Acta agriculturae slovenica, 83 - 1, junij 2004 str.

181 - 190

Agrovoc descriptors: Phaseolus vulgaris, potyviruses, bean common mosaic potyvirus,

serotypes, disease resistance, pathogenicity, host pathogen relations, necrosis, economic value

Agris category codes: H20, H01, F30

COBISS code 1.02

Virus diseases and resistance to Bean common mosaic and

Bean common mosaic necrosis potyvirus in common bean
(Phaseolus vulgaris L.)
Irena MAVRIČ1, Jelka ŠUŠTAR-VOZLIČ2

Received: March 2, 2004; accepted: May 20, 2004

Delo je prispelo 2. marca 2004; sprejeto 20. maja 2004

ABSTRACT

Bean common mosaic potyvirus (BCMV) and Bean common mosaic necrosis potyvirus
(BCMNV) are economically the most important viruses of common bean. They can reduce
yield and quality of harvested product. High percentage of seed transmission (up to 83%) is
one of the reasons for its distribution worldwide. They represent 7 pathogenicity groups and
10 strains. Pathogenicity groups can be determined by reactions of differential bean cultivars.
BCMV and BCMNV can be differentiated on serological and molecular level but all strains
cause similar symptoms in bean genotypes lacking resistance genes. The development of
different reactions to virus infections depends on virus strain, bean cultivar and temperature.
The host resistance genes and virus pathogenicity genes interact in development of different
responses of bean plants after infection. Different combinations of dominant and recessive
strain unspecific and recessive strain specific resistance genes confer more stable resistance
to wider spectrum of virus strains. The causal viruses, interactions of host resistance and
virus pathogenicity genes, in vivo recombinations of both viruses and methods for selecting
the desired host genotype are reviewed.

Key words: BCMV, BCMNV, resistance genes, pathogenicity genes, BCMV/BCMNV

resistance, Phaseolus vulgaris

IZVLEČEK

VIRUSNE BOLEZNI IN ODPORNOST NA VIRUS NAVADNEGA MOZAIKA FIŽOLA IN

VIRUS NAVADNEGA NEKROTIČNEGA MOZAIKA FIŽOLA PRI FIŽOLU (Phaseolus
vulgaris L.)

Virus navadnega mozaika fižola (BCMV) in virus navadnega mozaika in nekroze fižola
(BCMNV) sta ekonomsko najpomembnejša potivirusa, ki okužujeta fižol. Povzročata veliko
ekonomsko škodo pri pridelavi fižola, tako z zmanjševanjem pridelka, kot tudi s slabšo
kakovostjo pridelanega produkta. Virusa sta v svetu splošno razširjena, k temu pa je
pripomogla tudi njuna lastnost, da se v veliki meri prenašata s semenom. Prenos s semenom

1
Agricultural Institute of Slovenia, Hacquetova 17, SI-1000 Ljubljana, Slovenia; Dr., B.Sc.
biol.; irena.mavric@kis.si
2
Agricultural Institute of Slovenia, Hacquetova 17, SI-1000 Ljubljana, Slovenia; Dr., B.Sc.
agr.
182 Acta agriculturae slovenica, 83 - 1, junij 2004

lahko doseže do 83%. Virusne izolate obeh virusov uvrščamo v 7 patogrup in 10 različkov.
Uvrstitev v patogrupe in različke nam omogoča inokulacija diferencialnih sort fižola in
opazovanje njihove reakcije na virusno okužbo. Oba virusa se razlikujeta po seroloških in
molekulsko bioloških lastnostih, vendar pa na rastlinah brez genov za odpornost povzročata
zelo podobna bolezenska znamenja. Razvoj bolezenskih znamenj je odvisen od virusnega
različka, sorte gostiteljske rastline in temperature. Interakcije med produkti genov za
odpornost gostitelja in genov za patogenost virusa vplivajo na tip reakcije, ki se pojavi na
fižolu po okužbi z virusom. Kombinacije dominantnega gena za odpornost z recesivnimi geni
za odpornost omogočajo razvoj stabilnejše odpornosti na več različkov virusa, zato želje
žlahtniteljev po genotipu fižola, ki bi bil odporen na vse znane različke obeh virusov, niso
neosnovane. V prispevku sta predstavljena oba virusa, interakcije med produkti genov za
odpornost gostitelja in genov za patogenost virusa, rekombinacije obeh virusov ter metode za
selekcijo željenega genotipa gostitelja, odpornega na posamezne ali vse znane različke
BCMV in BCMNV.

