1. health and fitness
2. disease

International Journal of Farming and Allied Sciences
Available online at www.ijfas.com
©2015 IJFAS Journal-2015-4-3/207-214/ 31 March, 2015
ISSN 2322-4134 ©2015 IJFAS
Barley Yellow Dwarf occurrence and resistance
stability in wheat varieties of Pakistan
Muhammad Ibrahim* and Syed Jawad Ahmad Shah
Nuclear Institute for Food and Agriculture (NIFA), Tarnab, Peshawar
Corresponding author: Muhammad Ibrahim
ABSTRACT: Barley Yellow Dwarf Virus (BYDV) occurrence and resistance stability were studied in a set
of 17 varieties along with a susceptible control (Fakhr-e- Sarhad) over four years (2005-08) at Peshawar,
Pakistan. Consistent and uniform BYDV symptoms were observed over study years. Enzyme Linked
Immunosorbent Assay (ELISA) of 2008 experiment indicated the presence of BYDV-PAV. Phenotypic
assessments with regard to incidence (infected tillers/plot) and percent BYDV severity varied among
varieties. Maximum incidence (120) and severity (80%) was recorded during 2006 cropping cycle. BYDV
incidence and severity was positively correlated (r = 0.935) over four years. Varieties and years remained
significantly different while variety-year interaction was non-significant (P<0.05). Cvs.Punjab-96, Suleman96, Bakhtawar-93, Faisalabad-83 and Bahawalpur-95 displayed stability in severity levels and also
expressed a phenotypic marker of Leaf Tip Necrosis (LTN) more frequently over four year
experimentations which is linked with BYDV tolerance gene (Bdv1). Comparatively stable and tolerant
varieties identified through level of BYDV infection could be improved further by incorporating Bdv2 and
Bdv3 genes to manage this serious problem in Khyber Pakhtunkhwa province of Pakistan.
Keywords: Barley, stability, wheat, Pakistan
INTRODUCTION
Barley Yellow Dwarf (BYDV) is an economically important viral disease of cereals in the world (Singh., 1993).
Occurrence of BYDV in developing countries is well documented (Lister and Ranieri., 1995). In Pakistan, BYDV like
symptoms were known since 1964 in the border areas of Pakistan and Afghanistan where it was confirmed for the
first time in the country during 1987 (Aslam and Ahmad., 1987). Prevalence of BYDV symptoms with varying level of
chlorosis on commercial wheat varieties were recorded (Ibrahim , 2009, unpublished data) and is presented in Fig.1.
BYDV has gradually attained an important position among wheat diseases (Khalid., 1999) and reported from Khyber
Pakhtonkhaw Province of Pakistan (Bashir., 1997; Siddiqui., 2011) and Northern Punjab (Bashir., 1997). BYD losses
in wheat ranged from 20 to 30% (Pike, 1990) while in severe epidemic conditions, reduction in yield could reach up
to 86% (Gill., 1980). BYDVs are members of the Luteoviridae family of plant viruses, including BYDV-PAV, BYDVMAV, BYDV-RMV, BYDV-PAS, BYDV-GPV and BYDV-SGV and Cereal yellow dwarf virus (CYDV)-RPV and CYDVRPS. BYDVs and CYDVs are phloem limited and persistently transmitted by at least 25 aphid species (Halbert and
Voegtlin., 1995). Previously five BYDV strains i.e. PAV, MAV, RPV, RMV and SGV (Bashir., 1997) which are now
known as independent viruses (D’Arcy and Domier., 2005) are reported from the region alongwith their aphid vectors
(Anonymous., 1998; Khan., 2006).
Intl J Farm & Alli Sci. Vol., 4 (3): 207-214, 2015
Figure 1. Locations in Khyber Pakhtonkhaw where BYDV symptoms occur regularly under natural conditions
High level of BYDV resistance is not available in wheat while tolerance which is known since 1950s (Burnett.,
1995) is still one of the most promising mode of plant protection to limit yield losses in developing countries (Ginkel
and Henry., 2002). Almost all Pakistani wheat cultivars grown in Northern Punjab and KPK were susceptible to BYDV
(Khalid., 1999). Adult plant leaf tip necrosis could be used as a phenotypic marker for the presence of Bdv1 gene
(Singh., 1993) responsible for BYDV tolerant in wheat. In characterizing BYDV tolerance, environmental conditions
and infection level are important to be considered (Comeau and Jedlinski., 1990) because a cultivar which is
considered to be tolerant in one environment may be less tolerant in an other environment, thus complicating
selection for tolerance. Singh and Chaudhary (1977) reported that performance stability is one of the most desirable
traits of a genotype to be released as variety for general cultivation.
