Introduction
The brown planthopper (BPH), Nilaparvata lugens (Stål) (Homoptera:
Delphacidae)) has been known as a major
pest of rice cultivated in Asian countries.
In most cases, large scale infestation of BPH may cause
significant loss of rice production. Moreover, BPH also acts as vector for some viruses of diseases in rice such as stunt
virus and ragged stunt virus (Nagadhara et al. 2004), which may cause more severe losses in rice
yield. BPH infects plants by
sucking the phloem sap and causes physiological
stress or hopper burn. Development of resistance
rice lines against
BPH has been the ideal option for economic and effective management of BPH (Jena and Kim 2010). It is also safe for people and the environment
and compatible with other current pest
management strategies. Therefore, there is a need to prevent huge
losses of rice yield by developing
resistant rice lines
through gene transfer technology as applied previously by Maqbool et
al. (2001). The
application of gene transfer technology has been recognized
as an economical and environmentally
sustainable approach which may reduce the application
of insecticides.
By using agrobacterium-mediated
gene transfer, DB1 gene (Dioscorea batatas tuber lectin 1), which is isolated
from yam tuber and is known as mannose-binding lectin family with 12-kDa sub-units, has been inserted to
develop rice plant resistance to
sup-sucking insects (Toriyama 2010). Fifty eight percent of DB1 nucleotide has homology with snowdrop lectin Gna, therefore classifying DB1 into Gna-related lectin family (Gaidamashvili et al. 2004). Moreover, this
gene has been shown to be effective
against Helicoverpa armigera (Hübner) (Ohizumi et al. 2009) and
Myzus persicae (Sulzer) (Kato et al. 2010) in Japan.
Feeding 0.01% (w/v) DB1 corn to
larvae of H. armigera was proven to reduce the larva population that survived
until adulthood to 33% (Ohizumi et al.
2009). In another case, feeding 0.01 and 0.1%
(w/v) transgenic tobacco extract with DB1 insertion decreased the surviving M.
persicae
(Sulzer) population to 60% (Kato et al. 2010). These results show the
effectiveness of DB1 transgene that can
be applied to develop transgenic rice plants resistant to sap-sucking
insects. A transgenic rice cultivar (cv.
Taichung 65) expressing DB1 transgene, driven by sucrose-synthase-1 (RSs1) promoter, has
been successfully developed and a DB1 homozygous line directed by RSs1 promoter has been selected. In the leaf of this plant, DB1 accumulated at a level of 0.33% of total soluble protein
(Toriyama 2010). Currently there is no report informing the resistance of DB1 transgenic rice line to BPH especially to biotype 2 and 3 from
Indonesia which is currently the most destructive pest of rice. The objective of this research was
to determine the level of
resistance of DB1 transgenic rice against those two biotypes of BPH. Testing for resistance was conducted for crop damage, BPH preference for
laying eggs (oviposition), honey dew excretion
and population build-up. Two colonies of BPH were used, i.e., biotype 2 (Sukamandi) and biotype 3 (North Sumatera) which are very abundance in certain rice-growing areas of the country.
Materials and Methods
Plant materials and BPH colony preparation
Transgenic Taichung-65 inserted with DB1 transgene was tested for resistance
to BPH together with eight other
genotypes, i.e.,
Taichung-65, PTB-33, Rathu Heenati, IR-64,
IR-42, Babawee, Ciherang, and Cisadane, in a biosafety containment of Indonesia Centre for Agricultural
Biotechnology and Genetic Resources Research and Development (ICABIOGRAD), Bogor. Two colonies of BPH were
used as infection source. The first, biotype 2 (derived from Sukamandi) was obtained
from The Indonesian Centre for Rice Research (ICRR) and
the second one was biotype 3 (colony from North Sumatera) which was collected
from Experimental Station of ICRR,
Muara Bogor, Indonesia. Protocol for BPH rearing followed Matsumura et al. (2017) with
modification. BPH adults used in the study were originally collected from a
field population in Sukamandi and North Sumatera. For mass-rearing BPH, the
nylon screen cage by a small plastic jar was used. About 40–50 adult females of
BPH were reared in inside the nylon screen covered by small plastic jar (15 x
15 x 20 cm) containing rice plants cv. Ciherang for biotype 2, meanwhile rice
cv. IR-42 for biotype 3 and they were kept at room temperature (26–28°C). After
48 h, adult females were taken out from the jar using an aspirator and infested
on TN1 rice line. The colonies were continually fed with ≥ 30-days old
rice plants (TN1 host plant). Seven to ten days after infestation, the eggs
were hatched and these BPH nymphal were used for further experiments.