Ključne besede: BCMV, BCMNV, geni za odpornost, geni za patogenost, odpornost na

BCMV/BCMNV, Phaseolus vulgaris

1 INTRODUCTION

Common bean (Phaseolus vulgaris L.) is one of the major food legumes produced. Its
production is very important in North, Central and South America, eastern Africa,
eastern Asia and south eastern Europe. Virus diseases are a major yield reduction
factor in bean production. Most of the viruses infecting common bean are insect
transmitted, some of them are also seed transmitted. Insect transmission is very
important for virus spread on short distances while seed transmission is the most
important factor in spread of viruses around the world. Even low seed transmission
produces infected plants at the most suitable time for vector transmission and this way
spreading in the field can be very fast. The list of viruses infecting beans is very long
(Brunt et al., 1996 onwards; Kumar et al., 1994) but economically the most important
ones are potyviruses, Bean common mosaic potyvirus (BCMV), Bean common mosaic
necrosis potyvirus (BCMNV) and Bean yellow mosaic potyvirus (BYMV); Cucumber
mosaic cucumovirus (CMV), Southern bean mosaic sobemovirus (SBMV), Tobacco
streak ilarvirus (TSV) and Tomato aspermy cucumovirus (TAV). Because of high
seed transmission the most important ones are BCMV and BCMNV.

2 BEAN COMMON MOSAIC POTYVIRUS (BCMV) AND BEAN COMMON

MOSAIC NECROSIS POTYVIRUS (BCMNV)

BCMV was first reported in P. vulgaris in USA in 1917 and was called bean mosaic
virus. To distinguish it from BYMV, epithet common was added later. The virus is
now distributed worldwide (Brunt et al., 1996 onwards; Jeyandandarajah and Brunt,
1993; Klein et al., 1988; Mavrič et al., 2002 and 2003; Omunyin et al, 1995;
Ravnikar et al., 1996; Sáiz et al., 1995) and causes a big economic damage by
reducing yield (as much as 80%) and quality of harvested product (Drijfhout, 1991). It
is transmitted in non-persistent manner by several aphid species including
Acyrthosiphon pisum, Aphis craccivora, A. fabae and Myzus persicae. It is also
transmitted by mechanical inoculation, up to 83% by seed. It was found that the virus
could be transmitted to offspring from healthy plant through the pollen of infected
plant. Seed transmission is irregular and depends on plant age at time of infection,
 MAVRIČ, I., ŠUŠTAR-VOZLIČ, J.:Virus diseases and resistance to Bean... 183

cultivar and virus strain. Flower buds, infected just before or after fertilisation, never
produce infected seeds. Virions are 847-886 nm long filamentous, usually flexuous
particles 12-15 nm wide. They contain 5% nucleic acids and 95% protein of 32-
35kDa. 17 potyviruses are serologically related to BCMV, including Potato virus Y,
Watermelon mosaic virus 2, BYMV, Blackeye cowpea mosaic virus (BlCMV) and
Soybean mosaic virus (SMV) (Brunt et al., 1996 onwards, Drijfhout, 1978). The last
two are now considered to be strains of BCMV (Mink et al., 1994). The symptoms
induced on bean cultivars are severe and represent light and dark green mosaic, leaf
roll, malformation of leaves and pods, rugosity of lower leaves or yellow dots, often
causing growth reduction. In some cultivars severe vascular necrosis may occur and
infected plants may die. This phenomenon is known as 'black root'. The type of
symptoms induced depends on the interaction between host resistance genes and virus
pathogenicity genes (Brunt et al., 1996 onwards; Drijfhout, 1991; Frison et al., 1990).

