Chapter B2

Common Beans

Francisco J. Morales
Virology Research Unit, International Centre for Tropical Agriculture, Cali, Colombia

Introduction

The common bean (Phaseolus vulgaris L.) is one of the most widely
cultivated legumes in the world, occupying over 27 million hectares of
tropical and temperate agricultural land in the Americas, Europe, Africa and
Asia (FAO, 2003). The genus Phaseolus is of American origin and
comprises over 30 species (Debouck, 1999). P. vulgaris is the most widely
grown legume, occupying almost 90% of the area planted to Phaseolus
species in the world. The centre of origin and domestication of common
bean includes the Andean region of South America and Middle America,
from Chile up to approximately the Tropic of Cancer in Mexico (Singh,
2001). Genetic diversity in common bean is represented by large-seeded
Andean, and small- and medium-seeded Middle American gene pools
(Evans, 1980). There are two major commercial classes of common bean:
snap and dry beans. In the case of snap beans, the green pods are harvested,
whereas for dry beans, the seed is extracted from mature pods. The dry bean
is the preferred form of consumption, with over 70% of the total common
bean production area corresponding to this commercial class. In general
terms, the genetic base of common bean cultivars is narrow, because only a
small proportion of wild common bean populations were domesticated
(Gepts et al. 1986).
Legumes in general can be infected by over 140 different plant viruses
(Edwardson and Christie, 1991), and P. vulgaris is probably the most
‘infectible’ plant species in the Leguminosae. Yet, only about 20 different

367
G. Loebenstein and J. P. Carr (eds.), Natural Resistance Mechanisms of Plants to Viruses, 367-382.
© 2006 Springer. Printed in the Netherlands.
368 F. J. Morales

plant viruses are mentioned as important natural pathogens of common bean

around the world (APS, 1991), and no more than half a dozen viruses affect
common bean production in any given agricultural region of the world. This
observation suggests that the existing common bean cultivars possess a
broad spectrum of genetic resistance to many different plant viruses found in
common-bean production areas around the world.
Due to the early adoption of common bean as a popular food crop in
Europe and North America, the first viral disease of this legume was already
observed towards the end of the XIX century, coinciding with the first report
of a ‘virus’ (Tobacco mosaic virus) by Iwanowski (1894). However, it was
not until 1917, that Stewart and Reddick (1917) called the causal agent
‘bean mosaic virus’. This name was later modified (Pierce, 1934) by adding
the epithet ‘common’, in order to distiguish it from a second virus found to
induce mosaic in common bean: Bean yellow mosaic virus (BYMV). The
‘mosaic’ symptoms induced by Bean common mosaic virus (BCMV) vary
considerably according to the bean genotype infected, the time of infection
in relation to plant development, the environmental conditions, and the strain
of BCMV that infects a common bean plant. Most BCMV-susceptible
common bean genotypes express noticeable mosaic and leaf malformation
symptoms when infected by this virus, but mild mosaic symptoms are also
characteristic of infections in certain common bean genotypes. However,
even symptomless BCMV infections can induce significant (>50%) yield
losses in susceptible common bean genotypes (Zaumeyer and Thomas, 1957;
Morales and Bos, 1988).
The search for BCMV-resistant common bean genotypes started in 1918,
but a decade later, only one common bean genotype, ‘Robust’, had shown
to be resistant to bean common mosaic (Reddick and Stewart, 1918; Rands
and Brotherton, 1925). In 1935, Pierce (1935) pointed out that the BCMV
resistance present in cultivar ‘Robust’, was conditioned by recessive genes.
It would take four more decades before the painstaking and elaborate genetic
study of Drijfhout (1978) demonstrated that resistance to BCMV in
‘Robust’ and other mosaic-resistant common bean cultivars developed in the
early 1930s (Pierce, 1933, 1934) was determined by a strain-unspecific gene
and at least one strain-specific recessive gene effective against the
pathogenic BCMV strain inoculated. These recessive genes prevented the
chronic systemic infection (common mosaic) of the resistant common bean
genotype. Four recessive resistance genes in the host, some of which are
allelic, interact with corresponding pathogenicity genes in seven BCMV
strains, according to the gene-for-gene model of Flor (1956). On the basis of
their susceptibility or resistance to the existing BCMV strains, Drijfhout
(1978) created six groups of common bean cultivars, which may or may not
be infected by at least one BCMV strain.
 B2. Common Beans 369

