-932.
Otim-Nape G W, Thresh J M, Bua A, Baguma Y, Shaw M
W. 1998. Temporal spread of cassava mosaic virus disease
in a range of cassava cultivars in different agro-ecological
regions of Uganda. Annals of Applied Biology 133:415-430.
Padidam M, Sawyer S, Fauquet C M. 1999. Possible
emergence of new geminiviruses by frequent recombination.
Virology 265:218-225.
Palmer K E, Rybicki E P. 1998. The molecular biology of
mastreviruses. Advances in Virus Research 50:183-234.
Palumbo J C, Horowitz A R, Prabhaker N. 2001. Insecticidal
control and resistance management for Bemisia tabaci. Crop
126
Pico B, Diez M J, Nuez F. 1996. Viral diseases causing the

greatest economic losses to the tomato crop. II. The tomato
yellow leaf curl virus a review. Scientia Horticulturae
67:151-196.
Pico B, Diez M J, Nuez F. 1998. Evaluation of whiteflymediated inoculation techniques to screen Lycopersicon
esculentum and wild relatives for resistance to tomato yellow
leaf curl virus. Euphytica 101:259-271.
Pico B, Ferriol M, Diez M J, Nuez F. 1999. Developing tomato
breeding lines resistant to tomato yellow leaf curl virus. Plant
Breeding 118:537-542.
Pilowsky M, Cohen S. 1990. Tolerance to tomato yellow leaf
curl virus derived from Lycopersicon peruvianum. Plant
Disease 74:248-250.
Pilowsky M, Cohen S. 2000. Screening additional wild
tomatoes for resistance to the whitefly-borne tomato yellow
leaf curl virus. Acta Physiologia Plantarum 22:351-353.
Pilowsky M, Friedmann M, Lapidot M, Nahon S, Shlomo
H, Cohen S. 1997. TY-172 - a new source of resistance to
tomato yellow leaf curl virus. Eucarpia Tomato, Jerusalem,
Israel, p. 50.
Pita J S, Fondong A, Sangare A, Kokora R N N, Fauquet C
M. 2001a. Genomic and biological diversity of the African
cassava geminiviruses. Euphytica 120:115-125.
Pita J S, Fondong V N, Sangare A, Otim-Nape G W, Ogwal
S, Fauquet C M. 2001b. Recombination, pseudorecombination and synergism of geminiviruses are determinant
keys to the epidemic of severe cassava mosaic disease in
Uganda. Journal of General Virology 82:655-665.
Piven N M, Uzcategui R C de, Infante H D. 1995. Resistance
to tomato yellow mosaic virus in species of Lycopersicon.
Plant Disease 79:590-594.
Polston J E, Anderson P K. 1997. The emergence of whiteflytransmitted geminiviruses in tomato in the western
hemisphere. Plant Disease 81:1358-1369.
Polston J E, Hiebert E. 2001. Engineered resistance to tomato
geminiviruses. Proceedings of the Florida Tomato Institute.
University of Florida, Naples, FL, pp. 19-22.
Polston J E, McGovern R J, Brown L G. 1999. Introduction
of tomato yellow leaf curl virus in Florida and implications
for the spread of this and other geminiviruses of tomato. Plant
Disease 83:984-988.
Polston J E, Hunter W B, Abouzid A M, Hiebert E. 1998.
Field performance of tomatoes transformed with Tomato
mottle virus Rep gene. Second International Workshop on
Bemisia and Geminiviruses, San Juan, Porto Rico, p. 61.
Polston J E, Hiebert E, McGovern R J, Stansly P A, Schuster
D J. 1993. Host range of tomato mottle virus, a new
geminivirus infecting tomato in Florida. Plant Disease
77:1181-1184.
Polston J E, Yang Y, Sherwood T, Bucher C, Frietas-Astua
J, Hiebert E. 2001. Effective resistance to tomato yellow
leaf curl virus (TYLCV) in tomato and tobacco mediated by
a truncated TYLCV Rep gene. 3rd International Geminivirus
Symposium, Norwich, UK, p. 82.
Powell Abel P, Nelson R S, Hoffmann B De N, Rogers S G,
Fraley R T, Beachy R N. 1986. Delay of disease development in transgenic plants that express the tobacco mosaic
virus coat protein gene. Science 232:738-743.
Rahman H, Khan W S, Khan M, Sha M K N. 2001. Stability
of cotton cultivars under leaf curl virus epidemic in Pakistan.
Field Crops Research 69:251-257.
Rochester D E, DePaulo J J, Fauquet C M, Beachy R N.
1994. Complete nucleotide sequence of the geminivirus
tomato yellow leaf curl virus, Thailand isolate. Journal of
General Virology 75:477-485.
Rom M, Antignus Y, Gidoni D, Pilowsky M, Cohen S. 1993.
Accumulation of tomato yellow leaf curl virus DNA in
tolerant and susceptible tomato lines. Plant Disease 77:253257.
Russo M, Cohen S, Martelli G P. 1980. Virus-like particles in

