Euphytica (2008) 164:173–180

DOI 10.1007/s10681-008-9689-2

Resistance to bean common mosaic potyvirus strainsand its inheritance in some Indian land racesof common bean

P. N. Sharma · Anju Pathania · Renu Kapil · Prachi Sharma · O. P. Sharma · Madhu Patial · Vikas Kapoor

Received: 19 September 2007 / Accepted: 8 April 2008 / Published online: 22 April 2008© Springer Science+Business Media B.V. 2008

Abstract Evaluation of 397 common bean acces-sions of diverse origin revealed the presence of eVec-tive sources of resistance against bean commonmosaic potyvirus strains prevalent in Himachal Pra-desh, a north-western Himalayan state of India. 21accessions viz., KR 7, KR 225, KR 295, KRC 4, KRC7, KRC 11, KRC 12, KRC 13, KRC 16, KRC 22,Amanda, Black Turtle Soup, Contender, Hans, GreatNorthern UI 123, Improved Tender Green 40031,Jubila, Kentucky wonder, Monroe, Premier and Sani-lac, were found resistant to NL-1n and NL-7n strains.Some of the genotypes showed strain speciWc resis-tance. Pattern of inheritance studied in Hans, Con-tender, KRC 4 and KRC 22 of Indian origin againststrain NL-1n revealed that single dominant gene gov-erned the resistance in Hans and Contender whereassingle recessive gene determined the resistance inKRC 22 and KRC 4. SCAR marker SW13690 ampli-Wed a product of 690 bp in Hans and Contender, con-Wrmed the presence of I gene in these cultivars. Theimplications of above genes in breeding for pro-gramme for BCMV resistance are discussed.

Keywords BCMV · Common bean · Strains · Resistance · Inheritance · Land races · SCAR marker

Introduction

Bean common mosaic virus (BCMV) is present wher-ever the common bean (Phaseolus vulgaris L.) iscultivated in the world, due to its seed-borne nature(Drijfhout 1978; Mckern et al. 1992; Sharma et al.1999; Mavric and Vozlic 2004). The closely relatedBean ommon mosaic necrosis virus (BCMNV) is alsoa major concern of bean producers in certain regionsof the world, particularly in East Africa, Europe andNorth America, where this species has caused consid-erable damage in common bean plantings (Kelly1997). In India, common bean ultivation is spreadover 8.0 million hectares with an annual yield of3.2 million tons (FAO STAT 2005). The presence ofBCMV in India was reported in 1963 by Yaraguntaiahand Nariani (1963) and Nagaich and Vashisht (1963).The virus, however, has not been studied systemati-cally in India as compared to Latin America, Africa,Europe and USA (Morales and Bos, CMI/AABDescriptions of Plant Viruses; Mckern et al. 1992;Kelly 1997; Mavric and Vozlic 2004) where bothBCMV and BCMNV have been reported to occur(Spence and Walkey 1995; Sengooba et al. 1997; Sil-bernagel et al. 2001). In India, most of the work onBCMV has been conducted in Himachal Pradesh, aNorth-western Himalayan state, where evaluations ofover 100 virus isolates (unpublished data) have onlyrevealed the presence of BCMV (Sharma et al. 1999;Sharma 2000; Kapil et al. 2005). Wide variation existsin the common bean gene pool in India which has not

P. N. Sharma (&) · A. Pathania · R. Kapil · P. Sharma · O. P. Sharma · M. Patial · V. KapoorDepartment of Plant Pathology, Molecular Plant Pathology Laboratory, CSK HPAU, Palampur, HP 176 062, Indiae-mail: pns@hillagric.ernet.in; pns1960@gmail.com

