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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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Canadian Journal of Plant Protection. Volume 2, Number 1, Pages 9-16 ©2014 Canadian Science and Technology Press Inc.
Cotton leaf curl virus disease a principle cause of decline in cotton
productivity in Pakistan (a mini review)
J. Farooq1*, A. Farooq1, M. Riaz1 , M. R. Shahid1, F. Saeed1, M. S. Iqbal1. T. Hussain2, A. Batool3, and A. Mahmood4
1Assistant Research Officer, Cotton Research Institute, Ayub Agricultural Research Institute, Jhang Road, Faisalabad.
2 Consultant, Cotton in International Center for Agricultural Research in Dry Areas (ICARDA), Pakistan Office
3Assistant Plant Pathologist, Pulses Research Institute, Jhang Road, Faisalabad.
4Director General Agri. Research, Ayub Agricultural Research Institute, Jhang Road, Faisalabad, Pakistan
* Corresponding author’s email address: CJPP 02-01-04
Abstract
Among most serious threats of last two decades with reference to cotton crop in Pakistan is Cotton leaf Curl Virus.
This disease inflicted huge losses not only to the cotton crop but also to the economy of Pakistan. It first appeared in
1967 on few plants in Multan and in 1992-93, caused a decline in production down to 9.05 million bales and during
1993-94, to 8.04 million bales well below the estimated targets in Pakistan. Various disease inducing procedures like
grafting, delayed sowing, whitefly mediated disease transfer were exploited to screen out material against this
notorious disease. Climate change and weather fluctuations have a profound influence on the spread of Cotton Leaf
Curl Virus. Climate change is altering temperature and precipitation patterns, resulting in the shift of some
insect/pest from small population to large population thus effecting crops yield. The abiotic factors like temperature
and plant age influence cotton leaf curl virus disease epidemiology. Fiber quality traits like Ginning out turn, fiber
length, fiber uniformity index, fiber fineness, fiber bundle strength, maturity ratio also deteriorated because of
change in composition of major fiber components including cellulose, protein, wax and pectin. The ambiguity about
inheritance is also prevailing whether it could be through dominant or recessive genes which may be monogenic or
polygenic whereas Extrachrmosomal inheritance is also under discussion. The resistance break down depends upon
the evolutionary potential of the pathogen and possibility of recombinations, by which new variants of viruses
evolved. The resistance gained for Multan-CLCuV became susceptible to Burewala-CLCuV due to virus mutation
and lack of durable resistance. Virus tolerant cultivars along with management practices like changing sowing dates,
proper crop nutrition, better cultural practices, efficient vector control and buffer crops are the ways that can help to
get better crop. Systemic poisoning of cotton seed by seed treatment may make the cotton crop safe in initial 40-
50days after sowing. Biotechnology can also help in controlling this disease through transcriptional gene silencing.
By exploiting biotechnological tools broad spectrum resistance can be introduced against all viruses present in the
field.
Keywords: Epidemiology, Inheritance, Polygenic, Pakistan, Gene silencing, Extrachrmosomal
The importance of cotton is evident from the fact that
it is not only the most important fiber crop but also
the second most important oilseed crop of the world
(Cherry and Leffler, 1984). In Pakistan Cotton
(Gossypium hirsutum L.) is grown in warmer
climates throughout the country (Riaz et al. 2013). In
previous twenty years Cotton leaf curl virus disease
has become a serious threat to cotton productivity in
Pakistan. Sustainable cotton production requires
identification and cultivation of stable cultivars
Farooq et al. 2013. The yield sustainability in cotton
still not attains because of several causes but CLCuD
is notorious one. Cotton leaf curl virus has interesting
evolutionary story. It was reported first in Nigeria
(1912) on Gossypium peruvianum and Gossypium
vitifolia, Sudan (1924), Tanzania (1926), Philippine
(1959) but in Pakistan CLCuD was first recorded in
the 1967 in Multan district on scattered hirsutum
plants (Hussain and Ali, 1975). It was not well
thought-out as a serious disease up to 1987 but
appeared in epidemic form in 1992-1993 when 1.3
million bales of cotton were lost over an area of
24.28 hectares. The financial losses with the
estimated value of $5 billion (US) to the nation
occurred from 1992-1997 (Briddon and Markham.,
2001). In 1997, CLCuD was reported from Sindh
province of Pakistan which was previously free from
this disease (Mansoor et al., 1998). It is very
complicated to calculate the precise estimates
because the occurrence of CLCuD varies from year to
year and also varies from area to area under cotton
cultivation.