Testing for resistance of rice
lines
to BPH
Nine rice genotypes, including one transgenic line (DB1),
three resistant (PTB 33, Rathu Heenathi, Babawee), three susceptible (IR 42, Ciherang and Cisadane) and IR 64 as a moderate
resistant, were
subjected to resistance
assessment against
BPH. The experiments were arranged in a completely randomized design with three
replications. The design of experiment was also conducted for resistance to BPH, BPH preference for laying
eggs (oviposition), honey dew measurement and population build-up.
Resistance test to BPH
To evaluate resistance to BPH in rice genotypes, 20
seeds of each rice genotype were grown in a row of
plastic box under greenhouse conditions
(room temperature and natural lightly) (Matsumura et al. 2017). BPH infestation
was carried out at the 2.5 leaf stage with
second to third-instar BPH nymphs at a density of 3 nymphs per plant. After the dying the check plants (cv. Taichung 65 and IR 42), the seedlings were scored according to the Standard Evaluation System for Rice (IRRI 2013).
Honeydew test (feeding activity test)
Six-week-old rice seedlings were
enclosed individually in parafilm plastic boxes with filter paper at the bottom. The filter paper was measured before and
after treatment to identify the amount of honeydew
excreted by BPH. Three couples of adult BPH were infested and after 24 h, the BPH and filter papers were taken out of the box.
The filter paper was sprayed with 0.01% solution of ninhydrin in acetone and then dried at 80°C for 24 h.
Honeydew excretion was
observed by measuring the difference in weight of the paper
filter before and after treatment.
Ovipositional test
To measure the number of eggs produced by BPH, ten-day-old
plants from each rice genotype were covered individually in parafilm plastic
boxes followed KARC/NARO protocol
(Matsumura et al. 2017).
Three BPH gravid females were transferred to each
cultivar and permitted to oviposit on the host
plant. After seven days, oviposition was
observed by counting the number of eggs on
each cultivar (Matsumura et al. 2017).
Population build-up of BPH
Six-week-old of rice seedlings
were
enclosed individually in parafilm plastic box covered by mylar plastic sheets, 70 cm high and 12.5 cm in diameter and provided with three
couples of adult BPH. Three days
after infestation, the three couples of BPH were removed
from the box and the observation started once 70% of nymphs had metamorphosed to adults.
Population build-up data were obtained by counting the number
of BPH in each cultivar after every two days until the susceptible cv. IR 42
and Taichung 65 died.
Population build-up of the biotype 3 was
recorded from 1st (two days after 70% of nymphs
metamorphosed into adult insects) to 7th observation (14 days after
70% of nymphs metamorphosed into adult
insects).
Data analyses
Resistance
test to BPH was scored according to the Standard Evaluation System for Rice
(IRRI 2013). BPH preference for laying eggs (oviposition), honeydew measurement
and population build-up were analyzed using
univariate by analysis of variance (ANOVA) and post hoc analysis by Duncan’s Multiple Range Test (DMRT) and it was performed with the aid of SPSS v. 17.0
software.