Keeping in view the national importance of BYDV, varietal screening efforts for the identification of BYD tolerant
wheat varieties through phenotypic marker with low symptoms severity, disease identification through DAS-ELISA
and stability across different growing seasons was carried out and findings are reported here.
MATERIALS AND METHODS
Site selection and experimental detail
Nuclear Institute for Food and Agriculture (NIFA), Peshawar was selected due to its unique geographical position
(34° 0'N, 71°42'E, elevation: 304 m), soil fertility, irrigated conditions and BYD hotspot where it occur regularly in the
region (Aslam and Ahmad., 1987; Bashir., 1997; Siddiqui., 2011). Seventeen commercial wheat varieties along with
a susceptible check Fakhr e Sarhad (Table 3) were evaluated over a period of four years in a Randomized Complete
Block Design (RCB) with three replications where experimental unit consisted of 3.6 m 2 plot having 4 rows each 3 m
length with row to row distance of 30 cm.
Disease Assessment and leaf tip necrosis
Scoring of BYD incidence (number of infected tillers/plot) and severity (percentage of foliage with symptoms)
was carried out according to 0-9 scale as described by Singh., (1993) in early March each year due to the expression
of BYD symptoms and peak activity period of its vectors (i.e. Rhopalosiphum & Sitobion spp) in the area (Anonymous,
1997-98; Ibrahim., 2006) with the help of pictorial guide for identification of field wheat diseases and pests (Prescott.,
1986). Presence or absence of leaf tip necrosis (LTN) on flag leaf of each variety was recorded over four years (200508)/12 replications as mentioned by (Shah., 2010; Shah., 2011).
ELISA Analysis
Double Antibody Sandwich-Enzyme Linked Immunosorbent Assay (DAS-ELISA) was used as described by Clark
and Adams (1977), with little modifications in the incubation times, antibody concentration, and sample dilution. The
volume of sample and incubating solutions used was 100 μl in all steps, as described by Ayala., (2001). Polystyrene
microtiter plates were incubated at 37°C for 3 h with a coating of polyclonal antibodies (1 ng/μl) directed against BYDPAV (provided by Agdia Inc.). Plant sap (1:10, in 0.1 M phosphate buffer pH 7.0) was incubated for 3 h at 37°C.
Controls used consisted of phosphate buffer (blank) and infected PAV plant extract (leaf material containing BYDVPAV serotype from Agdia Inc.). Alkaline phosphatase-labeled antibodies (1:1000), anti-PAV, were incubated
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overnight at 4°C; P-nitrophenyl phosphate substrate (Sigma) was then added. Assay was by visual observation of
the yellow nitrophenolate, based on a “plus” and “minus” classification (Fargette., 1982).
Statistical Analysis
Symptoms severity data of BYD was analyzed using Analysis of Variance (ANOVA) as reported by Steel and
Torrie (1960). Means were separated for comparison through LSD test by following the method of Steel and Torrie
(1980) in MSTATC software (Michigan state University, 1991). Stability parameters were worked out as suggested
by Eberhart and Russel (1966) using SPSS. Percent BYD severity was expressed through Box plots (Tukey., 1990)
for % BYD foliage disease severity were also produced through SPSS for an overall descriptive presentation of the
data.
RESULTS AND DISCUSSION
BYDV Occurrence and leaf tip necrosis
BYDV occurrence varied over seasons in the tested varieties. Disease pressure as assessed by infected
tillers/plot of susceptible check (Fig.3) and %severity of commercial varieties (Fig.4) were highest in 2006 which were
followed by 2007, 2008 and 2005, respectively. Several factors involving virus, vectors, host and environment (Ginkel
and Henry., 2002; Harrington., 2002; Hoffman and Kolb., 1998) may have contributed to this observed variation.
