Innovative approaches towards aphid resistance prevention in brassica crops

Int. J. Life. Sci. Scienti. Res., 3(4): 1230-1237 JULY 2017
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Innovative Approaches towards Aphid
Resistance Prevention in Brassica Crops
Varsha Jain1
, Archana Tiwari1*
1
Dept. of Biotechnology, School of Sciences, Noida International University, GB Nagar, Greater Noida, Uttar
Pradesh, India
*
Address for Correspondence: Dr. Archana Tiwari, Director, Dept. of Biotechnology, School of Sciences,
Noida International University, GB Nagar, Greater Noida, Uttar Pradesh, India
Received: 15 March 2017/Revised: 24 May 2017/Accepted: 21 June 2017
ABSTRACT- Brassica juncea, the Indian mustard supplies a big amount of edible oil demand in India. Biotic and
Abiotic factors were responsible for serious reductions in B. juncea production in India. Several control measurements
had been taken to prevent the losses in crop. Biochemical control, Biological control and Genetic control are some of the
preventive methods used in this study to evaluate the yield loss in Indian Mustard. In India around 39 million hectares of
land was under mustard cultivation with a production of 10 million tonnes. It was estimated that the demand for oilseed in
India will be around 34 million tonnes by the year 2020. 41% of this demand (14 million tonnes) had to be met by
mustard alone. Apart from its use as oil, it has got some medicinal properties too. Among the oilseed crops grown in India,
mustard (Brassica sp.) was one the most important ones. In India around 26.11 million hectares of land was under mustard
cultivation during the year 2009-2010 (4th
advanced estimates released on 19.07.2010 by Ministry of Agriculture, Govt. of
India). It was estimated that the demand for oilseed in India will be around 34 million tonnes by the year 2020. 41% of
this demand 14 million tonnes must be met by mustard alone. The production of Indian mustard was severely affected by
mustard aphids. In this review, we had studied some of the control method to avoid aphid infestation, which will severely
affect the crop production.
Key-words- Biotic stress, Indian Mustard, Mustard Aphids, Genetic control
INTRODUCTION
Indian mustard (Brassica juncea L.) was introduced to the
northern part of India from China. It is a self-fertile annual.
Presently about 25-30% of the total oilseed production in
India is contributed by Brassica. Mustard seeds contain
6.2% Moisture, 24.6% Nitrogenous matter, 35.5% Fat, 8%
Fibre and 5.3% Ash. The oil content of the crop is about 30
to 38%. Mustard oil contains about 60% monounsaturated
fatty acid (MUFA) of which erucic acid oleic acid
constitutes 42% and 12% respectively. It has 21%
polyunsaturated fatty acid (PUFA) of which 6% is the
omega-3 alpha-linolenic acid and 15% omega-6 linoleic
acid and it has 12% saturated fats (SAFA). Indonesia is the
highest producer of mustard seed with annual production of
21 million tonnes [1]
. Apart from India, Brassica is also
grown in China, Europe and Egypt. India produces bulk of
mustard seed with annual productivity of 0.25 tonnes per ha
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and mustard is the second most important oilseed crop in
India. It is a common field crop of Rajasthan, Uttar
Pradesh, Haryana, Madhya Pradesh and Gujarat. Mustard
oil was once the most popular cooking oil in northern India.
In the second half of the 20th
century the popularity of
mustard oil receded due to the availability of
mass-produced vegetable oils. Related to all other field
crops mustard also suffers from various biotic stresses
which utmost the final yield. Among the various biotic
stresses experienced by mustard crop mustard aphid
(Lipaphis erysimi L.) is the most important, [2]
which causes severe yield losses all over the world. For
centuries, peasants in rural India used the plant to add
flavour to rice dishes. In that centuries, they called it the
'plant of long life', claiming it had powerful healing
properties. Recent research into Indian Mustard's ancient
medicinal claims has provided scientists with two
remarkable findings.