Bean common mosaic resistance had also been found in the early 1990s,
in the common bean cultivar ‘Corbett Refugee’. However, unlike the case
of the common mosaic-resistant cultivar ‘Robust’, the resistance of ‘Corbett
Refugee’ was shown by Pierce (1935) to be inherited dominantly. A decade
later, Grogan and Walker (1948) demonstrated that common bean cultivars
possessing this type of dominant common mosaic resistance, reacted to some
BCMV strains with systemic vascular necrosis but not mosaic. This
symptom, referred to as ‘black root’, had been previously described by
Jenkins (1940) as a new disease of common bean. The ‘black root’ symptoms
initially appear as local pin-point lesions, which later enlarge and give rise to
vein necrosis originating in the local lesions. The youngest trifoliate leaves
develop a net-like vein necrosis that extends down the stem in the form of
necrotic streaks, eventually affecting the entire vascular system, including
the roots (hence its name) and the pods if they are already formed. Affected
plants wilt and die within a few days after the onset of systemic necrosis.
Drijfhout (1978) confirmed earlier studies showing that ‘black root’ was a
necrotic systemic reaction induced by the presence of a dominant gene (I ),
which Drijfhout called the ‘necrosis’ gene. This systemic necrosis reaction is
only induced by ‘necrosis-inducing’ strains of BCMV (NL2 and NL6) and
by all strains of Bean common mosaic necrosis virus (BCMNV-NL3, NL5
and NL8). The latter strains were previously considered as pathogenic
variants of BCMV, until their molecular characterization showed them to be
strains of a related but distinct virus species named BCMNV (Berger, et al.
1997). Another difference between the necrosis-inducing strains of BCMV
and BCMNV is their different behaviour in relation to temperature
(Drijfhout, 1978). BCMV NL2 and NL6 require high (> 26º C) temperatures
to induce necrosis in II gene common bean genotypes (temperature-
dependent), whereas BCMNV strains can cause ‘black root’ at lower
temperatures (temperature-independent).
‘Black root’ is often considered a fatal disease of common bean,
sometimes causing total yield losses in regions where bean cultivars
possessing monogenic dominant resistance are attacked by necrosis-inducing
BCMV or BCMNV strains, particularly BCMNV-NL3. However, ‘black
root’ is a systemic hypersensitive response (HR) to the inoculation of
necrosis-inducing strains of BCMV or BCMNV, and, therefore, it should be
considered as a ‘resistance mechanism’. The dominant necrosis gene (I )
prevents the chronic systemic infection (mosaic) of common bean genotypes
by BCMV or BCMNV strains, and blocks the primary mechanism of
BCMV/BCMNV dispersal: their transmission via infected seed (Morales and
Bos, 1988). One could also argue that HR prevents the second most
important mode of BCMV/BCMNV dissemination: its transmission by
several aphid species in a non-persistent manner (Morales and Bos, 1988).
370 F. J. Morales