Highest incidence (120) was recorded on susceptible check during 2006, followed by 2007 (55), 2008 (35), and 2005
(07). Mean number of infected tillers/plot were highest (i.e.38) during 2006 which was followed by 23, 06 and 02 in
2007, 2008 and 2005 respectively (Fig. 2). Similarly, symptoms severity varied in different seasons where the data
distribution was not normal (Fig. 4). Maximum variability in BYDV severity was observed in 2008 which was followed
by 2006, 2007, and 2005 respectively (Fig 4). BYDV severity was normally distributed in 2007 while in each 2005
and 2006 it was positively skewed whereas in 2008 it was negatively skewed. Highest median value of 35 was
followed by 30, 18 and 04 in 2006, 2007, 2008 and 2005 seasons, respectively. This fluctuation in BYD severity
could be attributed to (i) high mean temperature in the months of January to April (Table 2) during season 2006
(16.81°C) as compare to 2007 (15.81°C), 2008 (14.83°C) and 2005 (14.56°C) in the peak activity period of aphid
vectors resulted in BYDV spread through vectors in the region (ii) low mean precipitation (121 mm) coupled with low
% relative humidity (%56.88) during peak aphid vector movement and BYDV transmission activity in 2006 enhanced
disease development followed by 2007, 2008, and least during 2005 with precipitation ranged from 194.8 to 285.9
mm and % relative humidity up to 64.8%. (iii) high frequencies (50) of temperature range i.e. 16-25°C during 2006
peak disease activity period enhanced BYD symptoms expression compared to 2007, 2008, and 2005 with frequency
ranged from 16 to 33. Environmental factors are reported to contribute in the aphid movement and BYDV
transmission (Smyrnioudis., 2001; Smyrnioudis., 2000). Cooler temperature (15 to 18°C) is reported to favor
symptoms expression and attract vectors to disease plants (D’ Arcy and Domier., 2000). Drought/low rainfall with is
reported to increase aphid vector movement and BYDV spread among host plants (Bailey., 1995). High temperature
(30°C) is reported to increase transmission abilities of inefficient vectors (D’ Arcy and Domier., 2000). The uneven
distribution of viruliferous aphid vectors and spreading virus from infection foci under natural field conditions might
have caused variation in BYDV incidence and severity level among wheat varieties both within and between seasons.
Such complications that a wheat variety appeared tolerant to BYDV in one season showed less tolerance in an other
season or environment was also reported by researchers (Comeau and Jedlinski., 1990).
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Table 2. Weather data recorded during 2005-08 wheat growing seasons
Month
s
Weather Data 2005
Mean
Tem
p.
(°C)
Mean
%
Relativ
e
Humidit
y
Jan
9.1
73.55
Feb
9.7
75.2
March 16.95 66.55
April
22.5
43.9
Mean
14.56
64.8
50.46
Total 194.8
Total
Precipitati
on
(mm)
Weather Data 2006
Weather Data 2007
Weather Data 2008
Mean
Tem
p.
(°C)
Mean
Tem
p.
(°C)
Mean
Tem
p.
(°C)
Mean
%
Relativ
e
Humidit
y
64.4
9.95
68.4
109.9
16.4
58.2
97.1
17.6
59.02
14.5
23.3
41.9
Total 285.9 Mean 16.81
Total
Precipitati
on
(mm)
56.4
15.2
32.4
17
56.88
Mean
Total
%
Precipitati
Relativ
on
e
(mm)
Humidit
y
10.3
57.35
0
12.25 69.75
177
15.9
62.65
82.4
24.8
45.7
20.4
Total 121 Mean 15.81
58.86
Mean
Total
%
Precipitati
Relativ
on
e
(mm)
Humidit
y
7.65
54.7
57.2
10.75 51.8
21.2
19.6
47.25
03
21.35 48.1
113.4
Total 279.8
Mean 14.83
Figure 2. Mean BYD incidence on Commercial Varieties during 2005-08
Figure 3. Mean BYD incidence on commercial wheat varieties during 2005-2008
Figure 4. Box plot depicting BYD % severity on commercial varieties during 2005-08 at NIFA, Peshawar, Pakistan
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Varieties were classified on the bases of LTN occurrence into three groups (Table 3). Group 1 varieties
possessed LTN symptoms which were less frequent in group 2 but not observed in group 3. In the present study, 12
replications (3 each year) were used to evaluate the presence or absence of LTN symptoms. Varieties in group
1(Faisalabad-83, Faisalabad-85, Suleman-96, Bahawalpur-95, Punjab-96 and Bakhtawar-93) expressed LTN
phenotypes in eight or more of the replications and were therefore considered positive for LTN. Relative BYDV