There used to be two serotypes of the virus, serotype A and B, which are now
considered two distinct viruses (McKern et al., 1992). BCMV, formerly BCMV
serotype B, has many different strains, some of them, like Azuki bean mosaic virus,
Blackeye cowpea mosaic virus, Cowpea aphid-borne mosaic virus, Cowpea
(blackeye) mosaic virus, Cowpea vein-banding mosaic virus, Peanut blotch virus,
Peanut stripe virus and some others, were once considered to be different viruses
(Brunt et al., 1996 onwards; Higgins et al., 1998; McKern et al., 1992a; Mink et al.,
1994). On the basis of new sequence data, serology and biological properties they
were proved to be strains of one virus. While sequence data are the major criteria for
discriminating between different viruses, biological and biophysical properties are the
major criteria for discriminating between virus strains. BCMV usually causes mosaic
symptoms on bean cultivars and only some strains can cause systemic lethal necrosis
on sensitive cultivars at higher temperatures. The BCMNV isolates, formerly BCMV
serotype A, cause systemic lethal necrosis on bean genotypes possessing dominant
resistance gene I at lower and higher temperatures (Silbernagel et al., 2001).
However, all known BCMV and BCMNV strains cause similar symptoms in bean
genotypes lacking resistance genes (Morales and Bos, 1988).

Additional differences were observed between serotype A and serotype B isolates or

between BCMNV and BCMV. Apparent molecular mass of serotype A isolates capsid
protein obtained by SDS polyacrylamide gel electrophoresis and Western blot
serology was lower (about 33 kDa) than that of the serotype B isolates (34.5 – 35
kDa). Also the normal lengths of the particles were different, 810-818 nm for serotype
A particles and 847-886 nm for serotype B. All isolates studied induced pinwheel and
scroll inclusions in cytoplasm, but only in cells infected with serotype A isolates a
specific type of proliferated endoplasmic reticulum was observed. The comparison of
3'-end of the genome of two serologically different isolates, representing both viruses,
showed considerable differences in the N-terminal part of the coat protein (CP) and 3'
non-coding region, while core region and C-terminal part of the CP appeared to be
highly conserved (Vetten et al., 1992).
184 Acta agriculturae slovenica, 83 - 1, junij 2004

Table 1: Differences between BCMV and BCMNV

BCMV BCMNV
mosaic symptoms, only some strains can systemic lethal necrosis on bean genotypes
cause systemic lethal necrosis on sensitive possessing dominant resistance gene I at
cultivars at higher temperatures lower and higher temperatures
serotype B serotype A
CP of 34.5-35 kDa CP of about 33 kDa
normal length 847-886 nm normal length 810-818 nm
only typical potyvirus inclusions proliferation of ER
sequence differences in CP and 3' non- sequence differences in CP and 3' non-coding
coding region region

Both viruses can be found on the same area and sometimes even infecting the same
plant (Silbernagel et al., 2001). Although P. vulgaris originates from Latin America
and BCMV is found there, BCMNV is not common in that part of the world.
However, BCMNV is widespread in Africa and in some parts the problems are so
serious that cultivars possessing the I gene resistance cannot be grown successfully
(Kelly et al., 1995; Omunyin et al., 1995).

For BCMV and BCMNV the first level of biological subdivision is the patogenicity
group or pathogroup, which is determined with ability of virus isolates to systemically
infect specific cultivars. Isolates inducing symptom variations (either intensity or
type) on specific hosts within a pathogroup are defined as virus strains (Silbernagel et
al., 2001).

3 PATHOGENICITY AND RESISTANCE GENES

According to the presence of pathogenicity genes (P0, P1, P12, P2, P22) and the
reactions on the differential bean cultivars, BCMV and BCMNV strains are grouped
into 7 pathogenicity groups (PGs) (I – VII) and 10 strains or subgroups with two
subgroups in each of PGs IV, V and VI (Drijfhout et al., 1978). They differ by the
number of pathogenicity genes present. PGs I, II and III have only one pathogenicity
gene, P0, P1 or P2, respectively. PGs IV and V have two genes each, P1, P12 and P1,
P2. The highest numbers of pathogenicity genes are in PG VI and PG VII. They both
have P1 and P12 in combination with P2 in PG VI and P22 in PG VII. All of the
BCMV strains used in the study of Drijfhout (1978) belong to one of PGs I, II, IV, V
or VII and all the BCMNV strains were classified as either PG III or PG VI
(Silbernagel et al., 2001). PGs are determined by the ability of virus isolate to
systemically infect a set of differential bean cultivars possessing defined
combinations of recessive and dominant resistance genes.

