Available via license: CC BY-NC-ND 4.0
Content may be subject to copyright.
© Benaki Phytopathological Institute
Hellenic Plant Protection Journal 11: 9-18, 2018
DOI 10.2478/hppj-2018-0002
Section of Plant Pathology and Nematology, Depart-
ment of Botany, Aligarh Muslim University, Aligarh,
India.
* Corresponding author: asifgc2616@gmail.com
Resistance screening of lentil cultivars against the root-knot
nematode Meloidogyne incognita
T. Ansari, M. Asif* and M.A. Siddiqui
Summary
The root-knot nematode Meloidogyne incognita is a major soil parasite of lentil crops. In-
creasing restrictions of chemical nematicides have triggered a growing attention and interest in alter-
nate root-knot nematode management. The present study was conducted to examine the level of re-
sistance and/or susceptibility of ve lentil cultivars (PL-456, KLS-218, Desi, DPL-62, Malika), grown in
pots, against the root-knot nematode M. incognita. Root-knot nematode reproduction and host dam-
age were assessed by recording the nematode infestation levels and reduction percentage of plant
growth parameters. Nematode response and plant growth di erentiated amongst the lentil cultivars.
None of the cultivars was found immune or highly resistant. The cultivar Malika was found moderate-
ly resistant as it showed the lowest number of galls and egg masses/root as well as the lowest reduc-
tion of plant fresh weight (10.4%) and dry weight (6.9%). On the other hand, the cultivar Desi manifest-
ed the highest susceptibility exhibiting the highest number of galls and egg masses. There was a sig-
ni cantly negative correlation between the number of galls and plant growth parameters (plant fresh
and dry weight and plant height).
Additional keywords: cultivars, lentil, Meloidogyne incognita, resistance, root-knot nematode
Introduction
Lentil (Lens culinaris Medik.) is one of the
most important pulse crops and a major
source of protein (30% weight, second pro-
tein content legume after soybeans) for the
predominant vegetarian population of In-
dia. India ranks second (after Canada) in
lentil production, with lentil cultivation oc-
cupying an area of 1,800,000 hectares and
annual production reaching 1,100,000 met-
ric tonnes of grain. The average yield is
6000kg/ha (FAO, 2014). Lentils are an im-
portant source for the Indian household in-
come.
Meloidogyne spp. cause yield losses in
pulses, which are estimated annually up to
20-35% (Gaur et al., 2001). In India, the aver-
age loss caused by root-knot nematodes on
pulses may be 14.6%, and could go as high
as 50-80% in some crops (Bhatti, 1992).
Root-knot nematodes are di cult to
control because of their short life cycle, high
population densities and reproductive po-
tential (Sikora and Fernandez, 2005). The im-
mense loss caused by root knot nematodes
can be minimized by using various strategies
such as soil treatment with chemicals, bio-
control agents (Vagelas and Gowen, 2012),
cultural practices such as crop rotation, an-
tagonistic plants (Hussain et al., 2011), re-
sistant cultivars (Tariq et al., 2016) and soil
amendments (Asif et al., 2017a, b; Ansari et
al., 2016), which are common methods of
nematode control.
Synthetic nematicides can rapidly re-
duce nematode population. However, their
indiscriminate and consistent use can be
toxic to bene cial soil ora and fauna, and
may induce emergence of resistant plant
parasitic nematodes (Akhtar, 1991). Never-
theless, nematode infestation levels in soil
could be reduced by using resistant cul-
tivars with crop rotation strategy of non-
hosts. According to Oostenbrink (1966), the
cultivation of a resistant cultivar may sup-
press the nematode population by 10-50%
of its harmful density. Susceptibility of dif-
ferent pulse crops has been reported by sev-
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Ansari et al.
10
eral researchers such as Pandey et al. (2016)
and Montasser et al. (2017). Sasser (1954)
found that the roots of resistant plants were
not invaded as rapidly as susceptible ones.
Such variability in tolerance might be relat-
ed to their genetic makeup, coding for a re-
sistance mechanism possessed by the par-
ticular cultivar (Anwar and McKenry, 2007).
All cultivars referred as resistant to root-knot
nematodes have comparatively better crop
yield as compared to susceptible cultivars
(Mukhtar et al., 2014).