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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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Symptoms
Cotton leaf curl disease (CLCuD) infected plants may
show a wide range of symptoms depending on the
severity of disease. Typical symptoms include
thickening and yellowing of small veins on the lower
surface of young leave. Under severe attack of
disease leaves curl downward or upward and plant
growth stunted due to reduction of inter-nodal
distance and in some cases an outgrowth called
enation appears on lower side of curled leaves (Qazi
et al., 2007). Cotton plant infected with CLCuD
showing veins thickening and yellowing, upward
curling (Fig. 1), down ward curling (Fig. 2), enations
(Fig. 3) on the underside of the leaves, Stunting of
cotton plant (Fig. 4).
Figure 1. Upward curling along with thickening of
leaves of cotton plant.
Fig 2. Severe curling along with thickening of leaves
of cotton plant.
Figure 3. Enations on the underside of Cotton leaf.
Figure 4. Stunting of the cotton plant.
Chasing symptoms
The attack of sucking pests (Jassid and Whitefly) on
cotton (Gossypium hirsutum L.) and their symptoms
resemblance with cotton leaf curl virus disease create
a difficulty by virtue of assessment among the
farmers and researchers at early stages of plant
development. The cotton leaf curl virus disease
(CLCuD) symptoms coincidence with attack of Jassid
(Empoasca facialis) that suck cell sap under side of
leaves by which leave render down ward curling, turn
yellowish to brown, retard fruiting capacity, sever
incidence results stunting growth of young plants,
reduce seed cotton yield and fiber quality. Whitefly
(Bemisia tabaci) is also sucking pest that causes
similar infection like Jassid but with an extra
responsibility of virus transmitting vehicle.
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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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As the symptoms are identified the percent asperity
and range of rating scales of symptoms are still under
discussion. Keeping in view the severity of disease
the rating scales for viral diseases are also used other
than cotton crop like tomato, Chilli, Cucumber and
Tobacco with the range of zero to six numerically,
where these scale give the symptom description also
determined the level of resistance or susceptibility. If
we keenly observe the scale 2 and 3 with reference to
moderately resistance and moderately susceptible
both are vice versa but used separately. The disease
scale that has been generally used in cotton is based
on Severity Index (SI) and Percent Disease Index
(PDI %). The formula used to calculate both of these
two parameters has been reported by Akhtar et al.
2003, 2010 and given in Table 1.
Table 1. Disease scale proposed by Akhtar et al. 2010
Symptoms
Disease index%
Rating
Disease Response
Complete absence of symptoms
0
0
Immune
Thickening of few small scattered veins or only presence of leaf enations on
one or few leaves of a plant observed after careful observations.
0.1–10
1
Highly resistant
Thickening of small group of veins, no leaf curling, no reduction in leaf size
and boll setting.
10.1-20
2
Resistant
Thickening of all veins, minor leaf curling & deformity of internode with minor
reduction in leaf size but no reduction in boll setting.
20.1-30
3
Moderately resistant
Severe vein thickening, moderate leaf curling followed by minor deformity of
internodes and minor reduction in leaf size and boll setting.
30.1-40
4
Moderately susceptible
Severe vein thickening, moderate leaf curling & deformity of internodes with
moderate reduction in leaf size and boll setting followed by moderate stunting.