However, as reported in the case of other viral pathosystems (Valkonen,

2002), HR does not prevent virus multiplication, but rather the movement
and establishment of the virus into susceptible cells. Thus, although the virus
can be recovered from non-inoculated trifoliate leaves of common bean
plants inoculated on their primary leaves with BCMNV (F.J. Morales,
unpublished data), the rapid development of ‘black root’ symptoms would
limit the usefulness of necrotic common bean plants as virus sources for
aphid vectors.
The dominant HR also confers ‘broad spectrum resistance’ in common
bean to other legume potyviruses related to BCMV and BCMNV. In 1979,
Tamayo et al. (1980) observed the typical hypersensitive reaction induced by
necrotic strains of BCMV/BCMNV in dominant I gene bean genotypes,
using a strain of Soybean mosaic virus (SMV) from the Cauca Valley,
Colombia, to inoculate the primary leaves of the common bean cultivar
‘Jubila’ (I bc-1). Kyle and Provvidenti (1987) observed that a single allele at
the I locus confers hypersensitivity to SMV, Blackeye cowpea mosaic virus
(BlCMV), Cowpea aphid-borne mosaic virus, and watermelon mosaic virus.
The latter two viruses are currently considered strains of BCMV and SMV,
respectively (Berger et al. 1997). The HR can also be elicited by strains of
Peanut mottle virus, sometimes resulting in very high incidences of ‘black
root’ (F.J. Morales, unpublished data).
However, the incorporation of broad spectrum dominant resistance in
common bean is not devoid of adverse side-effects. In certain common bean-
producing regions of the world, particularly in East Africa, Europe and some
temperate countries of the Americas, the frequency of BCMNV can be high
enough to cause occasional but severe ‘black root’ outbreaks. Also, in
Central America, Morales and Castaño (1992) reported on the occurrence of
a systemic hypersensitive reactions in I-gene common bean cultivars
infected by a comovirus related to Cowpea severe mosaic virus. This
disease, referred to as ‘severe mosaic’, does not kill diseased plants as
rapidly as ‘black root’, but it may eventually lead to plant death in common
bean genotypes possessing dominant resistance to BCMV. Some P. vulgaris
genotypes react with apical necrosis to the severe mosaic comovirus, but this
reaction is induced by a different dominant gene (Anv) that is epistatic over
the dominant gene (Lnv) that conditions the localized necrosis reaction
known as ‘severe mosaic’ (Morales and Singh, 1997).
As mentioned before, one of the reasons for the global importance of
BCMV and BCMNV as viral pathogens of common bean, is their ability to
infect a high proportion (30-50%) of the plants derived from seed produced
by systemically infected bean plants. Even a 1% level of seed infection,
accepted in seed certification programs for BCMV, represents 2,500 BCMV-
infected plants per hectare, as initial virus sources for aphid vectors. It was
 B2. Common Beans 371

also mentioned that common bean genotypes possessing the dominant I gene
do not transmit either BCMV or BCMNV through their seed. Thus, genetic
‘resistance to infection of the seed embryo or gametophyte tissue’ can be
considered a natural mechanism of resistance to plant viruses in certain
plant species or plant genotypes. Morales and Castaño (1987) demonstrated
that the incidence of BCMV/BCMNV transmission in common bean
depends not only on viral determinants but also on host genetic
determinants. In this investigation, five common bean cultivars transmitted
four BCMV strains and one BCMNV strain to 40-54% of the progeny,
whereas common bean genotypes Imuna, and the Great Northern lines 31
and 123, showed seed transmission incidences below 1%. Pinto 114 did not
transmit BCMV-NY 15 in tests involving over 1,000 seeds collected from
infected bean plants.
Viruses also have genetic determinants responsible for their transmission
in the seed of their hosts. Cucumber mosaic virus (CMV) is one of the most
ubiquitous viral pathogens in the world, due to its extremely broad host
range, including P. vulgaris. Some strains of CMV can be seed-borne in
common bean, and an investigation by Hampton and Francki (1992) using a
pseudo-recombinant virus obtained by combining RNA components of a
seed-transmitted and a non-seed-transmitted strains of CMV, showed that
the genetic determinant for seed transmission was in RNA1. This component
is primarily involved in viral replication and movement in the case of CMV.
Perhaps, viruses uncapable of fast movement and replication in
meristematic tissue cannot be seed transmitted.
Among the natural defence mechanisms displayed by P. vulgaris against
plant viruses, it is worth mentioning the production of a diverse array of
‘local lesions’. These localized reactions may appear as rings, spots, vein
necrosis, discoloration, or the typical pin-point local lesions (Drijfhout,
1978). Most of these reaction are elicited by plants inoculated artificially
with selected strains of BCMV, BCMNV or other related legume
potyviruses, but common bean plants may exhibit some of these localized
reactions under natural conditions. The expression of local lesions is
generally associated with the presence of the dominant I gene in P. vulgaris,
but ring-shaped lesions and localized vascular discolorations are
characteristic of some common bean genotypes, such as ‘Monroe’, devoid of
dominant resistance genes (Drijfhout, 1978). The expression of these
localized reactions in non-I-gene common bean genotypes, does not
necessarily preclude systemic invasion by the eliciting virus.
The expression of pin-point and similar localized lesions in I gene
common bean genotypes, on the other hand, is extremely useful for the
identification of genotypes possessing multiple resistance to both mosaic-
and necrosis-inducing strains of BCMV and BCMNV. As mentioned before,
372 F. J. Morales

