Aslam et al.

The Journal of Animal & Plant Sciences, 23(6): 2013, Page: J.

1679-1685
Anim. Plant Sci. 23(6):2013
ISSN: 1018-7081

ESTIMATION OF GENETIC VARIABILITY AND ASSOCIATION AMONG DIFFERENT

PHYSIOLOGICAL TRAITS RELATED TO BIOTIC STRESS (FUSARIUM OXYSPORUM
L.) IN CHICKPEA
M. Aslam*, M. A. Maqbool*, S. Akhtar* and W. Faisal**
*

**

Department Plant Breeding and Genetics, University of Agriculture Faisalabad, Punjab, Pakistan
Centre of Agricultural Biochemistry and Biotechnology, University of Agriculture, Faisalabad, Pakistan
Corresponding author e-mail: aslampbg@yahoo.com

ABSTRACT
Experiment was conducted to assess genetic differences among chickpea genotypes under normal and biotic stress
(inoculated with Fusarium oxysporum L.) conditions, to estimate the relationship among different biotic stress related
traits and to identify suitable parental material to be used in breeding programs for the development of genotypes
resistant to fusarium wilt. The responses of 70 different chickpea genotypes were evaluated on the basis of different
physiological traits by following principal component analysis (PCA). According to PCA, under normal and stress
conditions out of eight only 4 PCs had more than one eigen value in each case and collectively contributed 71.50% and
75.2% variability under normal and stress conditions respectively. Biplot analysis depicted that under normal condition
the genotypes 1007, 60101, 7008, 405, PB91, B3008, 3013, 7002, 7012, 1217, 6011, BITAL98, 6028 and CH-8 were
highly diversified, whereas under stress condition, genotypes 7059, 4004, 6001, 7046, 1288 and 1143 proved resistant
and presented the greatest diversity. Genotypes 6028, 7027, BRC236, 5028, 7056-1, 6010, 6003, 1217, 3013, 4028
6017, 7010, 3019, PB2000, 5006, 6255, 4046, PB2008, B3008, 1159, 2009-1, and 6011 were found with least diversity
and declared as susceptible because of poor performance.
Key words: Chickpea, Fusarium wilt, Biplot, PCA and Correlation.
protein contents and rich in zinc, dietary fiber, calcium,
magnesium, phosphorus, potassium, iron and vitamins
(Peksen and Artk, 2005; Kayan and Adak, 2012).
Fusarium wilt is a severe ailment of chickpea in
India, Iran, Pakistan, Nepal, Burma, Spain and Mexico.
In Pakistan Fusarium oxysporum is the second most
severe problem of chickpea after blight in the districts of
Jhang, Layyah, Khushab, Bhakkar and Mianwali (Shah et
al., 2009). Areas with low rainfall alongwith favorable
environmental conditions are prone to wilt (Nene et al.,
1996). Fusarium oxysporum f. sp. ciceri is a soil borne,
root pathogen which colonizes the xylem vessels and
blocks them entirely (Singh et al., 2006). An expected
loss of 12 million rupees annually was stated from
Pakistan due to this disease (Shah et al., 2009). Wilting at
earlier growth stage causes more loss than at lateral phase
of growth and seeds harvested from wilted plants looks
lighter and duller than those from healthy plants (Ahmad
et al. 2010). In a highly susceptible cultivar, wilt
symptoms can be observed within 25 days after sowing in
the field. Yellowing of leaves, flaccidity, chlorosis and
wilting (drooping of rachis, leaflets and petioles) are
among the critical effects of fusarium wilt on chickpea
plant (Haware, and Nene, 1982; Jimnez-Daz et al.,
1993). It may appear at vegetative and reproductive
growth stages accompanied with yield losses in both
cases (Navas-Cortes et al., 2000). In Pakistan 10 -50%
losses have been reported in chickpea due to fusarium