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174 Euphytica (2008) 164:173–180

so far been exploited as compared to Andean andMesoamerican bean gene pools (Pathania et al. 2006).The phenotypic recombination of BCMNV andBCMV strains (Silbernagel et al. 2001) indicates thelikely appearance of more complex disease problemscaused by these viruses in the future. The high rate ofseed transmission of these viruses and their manage-ment through physical and chemical means is diYcult(Galvez and Morales 1989). The classical work ofDrijfhout (1978) on genetics of resistance in commonbean demonstrates the involvement of four recessive(bc-1, bc-2, bc-3 and bc-u) and one dominant gene I.However, expression of various R-genes and theircombinations is eVective only in the presence of thenon-speciWc recessive gene bc-u, except bc-3 and I(Drijfhout 1978; Kelly 1997). Whereas the dominant Igene is eVective against most BCMV strains, it predis-poses common bean genotypes to attack by necrosis-inducing strains of BCMV and BCMNV (Drijfhout1975, others). BCMV and BCMNV resistance breed-ing programmes are primarily oriented to the develop-ment of multiple gene resistance to these viruses(Drijfhout 1978; Kelly et al. 1995; Kelly 1997).Molecular markers linked to resistance genes like bc-1, bcI2, bc-3 have been developed to facilitate theirdetection, particularly in the case of epistatic aVects ofsome genes in pathogenicity tests (Haley et al. 1994a;Melotto et al. 1996; Miklas et al. 2000; Mukeshimanaet al. 2005). The dominant I gene has been character-ized by various workers and molecular markers havebeen developed for its detection in bean genotypes(Haley et al. 1994a; Melotto et al. 1996; Kelly 1997;Cadle-Davidson and Jahn 2006). Both BCMV/BCMNV and its common bean host have been studiedsystematically in Latin America, US and Europe andeVective breeding programmes have resulted in alarge number of resistant varieties. However, no suchstudies have been conducted in India, except in ourlaboratory (Sharma et al. 1999; Sharma 2000; Kapilet al. 2005; Sharma 2007), where existence of diVer-ent BCMV strains and sources of resistance againstthe virus have been identiWed (Kapil et al. 2005; Kapil2007). However, the majority of locally grown landraces have been found susceptible to the disease(Kapil 2007). The objective of this study was to iden-tify sources of resistance against two BCMV-likestrains designated in India as NL-1n and NL-7n, andto study the genetics of resistance in some commonbean land races grown in India.

Material and methods

Virus culture, preparation of inoculum and methodof inoculation

Virus cultures of two BCMV-like strains, NL-1n andNL-7n (Table 1), available in our Laboratory, wereraised from infected seeds of highly susceptible culti-var Jawala, and used as a source of inoculum. Thecharacterization of the virus strains was done usingcommon bean diVerentials, DAS-ELISA (Kapil et al.2005) and RT-PCR with BCMV-speciWc primers,following the procedure of Xu and Hampton (1996).The virus inoculum was prepared from systemicallyinfected leaves washed under tap water, dried in Wlterpaper, chopped and then macerated in a chilled steril-ized pestle and mortar using cold phosphate buVer(0.01 M, pH 7.0). The slurry was sieved through dou-ble layer of muslin cloth and the sap extract used asinoculum. Seedlings were raised in the sterilizedpotting mixture (soil, FYM and sand; 3:1:1 w/w) inplastic pots under glass house conditions at 22–32°Cand inoculated at primary leaf stage by the leaf rubmethod. The leaves were dusted with carborundumpowder (400–600 mesh) before inoculation. Properprecautions were taken to avoid the contamination ofvirus strains during these studies.

Host resistance

Three hundred and ninety seven (397) common beanaccessions comprising land races, cultivars and exoticgenotypes were initially screened under natural epi-phytotic conditions at the experimental farm using 20seeds of each accession, sown in one meter rows with40 and 10 cm row and plant to plant spacing, respec-tively. The presence of BCMV in natural infectionswas conWrmed by DAS-ELISA and RT-PCR. Acces-sions showing Weld resistance were again evaluatedunder insect- proof glasshouse conditions by sapinoculation, to evaluate the observed Weld reaction ofthe cultivars. In glass house screening, Wve plants ofeach test cultivar were assayed with the inoculum ofthe test strains using the leaf rub method; and oneplant was kept as control (Drijfhout et al. 1978). Thetemperature of the glass house ranged between 24 and32°C. Test plants were kept under observation untilthe appearance of disease symptoms. Each cultivarwas tested twice. Plants showing resistant reaction

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Euphytica (2008) 164:173–180 175