even though ‘black root’ is a HR, poor farmers in East Africa cannot afford
to lose their common bean plantings to BCMNV or other related legume
potyviruses that can elicit this systemic necrosis reaction in bean cultivars
possessing monogenic dominant resistance conditioned by the I gene. To
protect this gene, Drijfhout (1978) showed that the combination of strain-
specific recessive genes, namely bc-22, which cannot be challenged by any
known necrosis-inducing BCMV or BCMNV strain, an the dominant I gene,
protected common bean genotypes from ‘black root’. Common bean plants
possessing the Ibc-22 genotype, react with typical pin-point local lesions on
artificially inoculated primary (cotyledonary) leaves.
‘Immunity’ to all known BCMV and BCMNV strains in common bean
was found by Drijfhout (1978) in a line selected in Holland from a common
bean accession maintained in New York State, U.S.A. The immunity of the
Dutch line IVT 7214 was conferred by a single recessive gene (bc-3) for
which no matching pathogenicity gene has been found to date in any BCMV
or BCMNV strain.
BCMV probably co-evolved for centuries with P. vulgaris in its Latin
American centers of origin before this legume was taken to other continents.
However, the main BCMV strain found in Latin America is the type strain,
the least pathogenic of all BCMV strains. In fact, most of the 30,000
accessions of P. vulgaris maintained in the main common bean germplasm
collection at the International Centre for Tropical Agriculture (CIAT), Cali,
Colombia, do not have any genes for resistance to BCMV. Yet, most
common bean landraces throughout Latin America yield acceptably (over
500kg/ha), considering BCMV incidences between 60-100% under field
conditions. Some common bean landraces planted year after year in the field
despite a 100% incidence of BCMV, are so severely malformed that farmers
believe that is their natural phenotype. Thus, ‘tolerance’ is probably the
main mechanism of resistance to BCMV found in the main landraces still
under cultivation in developing countries.
P. vulgaris is also commonly infected by some viruses that do not cause
noticeable symptoms or yield losses. Bean southern mosaic and bean mild
mosaic viruses are highly infectious viruses readily transmitted to common
bean by mechanical means and by chrysomelid beetles (Morales and Gámez,
1989). The absence of noticeable symptoms, at least to the untrained eye,
suggests that P. vulgaris can ‘tolerate’ these viruses. However, bean southern
mosaic can cause significant yield losses in some sensitive common bean
genotypes, and even in genotypes that express only mild symptoms. The
number and weight of seed produced by infected plants can be significantly
(>50%) reduced in the case of bean southern mosaic (Morales and Castaño,
1985). Hence, the term ‘tolerance’ as a natural mechanism of virus resistance
has to be used with caution in these cases, because some of these mild
 B2. Common Beans 373