The host resistance genes involved in these interactions form two groups, strain
unspecific and strain specific genes. The dominant strain unspecific gene is gene I and
the recessive strain unspecific gene is bc-u. All strain specific genes, bc-1, bc-12, bc-
2, bc-22 and bc-3, are recessive and are independently inherited except for the allelic
pairs bc-1, bc-12 and bc-2, bc-22. In the absence of the I gene, the bc-u gene is
required for the expression of all strain specific recessive resistance genes. Gene
combinations of bc-u with any of the strain specific recessive resistance genes but bc-
 MAVRIČ, I., ŠUŠTAR-VOZLIČ, J.:Virus diseases and resistance to Bean... 185

3, confer strain-specific recessive resistance. Only the combination bc-u, bc-3 gives
recessive resistance to all strains of both viruses (Drijfhout, 1978 and 1991).

The dominant I gene is known to inhibit all known strains of both viruses, but can be
overcome by necrosis-inducing strains, the BCMNV. They stimulate systemic
hypersensitive response and infected plants develop systemic lethal necrosis. This
reaction is a big disadvantage of resistance by unprotected I gene. However, dominant
I gene can be protected by combining it with recessive resistance genes. These
combinations can restrict, prevent or delay extreme hypersensitive response. In plants
infected with BCMV unprotected I gene conditions immune or temperature sensitive
response (Drijfhout, 1991; Miklas et al., 2000). Another disadvantage of resistance
induced using I gene is that it has a darkening effect on red and yellow coloured seed.
If bright red or yellow colour is desired, the bc-3 gene can be used in breeding for
resistance (Drijfhout, 1991). Kelly et al. (1995) demonstrated that in the presence of I
gene, bc-3 and bc-12 do not require bc-u for expression of activity while bc-22 does.

The recognition of gene combinations in bean genotypes is not always possible

because of the epistatic masking of the weaker recessive genes. This way bc-3 masks
bc-22 and bc-12, and bc-22 masks bc-12 when inoculated with NL-3 strain of BCMNV.
However, all combinations of I gene with recessive resistance genes can be
recognized when inoculated with BCMNV. The exception is the bc-3 gene which is
epistatic to the I gene while all other recessive resistance genes are hypostatic to the I
gene. In the I, bc-3 gene combination the discrimination between genotypes I, bc-3
and i, bc-3 is possible only by test-crossing or marker assisted selection (Kelly et al.,
1995).

A gene-for-gene relationship has been found between strain specific resistance genes
bc-1, bc-12, bc-2, bc-22, and virus pathogenicity genes with the same numerical codes.
According to this theory, each strain specific, host resistance gene can be overcome
(plant can be infected and systemically invaded) if the infecting virus strain contains
the appropriate pathogenicity gene(s). The resistance gene bc-3 has no corresponding
pathogenicity gene known so far and bean genotypes with this gene are resistant to all
know strains of BCMV and BCMNV. Strains possessing P0 can infect only bean
genotypes without resistance genes. (Drijfhout, 1978 and 1991).

4 EFFECT OF TEMPERATURE ON HOST PLANT REACTIONS

The differential bean cultivars used for determination of BCMV and BCMNV PGs
and strains are divided into two main groups according to the presence of dominant I
gene. Inside these groups different combinations of recessive strain specific resistance
gene combinations are representing each host resistance group (Table 2). For
determining PGs of BCMV and BCMNV at least one cultivar from each group should
be used for testing, and for precise strain identification at least two should be used,
where possible (Drijfhout et al., 1978).