Results
Resistance test to BPH
Based on the scale from the Standard Evaluation System for
rice (IRRI
2013), the
transgenic rice line (Taichung 65 DB1)
had moderate resistance to biotype 2 (Tables 1, 2), but was highly susceptible to biotype 3
(Table 3). These results indicated that DB1 gene has no horizontal resistance as we expected it and is thus considered less effective against Indonesian BPH biotypes. However, DB1 transgene
improved resistance against BPH of the original genotype by one level, from
susceptible (Taichung 65, original genotype) to moderately resistant (Taichung
65 DB1) to biotype 2. PTB-33
and Rathu Heenati had better resistance to both BPH biotypes
(Table 2 and 3). Meanwhile the
highly susceptible was found in cultivars IR-42, Taichung 65-DB1 and Taichung 65
to biotype 3 (Table 3).
Honeydew excretion test
There
were no
significant differences in the amount of honeydew excreted by BPH biotype 2 and biotype 3 among genotypes tested (Table 4). However, the faeces amount
of BPH biotype 3 was
significantly higher on cv. IR-42 %20125-130_files/image002.png)
Fig. 1: Number of eggs of BPH biotype 2 at 7 days after infestation on some rice genotypes. The same letters were not significantly different according to Duncan’s Multiple Range Test at 0.05
probability
%20125-130_files/image004.png)
Fig. 2: Number of eggs of BPH biotype 3 at 7
days after infestation on some rice genotypes.
The same letters were not significantly different according
to Duncan’s Multiple Range Test at 0.05 probability
than on other genotypes (Table 4).
Ovipositional response
There was a significant difference in laying eggs
both colonies as revealed in both Fig. 1–2. Almost
all tested cultivars were chosen by BPH females of biotype 2 for
laying their eggs, whereas Taichung-65 DB1, PTB-33, Babawee, IR-64 and IR-42 were much preferred
by biotype 3. Transgenic DB1 line was
significantly preferred by biotype 2 for laying eggs (Fig. 1).
Taichung-65 DB1 showed significant differences on the
number of eggs from cv. IR-64 for biotype 2,
but no differences for biotype 3. Fig. 1 and 2 also indicate no significant differences in egg
number among high resistant genotype
(PTB-33), resistant (Taichung-65 DB1, Rathu Heenati,
Babawee, IR-64)
and susceptible genotypes
(IR-42 and Cisadane).
Population
build-up of biotype 3 (Colony North Sumatera) of BPH
Population development of the biotype 3 was recorded
from 1st (two days after 70% of nymphs metamorphosed into adult
insects) to 7th observation (14 days after 70% of nymphs
metamorphosed into adult insects). There were no significant differences in total number of BPH population among nine genotypes at 1st observation (two days after 70% of nymphs metamorphosed
into adult), whereas significant different in total number of BPH were obtained
at 2nd observation (four days after 70%
of nymphs metamorphosed) to 7th observation (the last observation) (Table 5). The
population of BPH on PTB-33 was the lowest. Compared to other
cultivars, the population build up of BPH on PTB-33 was significantly
lower at 1st to 7th
observation.