First, the plant contains a robust mixture of anti-cancer
ingredients that consists of vitamins, antioxidants and
minerals with three times more calcium, potassium and iron
than is develop in ordinary green-leafy vegetables. Second,
it has a unique ability to absorb metals and minerals from
the earth it grows in. For consideration into account,
Russian agronomists have planted it near the site of the
Chernobyl reactor to de-contaminate the ground from
ARTICLEREVIEW

Int. J. Life. Sci. Scienti. Res., 3(4) JULY 2017
hazardous levels of lead and uranium.
Mustard is an annual herb cultivated mainly as oil seed
crop. It is the second most important oilseed crop in India
after Groundnut. Sometimes it is also used as vegetable or
as fodder. Out of many species, 3 species are known for its
condiment value. These are pale yellow or white mustard
(Brassica rapa), brown mustard (Brassica juncea) and
black mustard (Brassica nigra). It has been introduced
firstly to Northern India. The black mustard is endemic in
the Southern Mediterranean region. Mustard prefers loamy
or clayey loam soil. It is grown as Rabi crop in North India.
It is raised during rainy season from July to November in
South India.
CONTROL MEASURES
Aphid is one of the well-known and famous insect that is
quite hard to constraint due to its elevated rate of
reproduction. Aphid can be avoided to some extent if the
crop is sown before 20th
October. Applications of suggested
dose of fertilizers, harming the affected plant tissues having
aphid population at initial stages etc. are some cultural
practices to overcome the aphid population. Biological
control measures also offer some degree of crop protection.
Ladybird beetles viz., Cocciniella septempunctata,
Hippodamia variegata and cheilomones vicina are the most
effcient pradators of the mustard aphid. Adult beetle may
feed on an average of 10 to 15 adults per day. The
lacewing, Chrysoperla carnea predates on the mustard
aphid colony. Chemical control of mustard aphid includes
spraying of insecticides below the ETL (Economic
Threshold Level). Most commonly used chemicals are
Imidacloprid 17.8% @ 0.25 ml/l, Thiamethoxam 25 WG @
0.2g/l and Dimethoate 30EC @ 1 ml/l of water. But due to
their nonspecific actions, beneficial insects like honey bees
are adversely affected. More over chemical control
becomes almost futile once aphids successfully establish
and colonizes on the host plant due to their high rate of
reproduction through parthenogenesis. Chemical
insecticides cause environmental pollution which is a major
concern regarding their use. Realizing these facts attention
was given for generation of resistance in the host plant
itself. Spray of Chemical insecticides can almost control
the major insect pests and thus no more attempts have been
made to breed varieties resistant to insects [3]
. Traditional
breeding approaches are not so victorious due to lack of
resistance genes in the crossable gene pool [4]
. Thus, genetic
engineering technique accepts more importance to develop
aphid resistance. Bacillus thuringiensis endotoxins have
been studied extensively and proved to be effective against
several insects falling under the groups of lepidoptera and
coleoptera, which feed by chewing plant parts. But against
this hemipteran sucking pest Bt toxin was found
ineffective. Insecticidal properties of lectin genes have been
utilized to develop insect resistance in many cases.
Snowdrop lectin from Galanthus nivalis, commonly known
as Galanthus nivalis agglutinin (GNA), had been found to
be toxic to homopteran [5]
and other major insect pests [6]
.
Wheat germ lectin, WGA, has been engineered into
Brassica juncea and it was found that the transgenic plants
became resistant to aphid infestation. Oryza cystatin
encoding gene, OC-1 expressed in rapeseed affected the
fecundity of the sap-sucking aphids although did not have
much impact on insect survival [7]
. Constitutive and phloem
specific expression of Allium sativum leaf agglutinin
(ASAL) in transgenic Indian mustard (Brassica juncea) has
been found to be successful to combat aphid problem. So,
efforts were started to develop aphid resistant mustard
varieties by different methods which include Biological,
chemical and Genetic control (Fig. 1). The transgenic
Brassica plants were found to be tolerant to Lipaphis
erysimi infestation.