BCMNV induces a temperature insensitive, hypersensitive and often lethal necrosis in

bean cultivars possessing the dominant I gene, while BCMV causes only mosaic
symptoms in susceptible bean cultivars but can induce temperature-sensitive necrosis
186 Acta agriculturae slovenica, 83 - 1, junij 2004

in I gene cultivars at temperatures over 30°C. Cultivars from host groups 7 and 11 are
resistant to all known strains of both viruses (Drijfhout, 1978; Sengooba et al., 1997).

Table 2: Groups of host differentials on the basis of their genotype

host resistance group resistance genes

1
2 bc-u, bc-1
3 bc-u, bc-12
4 bc-u, bc-2
5 bc-u, bc-1, bc-2
6 bc-u, bc-12, bc-22
7 bc-u, bc-2, bc-3
8 I
9 bc-1, I
10 bc-12, I
11 bc-u, bc-12, bc-22, I

Bean cv. Black Turtle 1 (BT1) represents host group 8 possessing only dominant
resistance gene I. All strains of BCMNV induce systemic hypersensitive vascular
necrosis and dieback on plants of BT1 grown at constant temperatures of either 22°C
or 32°C. This phenomenon is called temperature insensitive necrosis (TIN). Some,
but not all strains of BCMV cause systemic vascular necrosis and death only when
BT1 plants are grown at constant 32°C. These strains can not infect BT1 plants grown
at 22°C – phenomenon called temperature sensitive necrosis (TSN). A few BCMV
strains will not infect BT1 at either temperature. These are called non-necrotic (NN)
strains (Silbernagel et al., 2001).

A significant aspect of BCMV/BCMNV resistance is that all virus strains are capable
of infecting the primary leaves of all bean cvs. in host groups 1 through 6 whereas no
strains are capable of infecting the primary leaves of host group 7 which possesses
recessive resistance gene bc-3. This type of resistance appears to involve a form of
immunity rather than the strain specific resistance to systemic movement determined
by the other recessive genes (Silbernagel et al., 2001).

5 IN VIVO RECOMBINATIONS OF BCMV AND BCMNV

Since BCMV and BCMNV can sometimes be found on the same area and even
infecting the same plant Silbernagel et al. (2001) suspected that both viruses can
somehow be capable of recombination in vivo to create new strains or even new
pathotypes. In their experiments they used US-5 strain of BCMV and NL-8 strain of
BCMNV representing two different PGs. NL-8 represents PG III, has only one
pathogenicity gene P2 and induces TIN on BT1 but not on other I gene cultivars. US-
5 from pathogenicity group IV has pathogenicity genes P1 and P12, is a non-necrotic
strain and can systemically infect cultivars from host groups 1, 2 and 3. During
cultivation of single strains on susceptible or resistant cultivars, no isolates with
unusual pathogenicity or serological characteristics were detected. This indicates that
spontaneous mutations in these characteristics are either extremely rare or do not
 MAVRIČ, I., ŠUŠTAR-VOZLIČ, J.:Virus diseases and resistance to Bean... 187

occur under used conditions. The same situation was observed when both strains were
used in the same inoculum for inoculation of bean cultivars which were either
susceptible or resistant to both strains. When inoculating plants, resistant to one strain
but susceptible to the other they obtained some isolates causing systemic infection in
resistant plant. These isolates were inoculated on differential cultivars and their
characteristics remained stable through serial transfers made over a period of at least
two years. That justified their classification as distinct virus strains. Three strains of
PG IV and serotype A were found, what is the first finding of this combination. All
serotype A isolates before represented PGs III or VI. They also obtained unusual
serotype B isolates representing PGs III and VI, which were not found before.
According to authors experience in vivo recombination between BCMV and BCMNV
can occur only when both strains are able to infect and replicate in the primary leaves
of the resistant plants and when plants are resistant to systemic movement of one of
the parental strains. The results of the study suggest that the recombinant virus strains
will retain the coat protein gene of the original incompatible strain while obtaining a
portion of the compatible strain genome which controls systemic movement. This in
turn suggests that the strain-specific recessive resistance host genes function in a way
as to modify the effects of virus-induced proteins. In this case the proteins that
regulate systemic movement of BCMV and BCMNV in beans are likely to be highly
strain-specific.