Discussion
Table 1: Scoring BPH resistance levels
|
Score |
Symptoms |
Resistance Level |
|
0 |
No injury |
Highly resistant |
|
1 |
Slight yellowing of a few plants |
Resistant |
|
3 |
Leaves partially yellow but with no hopper
burn |
Moderately resistant |
|
5 |
Leaves with pronounced yellowing and
stunting or wilting and 10-25% of plants with hopper burn, remaining plants
severely stunted |
Moderately susceptible |
|
7 |
More than half the plants wilting or with
hopper burn, remaining plants severely stunted |
Susceptible |
|
9 |
All plants dead |
Highly susceptible |
Note: Standard Evaluation System
for Rice (SES, IRRI 2013)
Table 2:
Resistance level of rice genotypes after infested by Biotype 2 (colony Sukamandi)
|
No. |
Genotype |
Damage level |
Resistance level |
|
1 |
PTB-33 |
0.70 |
Highly Resistant |
|
2 |
Rathu Heenati |
1.58 |
Resistant |
|
3 |
Babawee |
1.68 |
Resistant |
|
4 |
IR-64 |
4.00 |
Moderately Resistant |
|
5 |
Cisadane |
4.20 |
Moderately Resistant |
|
6 |
Taichung 65 DB1 (Transgenic) |
4.82 |
Moderately Resistant |
|
7 |
Ciherang |
5.27 |
Moderately Susceptible |
|
8 |
IR-42 |
5.43 |
Moderately Susceptible |
|
9 |
Taichung 65
(non-transgenic) |
7.70 |
Susceptible |
Note: - Damage level
on scale of 1-9 (IRRI 2013) were
observed after susceptible cultivars died
- Nine
rice cultivars were planted in lined plastic tray, with 20 plants per line, repeated 3 times,
and infested by 3 of 3rd
instar of BPH
Table
3: Resistance
level of rice cultivars after infested by Biotype 3 (colony north Sumatera)
|
No. |
Cultivars |
Damage level |
Resistance level |
|
1 |
PTB-33 |
0.00 |
Highly Resistant |
|
2 |
Ratu Heenati |
0.37 |
Highly Resistant |
|
3 |
IR-64 |
3.10 |
Moderately Resistant |
|
4 |
Ciherang |
3.80 |
Moderately Resistant |
|
5 |
Cisadane |
4.10 |
Moderately Resistant |
|
6 |
Babawee |
5.98 |
Moderately Susceptible |
|
7 |
IR-42 |
9.00 |
Highly Susceptible |
|
8 |
Taichung 65 DB1 (Transgenic) |
9.00 |
Highly Susceptible |
|
9 |
Taichung 65 (non-
Transgenic) |
9.00 |
Highly Susceptible |
Note: - Damage level
on scale of 1-9 (IRRI 2013) were
observed after susceptible cultivars died
- Nine
rice cultivars were planted in lined plastic tray, with 20 plants per line, repeated 3 times,
and infested by 3 of 3rd
instar of BPH
The present study
indicated the resistance of transgenic DB1 and other genotypes to BPH biotype 2
and 3 from Indonesia i.e., Sukamandi, West Java for biotype 2 and North
Sumatra for biotype 3. Resistance reaction of transgenic rice line (Taichung 65
DB1) was moderate to biotype 2, but highly susceptible to biotype 3. These
results indicated that DB1 gene has no horizontal resistance as we expected previously and is thus considered less effective against Indonesian BPH
biotypes. However, DB1 transgene
improved resistance level against BPH of the original genotype by one level,
from susceptible (Taichung 65, original genotype) to moderately resistant (Taichung
65 DB1) to biotype 2. PTB-33 and Rathu Heenati had better
resistance to both BPH biotypes (Table 2 and 3).
Overall
results indicate the
possibility of obtaining genotypes
with high resistance to
BPH by using PTB-33 and Rathu Heenati as donor parents through
common breeding program
besides using a
transfer gene
method (as in the DB1 case) although it may take several
years to be accomplished. PTB-33 and Rathu Heenati have been known
to be highly
resistant to various biotypes of BPH, possibly because both cultivars possessed some BPH resistance genes such as Bph3, which is located on chromosome
6 (Jairin et al.
2007a), Bph2 and Bph3 (Santhanalakshmi et al. 2010) and other
resistance genes against BPH. Moreover (Jairin et al. 2007b), clarified
that Bph3 of Rathu Heenati and Bph3
of PTB-33 are linked with Bph4 of Babawee. Information
concerning the
existence of DNA markers (SSR
markers)
which linked
with resistance genes in both cultivars (Jairin et
al. 2007b; Santhanalakshmi et al. 2010) would be beneficial for performing marker-assisted
backcrossing programs or gene pyramiding (combining several resistant genes into
one genotype) to develop cultivars with durable resistance against
BPH.