Fig 1: Different Parameters studied for aphid control in
Brassica
BIOLOGICAL CONTROL
In recent years, an effective and impressive body of
knowledge on the biology and ecology of natural enemies
of cereal aphids has been accumulated and as a result the
only integrated pest management (IPM) activities relate to
careful choice/application of pesticide and habitat
modifications. Entomopathogenic fungi
(Entomophthorales) are the most important microorganisms
attacking cereal aphids. Their efficiency depends mainly on
weather conditions during late spring and early summer:
under favourable conditions, they can cause epizootics, and
hence a fast crash of aphid populations [8-9]
. The role of
parasitoids is contradictory in the literature and often
overestimated. Their advantage is often a good
synchronization with their aphid hosts in time and space
due to their close relation to the hosts, even during winter.
However, only high parasitization rates during an early
stage of the aphid infestation have a substantial impact. In
addition, hyperparasitoids usually build up rapidly and limit
parasitoid efficacy. In most years, rates of parasitism of
cereal aphids during critical periods (e.g. the start of
exponential population growth) are below 10%, much too
low to influence aphid population dynamics [10-11]
. Mass

releases, habitat management, and increased diversity of
the landscape can enhance locally the effectiveness of
parasitoids [12-13]
. Polyphagous, and particularly aphid
specific, predators are more often the main factors in the
natural mortality of cereal aphids than parasitoids. The
predator community (in terms of species and guilds) in the
cereal ecosystem is highly diverse, and its impact depends
on the temporal and spatial synchronization, community
composition, prey preferences, and predatory potential at
given temperature conditions. Some species of
polyphagous predators are spatially associated with cereal
aphids through predation [14]
. Under optimal conditions,
polyphagous predators can reduce late aphid infestations in
cereals by up to 31% [15-19].
Carabids and most spiders show
continuous, but relatively low, aphid consumption rates
compared to aphid-specific predators [20-23]
. Similarly, [24-25]
showed (with seven potential generalist aphid predators)
low or non-preference of epigeal predators for aphids and
low food quality of cereal aphids. Thus, through early
predation when alternative prey is scarce [23, 26]
polyphagous
predators can reduce the initial density of cereal aphids.
Later, however, their voracity fails to keep up with
increasing aphid densities, or they switch to more
convenient prey [27]
. The high voracity of aphid-specific
predators [28-29]
and their good synchronization in time and
space with cereal aphids can greatly reduce the rate of
population increase [30-35]
. Syrphids and coccinellids
particularly have a strong potential to regulate cereal aphid
populations, showing both numerical and functional
responses to their prey [36-39]
. Despite a huge body of data, a
proper assessment of the effects of single predator species
on cereal aphid populations remains very difficult [40]
. A
simple addition of different predators with their varying
aphid consumption rates is not possible. Therefore, it was
devised the ‘predator unit’, whereby different predators can
be assessed for their potential for aphid consumption [41]
.
For instance, a female Coccinella septempunctata receives
the value 1.0, a male 0.88, and a green lacewing
Chrysoperla carnea larva only 0.14. Multiplying these
values with densities of each predator quantifies the impact
of a predator community on their prey. Simulation models
have been developed not only to describe the population
dynamics of cereal aphids, but also to assess the impact of
natural enemies [42-44]
. Running such models with and
without the presence of natural enemies provides a better
understanding of regulation capacities [44]
.
Biological control may be defined as the use of one
organism to reduce the population density of another
organism. Defined biological controls of arthropods are
defined as “the study and use of parasites, predators and
pathogens for the regulation of host (pest) densities” [45]
.
Predators and parasitoids both are among the most
important natural enemies of insects in many environments.
The identification of parasitoids and predators found
associated with aphids help to test their efficacy in
suppressing their host in field conditions. The secondary
symbiotic bacteria associated with aphids can confer
immunity to parasitoid attack causing death of parasitoid
eggs [46]
. However, such resistance is suggested to be
associated with a fecundity cost, as individual aphids with
parasitoid resistance produce fewer offspring. Interestingly,
secondary symbiont mediated resistance of A. pisum to
parasitism by Aphidius ervi is reported to increase when the
aphid line is co-infected with both Serratia symbiotica and
Hamiltonella defense compared to either of the singly
infected lines [47-48]
. Thus, a mechanism which can
dissociate secondary symbionts from aphids will enhance
the efficacy of biological control through parasitoid attack.