Tab

le1

Com

para

tive

reac

tion

of N

L-1

n an

d N

L-7

n st

rain

of

BC

MV

on

com

mon

bea

n diV

eren

tial v

arie

ties

aD

iVer

enti

al c

ulti

vars

(D

rijf

hout

1978

); b

Path

ogen

ecity

gro

up; c

Path

geni

city

sub

-gro

up; d

Vir

us s

trai

ns

+: H

ost g

roup

sus

cept

ible

to s

yste

mic

infe

ctio

n; +

N: N

ecro

sis

abov

e 30

o C (

susc

eptib

le);

–: R

esis

tant

, no

syst

emic

infe

ctio

n;

I+m

osai

c; I

sys

tem

ic n

ecro

sis

Hos

t gro

upD

iVer

entia

l cul

tiva

raB

CM

V s

trai

n gr

oups

/Iso

late

s

Alle

le o

f th

e In

hibi

tor

gene

PG I

bPG

II

Iac (

NL

-1)d

Ib (

NL

-1n)

IIa

(NL

-7)

IIb

(N

L-7

n)

BC

MV

-27

BC

MV

-28

BC

MV

-32

BC

MV

-17

BC

MV

-18

BC

MV

-19

BC

MV

-35

BC

MV

-31

1I+

Str

ingl

ess

gree

n R

efug

ee(S

GR

)/D

ubbe

le W

itte

++

++

++

++

2I,

bc-

u, b

c-1

Red

land

s gr

eenl

eaf

‘C’

¡–

––

––

++

3I,

bc-

u, b

c-12

Red

land

s gr

eenl

eaf

‘B’

––

––

––

––

4I,

bc-

u, b

c-2

Mic

heli

te ‘

62’

––

––

––

––

5I,

bc-

u, b

c-1,

bc-

22M

onro

e–

––

––

––

–

6I

bc-1

Jubi

la–

––

+N

+N

+N

–+

N

71,

bc-

1T

op c

rop

––

––

––

––

8I

Bla

ck tu

rtle

sou

p–

––

––

––

–

9I,

bc-

12A

man

da–

––

––

––

–

123

176 Euphytica (2008) 164:173–180

were back inoculated on to healthy seedlings of sus-ceptible cultivar Jawala to detect symptomless carri-ers. Plants showing mosaic, mild mosaic, leaf rolling,green vein banding and blistering symptoms weregraded susceptible, whereas symptomless plants wererated as resistant.

Inheritance of resistance

Inheritance of resistance was studied in three localland races Hans, KRC 4, KRC 22 and one exotic beancultivar, Contender, against the NL-1n strain ofBCMV. The susceptible recommended cultivar Jaw-ala was used as recipient parent. The agronomic traitsof diVerent parents are given in Table 3. The crosseswere attempted during summer season of 2004 atCSK HPKV, Mountain Agricultural Research andExtension Centre (MAREC), Sangla, Kinnaur locatedat 2600 meter above sea level and represent one of thecommercial bean growing areas of the state. Sowingof both parents was done at weekly intervals from theWrst week of May until the end of June 2004. In eachcross, 3–4 hundred Xower buds were used to get suY-cient F1 seed. Resistant accessions were crossed withsusceptible cultivars by hand emasculation and polli-nation. The genetic populations were inoculated asdescribed in the previous section. Data were classiWedinto discrete class frequencies and tested for goodnessof Wt with chi-square test.

Detection of dominant gene I

A SCAR marker SW13690 developed by Melotto et al.(1996) and custom-synthesized from Bio Serve Bio-technologies (India) Pvt Ltd., was used to amplify the

genomic DNA of Hans and Contender (found to pos-sess single dominant gene) along with KRC 22 andJawala. Jubila and Widusa, known to carry I gene,were used as checks to conWrm the marker activity.The genomic DNA was isolated from the Wrst trifoli-ate leaf of each cultivar as per the method of Afan-ador et al. (1993). The procedure and protocoldescribed by Melotto et al. (1996) was used for PCRampliWcation and gel electrophoresis of the ampliWedproduct.

