Protein J (2012) 31:439446
DOI 10.1007/s10930-012-9423-8
Receptors of Garlic (Allium sativum) Lectins and Their Role
in Insecticidal Action
Santosh K. Upadhyay Pradhyumna K. Singh
Published online: 24 May 2012
Springer Science+Business Media, LLC 2012
Abstract Garlic (Allium sativum) lectins are promising
candidate molecules for the protection against chewing
(lepidopteran) as well as sap sucking (homopteran) insect
pests. Molecular mechanism of toxicity and interaction of
lectins with midgut receptor proteins has been described in
many reports. Lectins show its effect right from sensory
receptors of mouth parts by disrupting the membrane
integrity and food detection ability. Subsequently, enter
into the gut lumen and interact with midgut glycosylated
proteins like alkaline phosphatase (ALP), aminopeptidase-
N (APN), cadherin-like proteins, polycalins, sucrase,
symbionin and others. These proteins play critical role in
life cycle of insect directly or indirectly. Lectins interfere
with the activity of these proteins and causes physiological
disorders leading to the death of insects. Lectins further
transported across the insect gut, accumulated in various
body parts (like haemolymph and ovary) and interact with
intracellular proteins like symbionin and cytochrome p450.
Binding with cytochrome p450 (which involve in ecdysone
synthesis) might interfere in the development of insects,
which results in growth retardation and pre-mature death.
Keywords Garlic lectins  Glycosylated  Homopteran 
Insect  Lepidopteran
Abbreviations
ALP Alkaline Phosphatase
APN Aminopeptidase-N
ASA Allium sativum agglutinin
S. K. Upadhyay  P. K. Singh (&)
CSIR-National Botanical Research Institute, Council
of Scientific and Industrial Research, Rana Pratap Marg,
Lucknow, UP 226001, India
e-mail: pradhyumnasingh@hotmail.com
ASAL Allium sativum leaf agglutinin
GNA Galanthus nivalis agglutinin
BBMV Brush border membrane vesicles
1 Introduction
Insecticidal d-endotoxins of Bacillus thuringiensis (Bt),
plant derived defence related proteins and siRNA molecules
provide protection against insect pests and are alternatives to
chemical pesticides [4, 64, 81, 83, 86]. Lectins are one of the
plant derived insecticidal proteins. These are also known as
agglutinins. Lectins contain at least one non-catalytic
domain which binds reversibly to specific monosaccharides
or oligosaccharides. Lectins are isolated from various plant
tissues and other organisms with specific carbohydrate
specificity. They have been categorized on the basis of sugar
specificity [27, 32, 40, 65, 71, 80, 86, 92, 94, 97].
Among the plant derived lectins, mannose-binding lec-
tins isolated from garlic bulb [95] and leaf [81] have gained
attention in recent decades. These are toxic to both chew-
ing (lepidopteran) and sap-sucking (homopteran) type
insect pests and considered to be safe in principle due to the
edible source of origin [5, 8, 23, 24, 59, 77, 78, 81]. Garlic
lectins also show rapid agglutination of rabbit erythrocytes
[8, 81] and inhibitory effect against HIV1 and HIV2
induced cytopathicity in MT-4 cells [8].
2 Structure of Garlic Lectins
Garlic lectins are dimeric proteins. Garlic bulb lectins are
either heterodimer (ASAI) of *11.5 and *12.5 kDa subunits
or homodimer (ASAII) of *12 kDa subunits [95]. However,
garlic leaf lectin is a homodimer of *12 kDa subunits. These
123
440
Dysdercus
cingulatus
Aphis gossypii
Nephottix
Nilaparvata lugens
Allium sativum agglutinin
Sogatella furcifera
Aphis craccivora
Tetranychus kanzawai
Fig. 1 Insects, which are sensitive to garlic lectins. Bioassay was performed with protein preparations from native (garlic bulb and leaf) and
recombinant source (expressed in E. coli, yeast and transgenic plants)
are structurally and evolutionarily related to Galanthus nivalis
agglutinin (GNA) [81, 95]. Primary structures of both bulb
and leaf lectins of garlic are more than 80 % similar [15, 81].