40.1-50
5
Susceptible
Severe vein thickening, leaf curling, reduction in leaf size, deformed internodes
and stunting of the plant with no or few boll setting.
>50
6
Highly susceptible
Foliar outgrowths (enation) will be marked with ‘‘E’’ where observed. (This rating scale is proposed by Akhtar et al. 2010 in cotton).
Whitefly and virus
A notorious group of viruses belongs to genus
Begomovirus cause major threat to cotton crop,
which is well known as Cotton Leaf Curl Virus
disease (CLCuD) and is transmitted by whitefly i.e.
Bemisia tabaci complex (including B. argentifolii) in
persistent manner (Rybicki and Fauquet, 1998). Most
of the begomoviruses comprised of two genomic
components called DNA-A and DNA-B, which are
indispensable for disease that is transmitted by
whitefly Bemisia tabaci (Monga et al. 2011).
Cotton whitefly reported as pest of Tobbaco over 100
years ago (Anonymous, 1993). It is the most vital
sucking pest of both industrial and food crops like
Cotton, Sunflower, Melon, tomato, Brinjal etc. (Rafiq
et al., 2008). Its polyphagous nature is confirmed
over 500 plant species all over the world including
Asia, Africa, America, Europe, Russia, Australia and
Pacific Islands (Greathead, 1986). In cotton growing
areas of Central Punjab it has been reported in about
164 plant species (Attique et al., 2003). In 16 of the
27 cotton growing countries whitefly is recognized as
a major pest during mid to late sowing time.
Conditions suitable for the spread of disease
Climatic conditions like rainfall, wind and
temperature have an influence in the spread of
CLCuD in Africa. Rainfall prior to seedling may
result in the development of increased population of
vector due to abundance in food source (Bink, 1975).
Ahmed et al .2013 found significant correlation
between CLCuD and temperature and between
CLCV and PAN evaporation during the month of
July in Multan district of Pakistan which is
considered to be the hot spot area for this disease.
As cotton is grown only for part of the year
cultivated hosts and alternate weeds serve as virus
reservoirs. Whitefly infects cotton fields and primary
sites of infections established. Secondary spread to
other plants may occur from the primary sites and
from additional vector which enter the field during
the whole growing season (Giha and Nour, 1969).
Khan et al. (1998) used regression analysis on
weekly air temperature (Maximum and Minimum),
rainfall, relative humidity and wind movement
relationship with % plant infection by CLCuD on
eight varieties of cotton. Disease infestation increased
in the range of Maximum and Minimum temperatures
of 33-45°C and 25-30°C, respectively. They also
reported poor correlation of weekly rainfall and
humidity with disease development and non
significant between CLCuD intensity and whitefly
population on all varieties studied. Akhtar et al.,
2002b found non significant correlation of weekly
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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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maximum air temperature (°C), % relative humidity
(5 p.m.), wind velocity, rainfall, sunshine and white
fly population on thirteen mutant/varieties and
negative significant correlation between minimum air
temperature and wind velocity (8 a.m.) for CLCuV
disease development. They also found positive and
significant correlation between % disease incidence
and plant age. Maximum disease index % was
recorded at 6 week old seedlings and it gradually
decreased with increase in age of plant. Many
researchers found non significant relationship of
white fly population with disease (Briddon et al.,
1998).
Effect of CLCuD on yield and fiber traits
Losses due to CLCuD are dependant on infectivity
time and variety. The pronounced damage of CLCuD
is at early stages but at later stages results minor
infections (Akhtar et al., 2003). CLCuD damage
differs on various plant parts and ultimately results in
reduction of yield. It can reduce boll weight 33.8%,
73.5% in bolls per plant, GOT% upto 3.93%, seed
index 17.0% and yield per plant 64.5% (Ahmed,
1999). Production losses due to CLCuV during last
20 years are given in Table 2. The cotton fiber (lint)
is the most important commodity for textile industry
and CLCuD also affects fiber quality traits (Kalhoro
et al., 2002). According to Ahmed et al., 1999
CLCuD can decrease fiber length 3.44%, fiber
strength 10% and elongation percentage upto 10%.