Results and discussion

Host resistance

The screening of three hundred ninety seven (397)common bean accessions for their reaction to theselected virus strains showed eighty one (81) acces-sions as resistant, whereas all other genotypes weresusceptible. DAS-ELISA conWrmed the presence ofBCMV in the infected plants. The resistant accessionsincluded both indigenous and exotic bean genotypes.The Weld resistant accessions further evaluated underglasshouse conditions against the two Indian virusstrains (NL-1n & NL-7n) showed that only 28 geno-types were resistant to the test virus strains (Table 2).Strain speciWc resistance was noticed in three acces-sions viz., SR-7-6, KR 191 and Redlands Green LeafC, against NL-1n, and in four land races E-346, KR175, KR 200 and KR 48-6, to strain NL-7n. However,21 accessions viz., KR 7, KR 225, KR 295, KRC 4,KRC 7, KRC 11, KRC 12, KRC 13, KRC 16, KRC22, Amanda, Black Turtle Soup, Contender, Hans,Great Northern UI 123, Improved Tender Green

Table 2 Reaction of common bean germplasm to BCMV strains under glass house conditions

Reaction Virus strain Cultivar

Resistant NL-1n SR-7-6, KR191, Redlands Greenleaf C

NL-7n E 346, KR 175, KR 200, KR 48-6

NL-1n & NL-7n KR 7, KR 225, KR 295, KRC 4, KRC 7, KRC 11, KRC 12, KRC 13, KRC 16, KRC 22, Amanda, Black Turtle Soup, Contender, Great Northern UI 123, Hans, Improved Tender Green 40031, Jubila, Kentucky wonder, Monroe, Premier, Sanilac

Susceptible NL-1n & NL-7n SR 74, SR-1-5, SR-1-15, SR-4-15, SR-29-1, SR-2-1, SR-20-1-14, SR-20-1-18, SR-61-3, SR-20-1-15, SR-20-1-11, SR-61-2, SR-6-14, SR-20-1-50, SR-6-4, SR-4-1, SR-6-13, SR-6-12, SR-4-6, SR-7-1, SR-71-1, SR-6-9, SR-10-2, SR-6-10, SR-22-3, SR-10-1, SR-10-6, SR-23-1, SR-6-11, SR-5-2, SR-5-3, SR-5-5, KR 14, KR 71, KR 129, KR 137, KR 260, KR 99, KR 238, KR 124, KR 135, E 429, E 433, KRC 1, KRC 5, KRC 6, KRC 9, KRC 17, KRC 15, KRC 19, Baspa, Dubbele Witte, Jawala, Kanchan

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Euphytica (2008) 164:173–180 177

40031, Jubila, Kentucky wonder, Monroe, Premierand Sanilac, were found to be resistant to both virusstrains. Among various cultivars, only Jubila showedlocal necrotic lesions followed by veinal necrosisafter four days of inoculation at temperatures above32°C. However, no virus was detected from subse-quent trifoliate leaves of the same plants using DAS-ELISA and RT-PCR analyses. There are reports ofscreening of common bean against BCMV isolates inIndia by diVerent workers, mostly based on one iso-late of the area speciWc virus except our laboratory(Ramanjulu et al. 2004; Khetarpal et al. 1994; Guptaand ChowXa 1990; Dhanju et al. 1995; Sharma andDhar 1994). 14 germplasm lines viz., Contender, EC3, EC 29, EC 41, EC 43, IC 7, IC 11900, IC 16453, IC17851, IC 18546, IIHR 220, IIHR 909, Pant Anup-ama and Premier were found free from the disease byRamanjulu et al. (2004). Khetarpal et al. (1994) inter-cepted BCMV in 15 accessions amongst the 242exotic accessions imported from Colombia, USA andHungary. Sharma (2000) also found resistance in cul-tivars, KRC 2, KRC 4, KRC 14, KRC 21, KRC 22,Hans, Kentucky Wonder, Contender and Premier inHimachal Pradesh. Dhanju et al. (1995) reportedresistance in only EC 94469 and EC 94929 to BCMVout of 44 common bean genotypes both under Weldand glass house conditions. Resistance in exotic com-mon bean accessions used in the present study hasalso been reported by various workers (Drijfhoutet al. 1978; Al-Fadhil and Al-Ani 1987; Spence andWalkey 1995; Sharma 2000). Exotic cultivars TopCrop and Amanda were found resistant to diVerentstrains of BCMV in Africa and Europe except strainVIb (Drijfhout et al. 1978 and Spence and Walkey1995). A number of resistance sources have beenidentiWed against BCMV or its strains from diVerentparts of the world mainly Africa, Europe and USA(Silbernagel et al. 1986; Al- Fadhil and Al-Ani 1987;Omunyin et al. 1988; Pellicano et al. 1993; Njau andLyimo 2000; Gonzalez 2004).