Rhopalosiphum padi is a ubiquitous aphid vector of major
cereal viruses like R. padi virus (RhPV). Upon infection
with RhPV, aphid longevity and fitness decreases leading to
reduction in colony populations. A recombinant baculovirus
expression vector that expresses a full-length cDNA clone
of RhPV was infectious in R. padi and was also transmitted
efficiently between aphids [49]
. Thus, the use of a
baculovirus to express a small RNA virus RhPV opens
avenues for large-scale production of small RNA virus
bio-pesticides against aphids.
However, the contribution of parasitoids, predators, and
fungal entomopathogens to suppression of aphid
populations is less recognized by seed potato growers. It
had been seen that unlikely the biological control agents
could be effective given the intensive use of pesticides in
seed potato production. However, the tremendous outbreaks
that can be induced by insecticides when the aphids had
developed resistance are indirect evidence of the
importance of natural enemies [50-52]
.
CHEMICAL CONTROL
If aphid population exceeds through action thresholds, an
insecticide treatment is recommended. In European
countries, several efficient insecticides are registered for
control of cereal aphids, both as BYDV vectors and as
direct pests. The treatment decision is often based on
simple economic considerations regarding both cost of
application and amount of work involved. Hence,
combined applications with fungicides before flowering are
done. Of major concern are the possible side effects of drift
on non-target organisms (both in the crop and on adjacent
non-cereal areas) since, with cereals, large areas are treated
simultaneously. Broad-spectrum insecticides like
λ-cyhalothrin negatively affected several non-target
organisms immediately after application [53]
. However, such
effects were often ephemeral, with rapid recovery and
recolonization. Good agricultural practice (e.g. spraying at
low wind speed using drift-reducing nozzles) can protect
non-crop areas, even from highly toxic chemicals. Some
European countries place restrictions on using pesticides in
and near field margins to protect arthropod communities
from spray drift [54]
. Inherently more selective compounds
like pirimicarb can be used; alternatively, some potent
insecticides for cereal aphid control can be applied
successfully at considerably reduced dose rates, especially
if infestation is late and levels only marginally exceed the

action threshold, as shown by [36-55]
for λ-cyhalothrin and
pirimicarb. Low dosage strategies are a very important
element of IPM in cereals because of the considerably
reduced side-effects on predators and parasitoids.
Although much of the insecticide used on potato is targeted
against other pests, more than one-third of all applications
in the USA are specifically for aphid control [56]
.
Insecticides are the only practical means of suppressing
colonizing aphids on the crop, but are of inconsistent
benefit in controlling virus spread. Among reported
successes in controlling virus spread with insecticides (all
crops and insect vectors), 94 of 119 cases involved
persistent and semi-persistent viruses, [57]
whereas most
failures, 32 of 48 cases, involved non-persistent viruses.
Viruliferous alatae are not killed quickly enough to prevent
PVY transmission [58]
. In contrast, spread of PLRV from
within-field sources can be interrupted because of the ex-
tended post-acquisition latent period before an aphid can
transmit [59-61]
. Systemic insecticides applied at planting or
plant emergence can reduce within-field spread of PLRV
significantly [60-63]
. Such timing gives the greatest benefit in
locations where migrant aphids are rarely viruliferous.
However, in the Pacific Northwest, PLRV infection rates
can approach 100% if M. persicae is not controlled with
insecticides [64]
. Insecticide resistance often severely limits
a grower’s choice of aphicides [65]
. With M. persicae, this is
a worldwide problem [66-67]
and resistance has developed to
all major insecticide classes except neonicotinoids [68-72]
demonstrated that non-toxic mineral oils applied to plants
substantially reduced PVY transmission. It is unclear why
field control is generally inferior to that obtained in
laboratory studies [73-75]
but reasons probably include
weathering of oil deposits [76]
new plant growth between
applications, and incomplete coverage.