Akhtar et al. 2009 studied impact of CLCuD on fiber
quality traits and the findings depicts that the CLCuD
significantly affect traits like GOT, fiber length, fiber
uniformity index, short fiber index, fiber fineness,
fiber bundle strength yellowness and maturity ratio.
In their studies they observed significant affects of
this viral disease on cellulose, protein, wax and pectin
which are the major constituent of fiber. But in view
of Idris (1990) virus has significant impact on yield
but not on fiber quality.
Table 2. Losses to area (1000) hectares and production (1000) bales of cotton due to CLCuV in Pakistan in last 20 years.
Year
Partial losses
Complete losses
Total area affected (1000) hectares
Losses (1000) bales
1988-89
-
0.06
0.06
0.3
1989-90
-
0.2
0.2
1
1990-91
-
0.8
0.8
4
1991-92
11.3
2.8
14
20
1992-93
364
121
485
750
1993-94
607
282
889
1880
1994-95
407
-
407
221
1995-96
882
-
882
447
1996-97
1623.9
137.4
1761
2100
1997-98
762.9
19.5
782
1118.1
1998-99
457.9
-
458
587.1
1999-00
289.1
-
289
370.5
2000-01
90.1
-
90
111.2
2001-02
66.6
-
67
82.3
2002-03
357.7
2.15
359
265
2003-04
488.7
14.1
503
503.9
2004-05
127.8
31.1
130
967.1
2006-07
1686
25.21
1712
1231.7
2007-08
1432.8
2.5
1435
953.5
2008-09
1440.1
40.25
1480
1115.7
Resistance inheritance
When the actual designation of disease is realized
about its symptoms, vector (whitefly), transmission
and environmental conditions then the next step is to
solve the problem only on genetic basis rather than
the Entomological, Pathological and Agronomical
schools of thoughts, which are also important. As the
inheritance of resistant genes for disease is still under
discussion whether it is nuclear (nucleus) or extra-
nuclear (cytoplasm) but both reports about maternal
effects are available (Khan et al., 2007). The breeding
for cotton leaf curl disease (CLCuD) resistance has
been achieved through assemblage of minor genes by
recurrent selection (Hutchinson and Knight, 1950)
and similar sayings by Azhar et al., (2010) that the
resistance depends on major genes (dominant genes)
may lost quickly because of evolution of pathogen for
these genes. An alternative approach is needed for
partial resistance that depends on the recombination
of minor genes (recessive genes).
Resistance breakdown
The secret of inheritance is still under discussion and
another idea of resistance breakdown was initiated
that so called achieved resistance has been broken
down by virus mutation whereas the symptoms and
parameters for identification are still same in practice.
García and McDonald, 2003 reported that the virus
mutation requires 25 years at least then who does it
possible after 1967s our researchers get early
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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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resistance and instantly destroyed the integrity.
Whereas the changing climate scenario, cotton
varieties either susceptible are sown early can escape
from virus and whitefly but the resistant one could be
susceptible in late sowing which is the cause of
ambiguity between susceptible and resistant.
The concept of polygenic mode of inheritance of
cotton leaf curl disease was changed into single
dominant gene (with minor modifier genes) as
determined by Saddig (1968) and also clarified by
Ahuja et al. (2007). The cross between Gossypium
barbadense L. (Giza-45) and Gossypium hirsutum L.
(Reba P-288) determined the effects of single
dominant gene supported by Aslam et al. (2000). The
F1 of crosses between highly susceptible S-12, highly
resistant LRA-5166 varieties were found all virus
free plants and their F2 was close to 1:3 ratios which
exhibit the presence of single gene for the inheritance
of resistance against CLCuD reported by Rehman et
al. (2005), Whereas in same cross (LRA-5166 × S-
12) no single gene of major effect found to be
responsible for cotton leaf curl disease (Khan et al.,
2007).