The present investigation was carried out
as a resistance screening of ve of the most
commonly grown cultivars of lentil in India
against Meloidogyne incognita (Kofoid and
White) Chitwood under greenhouse condi-
tions with a view to better exploit the use of
most resistant cultivars for the suppression
of root-knot nematodes in integrated man-
agement programmes.
Materials and Methods
Meloidogyne incognita was collected from
naturally infested eggplant (Solanum me-
longena L.) elds near Punjipur village, Ali-
garh (U.P). Meloidogyne incognita was mass
cultured from a single egg mass on a sus-
ceptible variety of tomato, S-22, in a green-
house of the Section of Plant Pathology and
Plant Nematology, Department of Botany,
A.M.U., Aligarh. Second-stage juveniles (J2)
were obtained from hatched eggs by incu-
bating handpicked egg masses in sterile dis-
tilled water at 28 ± 1°C.
Seeds of ve lentil cultivars namely, PL-
456, KLS-218, Desi, DPL-62 and Malika were
obtained from the Indian Institute of Puls-
es Research, Kanpur, India as these are most
commonly grown and chief cultivars con-
cerning with the productivity of lentil in In-
dia. Lentil seeds of all ve cultivars were sur-
face sterilized with 0.1% mercuric chloride
and sown in clay pots of 15cm diameter con-
taining 1kg sterilized sandy loam soil. Four
lentil seeds of each cultivar were sown per
pot, which was considered one replication.
The pots were placed in a greenhouse at a
completely randomized design (CRD). The
experiment had four replications per culti-
var and it was repeated twice in time. Three
weeks after seed germination, thinning was
performed, leaving one plant per pot. Two
days after thinning, approximately 1500 sec-
ond stage juveniles of M. incognita were pi-
petted around each plant by making holes
in soil. A total of eight plants (four inoculat-
ed and four uninoculated) of each cultivar
were used for this experiment. The uninocu-
lated plants served as controls. Ninety days
after inoculation, the plants were uproot-
ed gently from the pots and di erent plant
growth parameters were noted.
Varietal response against M. incognita in-
festation of di erent crops is accessed on
the basis of growth parameters and nema-
tode reproduction parameters (Hayat, 2011).
Hence, in the present study data were re-
corded for plant growth viz., shoot height
and root length, dry and fresh shoot and
root weight, number of pods, number of
nodules per root system, weight of 100
seeds and nematode reproduction parame-
ters like number of egg masses, number of
eggs/root system, root-knot index and nal
nematode population. Physiological param-
eters like chlorophyll content (MacKinney,
1941) and carotenoid content were also esti-
mated. The percent increase and reduction
in the growth parameters over the control
were calculated by using the formula
% reduction or increase =
(
Uninoculated - Inoculated
)
x 100
Uninoculated
(Irshad et al., 2012; Mukhtar et al., 2014).
Analysis of Variance was conducted and
the Duncan’s Multiple Range Test was em-
ployed for the comparison of means be-
tween the cultivars according to Critical
Di erence (C.D.) at P=0.05 level. To detect
relation between the parameters, Pearson
correlation and multiple linear regression
was performed. The data were analysed us-
ing SPSS 12.00 software (SPSS Inc., Chicago,
IL, USA).
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Resistance of lentil cultivars to root-knot nematodes 11
Results
None of the cultivars was found immune ac-
cording to the rating scale of Table 1 based
on number of galls on the root system (Ta-
ble 2). The resistance rating of the cultivars
was: Malika (moderately resistant), KLS-218
(moderately susceptible), PL-456 (moder-
ately susceptible), DPL-62 (susceptible), Desi
(susceptible). The same trend was observed
for the egg masses and the nematode pop-
ulation per root system (Table 2).
The cultivars Malika, KLS-218, PL-456 had
a comparable shoot height before infesta-
tion by M. incognita, which was signi cant-
ly higher than the one of the DPL-62 and
Desi. After infestation by the nematode, Ma-
lika continued to have signi cantly high-
er shoot compared to the other cultivars.
These heights di erentiated in the follow-
ing descending order: KLS-218, PL-456, DPL-
62 and Desi (Table 3).
Prior to the infestation by the nematode,
the root length of the cultivars Malika, KLS-
218, PL-456 was signi cantly higher than the
one of the cultivars DPL-62 and Desi. After
infestation, Malika had the least reduction
in root length as compared to the other cul-
tivars (Table 3).