The only and the most important method for controlling
aphid infestation is the usage of high doses of
agrochemicals but it is cost intensive in addition to being
environmentally hazardous. The chemical pesticides
include both contact and systemic insecticides. However,
aphids are rarely killed with contact insecticides because
they often infest the abaxial surface of leaves and feed
directly from the phloem sap. Systemic insecticides which
are absorbed by the plants are mainly used and popularly to
control aphids, as it is ingested through phloem sap and kill
the aphids irrespective of their shelter and feeding even if
under the leaf. The prevalent agrochemicals used in the
control of aphids include carbamates, organo-phosphates,
pyrethroids, cyclodienes etc. group of pesticides [77-78]
.
Resistant populations of aphids develop against the usually
sprayed organophosphate group of insecticides [79]
.
GENETIC CONTROL
Genetic resistance against any insect pest or pathogen can
be achieved through conventional breeding approaches by
transferring resistance genes from sexually compatible
germplasms. In developing aphid resistance, despite of
substantial breeding efforts, resistant genotypes could not
be bred mainly because of lack of resistance genes within
the crossable gene pool [4]
. To overcome the bottleneck of
unavailable resistance source transgenic technology offers
new avenues to explore resistance genes even from distant
organisms.
Transgenic strategies expressing insecticidal Bacillus
thuringiensis toxin, have been found to be effective against
many insect pests belonging to the order Lepidoptera and
Coleoptera. But for sap sucking hemipteran aphids Bt toxin
is ineffective. Engineering of other insecticidal proteins
such as protease inhibitors, lectins, amylase inhibitors in
crop cultivars also did not yield much resistance and as a
result such researches remained confined to laboratory
studies only. Therefore, it is imperative to look for new
strategies by making use of new biological phenomenon to
develop resistance against aphids. Transgenic cultivars
were released in the USA that expressed the Leptinotarsa
decemlineata (Colorado beetle) specific toxin Bacillus
thuringiensis var. tenebrionis (Bt) combined with PLRV
replicase [80]
and other cultivars expressed Bt and PVY coat
protein. This technology was far more effective than any
presently used tactic, but these cultivars have been
withdrawn because of concerns over a public backlash
against genetically modified food.
Resistant and tolerant varieties can provide excellent
control of aphid-vectored viruses [81-83]
. Commercially
available cucumber, zucchini, and yellow summer squash
varieties [84]
that have resistance or tolerance to one or more
viruses, including genetically modified varieties that
contain the coat protein genes of one or more viruses [82,85]
.
A new cantaloupe variety, ‘Hannah’s Choice’, developed in
the USA by M. Jahn, a plant breeder at Cornell University,
has resistance to WMV, PRSV-W, and ZYMV [86]
. Recently,
Harris Moran released the first pumpkin (Cucurbita pepo)
variety, ‘Magician F1’, with tolerance to ZYMV. In
Australia, a ‘Jarrahdale’ type pumpkin (C. maxima) has
been released that is highly resistant to ZYMV, PRSV-W,
and WMV [87]
. Now, there are no commercially available
virus-resistant or virus-tolerant varieties of watermelon in
the USA. Resistance to A. gossypii and its transmission of
viruses has been identified in muskmelon germplasm from
India [88]
and Korea [89]
. However, examples of the practical
use of this resistance are lacking. In Bangladesh, local
genotypes of ash gourd (Benincasa hispida), also known as
wax gourd or winter melon, are relatively resistant to A.
gossypii [90]
. The density of trichomes on leaves was
negatively correlated with the number of aphids per leaf.
Many wild potato species are highly resistant to aphids [91]
.