Only the serotype A recombinant strains obtained in this study produced TIN on
cultivars with the dominant I gene, the same as in nature. This indicates a close
relationship between serotype A and ability to induce TIN. In contrast the association
of serotype B epitope and ability to induce TSN was not linked.

According to the authors the results of this study also suggest that serotype and
pathogenicity gene determinants are independent, pathogenicity and symptomatology
have different determinants and under the conditions in experiment multiple
exchanges can occur between virus strains within a single plant. New pathotypes of
BCMV are known to occur in bean growing areas after the introduction of cultivars
having resistance controlled only by combinations of the strain-specific recessive
resistance genes. In the US, breeders now incorporate the non-strain specific
dominant I gene along with various recessive genes to reduce the potential
development of new pathotypes (Silbernagel et al., 2001).

6 SELECTION OF SPECIFIC GENOTYPES

The I gene was effectively used in breeding for resistance to BCMV until necrosis
inducing strains of BCMNV appeared. After that attempts to protect I gene with
recessive resistance genes (primarily bc-22 and bc-3) were made. The cultivars with
multiple resistance genes are known to possess more stable resistance against a
broader spectrum of virus strains (Miklas et al., 2000). The recognition of specific
resistance gene combinations in a single bean genotype is not always possible because
of the epistatic masking of expression of the weaker recessive genes. However, all
combinations of I gene with strain specific recessive resistance genes are
recognizable, when inoculated with BCMNV strains. The exception is the bc-3 gene
which is epistatic to the I gene while all the other recessive genes are hypostatic to it
in their mode of action. It is also known that the bc-3 gene alone conditions resistance
188 Acta agriculturae slovenica, 83 - 1, junij 2004

to all BCMV and BCMNV strains, so it is not possible to detect accompanying

resistance sources without a test cross (Haley et al., 1994). The alternative to test-
crossing would be marker assisted selection of desired genotypes. This method would
enable breeders to discriminate also between I, bc-3 genotypes and i, bc-3 genotypes
when needed and also to select for specific resistance genes in the absence of the
virus. Molecular markers linked to some of bean resistance genes were developed in
past years (Haley et al., 1994; Melotto et al., 1996; Miklas et al., 2000; Strausbaugh
et al., 1999).

The most resistant bean genotype suggested by Drijfhout would be I, bc-u, bc-12, bc-
22, bc-3. He also clearly demonstrated that, in the absence of the I gene, the bc-u gene
was required for the expression of all other recessive strain specific resistance genes.
However, in plants with the I gene, bc-u is not always necessary to be present. The
bc-u gene is not required for expression of resistance, for instance in I, bc-3 genotypes
but would be needed for expression of the bc-22 resistance genotype I, bc-22, bc-3. In
this case a marker linked to the bc-u gene would be needed to assure that all recessive
resistance genes are present and active.

7 CONCLUSIONS

BCMV and BCMNV are two economically very important bean viruses transmitted
by several aphid species and by seed. Seed transmission is the major mode of
transmission of both viruses on long distances. BCMNV induces a temperature
insensitive, hypersensitive and often lethal necrosis in bean cultivars possessing the
dominant I gene, while BCMV causes only mosaic symptoms in susceptible bean
cultivars but can induce temperature-sensitive necrosis in I gene cultivars at
temperatures over 30°C. Since both viruses can be found on the same area and even in
the same plant, recombinations between them are possible and can lead to creation of
new strains or even new pathotypes. The I gene was effectively used in breeding for
resistance to BCMV until necrosis inducing strains of BCMNV appeared. Later,
attempts were made to protect I gene with recessive resistance genes. It is now known
that the cultivars with multiple resistance genes possess more stable resistance against
a broader spectrum of virus strains.

Viruses are known to greatly reduce bean yield. BCMV can reduce yield up to 24%,
and BYMV up to 40% (Kumar et al., 1994). 40% increase of yield was observed by
Benedičič and Berljak (1996) after pathogen elimination from bean cv. Zorin.
However, it is important for the breeders to use every available methods and tools for
breeding for resistance to BCMV and BCMNV to increase the yield and improve the
quality of beans.

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