The cultivar Malika had signi cantly
heavier shoot fresh and dry weight than the
other cultivars both before and after nem-
atode infestation. The cultivars had the fol-
lowing decreasing order in shoot fresh and
dry weights: KLS-218, PL-456, DPL-62 and
Desi. A similar trend was also observed in
Tab l e 1: Rating scale for the assessment of level of resistance of plant cultivars against root-
knot nematodes, based on number of galls (Sasser and Taylor, 1978).
Root knot Index No. of galls/root system Resistance rating
00 Immune
1 1-2 Highly Resistant
2 3-10 Moderately Resistant
3 11-30 Moderately Susceptible
431-100 Susceptible
5>100 Highly Susceptible
Tab l e 2. Reproduction of the root-knot nematode Meloidogyne incognita on ve lentil culti-
vars and resistance rating of the nematode.
Cultivars
No. of
egg masses/
root
No. of eggs/
egg mass
Nematode
population
Number of
galls Reaction
Desi Control - - - - Susceptible
Inoculated 112±0.43a196± 0.4 0a2000±0.42a43±0.84a
DPL-62 Control - - - - Susceptible
Inoculated 89±0.48b154± 0.45b1692±0.32b35±0.76b
PL- 456 Control - - - - Moderately
Susceptible
Inoculated 58±0.72c97±0.46c1590±0.21bc24±0.72c
KLS- 218 Control - - - - Moderately
Susceptible
Inoculated 26±0.88d69±0.68d1440±0.25cd16±0.88 d
Malika Control - - - - Moderately
Resistant
Inoculated 8±1.20e25±1.15e1161± 0 .19 e6±1.00e
Values are mean of eight replicates.
Values in each column followed by the same letters are not signi cantly di erent according to Duncan’s Multiple
Range Test (P ≤ 0.05).
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Tab l e 3. E ect of infestation by the root-knot nematode Meloidogyne incognita on growth parameters of ve lentil cultivars.
Cultivars
Fresh weight
(g)
Dry weight
(g)
Shoot
height
Root
length
Total
plant
height
% Re-
duction
of plant
height
over
control
Shoot Root Total
% Re-
duction
of plant
fresh
weight
over
control
Shoot Root Total
% Reduc-
tion of plant
dry weight
over
control
Desi
Control 21.8±0.48f12 .9±0.74ef 41.7±0.44fg
35.4%
4.8±0.43fg 1.9±0.48ef 6.7±1.02fg
32.8%
1.2 ±0.43fg 0.7±0.47bc 1.9±0.49fg
31.5%
Inoculated 17.5±0.76g9.4±1.08h26.9±0.56j2.9±0.41i1.6±0.42g4.5±1.29h1.0 ±0.48g0.5±0.42cd 1.3 ±0.4 4g
DPL-62
Control 31.8±0.68bc 14.9±0.75cd 46.7±0.57cd
29.7%
6.5±0.28de 2.1±0.45de 8.6 ±0.76ef
29.0%
1.7 ±0. 50ef 0.7±0.68bc 2.4 ±0.30ef
25.0%
Inoculated 21.1±0.74f11.7± 0.81fg 32.8±0.52i3.9±0.37gh 2.2±0.38de 6.1±1.21gh 1.2±0.53fg 0.6±0.32cd 1.8 ±0.48fg
PL- 456
Control 34.3±0.57a16.9±0.98b51.2±0.52ab
22.4%
8.3±0.19bc 2.8±0.39bc 11.1± 0. 67cd
24.3%
2.3 ±0.37cd 1.0±0.38a3.3 ±0.31cd
21.2%
Inoculated 25.4±0.63e14.3±0.97de 39.7±0.43gh 5.8±0.30ef 2.6 ±0.40cd 8.4±1.06ef 1.7±0.50fe 0.9±0.52ab 2.6±0.40ef
KLS- 218
Control 34.9±0.56a18.6±0.61a53.5±0.36a
17.0 %
9.2±0.18b3.1±0.36ab 12 . 3±0. 6 6bc
15.4%
2.6 ±0.43bc 1.1±0.36a3.7±0.24bc
18.9%
Inoculated 28.4±0.60d16.0±0.87bc 44.4±0.49de 7.1±0. 20 cd 2.9±0.39bc 10.4±0.86de 2.1±0.32de 0.9±0.40ab 3.0±0.27de
Malika
Control 32.4±0.75ab 15. 2±0. 86cd 47.6±0.43c
8.4%
11. 8 ± 0.63a3.6±0.31a14.4±0.61a
10.4%
3.1±0.36a1.2±0. 27a4.3 ±0.22a
6.9%
Inoculated 31.8±0.74bc 11.8±0.82fg 43.6±0.54ef 9.5±0.21b3.4±0.27ab 12.9±0 .77ab 2.9±0.35ab 1.1±0.29a4.0±0.20ab
Values are mean of eight replicates.