Resistance sources
The wild species of Gossypium are potential source
of resistance to biotic (insect and diseases) and
abiotic (salinity, cold, drought, heat) stresses. G.
anomalum, G. longicalyx, G. stocksii, G, raimondii
and G. sturtianum have a source for the improvement
of fiber quality characters whereas G. thurberri, G.
anomalum, G. raimondii, G. armourianum and G.
tomentosum are the best sources for resistance of
insect pests including whitefly which is the main
vector for the inoculation of CLCuD (Azhar et al.,
2010).
Screening methods employed to develop CLCuD
tolerant materials
Screening methods those commonly used is the
exploitation of virus spreader line (S-12) and white
fly as a source of transmission vector Shah et al.
2004 and Perveen et al. 2005. For transmission
through spreader line these researcher used S-12 the
popular and most susceptible variety to CLCuD
disease. This variety was planted in rows among the
tested genotypes for natural spreader of disease. Shah
et al. 2004 proposed whitefly mediated transmission
using insect proof cages. Another method that was
used for screening is the sowing time difference i.e.
normal and late sowing along with disease nursery
(Ahuja et al., 2007; Perveen et al., 2010). They
established CLCuD nursery near the experimental
area to allow the spread of whitefly vector throughout
the season and tested different sowing dates.
Grafting is the most efficient method to transmit the
causal agent as grafted plants develop symptoms
within 14-30 days depending upon varietal
susceptibility/resistance (Akhtar et al. 2001; 2002b).
Grafting as a successful method to inoculate CLCuD
was used by Akhtar et al. 2002 (a, b, c), 2004, 2010
and Shah et al. 2004. For grafting researchers
employed three procedures like Bottle graft, top cleft
and wedge graft. In this procedure the stock used as
resistant and scion as susceptible source for
inoculation of disease and later presence of virus was
confirmed by the use of ELISA.
PCR can be used as a reliable tool for the detection of
viruses. As the geminiviruses are small, single
stranded and have circular genome thus PCR can be
efficiently used for their detection. Several
degenerate primers have been designed for the
detection of these viruses (Briddon and Markham
1994). With the help of these primers previously
uncharacterized geminiviruses can be amplified, and
primers designed on the basis of non-conserved
sequence can be exploited to detect a particular virus
and strain of that virus (McGovern et al., 1994).
Another method to screen the germplasm against
cotton leaf curl virus is through inoculation using
veruliferous whiteflies in net house conditions either
by open choice method or through release of counted
veruliferous flies on test plants under plastic jars in
polyhouse for fixed interval (Monga et al., 2011)
Pollen irradiation technique may be used as a
criterion to develop CLCuV tolerant material for
creating genetic variability in cotton germplasm.
Aslam and Elhai 2000 used pollen irradiation
technique. They attempted different crosses as
reported earlier by Doak, (1934) by applying
irradiation doses i.e., 5-10Gy (Aslam and Stelly,
1994) to create more genetic variability.
Control measures (non-biotechnological tools) and
recommendations
Though the solution of various diseases is the
development of disease tolerant varieties but disease
management is quite appropriate when resistance
sources are inadequate. In cotton host plant resistance
is the best long term and explored strategy to protect
the plants from CLCuD (Solomon-Blackburn and
Bradshaw, 2007). Cotton leaf curl disease spread
from the primary inoculum that is present in off
season in the form of weeds and other hosts (Monga
et al., 2001). The management of CLCuD includes
control of vector whitefly and eradication of weeds
that contribute the hospitality of Cotton leaf curl virus
(Monga et al., 2001).