infections can significantly reduce yield, and neither the term ‘resistant’ nor
‘susceptible’, apply to these viruses that can reach very high titers in infected
common bean plants despite the absence of noticeable symptoms. An
alternative explanation may be that breeders have been unconciously
selecting against common bean genotypes that show mild but appreciable
virus-induced symptoms (leaf curling, chlorosis, etc), favouring the selection
of genotypes with inapparent virus infections. The absence of noticeable
symptoms characteristic of bean southern mosaic or bean mild mosaic, does
not necessarily imply that their incidence is low. A few years ago, the author
witnessed the complete destruction of several breeding materials obtained
from interspecific crosses made between P. vulgaris and P. acutifolius at
CIAT, Palmira, Colombia. Artificial inoculation of the parental tepary bean
(P. acutifolius) accessions with Bean southern mosaic virus, showed this
species to be highly sensitive to the virus.
As mentioned above, different legume potyviruses attack P. vulgaris
under natural conditions, particularly in temperate countries. Bean yellow
mosaic virus (BYMV) is the third most important potyvirus attacking P.
vulgaris in the Americas (i.e. southern cone of South America and North
America), Europe and Asia. The importance of BYMV as a common bean
pathogen lies in its wider host range and greater pathogenic variability,
compared to BCMV and BCMNV. Even ‘mild’ BYMV strains have an
extended pathogenicity range and greater virulence in common bean
genotypes used to differentiate BCMV/BCMNV strains; inducing mosaic,
epinasty, dwarfing, vein and top necrosis, plant malformation, and even
plant death. These symptoms occur both in I gene and non-I gene common
bean genotypes, but bean genotypes possessing the dominant necrosis gene
(I) usually display more severe symptoms, including systemic and top
necrosis (F. Morales and M. Castaño, unpublished data). In Chile, South
America, two Great Northern genotypes (31 and 123), Pinto 114, and Imuna,
showed adequate levels of resistance to BYMV A simple cross between
Great Northern 31 and a susceptible local black-seeded cultivar, led to the
development of a BYMV-resistant cultivar (Cafati et al. 1976). Great
Northern has also been used as a source of resistance to BYMV since the
early 1950’s (Thomas and Zaumeyer, 1953). Although some BYMV strains
can overcome the apparently recessive resistance genes present in Great
Northern genotypes (Tatchell et al. 1985), usually weak or incompatible
reactions are observed between the virus and the host, leading to attenuated
symptom development. This recessive resistance mechanism has been
observed in other plant-virus interactions (Valkonen, 2002). Resistance to
BYMV has also been identified in P. coccineus (Bagget, 1956). A single
dominant gene, By-2, conditions this resistance (Dickson and Natti, 1968).
374 F. J. Morales

Another group of plant viruses that exhibit considerable pathogenic

variability in P. vulgaris, is the cucumovirus genus. Fortunately, the use of
molecular techniques to characterise different cucumovirus strains isolated
from common bean (F.J. Morales, unpublished data), has shown that the
majority of cucumovirus isolates belong to two different species: Cucumber
mosaic virus (CMV), and Peanut stunt virus (PSV). Of the two
cucumoviruses, PSV tends to predominate and cause more damage to
susceptible common bean cultivars in temperate agricultural regions, where
different legume species are inter-cropped. In areas planted with both
cucurbits and common bean, CMV can easily jump from cucurbits to
common bean plants. Resistance to mild strains of PSV have been identified
in Great Northern, Red Mexican, Pinto and some navy bean cultivars (F. J.
Morales, unpublished data). The main natural mechanism of resistance to
both PSV and CMV is a localised hypersensitive response, although the HR
does not preclude the systemic invasion of the plant by these viruses in many
susceptible common bean genotypes. The author found a very aggressive
natural PSV/CMV recombinant virus affecting common bean in Chile, South
America (White et al. 1995).
Whitefly-transmitted geminiviruses (begomoviruses) are currently the
main threat to common bean production in the lowlands and mid-altitude
valleys of tropical and subtropical South America, Mexico, Central America
and the Caribbean region (Morales and Anderson, 2000). These single-
stranded DNA viruses replicate in the nuclei of infected cells, and cause
severe plant damage and total yield losses in most common bean cultivars
grown to date. Despite the evaluation of thousands of common bean
genotypes available commercially and in gene banks, no immune genotypes
have been identified so far against the main begomoviruses that affect
common bean production in the region (Morales and Niessen, 1988).
Bean golden mosaic virus (BGMV) was first observed in 1961, in
Brazil (Costa, 1965). Within the following two decades, this virus had
become the most limiting problem of common bean production in eastern
Brazil, northwestern Argentina and south-eastern Bolivia, due to the rapid
expansion of soybean as a non-traditional export crop. Soybean is a suitable
breeding host for Bemisia tabaci, the whitefly vector of begomoviruses. A
closely relatedbegomovirus, Bean golden yellow mosaic virus (BGYMV),
originally thought to be BGMV, infects common bean in southern Mexico,
Central America and the Caribbean region (Morales and Anderson, 2000).
Bean dwarf mosaic virus (BDMV), first described in Brazil (Costa, 1965),
became economically important in the early 1980s, when it totally destroyed
over 40,000 hectares of common bean plantings in northwestern Argentina
(Morales et al. 1990). Bean calico mosaic virus (BCaMV) is a geminivirus
transmitted by B. tabaci to common bean in northwestern Mexico (Brown
 B2. Common Beans 375