Values in each column followed by the same letters are not signi cantly di erent according to Duncan’s Multiple Range Test (P ≤ 0.05).
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Resistance of lentil cultivars to root-knot nematodes 13
the root fresh and dry weight (Table 3).
When the higher number of nodules/
root system was compared between culti-
vars, Malika had signi cantly higher number
of nodules/root system. Inoculation of M. in-
cognita caused reduction in nodulation in
all lentil cultivars. Malika continued to have
signi cantly the highest number of nodules
after nematode inoculation while Desi had
the least number of nodules compared to
the other cultivars (Table 4).
Yield parameters in terms of number of
pods/plant and weight of seeds showed sig-
ni cant reductions after inoculation with
nematodes in all lentil cultivars when com-
pared to their respective controls. Among
all cultivars, Malika had signi cantly more
pods/plant and higher weight of seeds fol-
lowed by KLS-218, PL-456, DPL-62 and Desi
(Table 4).
Before infestation by M. incognita the
cultivars Malika and KLS-218 had compa-
rable chlorophyll and carotenoid content,
which was signi cantly higher than PL-456,
DPL-62 and Desi. Chlorophyll and carote-
noid content of leaves was signi cantly re-
duced by nematode infestation in all lentil
cultivars (Table 4).
Regression
analysis showed a signi cant
positive relation between the number of galls
and reduction in plant fresh weight (R
2
=0.974)
(Fig. 1a), plant dry weight (R
2
=0.930) (Fig. 1b),
plant height (R
2
=0.997) (Fig. 1c), number of
pods/plant (R
2
=0.988) (Fig. 1d), number of
nodules/root system (R
2
=0.918) (Fig. 1e).
Pearson correlation coe cients (r) in-
dicate a signi cantly negative relation be-
tween nematode infestation parameters
and all the plant growth parameters (Table
5): Total plant length (r= -0.948, P=0.05), To-
tal plant fresh weight (r= -0.999, P=0.01), To-
tal plant dry weight (r= -0.995, P=0.01), No.
of pods (r= -0.961, P=0.01), No. of nodules/
root system (r= -0.974, P=0.01), Chlorophyll
content (r= -0.964, P=0.01), Carotenoid con-
tent (r= -0.895, P=0.05). Correlation between
weight of seeds and nematode infestation
in terms of eggs, eggs/egg masses, nema-
tode population and galls had a negative re-
lation, but not signi cant.
Discussion
M. incognita failed to reproduce and multi-
ply on the cultivar Malika and exhibited the
lowest reduction in growth, responding as
moderately resistant against M. incognita
infestation. The cultivar Desi was the most
susceptible to the root-knot nematodes.
The cultivars KLS-218 and PL-456 showed a
moderately susceptible response in terms
of reproduction and an intermediate reduc-
tion in growth parameters, which was less
severe than that observed for the suscepti-
ble cultivar. The cultivars PL-456 and DPL-62
were found moderately susceptible and sus-
ceptible, respectively, but showed less se-
vere damage by the nematode as compared
to the most susceptible cultivar.
Most of the plant growth characters of
the lentil cultivars were signi cantly nega-
tive correlated with the number of galls of
M. incognita. Moreover it can be suggest-
ed that eggs, eggs/egg masses and nema-
tode population also had a direct e ect on
the reduction of plant growth. Meloidogyne
spp. induces galling in the roots and giant
cells formation in the stellar region, which
destroys the xylem tissues and ultimately
reduces the absorption and movement of
water and nutrients (Abad et al., 2003). This
limitation of nutrient elements in the plant
is probably the rst e ect that the nema-
tode infestation has on the physiology and
metabolism of its host (Lu et al., 2014). These
e ects increase with the duration of infesta-
tion (Melakeberhan et al., 1987).