tomato plants affected by the yellow leaf curl disease. Journal
of General Virology 49:209-213.
Sanchez-Campos S, Navas-Castillo J, Camero R, Soria C,
Diaz J A, Moriones E. 1999. Displacement of tomato yellow
leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato
epidemics in Spain. Phytopathology 89:1038-1043.
Sanderfoot A A, Lazarowitz S G. 1996. Getting it together in
plant virus movement: Cooperative interactions between
bipartite geminivirus movement proteins. Trends in Cell
Biology 6:353-358.
Sanford J C, Johnson S A. 1985. The concept of parasitederived resistance: deriving resistance genes from the parasite
own genome. Journal of Theoretical Biology 115:395-405.
Sangare A, Deng D, Fauquet C M, Beachy R N. 1999.
Resistance to African cassava mosaic virus conferred by a
mutant of the putative NTP-binding domain of the Rep gene
(AC1) in Nicotiana benthamiana. Molecular Biology Reports
5:95-102.
Scott J W, Stevens M R, Barten J H M, Thome C R, Polston
J E, Schuster D J, Serra C A. 1996. Introgression of
resistance to whitefly-transmitted geminiviruses from
Lycopersicon chilense to tomato. In Taxonomy, Biology,
Damage, Control and Management Bemisia : 1995, pp. 357367. Ed D Gerling. Andover, Hants, UK: Intercept.
Singh S P, Morales F J, Teran H. 2000a. Registration of bean
golden mosaic resistant dry bean germplasm GMR 1 and
GMR 5. Crop Science 40:1836.
Singh S P, Morales F J, Miklas P N, Teran H. 2000b. Selection
for bean golden mosaic resistance in intra- and interracial
bean populations. Crop Science 40:1565-1572.
Singh S P, Teran H, Munoz C G, Takegami J C. 2000c.
Registration of multiple-disease resistant carioca dry bean A
801 and A 804 germplasm. Crop Science 40:1836-1837.
Sinisterra X H, Polston J E, Abouzid A M, Hiebert E. 1999.
Tobacco plants transformed with a modified coat protein of
tomato mottle begomovirus show resistance to virus infection.
Stanley J. 1990. Characterisation and exploitation of plant virus
DI DNA. The Exploitation of Micro-organisms in Applied
Biology, Aspects of Applied Biology, No. 24. pp. 87-95.
Storey H H. 1936. Virus diseases of East African plants: VI. A
progress report on studies of the diseases of cassava. East
Africa Journal of Agricultural Sciences 2:34-39.
Swanson M M, Harrison B D. 1994. Properties, relationships
and distribution of cassava mosaic geminiviruses. Tropical
Science 34:15-25.
Thomas P E, Mink G I. 1998. Tomato hybrids with nonspecific
immunity to viral and mycoplasma pathogens of potato and
tomato. HortScience 33:764-765.
Thresh J M, Otim-Nape G W. 1994. Strategies for controlling
African cassava mosaic geminivirus. Advances in Disease
and Vector Research 10:215-236.
Thresh J M, Otim-Nape G W, Fargette D. 1998a. The control
of African cassava mosaic virus disease: phytosanitation and/
or resistance? In Plant Virus Disease Control, pp. 670-677.
Eds A Hadidi, R K Khetarpal and H Koganezawa. St. Paul:
APS Press.
Thresh J M, Otim-Nape G W, Fargette D. 1998b. The
components and deployment of resistance to cassava mosaic
virus disease. Integrated Pest Management Reviews 3:209224.
Thresh J M, Otim-Nape G W, Thankappan M, Muniyappa
V. 1998c. The mosaic diseases of cassava in Africa and India
caused by whitefly-borne geminiviruses. Review of Plant
Pathology 77:935-945.
Urrea C A, Miklas P N, Beaver J S, Riley H. 1996. A
codominant randomly amplified polymorphic DNA (RAPD)
marker useful for indirect selection of bean golden mosaic
virus resistance in common bean. Journal of the American
Society for Horticultural Science 121:1035-1039.