INTRODUCTION
Plant genetic resources are actually the
guarantee of world food security. Genetic resources
possess genetic material variability contained in
traditional varieties, cultivars, wild crop relatives and
other wild species. It is necessary to exploit genetic
resources to meet global food requirement (Farshadfar
and Farshadfar, 2008).
Chickpea (Cicer arietinum L.) is an important
crop possessing high variability for different qualitative
and quantitative traits with 17-24% protein, 41-50.8%
carbohydrates, high percentage of other mineral nutrients
and unsaturated linoleic and oleic acid in seed. It is
grown throughout the world with different names i.e.
Chickpea in UK, Bengal gram in India, Garbanzo in
Latin America, Hommes or Hamaz in Arabic world,
Nohud or Loblebi in Turkey and Shimbra in Ethopia.
Chickpea restores and retains the soil fertility by its
nitrogen fixing ability predominantly in dry areas
(Ahmad et al, 2010), and fit very well in different
cropping patterns. Its yield is mostly concentrated in
rainfed areas of Punjab (910.7 thousand hectares)
followed by Sindh (55.9 thousand hectares) and Khyber
Pakhtunkhwa (KPK) (49.0 thousand hectares), whereas in
Balochistan it is cultivated on 36.7 thousand hectares
(Bokhari et al., 2011). Globally, over 90% of the total
chickpea is produced and used in Asia. It contains high

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J. Anim. Plant Sci. 23(6):2013

wilt during last few decades (Ikramul and Farhat, 1992;

Mukhtar, 2007).
The cheapest, cost-efficient and the most ideal
way to manage chickpea wilt, is the use of resistant
cultivars. Chemical control of wilt is not reasonable and
economical because of the soil as well as seed-borne
nature of the pathogen. This pathogen can stay alive in
soil for numerous years by means of chlamydospores
(Ahmad et al. 2010). Fungal chlamydospores can stay
alive in soil up to 6 years in the absence of the host plants
(Iqbal et al., 2010). Therefore, this disease can be
managed principally by the use of resistant cultivars
(Ahmad et al. 2010). Estimation of genetic variability
based on physiological and morphological standards is
the main step in breeding programs as improvement
depends upon the magnitude of variability and this leads
towards selection of parents. High level magnitude of
variability enables the researcher to use appropriate gene
pool for improvement. There is a need to identify the
resistant sources against different isolates of Fusarium
oxysporum (Shah et al., 2009).
Present study was planned to assess the newly
developed germplasm of chickpea for resistance against
local isolates of wilt fungus on the basis of different
physiological standards by using multivariate technique.
There is dire need for continuous screening of chickpea
germplasm for resistant against fusarium wilt because
resistant varieties become susceptible with the passage of
time. This conversion from resistance to susceptibility
might be either due to resistance breakdown or
evolutionary changes in pathogenic variability (Nikam et
al., 2007).

resources of the department of Plant Breeding and

Genetics, University of Agriculture, Faisalabad. Pathogen
(Fusarium oxysporum) was collected from Nuclear
Institute of Agriculture and Biology (NIAB) Faisalabad,
Pakistan in petri plates filled with potato dextrose media.
Experiment was divided in to two subunits. Each
unit comprised of 10 seedlings per genotype per
replication. One subunit was treated with inoculum and
named as inoculated and second as standard / normal in
which no inoculum was applied. Two factor factorial
triplicated complete randomized design (70 genotypes
and 2 treatments) was followed to plant the seeds of all
the genotypes in polythene bags (7 4). Initially two
seeds per polythene bag were sown and thinned up to one
seedling per bag after the establishment of seedlings.
Pathogen was multiplied in petri plates filled
with potato dextrose media for two weeks at room
temperature. Inoculum solution was prepared by mixing
pathogen with distilled water and was applied at seedling
stage with shower in root zone. Totally dry condition was
maintained in order to provide favorable environment to
pathogen for its dissemination. To maintain uniform
intensity of pathogen and to increase the severity,
inoculation in the inoculated set was repeated twice with
the uniform interval of one week. Data were recorded
after 25 days of inoculum application for leaf rolling
(LR), survival rate (SR), ascorbic acid (AA), carotenoids, chlorophyll a, chlorophyll b, root/shoot ratio
(RS) and root density (RD). Ascorbic acid contents in the
plant samples were estimated by using Kampfenkel
method (Kampfenkel et al., 1995). Chlorophyll contents
were estimated by following formulae designed by
Nagata and Yamashita (1992).
The level of resistance/susceptibility of each
genotype was determined by using the rating scale (Iqbal
et al. 2010; Table 2).