and Bird, 1992). This begomovirus was initially thought to be BGMV, but it
was later shown to be a distinct virus species related to Squash leaf curl
virus (Loniello et al. 1992). BCaMV causes widespread epidemics in
common bean plantings in the states of Sonora, Sinaloa and Nayarit,
Mexico (Morales and Anderson, 2000).
Initial attempts in Brazil, to breed common bean for BGMV resistance
were disappointing. Pompeu and Krantz (1977) made individual plant
selections of symptomless common bean plants found in BGMV-affected
plantings of three common bean cultivars: Rosinha G2, Aetê 1, and Carioca
99. These symptomless plants were shown to be fully susceptible to the virus
in subsequent evaluations (Costa, 1987). The presence of ‘escapes’ in
common bean fields showing high BGMV incidence, is a common
phenomenon associated with begomovirus attacks.
The failure to identify natural sources of BGMV resistance at that time,
led Brazilian scientists to create atomic mutants (Tulman-Neto, 1979). One
of these common bean mutants named TMD-1, showed partial resistance to
the virus but its use in conventional breeding programs did not produce any
outstanding progenies.
Another breeding project was initiated in 1974, to solve the bean golden
yellow mosaic problem in Central America, Mexico and the Caribbean.
Approximately, 7,000 germplasm bank accessions of common bean were
evaluated under natural disease pressure in southeastern Guatemala, but no
immune genotypes could be identified. However, a group of black-seeded
genotypes, namely Turrialba 1, Porrillo 70, Porrillo Sintetico, ICA-Pijao and
ICA-Tui, exhibited moderate levels of resistance to BGYMV (Yoshii et al.
1980). The natural resistance mechanism of these genotypes was thought to
be tolerance (acceptable yield despite noticeable foliar yellowing), but
systemically infected plants showed mosaic symptoms and distorted pods. A
careful analysis of these black-seeded genotypes showed that yield was the
result of low to moderate disease incidence in populations of these
genotypes. Porrillo Sintetico and ICA-Pijao were ultimately selected,
together with Turrialba 1, as potential parental materials. The best lines
derived from different crossed between the selected parental genotypes:
DOR 41 (Porrillo Sintético X ICA-Pijao), DOR 42 (ICA-Pijao X Turrialba
1) and DOR 44 (sister line from the cross ICA-Pijao X Turrialba 1), were
soon released in Guatemala as cultivars ICTA-Quetzal, ICTA-Jutiapan and
ICTA-Tamazulapa, respectively (Yoshii et al. 1980). In the absence of
pesticide applications, ICTA-Jutiapan, ICA-Pijao and the local black-seeded
land-race, Rabia de Gato, sustained yield losses of 38%, 53% and 86%,
respectively. An artificial inoculation test using the best source of resistance,
Porrillo Sintético, revealed that early (7-8 days after sowing) inoculation of
this genotype resulted in 100% disease incidence, whereas inoculation 9-11
376 F. J. Morales