A reduction in total chlorophyll, as in the
case of our experiment, has also been re-
ported in French bean and rice infested by
M. javanica (Melakeberhan et al., 1986; Swain
and Prasad, 1988). Reduction in chlorophyll
content has also been reported to lead to
the disturbance of nodule function (Chahal
et al., 1983).
In conclusion, the current study demon-
strated that ve of the most broadly cultivat-
ed lentil cultivars in India are susceptible to
moderately susceptible to M. incognita with
the exception of the cultivar Malika, which
was found moderately resistant. The culti-
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Tab l e 4. E ect of infestation by the root-knot nematode Meloidogyne incognita on yield and physiological parameters of ve lentil cultivars.
Cultivars No. of pods per plant No. of nodules per
root system
Weight of 100 seeds
(g)
Chlorophyll content
(mg/g)
Carotenoid content
(mg/g)
Desi Control 28±0.88g22±0.75h 1.2±0.20de 1.86±0.041ef 0.800±0.005cd
Inoculated 16±0.93h13±0.9 6i0.9±0.19ef 1.31±0.023g0.624±0.004i
DPL-62 Control 59±0.73d34±0.80f1.4±0.14de 2.57±0.022ab 0.842±0.005ab
Inoculated 40±0.72f23±0.98h1.0±0.28ef 1.85±0.026ef 0.719±0.009g
PL- 456 Control 53±0.64de 42±0.72e1.8±0.21c2.42±0.017bc 0.791±0.004ef
Inoculated 40±0.73f29±0.87g1.4±0.15de 1.96±0.025e0.691±0.006h
KLS- 218 Control 74±0.54c68±0.56ab 1.6±0.14cd 2.61±0.016ab 0.860±0.007a
Inoculated 60±0.71d52±0.50d1.3±0.09de 2.14±0.025d0.796±0.005de
Malika Control 92±0.48a72±0.54a3.4±0.11a2.78±0.018a0.820±0.006bc
Inoculated 83±0.51b65±0.57bc 3.1±0.11b2.56±0.022ab 0.801±0.006cd
Values are mean of eight replicates.
Values in each column followed by the same letters are not signi cantly di erent according to Duncan’s Multiple Range Test (P ≤ 0.05).
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Resistance of lentil cultivars to root-knot nematodes 15
Fig.1. Relationship between number of galls by the root-knot
nematode Meloidogyne incognita and growth parameters of
v e l e n t i l c u l t i v a r s .
y = 0,6256x + 6,8648
R² = 0,974
0
5
10
15
20
25
30
35
40
45
50
0 5 10 15 20 25 30 35 40 45 50
(a)
Number of galls
% reduction in fresh weight
y = 0,5945x + 5,9568
R² = 0,9309
0
5
10
15
20
25
30
35
40
45
50
0 5 10 15 20 25 30 35 40 45 50
(b)
Number of galls
% reduction in dry weight
y = 0,7173x + 4,7903
R² = 0,9972
0
5
10
15
20
25
30
35
40
45
50
0 5 10 15 20 25 30 35 40 45 50
(c)
Number of galls
% reduction in plant height
y = 0.8464x + 4.5693
R² = 0.988
0
5
10
15
20
25
30
35
40
45
50
0 5 10 15 20 25 30 35 40 45 50
(d)
Number of galls
% reduction in no. of pods
y = 0,7614x + 8,5779
R² = 0,9186
0
5
10
15
20
25
30
35
40
45
50
0 5 10 15 20 25 30 35 40 45 50
(e)
Number of galls
% reduction in no. of nodules
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Tab l e 5. Matrix of Pearson’s correlation coe cients between plant growth parameters and nematode infestation variables of lentil cultivars.