Inheritance of resistance

Reaction pattern of KRC 4, KRC 22, Hans and Con-tender to NL-In strain of BCMV presented in Table 3revealed all the plants to be free of disease. Recoverytests through back inoculation on Jawala, ELISA andRT-PCR further conWrmed the resistant nature of thedonors. Susceptible cv. Jawala exhibited mosaic,downward leaf rolling and green vein banding symp-toms. F1 plants of Jawala £ Hans and Jawala £Contender also showed resistant reaction whereasKRC 22 and KRC 4 was susceptible to NL-In(Table 3) exhibiting mosaic and leaf roll symptoms.

The observed and expected frequencies of resistantand susceptible reaction of parent Jawala, Hans, Con-tender, KRC 22, KRC 4 and F2 s are given in Table 4.The perusal of the Table 4 reveals a good Wt in theratio of 3 resistant to 1 susceptible in F2 generation ofcross Jawala £ Hans and Jawala £ Contender. Thesegregation ratio of 3 resistant to 1 susceptible in F2

generation revealed that a single dominant gene gov-erned the resistance in Hans and Contender againstNL-1n strain. However, in Jawala £ KRC 22 cross, agood Wt of a segregation ratio of 1 resistant to 3 sus-ceptible in F2 generation was observed, which indi-cates that resistance in KRC 22 to BCMV is governedby a single recessive gene. Similarly, in another crossbetween Jawala £ KRC 4, the ratio of 1 resistant to 3susceptible in F2 population did not Wt well indicatinginvolvement of linked gene in resistance of KRC 4(Table 4). The pattern of inheritance of resistance inland races of common bean conWrms the earlier Wnd-ings of Ali (1950) and Drijfhout (1978) who reportedthat the resistance in bean to BCMV/BCMNV andtheir strains, is governed by non-speciWc dominantgene I, Wve strain speciWc recessive genes bc-1, bc-12,bc-2, bc-22 and bc-3 and one strain non-speciWcrecessive gene (bc-u). Strain speciWc recessive hostgenes function in a way as to modify the eVects ofvirus induced proteins and in this case the proteins

Table 3 Agronomic traits and reaction of parents to NL-1n strain of BCMV

Accession Growth habit Colour Seed size Disease reactionWeld glass house

Maturity

Jawala I Dark red Large S S Early

Contender I Creamish Large R R Early

Hans II white Small R R Late

KRC 4 I Spotted light red Medium R R Early

KRC 22 I Black Small R R Late

I: Determinate type; II: Indeterminate type; S: Susceptible; R: Resistance

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178 Euphytica (2008) 164:173–180

that regulate systemic movement of BCMV andBCMNV in beans are likely to be highly strain spe-ciWc (Silbernagel et al. 2001). The recessive mode ofinheritance of resistance in KRC 4 and KRC 22 indi-cates the possible presence of one of the Wve recessivegenes bc-1, bc-12, bc-2, bc-22 and bc-3 in these culti-vars (Drijfhout 1978; Sengooba et al. 1997). Newpathotypes of BCMV are known to occur in beangrowing areas after the introduction of resistant culti-vars having combinations of the strain- speciWc reces-sive resistance genes. The breeders all over the worldworking on bean improvement program are nowincorporating the non-strain speciWc dominant I genealong with various recessive genes to reduce the like-lihood of new pathotypes (Kelly et al. 1994, 1995;Kelly 1997; Miklas et al. 2000; Silbernagel et al.2001; Mukeshimana et al. 2005). The recognition ofspeciWc resistance gene combination in a single beangenotype is not always possible because of theepistatic masking of expression of recessive genes.However, all the combinations of I gene with strainspeciWc recessive resistance genes are recognizable,when inoculated with BCMNV strains with an excep-tion of bc-3 gene conditioning resistance to all thestrains of BCMV and BCMNV which is epistatic tothe dominant I gene (Mukeshimana et al. 2005).Therefore, the cultivars with multiple resistance genesimpart more stable resistance to a broad spectrum of

virus strains (Miklas et al. 2000) and in commonbean, the most eVective strategy for broad spectrumcontrol of BCMV is to combine I and bc-3 genes byindirect selection using tightly linked makers whichwould facilitate the breeding of desired epistatic resis-tance gene combinations.