days after sowing, reduced disease incidence by 50%. This mechanism of

resistance seems to be related to the considerable ‘plant vigor’ (rapid rate of
vegetative growth) characteristic of these Mesoamerican, black-seeded
genotypes. Additionally, most common bean genotypes show ‘mature plant
resistance’ to begomoviruses, and, thus, virus inoculation during the
reproductive phase of the plant often results in disease escape or moderate
yield reduction.
Despite initial successes in developing BGYMV-resistant common bean
genotypes, two constraints remained. First, yield losses fluctuated
proportionally with viruliferous B. tabaci populations, and, secondly, there
was no progress in breeding for BGYMV resistance in non-black-seeded
common bean cultivars. This situation persisted for some years, with only
some agronomic improvements to the first generation of black-seeded DOR
lines, such as the recovery of ‘earliness’ (short life cycle) from the BGYMV-
susceptible landraces. This physiological trait also contributed to lower
disease incidence because early common bean genotypes reached maturity
sooner and grew faster, resulting in ‘disease escape’.
In the mid 1980s, a common bean line (A 429) developed at CIAT,
Colombia, for superior upright architecture, showed an unexpected high
level of BGYMV resistance under field conditions in Central America. An
evaluation of its parental genotypes for their reaction to BGYMV, did not
reveal genotypes possessing a high level of resistance. However, one parent,
a common bean genotype belonging to the Mexican Durango race (Singh et
al. 1991), did not react with the characteristic yellowing when inoculated
with BGYMV, despite being systemically affected by plant malformation
and severe flower abortion caused by the virus (Morales and Niessen, 1988).
This common bean genotype, called ‘Garrapato’, soon became one of the
most widely used sources of begomovirus resistance in common bean-
breeding programs in Latin America (Singh et al. 2000). The gene bgm-1
was shown to condition mosaic resistance in Garrapato (Morales and
Niessen, 1988; Blair and Beaver, 1993). A new natural mechanism of
resistance to disruption of the photosynthetic capacity (mosaic) induced by
mosaic-inducing begomoviruses, had thus been identified in P. vulgaris
(Morales and Niessen, 1988).
Later on, a red kidney line (DOR 303) was also selected for its high
level of BGYMV resistance under field conditions in Central America. An
evaluation of the parental materials selected to produce this line, revealed the
presence of a red kidney genotype, Red Kloud, of Andean (race Nueva
Granada) origin (Singh et al. 1991), besides the traditional black-seeded
source of resistance, Porrillo Sintetico. Red Kloud was shown to exhibit
‘tolerance’ to BGYMV, producing flowers and pods despite the presence of
striking mosaic/yellowing foliar symptoms (Morales and Niessen, 1988).
 B2. Common Beans 377

Based on this finding, several other common bean genotypes of Andean

origin have been selected as sources of tolerance to whitefly-transmitted
viruses. The retention of the flowering capacity of several Andean common
bean genotypes infected by begomoviruses, is another natural mechanism of
‘resistance to flower abortion’ induced by begomoviruses in other races of
common bean, such as the Mesoamerican and Mexican (Durango) races.
The interracial recombination of Mesoamerican and Andean genes
produced a red-seeded common bean genotype possessing high levels of
BGYMV resistance. The BGYMV-resistance gene in DOR 303 was later
identified as bgm-2 (Velez et al. 1998). Some Andean common bean
genotypes also possess genes for ‘resistance to the pod malformation’,
characteristically induced by BGYMV in susceptible bean cultivars (Morales
and Niessen, 1988). Molina and Beaver (1998) reported on the existence of a
dominant gene, Bgp, responsible for this trait, which apparently requires the
presence of bgm-1 for complete expression. Pod malformation affects
critical yield components, such as the number of pods per plant and number
of seeds per pod.
Based on the above findings, an extensive search for new sources of
resistance was launched using the common bean collection maintained at
CIAT. A selection of diverse grain types was evaluated in different countries
of Latin America, from Argentina to northern Mexico, to identify different
mechanisms of virus resistance and sources of resistance to begomoviruses
infecting common bean in this region. At least 10 new sources of resistance
were identified in the P. vulgaris accessions possessing grain colors different
than black. The most interesting bean begomovirus-resistance mechanisms
were: disease escape, low mosaic expression, hypersensitivity, reduced
flower abortion, and resistance to pod malformation (Morales and Niessen,
1988).
The general combining ability of these traits was highly significant
(P<0.01) and greater than values for specific combining abilities, suggesting
that selection for the various traits was possible in true breeding lines, due to
significant additive genetic variance (Morales and Singh, 1991). In
subsequent studies, 83 recombinant inbred lines (RIL) selected from a
population generated from the cross between a Mexican (Pinto UI 114) and a
Mesoamerican (ICA-Pijao) common bean genotype, were evaluated for their
reaction to BGYMV. Of these lines, 11 did not show symptoms, 24 lines had
mean disease incidence of 8%, 28 lines had a disease incidence of 26.6%
and developed intermediate mosaic symptoms, and 20 lines were more
susceptible than either of the parents. Thus, values for the 83 RILs
transgressed the reactions observed for the two parents, showing both higher
and lower levels of disease incidence and mosaic expression (‘transgressive
segregation’). These results suggested that the BGYMV-resistance genes in
378 F. J. Morales