The feeding response of BPH is assessed through
amount of honeydew, its related to resistance or susceptibility of the
genotype. This indicates that an interaction between BPH and rice plant exists to establish its host
plant. Ling and
Weilin (2016) have demonstrated that biochemical mechanisms rice resistance to
BPH. Table 4: Test for measuring amount of honeydew
excreted by BPH biotype 2 and biotype3 in nine rice genotypes
|
No. |
Genotype |
Feces
amount (g) |
|||
|
Biotype
2 |
Biotype
3 |
||||
|
1 |
Taichung-65 DB1 (Transgenic) |
0.0217 |
a |
0.5710 |
a |
|
2 |
Taichung 65 |
0.0311 |
a |
0.5786 |
a |
|
3 |
PTB 33 |
0.0386 |
a |
0.5484 |
a |
|
4 |
Rathu Heenati |
0.0001 |
a |
0.5608 |
a |
|
5 |
Babawee |
0.0008 |
a |
0.5674 |
a |
|
6 |
IR 64 |
0.0000 |
a |
0.5819 |
a |
|
7 |
IR 42 |
0.0000 |
a |
0.6888 |
b |
|
8 |
Ciherang |
0.0207 |
a |
0.5911 |
a |
|
9 |
Cisadane |
0.0064 |
a |
0.5515 |
a |
Note: The same letters were not
significantly different according to Duncan’s Multiple Range Test at 0.05
probability
Table
5: Number of BPH
of biotype 3 on some rice genotypes
|
No |
Genotypes |
Observation day |
|||||||||||||
|
1 |
2 |
3 |
4 |
5 |
6 |
7 |
|||||||||
|
1 |
Taichung-65 DB1 (Transgenic) |
1.0 |
a |
0.3 |
a |
11.0 |
ab |
17.3 |
bcd |
44.3 |
b |
50.0 |
b |
57.3 |
b |
|
2 |
Taichung 65 |
0.0 |
a |
1.7 |
ab |
7.0 |
ab |
11.0 |
abc |
44.7 |
b |
58.7 |
b |
71.7 |
b |
|
3 |
PTB 33 |
1.0 |
a |
0.0 |
a |
1.0 |
a |
2.3 |
a |
2.7 |
a |
3.3 |
a |
1.0 |
a |
|
4 |
Rathu Heenati |
2.0 |
a |
9.0 |
ab |
23.3 |
b |
25.7 |
cd |
58.7 |
b |
66.0 |
b |
97.0 |
b |
|
5 |
Babawee |
7.0 |
a |
56.7 |
c |
83.3 |
c |
86.0 |
d |
117.7 |
b |
131.0 |
b |
142.7 |
b |
|
6 |
IR 64 |
0.7 |
a |
2.7 |
ab |
4.3 |
ab |
5.7 |
ab |
38.3 |
a |
41.7 |
a |
57.0 |
b |
|
7 |
IR 42 |
5.3 |
a |
4.0 |
ab |
21.7 |
ab |
28.0 |
bcd |
54.0 |
b |
62.0 |
b |
117.3 |
b |
|
8 |
Ciherang |
1.3 |
a |
0.0 |
a |
21.0 |
b |
26.7 |
cd |
105.3 |
b |
131.3 |
b |
139.7 |
b |
|
9 |
Cisadane |
0.7 |
a |
18.3 |
b |
31.0 |
b |
35.0 |
cd |
47.7 |
b |
61.7 |
b |
60.3 |
b |
Note: Numbers followed by
the same letter in
the same column were not significantly different according to
Duncan’s Multiple Range Test at 0.05 probability level. The observations were conducted from two
days after 70% of nymphs
metamorphosed into imago (1st observation) to 14 days later (7th
observation)
According
to Manuwoto and Adijuwana (1991) BPH
feeding activities
are performed through several stages i.e., (i)
recognizing and orientating toward the host
plant, (ii) tasting the food, (iii) assuring the food and (iv) sceasing to eat. Each stage is implemented
by insects when the plant releases a specific signal or stimulus that they receive, and hence the plant does not provide a
barrier that could inhibit BPH feeding activities. These conditions might
establish a plant-pest interaction. However, Cheng et al.
(2013) stated that feeding behaviors of BPH are complicated in that they are
mainly related to host resistance, indicating a gene for gene relationship.