Detection of I gene

A SCAR marker SW 13690 used to amplify the geno-mic DNA of the test cultivars resulted in the ampliW-cation of 690 bp DNA fragment only in cultivar Hansand Contender along with Jubila and Widusa knownto carry dominant I gene (Fig. 1). However, no ampli-Wcation was observed in susceptible cultivar Jawalaafter repeated testing. Similarly no ampliWcation wasnoticed in resistant cultivar KRC 22 having a reces-sive gene, thereby establishing the presence of I genein the Indian subcontinent. The presence of I geneusing SCAR marker SW13 has also been detected inmany common bean genotypes including Widusa byMelotto et al. (1996). Since the presence of the domi-nant gene I is only detected by necrosis-inducingstrains of BCMV or BCMNV in the absence of reces-sive (protective) genes, inoculation can now be deter-mined by using robust SCAR marker SW13 in areaswhere suitable necrosis-inducing strains are not pres-ent, it will certainly facilitate the marker assisted

Table 4 Inheritance of resistance in common bean cultivars against BCMV

Parent/Cross No. of seedlings Expected ratio Chi-square P

Resistant Susceptible

Cross I

Jawala P1 – 25 – – –

Hans P2 25 – – – –

Jawala £ Hans F2 74 25 3:1 0.003NS 0.95–0.98

Cross II

Jawala P1 – 25 – – –

Contender P2 25 – – – –

Jawala £ Contender F2 57 24 3:1 0.926NS 0.30–0.50

Cross III

Jawala P1 – 25 – – –

KRC 22 P2 25 – – – –

Jawala £ KRC 22 F2 24 74 1:3 0.014NS 0.90–0.95

Cross IV

Jawala P1 – 25 – – –

KRC 4 P2 25 – – – –

Jawala £ KRC 4 F2 28 48 1:3 5.684* 0.01–0.05

P1 = Parent 1; P2 = Parent 2

* SigniWcant at 5% level; NS non-signiWcant at 5% level

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Euphytica (2008) 164:173–180 179

selection (MAS) in the breeding programme. Simi-larly, the presence of other resistance genes bc-12 andbc-3 have also been detected through molecularmarkers in common beans of diVerent gene pools(Mukeshimana et al. 2005; Miklas et al. 2000). Pres-ent study reports the Wrst evidence of dominant andrecessive resistance genes in Indian common beanaccessions and their detection through molecularmarkers developed in exotic genotypes. The resis-tance genes identiWed in the Indian land races can bepyramided easily in commercial bean varieties. How-ever, lack of information regarding genetic makeup ofresistance sources in Indian common bean necessi-tates detailed and systematic studies on BCMV resis-tance to initiate an eVective breeding program. Basedon perusal of literature pertaining to BCMV resis-tance in the Indian context, BCMNV has not beenreported yet and its occurrence can only be elucidatedafter analysis of bean mosaic infected samples fromdiVerent areas on bean diVerentials. So for the detec-tion of dominant I gene in Indian common bean geno-types, marker assisted selection will be the onlyalternative since I gene possesses a high degree ofresistance to all the strains of BCMV.

Acknowledgements We are grateful to Indian Council ofAgricultural Research, New Delhi, INDIA for Wnancial assis-tance in the form of an adhoc project. The senior author is highlygrateful to Prof. (Dr.) James D Kelly of MSU, USA, for hisvaluable guidance regarding BCMV resistance, providingreprints of research articles and using SCAR marker SW13 indetecting I gene in our resistant material. We are thankful to

Prof. R P Kaushal and reviewers of Euphytica for critical reviewof the manuscript.

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Fig. 1 AmpliWcation of common bean cultivars genomic DNAusing SCAR marker SW 13690 linked with I gene. M1: � DNA/EcoRI + HindIII DNA marker, Lane 1: Hans, 2; Jubila, 3:Widusa, 4: Contender, 5: KRC 22, 6: Jawala, M2: 100 bp ladder

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