the two parental genotypes were different and complementary to each other
and, consequently, that gene pyramiding may be a viable breeding strategy.
Subsequent interracial crosses produced highly resistant lines, which
have become cultivars in different countries of Central America.
Begomovirus replication in these improved genotypes was highly restricted
during the initial stages of infection (up to 15 days after inoculation)
according to nucleic acid hybridization tests performed on these lines
(Morales, 2000). This type of resistance has also been associated to
quantitative traits (QTLs), which reduce symptom expression (Miklas et al.
1996). On the contrary, common bean genotypes derived from intra-racial
populations (e.g. DOR 41, DOR 390, DOR 500), usually behave as
moderately resistant under severe whitefly/virus pressure (Singh, et al.
2000).
The ‘hypersensitive response’ (HR) is not a common natural resistance
mechanism against begomoviruses, but it has been observed in a bean
genotype of Mexican (race Durango) origin, Red Mexican 35, following its
manual inoculation with BGYMV (Morales and Niessen, 1988).
Some of the sources of resistance to BGMV and BGYMV identified in
P. vulgaris are also effective against the other begomoviruses that attack
common bean. For instance, Azufrado Higuera is a new cultivar developed
from Nueva Granada (Andean) sources of resistance (originally identified in
South America) released in north-western Mexico to control Bean calico
mosaic virus (Morales, 2000). The resistance mechanisms found in race
Nueva Granada, are not only effective in controlling flower abortion due to
virus infection, but also flower abortion caused by high temperatures during
certain months of the year. Some common bean genotypes, such as Pinto
114 and Red Mexican 35, known sources of resistance to BGMV and
BGYMV, are immune to Bean dwarf mosaic virus (Morales et al. 1990).
It is interesting to note that the above-mentioned common bean
genotypes belonging to race Durango of P. vulgaris, have resistance to
different whitefly-transmitted viruses. In fact, these and other bean
genotypes from the central plateau of Mexico, show resistance to several
other common bean viruses, including BCMV, BYMV, and CMV (F.J.
Morales, unpublished data). However, only BCMV has been observed by
the author to occur in their semi-arid region of origin in central Mexico. It is
possible that these genotypes possess ‘generalized stress tolerance’, also
referred to as ‘rusticity’ (White and Izquierdo, 1991), rather than virus-
specific genes for resistance. These ‘rustic’ genotypes also possess other
traits, such as ‘earliness’ and ‘vigour’, which have been observed to help
plants escape virus infection.
The natural resistance mechanisms described here can be efficiently
exploited in crop improvement programs, to prevent or reduce yield losses
 B2. Common Beans 379

caused by plant viruses known to attack common bean. Unfortunately, some

of these resistance mechanisms are conditioned by multiple genes, which are
not readily identified by molecular markers. In the absence of effective
multiple gene tagging techniques and conventional breeding work under
field conditions, some of these valuable natural resistance mechanisms are
being under-utilised in current common bean improvement projects.

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