Yet only limited use has been made of wild potato species
in developing insect-resistant cultivars [91]
. Various
Agrobacterium-mediated transformations have produced
potato lines expressing genes that confer pathogen-derived
resistance to viruses. Transgenic lines have been developed
that are highly resistant, but not immune, to infection by
PLRV, PVY, and PVX [92]
. While aphids can still acquire
virus from low titre plants, efficiency of transmission is
greatly reduced [64]
. Transgenic cultivars were released in

the USA that expressed the Leptinotarsa decemlineata
(Colorado beetle) specific toxin Bacillus thuringiensis var.
tenebrionis (Bt) combined with PLRV replicase [80]
other
cultivars expressed Bt and PVY coat protein. This
technology of Agrobacterium-mediated transformation was
far more effective than any presently used tactic, but these
cultivars have been withdrawn because of concerns over a
public backlash against genetically modified food crop.
Another most important genetic approach is to knockdown
the genes responsible for aphid infestation is RNAi method.
RNAi is known to be an effective way of gene silencing [93]
in various organisms including plants [94]
and insects [95]
.
The probability of using RNAi to kill the target insects by
down regulating essential gene functions has been
appreciated for several years [96]
. One of need to explore
RNAi technology for growing aphid resistance crop plants
is to identify aphid genes which are significantly important
for survival and colonization of the insect nymphs on host
plants. cDNA sequences of genes or identified ESTs in
mustard aphids are still limited in available databases.
Additionally, the recognition of genes involved in early
stage of infestation and colonization process by aphid
insects will give the potential target for RNAi mediated
down regulation and resistance. Targeted inactivation of
indispensable aphid genes will lead to either retarded
breeding cycle or induce lethality to aphids, which could be
utilised as a strategy to breed aphid resistant crop cultivars.
There are limited reports where RNAi has been strived to
develop insect resistance.
BIOCHEMICAL RESPONSE DURING APHID
INFESTATION
Plants respond through various morphological,
biochemicals, and molecular mechanisms to counter the
effects of aphid attack. The biochemical mechanisms of
defense against the aphids are wide-ranging, highly
dynamic, and are mediated both by direct and indirect
defenses. The defensive compounds are either produced
constitutively or in response to plant damage, and affect
feeding, growth, and survival of aphids. In addition, plants
also release volatile organic compounds that attract the
natural enemies of the aphids. These strategies may act
independently or in conjunction with each other. Although,
the understanding of these defensive mechanisms is still
restricted. The level of redox enzymes CAT, APX, and
SOD, involved in ROS homeostasis in defense signaling,
and several defense enzymes viz. POD, PPO, and PAL,
remained high in infested plants [97]
. Superoxide dismutase
(SOD) protects the cell from oxidation due to reactive
oxygen species (ROS) which interferes with the cellular
metabolism [98-99]
.
CONCLUSIONS
In India, population is increasing day by day, to feed all
these increased population we need to increase the yield per
unit area as well as improve the resources used for
efficiency of crops. 70% of Indian Mustard is cultivated in
India is effected by Aphids. Losses in production due to
biotic or abiotic factors are the major concerns.
Traditionally, farmers are using chemicals to deal with
aphids in Brassica fields. Moreover, in recent days,
knowledge of plant-pathogen interaction, advanced
breeding techniques including agricultural biotechnology
are aided for resistance in response to aphid infestation in
many crops like soybean, tomato, potato, brinjal, legumes,
wheat, maize, melon, cotton, rice, barley, papaya and in
rapeseed mustard. These approaches are much efficiently
used in worldwide. QTLs is one of the most powerful
approaches of molecular plant breeding used in genetic
crop improvement. In QTL, important traits and genes
associated with plant resistance to aphids are identified and
incorporated into new cultivars using agriculture crop
improvements tools. In this present review, we have tried to
provide some of the innovative methods in response to
aphid infestation. By considering the Genetic control,
Chemical control and Biological control on this
economically important crop, it is expected that the
increased production trend can be achieved in a near future.
ACKNOWLEDGMENT
The authors are thankful to the Noida International
University, India.
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Jain V, Tiwari A: Innovative Approaches towards Aphid Resistance Prevention in Brassica Crops. Int. J. Life. Sci. Scienti.
Res., 2017; 3(4):1230-1237. DOI:10.21276/ijlssr.2017.3.4.21
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