severities of these six varieties of group 1 were 42-70% less infected than the susceptible check. Varieties of group
2 (Inqilab-91, Zardana-89 and Rohtas-90) expressed LTN less frequently and inconsistently in four or fewer of the
replications and was therefore considered absent while BYDV severity was reduced from 52-64% of the susceptible
check. LTN was not displayed by varieties of group 3 (Sarsabz, Shaheen-94, Kaghan-93, Watan-94, Soughat-90,
Shahkar-95, Kohsar-95, Local White and Fakhar-e-Sarhad) which were able to reduce BYDV severity from 45-73%
of the susceptible check. Bdv1 gene was first identified in Anza wheat variety as BYDV tolerant gene which confers
slow yellowing (Singh , 1993). Leaf tip necrosis (LTN), a morphological trait reported of showing complete linkage or
pleiotropism with Bdv1, Yr18 and Lr34 genes (Singh., 1992a, b) which was suggested to use as phenotypic marker
to identify wheat varieties carrying the gene. Adult leaf tip necrosis, a phenotypic marker was observed at adult plant
stage. In the present studies high LTN frequencies were observed in group-1 varieties and were considered positive,
less frequent in group-2 while this trait was completely absent in group-3 varieties. Varieties which expressed LTN
phenotypes ≥ 8 are considered carrying Bdv1 gene and this gene is believed to occur very frequently in CIMMYT
wheats (Singh., 1993). Similar findings regarding LTN phenotypes and their molecular confirmation of Yr18
presence/absence were reported on the same commercial varieties by Shah (2010). The phenotypic marker (LTN)
for Bdv1 gene was not 100% expressed in the LTN positive varieties across different replications and is reported to
be obscured by genetic background (Singh., 1999) and variable influences of environment (Dyck., 1991). Watan-94
and Shahkar-95 of group-3 developed less foliar chlorosis but could not express LTN. There may be the possibility
that varieties that could not expressed LTN may even carry Bdv1 as Singh (1999) reported that varieties which don’t
express LTN may still carry Lr34.
Table 3. Pedigrees, BYDV severity (%), leaf tip necrosis (LTN), stability parameters of severity trait and indexing through DASELISA of tested wheat varieties
Varieties
Pedigree
Mean
BYDV
Severity
Group-1(Possess LTN)
Faisalabad-83 FURY/KAL/BB
Faisalabad-85
MAYA/MON//KVZ/TRM
Suleman-96
F6.74/BUN//SIS/3/VEE#7
Bahawalpur95
Punjab-96
AVRORA/UP301//GALLO/SUPER-X/3/(SIB)
PEWEE/4/MAIPO(SIB)/
(SIB)MAYA-74//PEWEE
SA 42 *2/4CC/INIA//BB/3/ INIA/HD832
Bakhtawar-93
JUP/BJYG//URES
Group-2(LTN less frequent)
Inqilab-91
WL 711/CROWS’
Zardana-89
CNO S/8156 TOB 66 CNO6-PVN
Rohtas-90
INIA F 66/ A.DISTCHUM//INIA66/3/GEN
Group-3(LTN not observed)
Sarsabz
P1/FRND//MXP/3/P1/M20/79
Shaheen-94
MLT “S”
Kaghan-93
TTR/JUN 31.36
Watan-94
Lu26/HD2179
26.6
Soughat-90
Pavon Mutant-3
31.51
35.6
Resistance
class
LTN
Stability
Parameters
bi
S2d
ELISA
32.00
(58)*
16.00
(30)
26.00
(47)
24.00
(44)
17.00
(32)
23.00
(41)
LR**
8
1.03
-1.09
++
R
7
0.53
0.54
+
LR
9
1.19
4.59
+
LR
10
0.80
-1.36
++
R
10
1.00
5.25
++
LR
9
1.47
- 0.99
+
20.00
(36)
27.00
(48)
27.00
(48)
R
3
1.21
- 0.13
+
LR
4
0.96
-1.39
++
LR
3
1.20
6.59
+
15.00
(28)
20.00
(36)
17.00
(31)
15.00
(27)
17.00
(32)
R
Absent
1.06
- 0.32
++
R
Absent
1.31
3.69
+
R
Absent
1.09
- 0.57
+
R
Absent
1.03
3.40
++
R
Absent
0.43
- 1.31
++
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Shahkar-95
WL 711//F3.71/TRM
Kohsar-95
PSN/BOW
Local White
Land race
FakhrSarhad
e-
35.45
35.76
54.85
PFAU “S”/SERI/BOW “S”
100.00
20.00
(35)
20.00
(35)
30.00
(55)
55.00
(100)
R
Absent
0.79
5.09
++
R
Absent
1.60
1.51
++
LR
Absent
0.64
- 1.22
++
I
Absent
0.63
- 0.98
++
BYD Symptoms Stability and ELISA analysis
Analysis of variance for percent BYDV severity showed highly significant (P<0.01) differences for both genotypes
and years while genotypes x years interaction remained non-significant (Table 1). BYDV incidence and severity was
positively correlated (r = 0.935) over four years. Performance of individual varieties with regard to comparative
stability of BYDV severity is presented in Table 3. Stability parameter, coefficient of regression (bi) value deviated