Variables TTL TTF TTD NPD NOD WTS CHL CAR EGMS EGS NMP GALLS
TTL 1
TTF .800** 1
TTD .770** .996** 1
NPD .713*.951** .943** 1
NOD .738*.968** .964** .958** 1
WTS .456 .847** .860** .841** .793** 1
CHL .876** .902** .880** .926** .856** .728*1
CAR .889** .704*.659*.729*.703*.442ns .862** 1
EGMS -.966** -.993** -.981** -.952*-.977** -.789ns -.950*-.914*1
EGS -.960** -.993** -.991** -.950*-.958*-.822ns -.966** -.884*.992** 1
NMP -.914*-.979** -.980** -.989** -.961** -.856ns -.997** -.922*.968** .978** 1
GALLS -.948*-.999** -.995** -.961** -.974** -.839ns -.964** -.895*.995** .998** .980** 1
**. Correlation is signi cant at the 0.01 level (2-tailed).
*. Correlation is signi cant at the 0.05 level (2-tailed)
ns: correlation is not signi cant..
TTL=Total Plant Length, T TF=Total Plant Fresh Weight , TTD=Total Plant Dry Wei ght, NPD=No. of Pods , NOD=No. of No dules/Root sys tem, WTS=Weight of 100 Seeds, CHL=Chlorophyll
Content, CAR=Carotenoid Content, EGMS=No. of Eggmasses/Root, EGS=No. of Eggs/Eggmass, NMP=Nematode population, GALLS=Number of Galls
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Resistance of lentil cultivars to root-knot nematodes 17
vars KLS-218 and PL-456 were moderately
susceptible whereas DPL-62 and Desi were
susceptible. There was an intense reduction
of the plant growth parameters in suscepti-
ble cultivars as compared to less susceptible
ones. Growing of the moderately resistant
cultivar Malika in severely infested elds
with M. incognita may assist to minimize
root-knot nematode multiplication. Further
studies are necessary in search of possibly
higher resistance levels to root-knot nema-
todes in other commercially available lentil
cultivars and the development of resistant
cultivars.
The authors are grateful for nancial support
from the University Grant Commission, New
Delhi (UGC-Non NET) and the chairman, De-
partment of Botany for providing necessary
assistance.
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Received: 1 November 2017; Accepted: 2 January 2018
Διερεύνηση ανθεκτικότητας ποικιλιών φακής κατά του
κομβονηματώδη Meloidogyne incognita
T. Ansari, M. Asif και M.A. Siddiqui
Περίληψη
Ο κομβονηματώδης Meloidogyne incognita είναι ένα σημαντικό παράσιτο εδάφους για την
καλλιέργεια της φακής. Οι αυξανόμενοι περιορισμοί των συνθετικών νηματωδοκτόνων έχουν αυξήσει
την προσοχή και το ενδιαφέρον για εναλλακτικά μέσα διαχείρισης των κομβονηματωδών. Στην παρού-
σα μελέτη εξετάστηκε το επίπεδο αντοχής και / ή ευαισθησίας πέντε ποικιλιών φακής (PL-456, KLS-218,
Desi, DPL-62, Malika), σε φυτά σε γλάστρες, έναντι του κομβονηματώδη M. incognita. Η αναπαραγω-
γή του κομβονηματώδη και η ζημιά στον ξενιστή αξιολογήθηκαν με βάση τα επίπεδα προσβολής από
το νηματώδη και το ποσοστό μείωσης διαφόρων παραμέτρων ανάπτυξης των φυτών. Η απόκριση των
νηματωδών και η ανάπτυξη των φυτών διαφοροποιήθηκαν μεταξύ των ποικιλιών φακής που μελετή-
θηκαν. Καμία από τις ποικιλίες δεν βρέθηκε απρόσβλητη ή πολύ ανθεκτική. Η ποικιλία Malika βρέθηκε
μέτρια ανθεκτική, καθώς παρουσίασε το μικρότερο αριθμό όγκων και ωόσακων/ρίζα και τη χαμηλότε-
ρη μείωση του νωπού (10,4%) και του ξηρού (6,9%) βάρους των φυτών. Η ποικιλία Desi παρουσίασε τη
μεγαλύτερη ευαισθησία, με το μεγαλύτερο αριθμό όγκων και ωόσακων. Διαπιστώθηκε σημαντικά αρ-
νητική συσχέτιση μεταξύ του αριθμού των όγκων και των παραμέτρων ανάπτυξης των φυτών (νωπό
και ξηρό βάρος φυτού και ύψος φυτού).
Hellenic Plant Protection Journal 11: 9-18, 2018
Unauthenticated
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