MATERIALS AND METHODS

Germplasm of variable origin used in this study
(70 genotypes) was collected from chickpea germplasm

Table-2. Scale for evaluation of genotypes under stress condition (Inoculum applied).
Disease incidence
0-10 percent
11-20 percent
21-30 percent
31-50 percent
51-100 percent

Response
Highly resistant
Resistant
Moderately resistant/ Tolerant
Susceptible
Highly susceptible

Statistical Analysis: Data were analyzed for the

significance of differences using factorial analysis of
variance (ANOVA) devised by Steel and Torrie (1980).
Survival rate was recorded as the percentage of survived
plants. The principal component analysis is a multivariate
statistical procedure for investigation and simplifying
complex data sets. The ability of this method to transform
several possibly associated variables into a smaller

Scale
1
2
3
4
5

Response
No leaf rolling
1/4 leaf rolling
1/2 leaf rolling
3/4 leaf rolling
Complete leaf rolling

number of variables called principal components. This

method has been established by Everitt and Dunn (1992)
and followed by Kayan and Adak (2012). Biplot analysis
was used to study the diversity among genotypes.
Correlation coefficient reflects how stronger or weaker
association is present among variables and provides the
basis for the selection standards to be used in selection
procedure.

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J. Anim. Plant Sci. 23(6):2013

contents contributed positively and the contribution of all

other parameters was negative (Table-3).
In
biplot
graph
the
lengths
of
environment/parameter vectors show the discriminating
nature of environment/parameter (Yan and tinker, 2006).
Longer the vector length greater the parameter is
informative about the performance of genotypes in biplot
graph. Chlorophyll a, chlorophyll b, ascorbic acid, root
shoot ratio, root density and survival rate % were more
discriminating as compared to other parameters in present
studies. These discriminating parameters were important
for selection of adapted genotypes (Yan and Tinker,
2006). Under normal condition, significant variability
was observed among genotypes for the desired
characters. Genotypes 1007, 60101, 7008, 405, PB91,
B3008, 3013, 7002, 7012, 1217, 6011, BITAL98, 6028
and CH-8 exhibited the highest level of variability for the
parameters under study. This variability indicated the
wide dispersion of genotypes on biplot graph (Figure-1).
Genotypes 1288, 7046, 4004, 6001, 7059, 1017, 504,
6010, 2052, 405, 1143 and 5006-1 performed well and
exhibited the highest level of variability under inoculated
condition. These genotypes showed wide dispersion from
the origin of biplot graph. Genotypes which were
concentrated towards the origin the graph had low
variability for the studied parameters under stress
environment (Figure-2).
Under normal condition, ascorbic acid (AA) was
non-significantly and positively correlated with betacarotenoids (-C), chlorophyll-a (Ch. a), root shoot ratio
(R/S), root density (RD) and survival rate (SR) and
negatively correlated with chlorophyll b (Ch. b) and leaf
rolling (LR). Beta carotenoid (-C) had positive
correlation with Ch. a, RD and SR whereas negatively
correlated with Ch. b, LR, and R/S. Chlorophyll a was
positively correlated with Ch. b, RD and SR. The
correlation between chlorophyll a and b was positive and
strongest among all the parameters (0.8414). Chlorophyll
a and b were negatively correlated with LR and R/S,
whereas chlorophyll b was positively associated with RD
and SR. Leaf rolling showed negative correlation with all
the parameters. R/S showed positive association with RD
and SR (Table-4).
Under inoculated environment, AA positively
and non-significantly correlated with all parameters
except -C and LR. -C showed negative association
with all parameters except leaf rolling (Table-4).
Chlorophyll a exhibited non-significant and negative
association with SR and LR. Chlorophyll b positively
correlated with R/S and SR while negatively correlated
with RD. LR showed negative correlation with all
parameters except -C. R/S exhibited negative correlation
with SR, -C and LR but positively associated with all
the parameters. RD had negative association with R/S, C, chlorophyll b and LR but positive with rest of the
parameters.