from unity (bi=1) and ranged from 0.43 to 1.60 in the tested varieties. Based on mean BYDV severity over years,
tested varieties were classified into resistant (1-20% severity), low resistance (21-50% severity) and intermediate
(51-70% severity). Five varieties (Faisalabad-83, Punjab-96, Sarsabz, Kaghan-93 and Watan-94) were found stable
for this trait over four years of study as their bi value was 1 or near to 1. Apart from the check variety (Fakhr-eSarhad), all remaining genotypes fell into resistant or low resistance classes but remained highly unstable for severity
trait over four years. Wheat commercial varieties were assessed against BYD natural infection across different
seasons to know disease symptoms stability (tolerance) on the tested varieties. BYD severity fluctuated between
years and greatly influenced by environment which is important for its tolerance characterization through foliar
chlorosis (Comeau and Jedlinski., 1990). Faisalabad-83, Sarsabz, Shaheen-94, Suleman-96, Kaghan-93, Rohtas90, Inqilab-91, Kohsar-93, Watan-94 and Bakhtawar-93 showed regression of coefficient value greater than unity
(b>1) and thus produced symptoms under BYD favorable environmental conditions. While Bahawalpur-95, Zardana89, Faisalabad-85, Soughat, Shahkar-95, Local white and susceptible check Fakhr e sarhad with coefficient of
regression value less than unity (b<1) therefore, produced symptoms under less favorable conditions (Eberhart and
Russel., 1966). Furthermore, Punjab-96 remained stable (b=1) with coefficient of regression value equal to unity
(Eberhart and Russel, 1966) and expressed similar disease symptoms at different environmental conditions. BYDVPAV was detected through DAS-ELISA in the infected leaves of wheat exhibiting typical yellowing symptoms of BYD.
BYD-PAV infection was dominant due to abundance of their aphid vectors i.e. Rhopalosiphum padi and Sitobion
avenae and was frequently detected during peak aphid BYD activity period from the region in earlier studies (Bashir
et at., 1997; Ibrahim., 2006; Suddiqui., 2011).
Table 1. Pooled analysis of variance of BYD % severity during 2004-2008 at NIFA, Peshawar Pakistan
Source
Replications
Genotypes (G)
Years (Y)
GxY
Error
Degrees of Freedom
2
17
3
51
142
Sum of Squares
1.349
223.060
650.684
309.446
623.517
Mean Square
0.674
13.121
216.895
6.068
4.391
F value
0.1536
2.9882
49.3957
1.3818
Prob
0.0002**
0.0001**
0.0512
Coefficient of Variation: 19.20%
Tested varieties were indexed for the infection of Barley Yellow Dwarf Virus (BYDV) through DAS-ELISA during
2007-08. The overnight incubation of conjugate with antigen gave lower background values and allowed easier visual
discrimination between positive and negative reactions. Assay was done by visual observation of the yellow
nitrophenolate, based on “+” and “++” as presented in Table 3. Presence of BYDV-PAV was confirmed in the infected
leaves of all tested varieties, of which ten (Faisalabad-83, Sarsabz, Bahawalpur-95, Zardana, Kohsar-93, Watan-94,
Shahkar-95, Soughat, Local white and Fakhr e Sarhad) had strong positive reaction.
In our environment varieties possessing Bdv1 gene identified through phenotypic marker did not show tolerance
against BYD. LTN positive varieties showed high level of disease severity as compared to varieties with less frequent
LTN or with no LTN. Thus the hypothesis that common wheat possessing Lr34/Yr18/Bdv1 increases tolerance
against BYD was not confirmed. Similar results regarding the Bdv1 tolerance was reported by Ayala. (2002) and
Slamova., (2009) that the effect of the Bdv1 gene is not as effective as expected in the previous study by Singh.
(1993). As the Bdv1 gene does not provide true resistance, therefore breeders identified Thinopyrum intermedium
which is a wild grass and show a very high level of resistance possessing Bdv2 and Bdv3genes. These genes present
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in many translocated wheat lines conferring different levels of tolerance to BYD infection should be incorporated in
national breeding program of the country to instill the crop with an inbuilt ability to avoid losses due to this serious
disease.
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