The seed treatment with systemic insecticides may
prevent the cotton crop up to 50-60 days. By using
insecticides even if infection occurs at later stage the
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Farooq et al. (2014) Canadian Journal of Plant Protection. Vol. 2, No. 1
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severity of losses may be avoided as symptoms
appearance will begin after 65-90 days and plants
avoid the most susceptible stage (Monga et al.,
2011).
Growth and production of cotton is reduced by both
abiotic and biotic stresses Zafar and Athar 2013.
Biotic stresses or diseases affect uptake and
utilization of nutrients by plants. It is therefore, plant
mineral nutrition management not only used for
producing higher crop productivity; it also used to
change plant responses to biotic stresses disease
incidences (Walters & Bingham, 2007). Various
agronomic practices like sowing time and application
of nutrients (Nitrogen and Potassium) can serve the
purpose. The knowledge about K nutrition on
association between plants and pests may help in
developing strategies to set up high yielding
production system by reducing disease incidence
Zafar and Athar. 2013. Choosing best sowing time
for a particular variety in different regions is difficult
as too early and too late sowing may result in
problems of diseases and pests. Appropriate sowing
time preferably mid April to mid May results in
decrease of disease incidence (Ghazanfar et al., 2007)
as compared to delay in sowing from mid May to
June. Iqbal and Khan 2010 reported that increased
plant spacing in case of early sowing and decreased
plant spacing under late sown conditions is effective
in management of CLCuD. They also concluded that
CLCuD infestation reached its maximum after 105
days of sowing and in case of late sown crop i.e. 15
June or later infestation become severe after 45 days
of sowing. They recommended 15 cm plant spacing
in order to manage CLCuD in case of planting later
than 15th of June.
According to Zafar et al. 2010 by understanding the
physiological basis of nutrition (nitrogen) strategies
can be designed to prevent, escape, avoid and control
viral diseases. In case of resistant cultivars nitrogen
concentration does not affect but in susceptible
cultivars its concentration plays an important role to
tackle disease severity. The most recommended
management practices to tackle CLCuD disease
include virus resistant cultivars, management of
causal agents and mineral nutrition (Akhtar et al.,
2004). The influence of Potassium (K) application on
disease through specific metabolic functions alters
the relationship of host-parasite environment (Kafkafi
et al., 2001). Pervez et al. 2007 conducted an
experiment on role of Potassium (K) in the control of
CLCuD. According to their studies by increased
application of Potassium upto 250kg/ha results in the
reduction of disease from 12 to 38%. This increased
application contributed considerably as seed cotton
yield increased up to 37% as compared to Zero-K.
ACoording to Farooq et al. 2013 the traits like plant
height, bolls per plant and sympodia per plant may be
considered for selection in virus intensive conditions
as they found higher estimates of broad sense
heritability along with positive and significant
genotypic correlation with seed cotton yield in virus
intensive environment.
Recent advances to combat clcuv through
biotechnological tools
In plants lacking natural disease resistance PDR
approach has been documented to combat different
viruses. According to Hashmi et al. (2011) by
exploiting transcriptional control two truncated forms
of replicase (tACI) gene, capable of expressing only
N-terminal 669bp (5'ACI) and C-Terminal
783bp(3'ACI) nucleotides were introduced into
Gossypium hirsutum through cloning. A strain LBA
4404 of Agrobacterium tumefaciens was used
through interference technology to impair cotton leaf
curl virus in transgenic cotton. When transformed
plants were compared with control non-transformed
plants the over expression of either of the above
mentioned nucleotides confer resistance by inhibition
of viral genomic and β satellites DNA components.
In early and late growth stages Northern blot
hybridization revealed high transgene expression
(Hashmi et al., 2011).
Conclusion
Various aforementioned procedures of controlling
CLCuD can be implemented depending upon
situation. Development of resistant varieties along
with Agronomic, fertilizer, insecticidal control and
biotechnological methods can be used alone and in
combination to control this severe disease which is
still a challenge even after twenty years of extensive
research.
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