RESULTS
Analysis of variance (ANOVA) presented
highly significant differences among genotypes and
treatments for all the traits (Table-1). Under normal
condition there was slight or no leaf rolling in all
genotypes except 60101 and 6028 which showed high
level of leaf rolling. However, under stress condition, a
range of leaf rolling from 1 to 5 was observed. Genotypes
PB2000, 5006, 6255, 4046, PB2008, B3008, 1159, 20091, 6011, 6028, 7027, BRC236, 5028, 7056-1, 6010, 6003,
1217, 3013, 4028 6017, 7010, and 3019 were ranked 5
on the basis of leaf rolling strength. Genotypes 7059,
4004, 6001, 7046, 1288 and 1143 showed from no to
very slight leaf rolling. Analysis exhibited that genotypes
with high level of leaf rolling showed very low survival
rate i.e. upto 10%, whereas, genotypes with little or no
leaf rolling showed high survival rate upto 50% (data not
shown).
Under normal condition out of eight, four PCs
had more than one eigen-value and collectively
contributed 71.50% of the total variability (Table-3).
These four PCs were given due consideration for further
interpretation. PC1, PC2, PC3 and PC4 contributed
29.6%, 15.4%, 14.0% and 12.5% of the total variability
respectively among the characters under study (Table-3).
The PC1 showed that all the traits contributed positively
towards variability (29.6%) except leaf rolling (Table-3).
However in PC2 leaf rolling, chlorophyll contents (a & b)
and beta carotenoids contributed positively while,
survival rate, ascorbic acid, root shoot ratio and root
density contributed negatively (Table-3). Ascorbic acid,
beta carotenoids and root density reflected positive and
increasing effects while rest of the traits showed negative
and decreasing effects in PC3. According to results of
PC4, leaf rolling, survival rate, ascorbic acid, chlorophyll
a and beta carotenoids were decreasing and contributed
negatively whereas chlorophyll b, root shoot ratio and
root density were increasing and contributed positively
(Table-3).
Under inoculated conditions, out of eight, four
PCs had more than one eigen value and cumulatively
contributed 75.2% of the total variability. PC1
contributed 27.7% of the total variability while
contributions of PC2, PC3 and PC4 were 19%, 16.1%
and 12.4%, respectively for all parameters under study.
Results of PC1 showed that leaf rolling was not
increasing positively whereas all other parameters were
positively increasing. In PC2 the contribution of survival
rate, ascorbic acid contents and beta carotenoids was
positive towards variability and rest of the traits
contributed negatively. In case of PC3, the positive
contribution was only of survival rate, ascorbic acid
contents, root shoot ratio and root density. However in
case of PC4 leaf rolling, ascorbic acid and chlorophyll b

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J. Anim. Plant Sci. 23(6):2013

Table-1. Analysis of variance for various chickpea genotypes under stress conditions
Source

DF

LR

SR

A.A
(gm/ml)
318.055**
7.03929**

Ch. a
(mg/100ml)
57.1301**
1.38297**

Treatment(T) 1
432.086**
112374**
Genotype
69
3.29317**
1169.72**
(G)
T*G
69
3.86832**
1090.96**
7.93955**
1.30291**
Error
280 0.00082
0.00124
0.00727
0.01306
Total
419
Where *= Significant, **= Highly Significant and NS= non-significant

Ch. b
(mg/100ml)
91.6394**
2.46396**

-C
(mg/100ml)
92.3752**
129.353**

R/S

RD

3.20723**
0.70156**

1.64062**
0.13129**

1.93889**
0.000222

126.214**
0.000926

0.76956**
0.00486

0.11056**
0.00144

0.7410,
0.6290
0.093,
0.079
0.913,
0.922

0.5925,
0.3472
0.074,
0.043
0.987,
0.966

0.1017,
0.2741
0.013,
0.034
1.000,
1.000

PC7
0.628,
-0.632
0.644 ,
-0.534
0.124,
0.008
0.020,
0.158
-0.014,
-0.452
-0.106,
-0.055
-0.302,
-0.002
0.269,
-0.289

PC8
-0.130,
0.366
-0.004,
0.274
-0.034,
0.157
0.655,
0.678
-0.710,
-0.535
-0.190,
-0.041
-0.062,
0.104
0.099,
-0.087

Table-3. PCA under normal and stress conditions:

Eigen-analysis of the Correlation Matrix
Eigenvalue
Proportion
Cumulative

2.3694,
2.2141
0.296,
0.277
0.296,
0.277

1.2344,
1.5221
0.154,
0.190
0.450,
0.467

1.1161,
1.2873
0.140,
0.161
0.590,
0.628

1.0070,
1.0037
0.125,
0.124
0.715,
0.752

0.8478,
0.7326
0.106,
0.092
0.821,
0.844

Note: Bold values represent normal treatment and non-bold values represent data of inoculated set.