Valverde R A, Lotrakul P, Landry A D. 2001. First report of
Tomato yellow leaf curl virus in Louisiana. Plant Disease
85:230.
Velez J J, Bassett M J, Beaver J S, Molina A. 1998. Inheritance
of resistance to bean golden mosaic virus in common bean.
Journal of the American Society for Horticultural Science
123:628-631.
Vidavsky F, Czosnek H. 1998. Tomato breeding lines resistant
and tolerant to tomato yellow leaf curl virus issued from
Lycopersicon hirsutum. Phytopathology 88:910-914.
Vidavsky F, Leviatov S, Milo J, Rabinowitch H D, Kedar N,
Czosnek H. 1998. Response of tolerant breeding lines of
tomato, Lycopersicon esculentum, originating from three
different sources (L. peruvianum, L. pimpinellifolium and L.
chilense) to early controlled inoculation by tomato yellow
leaf curl virus (TYLCV). Plant Breeding 117:165-169.
von Arnim A, Stanley J. 1992. Inhibition of African cassava
mosaic virus systemic infection by a movement protein from
the related geminvirus tomato golden mosaic virus. Virology
187:555-564.
127
Walkey D G A. 1985. Applied Plant Virology. New York: WileyInterscience. pp. 236-242.
Wilson F D, Brown J K. 1991. Inheritance of response to cotton
leaf crumple virus infection in cotton. Journal of Heredity
82:508-509.
Zakay Y, Navot N, Zeidan M, Kedar N, Rabinowitch H,
Czosnek H, Zamir D. 1991. Screening Lycopersicon
accessions for resistance to tomato yellow leaf curl virus:
presence of viral DNA and symptom development. Plant
Disease 75:279-281.
Zamir D, Ekstein-Michelson I, Zakay Y, Navot N, Zeidan
M, Sarfatti M, Eshed Y, Harel E, Pleban T, van Oss H,
Kedar N, Rabinowitch H D, Czosnek H. 1994. Mapping
and introgression of a tomato yellow leaf curl virus tolerance
gene, TY-1. Theoretical and Applied Genetics 88:141-146.
Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape G W,
Robinson D J, Harrison B D. 1997. Evidence that DNA-A
of a geminivirus associated with severe cassava mosaic
disease in Uganda has arisen by interspecific recombination.
Journal of General Virology 78:2101-2111.
128

Breeding For Resistance To Whitefly-Transmited Geminivirus PDF

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Breeding For Resistance To Whitefly-Transmited Geminivirus PDF

Uploaded by

Copyright:

Available Formats

Ann. appl. Biol.

Breeding for resistance to whitefly-transmitted geminiviruses

have bipartite genomes (A and B components);

MOSHE LAPIDOT & MICHAEL FRIEDMANN

as fine-mesh screens have been used in the

et al., 2000). The recent finding that recombination

Breeding for resistance to whitefly-transmitted geminiviruses

virus than the susceptible host, and will express

(Bedford et al., 1994; Polston & Anderson, 1997;

MOSHE LAPIDOT & MICHAEL FRIEDMANN

Breeding for resistance to whitefly-transmitted geminiviruses

uninfected plants; information which is necessary

south India (Kallo & Banerjee, 1990; Hanson et al.,

MOSHE LAPIDOT & MICHAEL FRIEDMANN

mechanically, suggesting either avoidance of

America and the Caribbean, and has caused severe

Breeding for resistance to whitefly-transmitted geminiviruses

resistant varieties. There are two major groups of

BGYMV resistance in the parent lines were different

MOSHE LAPIDOT & MICHAEL FRIEDMANN

Therefore, this has a direct bearing on the breeders

This is a result of the virus not becoming fully

Breeding for resistance to whitefly-transmitted geminiviruses

1994). In fact, a number of inter-specific hybrids

was negatively correlated with tuberous root number

MOSHE LAPIDOT & MICHAEL FRIEDMANN

begomovirus was found in CLCuD-infected cotton

therefore be advisable to develop protocols of

Breeding for resistance to whitefly-transmitted geminiviruses

curl Bangalore virus (ToLCBV; Hanson et al., 2000).

2000). Although a particular AFLP marker linked

MOSHE LAPIDOT & MICHAEL FRIEDMANN

hybrid transformed with the TYLCV CP gene (V1)

Breeding for resistance to whitefly-transmitted geminiviruses

Inhibition of viral replication

reduction in viral replication, was demonstrated in

MOSHE LAPIDOT & MICHAEL FRIEDMANN

and greatly superior in the presence of ToMoV.

mutations in the oligomerisation and DNA binding

Breeding for resistance to whitefly-transmitted geminiviruses

infect the crop will serve as a source of resistance

Bejarano E R, Lichtenstein C P. 1994. Expression of TGMV

MOSHE LAPIDOT & MICHAEL FRIEDMANN

Cohen S, Harpaz I. 1964. Periodic, rather than continual

Breeding for resistance to whitefly-transmitted geminiviruses

managing Bemisia tabaci and associated viral diseases. Crop

associated with cotton leaf curl disease in Pakistan. Virology

MOSHE LAPIDOT & MICHAEL FRIEDMANN

Pico B, Diez M J, Nuez F. 1996. Viral diseases causing the

Russo M, Cohen S, Martelli G P. 1980. Virus-like particles in

Breeding for resistance to whitefly-transmitted geminiviruses

Society for Horticultural Science 121:1035-1039.

MOSHE LAPIDOT & MICHAEL FRIEDMANN

You might also like