Further molecular studies revealed that plant hormones such as salicylic acid
and jasmonate/ethylene (Wang et al. 2020), Ca+2 ion, mitogen-activated protein kinases (MAPKs) (Nanda
et al. 2018) and OsRac1 play
important roles in the immune response of rice to BPH (Cheng et al.
2013).
BPH
ovipositional response as indicated by the number of eggs. No
significant differences among the highly resistant genotype (PTB-33), resistant (Taichung-65 DB1, Rathu Heenati, Babawee, IR-64) and
susceptible genotypes (IR-42 and Cisadane; Fig. 1 and 2) on the number of eggs for biotype 2.
These results indicate
that the other factor may cause BPH interested in laying eggs, although in highly
resistance cultivars,
BPH did not suck the plant sap excessively (Pathak and Khan 1994; Rashid et
al. 2016). It was considered that laying eggs and feeding (sucking the
plant sap) as different activity and no linear relationship between these two
activities.
However, Horgan et al. (2018) found that PTB 33 become unsuitable for
egg laying after the plant reaches maturity, indicating inability of BPH to
insert eggs into maturing tissues of the plant. Furthermore, there are several stages of BPH in laying eggs on the plant, i.e., (i) recognition and orientation to
the host plant, (ii) orientation in certain parts of the host plant,
(iii) and then laying
eggs (Cheng et
al. 2013). Each stage is implemented by insects if plants
released a specific signal or stimulus that was received by insects, and plant do not provide
a barrier that could inhibit insects in laying the eggs (Kumari and Kaushik 2016).
Addressing
no decrease of BPH populations on DB1 transgenic rice line from the 3rd
to the last observation, the number tended to increase (Table 5). These results reveal
that the DB1 transgene
is considered less effective against
BPH biotype 3 than
resistant genes on PTB 33. These results also indicate that there are BPH preferences to increase number
of BPH population on preferred cultivars. In addition, there were mechanisms that possible to
inhibit growing population
of BPH as
shown on
PTB 33.
A
significant low number of BPH populations at 1st to 7th
observation on PTB 33 could be attributed by genetic composition of the plant. The resistance
trait of PTB 33 is controlled by one major gene with some minor genes or determined by
quantitative inheritance (Nugaliyadde et al. 2007). In addition, Sarao and Bentur (2018) found that PTB 33
has lower nymphal survival compared to other genotypes i.e., Rathu
Heenati and Sinnasivappu. The authors also reported that nymphal emergence,
nymphal survival percentage, and proportion of brachypterous females have a significant
linear relationship to damage score and rice resistance to BPH. Nymphal
survival is the most direct way of host plant resistance and its effect on pest
population build-up.
We found that DB1
transgene improved resistance by one level against BPH biotype 2 from
susceptible to moderately resistant. There was a difference between the feeding
behavior of BPH and its preference for laying eggs. DB1 transgene is less effective against both biotypes (2 and 3).
Two genotypes, i.e., PTB-33 and Rathu Heenati were highly resistant to
these two colonies and may be a promising source of BPH resistant genes against some ever-growing biotypes of BPH. Although DB1
gene improve one resistant level, DB1 transgenic rice line offers
environmentally friendly approach for protecting rice from BPH attack.
Pyramiding this gene with other genes would be beneficial for developing BPH
resistant rice.
Acknowledgements
The authors wish to
thank Ms. Nuri K. Willis, Ms. Ristiani Amalia and Ms. Junengsih for
helping in
collecting data and to Universitas Padjadjaran for partly funding the research.
Author Contributions
NC, GIP and
DD planned the experiments, GIP, SS, DD and NC interpreted the results, GIP, KT
and NC made the write up, DD and SS statistically analyzed the data and made
illustrations, KT provided genetic materials.
Conflicts of Interest
All authors
declare no conflicts of interest.
Data Availability
Data
presented in this paper will be available on a fair request to the
corresponding author.
Ethics Approval
Not
applicable in this paper.
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