Variable
L.R
S.R
(%age)
A.A
(gm/ml)
Ch. a
(mg/100ml)
Ch. a
(mg/100ml)
-C
(mg/100ml)
R/S
R.D.

PC1
-0.434,
-0.549
0.365,
0.346
0.089,
0.323
0.556,
0.457
0.577,
0.493
0.103,
-0.072
0.008,
0.118
0.137,
0.063

PC2
0.179,
-0.131
-0.355,
0.498
-0.510,
0.219
0.227,
-0.293
0.222,
-0.159
0.116,
0.120
-0.681,
-0.501
-0.060,
-0.557

PC3
-0.056,
-0.201
-0.237,
0.267
0.444,
0.399
-0.052,
-0.448
-0.143,
-0.426
0.651,
0.104
-0.221,
0.424
0.498,
0.397

PC4
-0.081,
0.114
-0.273,
-0.033
-0.103,
0.061
-0.116,
-0.072
0.163,
0.074
-0.561,
-0.970
0.051,
-0.073
0.742,
-0.158

PC5
-0.175,
-0.246
-0.133,
0.438
0.642,
-0.793
-0.060,
-0.017
0.066 ,
-0.117
-0.435,
-0.106
-0.504,
0.288
-0.298,
-0.102

PC6
-0.572,
-0.184
0.423,
0.092
-0.309,
-0.177
-0.437,
0.121
-0.250,
-0.202
0.034,
-0.113
-0.368 ,
-0.676
0.087,
0.634

Fig-1: Principle Component Biplot graph of seventy genotypes under normal environment.

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Based on the results of leaf rolling scale and

biplot analysis it was concluded that genotypes 7059,
4004, 6001, 7046, 1288 and 1143 had tolerance against
fusarium wilt whereas, PB2000, 5006, 6255, 4046,

PB2008, B3008, 1159, 2009-1, 6011, 6028, 7027,

BRC236, 5028, 7056-1, 6010, 6003, 1217, 3013, 4028
6017, 7010, and 3019 proved as susceptible among all
studied chickpea genotypes.

Fig-2: Principle Component Biplot graph of seventy genotypes under stress environment.
Table-4. Correlation coefficients among different studied parameters under normal and stress environments.
C
Chl. A
Chl. B
L.R
R/S
R.D
S.R

0.0769ns,
-0.0508**
0.0271ns,
0.0207**
-0.0112ns,
0.1520**
-0.1413*,
-0.3563**
0.1041ns,
0.0424ns
0.0753ns,
0.0380*
0.0887ns,
0.2939ns
A.A

0.1931**,
-0.0148**
-0.0377ns,
-0.0835ns
-0.0625ns,
0.0199ns
-0.0878ns,
-0.0718ns
0.0647ns,
-0.0425ns
0.0383ns,
-0.0017**
-C

0.8414**,
0.6710ns
-0.3152**,
-0.3661*
-0.0364ns,
0.0681ns
0.0451ns,
0.1130ns
0.3032**,
-0.0010ns
Chl. a

-0.4475**,
-0.3589**
-0.0855**,
0.0585ns
0.1697ns,
-0.0390ns
0.3036**,
0.1026ns
Chl. B

-0.0297*,
-0.1242ns
-0.1393ns,
-0.0867ns
-0.3362**,
-0.5377ns
L. R

0.0223ns,
0.3760ns
0.1759ns,
-0.0801ns
R/ S

-0.0255**,
-0.1810**
R. D

Note: Bold values represent correlation under normal condition while non-bold values represent data under stress condition.

assessment of tolerance against abiotic stress in barley

genotypes.
Correlation coefficient helps the researcher to
set different standards for selection and use best of them.
Farshadfar and Farshadfar (2008) analyzed the data of
chickpea by using correlation coefficient analysis.
Results showed that inoculum application
favored the disease proliferation and enabled us to study
the differential responses of the genotypes under
prevalence of fusarium wilt. Environmental conditions
and concentration of inoculum was same for all
genotypes so, different responses were due to differences
in their genetic makeup. Evaluation for leaf rolling based
on devised scale; revealed that great variation was present

DISCUSSION
Multivariate analysis such as clustering,
metroglyph and principle component analysis (PCA) are
used to determine the genetic variability for various traits.
Many researchers evaluated chickpea germplasm by
following PCA to search out resistance against different
types of abiotic stresses. Hasan et al. (2007) evaluated 11
chickpea genotypes to find suitable genotypes for Isparta,
Turkey local climatic conditions using principle
component analysis. Naseer et al. (2011) assessed the
genetic diversity among the Iranian north-western
chickpea genotypes with the help of RAPD marker.
Nazari and Pakniyat (2010) used biplot analyses for the

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in chickpea germplasm for leaf rolling. These findings

are also in agreement with previous findings which
declared leaf drooping as primary indicator for disease
prevalence (Haware, and Nene, 1982; Jimnez-Daz et
al., 1993; Navas-Cortes et al., 2000). Leaf rolling results
in reduced leaf surface area exposed to sunlight and
impaired photosynthetic activity. Leaf rolling is the result
of closure of stomata due to loss of turgor which
ultimately affect gaseous exchange.
Variation for survival rate was studied on
percentage basis. Higher survival rate was corroborated
with lower mortality and lower survival rate with higher
mortality. Mortality effects have also been revealed by
previous experiments and they remarked that drooping
and chlorosis lead towards plant mortality (Haware, and
Nene, 1982; Jimnez-Daz et al., 1993; Navas-Cortes et
al., 2000).
Chlorophyll contents showed variability among
genotypes under fusarium prevalence. Tolerant genotypes
were able to retain the higher chlorophyll and betacarotenoid contents than susceptible genotypes. Reason
for higher chlorophyll and beta-carotenoid contents might
be due to strong defense mechanism of intended
genotypes. It was previously reported that chlorophyll
and beta-carotenoid contents were reduced by Fusarium
oxysporum in Pea plant (Siddiqui et al, 1999). Reduced
chlorophyll contents are responsible for chlorosis and
impaired photosynthetic activity followed by yield
reduction.
Root vascular tissues were adversely affected by
Fusarium oxysporum up to blockage (Harveson, 2011),
so reduced water uptake followed by loss of leaf turgor
and increased leaf rolling. Leaf death and even death of
the whole plant might be due to sever leaf rolling (Singh
et al. 2007). It was reported that resistance against
fusarium wilt was conferred by recessive gene and to get
complete resistance, susceptible parents are needed to be
used in breeding program (Kumar and Haware, 1982). It
can be inferred from this statement that resistant
genotypes in present studies are homozygous recessive
for that particular locus.
Interaction between plant and pathogen results
in the regulation of expression of genes related to either
defense or pathogenicity. Relationship of these genes is
responsible for either development of disease or
resistance in plants. Defense mechanisms are backboned
by array of genes which confer resistance either in
oligogenic or polygenic form (Giri et al, 1998; Gurjar et
al, 2012). In present study it was observed that there were
differential responses of chickpea genotypes for fusarium
wilt. Differential tolerance responses of chickpea
genotypes might be due to differences in their defense
mechanisms. It was reported that proteases, glucanases
and chitinases were involved in defense of chickpea
against fusarium oxysporum. It can be perceived that
tolerant genotypes of present study are bestowed with

these enzymatic defenders whereas; susceptible

genotypes are lacking these enzymes. There are also
several genes for causing pathogenicity which are
regulated by certain regulators and have host specificity
(Gurjar et al, 2012).
Conclusion: Leaf rolling, survival rate, chlorophyll and
carotenoid contents, and root traits are suitable for
selection of resistant genotypes against fusarium wilt.
Pathogen effects reflected through all the studied traits of
chickpea and genotypic responses were different which
depicted the different liabilities of defense mechanisms.
Genotypes 7059, 4004, 6001, 7046, 1288 and 1143
proved resistant against fusarium wilt whereas, PB2000,
5006, 6255, 4046, PB2008, B3008, 1159, 2009-1, 6011,
6028, 7027, BRC236, 5028, 7056-1, 6010, 6003, 1217,
3013, 4028 6017, 7010, and 3019 proved as susceptible
among all the chickpea genotypes. Resistant genotypes
could be grown as such. Susceptible genotypes can be
used as parent in breeding program for development of
resistance because resistance is controlled by recessive
genes.

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