Crystal structure of dimeric garlic bulb lectin shows b-prism II
fold structure, similar to GNA. It contains three 4-stranded
anti-parallel b-sheets, arranged on three surfaces of a trian-
gular prism, forming a 12-stranded b-barrel and inter-related
by an approximate threefold internal symmetry. This is con-
sistent with the tandem sequence repeats in primary structure,
suggesting domain triplication in the gene during evolution
[15]. Unlike the snowdrop lectin which exists as a tetramer,
garlic lectins always exist as dimer, despite of high degree of
sequence similarity between them. Each subunit of garlic
lectins contains three highly conserved mannose binding sites,
QXDXNXVXY [15, 6870].
3 Garlic Lectins as Bio-pesticides
Lectins are one of the most promising family of proteins
for the development of insect resistant transgenic plants
123
S. K. Upadhyay, P. K. Singh
Spodoptera litura
Helicoverpa armigera
Acyrthosiphon
pisum
Myzus persicae
Myzus nicotianae
Lypaphis erysimi
[16, 48, 55, 62, 78, 88]. These are toxic to a number of
insect pests of order lepidoptera and homoptera [8, 77, 78,
81]. The insecticidal properties of garlic lectins have been
explored by the protein preparations from native source
(i.e. bulb and leaves), recombinant source (i.e. E. coli and
yeast) and in transgenic plants [29, 30, 77, 85]. Several
transgenic plants expressing garlic lectin have shown
resistance against different insect pests (Fig. 1, Table 1).
Transgenic tobacco expressing garlic lectin offers resis-
tance against Spodoptera litura [77] and Myzus persicae
[23], transgenic rice against brown plant hopper, green
leafhopper and white backed plant hopper [10, 105] and
transgenic chickpea against Aphis craccivora [14].
Although, the potential of garlic lectins for the insect
control has been established, d-endotoxins of Bt are more
toxic against lepidopteran pests. Nevertheless, none of the
d-endotoxins have shown insecticidal activity against
homopteran pests [22, 99]. Therefore, pest control strate-
gies in future would be based on the pyramiding of two
toxins for the effective control of both types of insects. It
has been demonstrated that garlic leaf lectin and Cry1Ac
Receptors of Garlic 441

Table 1 Insecticidal activity of garlic lectins Table 2 Putative receptors of garlic lectins in midgut of different
insects
Insect Method of toxicity References
assay Insect Size of Identification References
putative
Helicoverpa armigera Synthetic diet [5, 85] receptor
Spodoptera littoralis Transgenic tobacco [77, 85] (kDa)
Nilaparvata lugens Transgenic rice [10, 105]
Helicoverpa 113 Midgut [84]
(brown plant hopper)
armigera aminopeptidase
Nephotettix spp. Synthetic died [54] APN2
(green leafhopper)
Helicoverpa 104 AGAP009726-PA, [84]
Nephotettix spp. Transgenic rice [10, 105] armigera partial (Cadherin-N
(green leafhopper) protein)
Sogatella furcifera Transgenic rice [10, 105] Helicoverpa 102 Polycalin [84]
(White backed plant armigera
hopper)
Helicoverpa 82 Polycalin [84]
Lypaphis erysimi Synthetic diet [8, 54] armigera
(Aphid)
Helicoverpa 59 Alkaline phosphatase [84]
Lipaphis erysimi Transgenic Indian [24] armigera 2
mustard
Helicoverpa 59 Alkaline phosphatase [84]
Myzus persicae Transgenic tobacco [23] armigera 1
(peach potato Aphid)
Helicoverpa 57 Cytochrome P450 [84]
Myzus nicotianae Transgenic Arabidopsis [77] armigera CYP315A1
(Tobacco aphid) thaliana
Acyrthosiphon 110 Alanyl [30]
Aphis craccivora Synthetic died [54] pisum aminopeptidase N
(cow-Pea aphid)
Acyrthosiphon 66 Sucrase [30]
Aphis craccivora Transgenic chickpea [14] pisum
(cow-Pea aphid)
Lipaphis 57 Symbionin from [9]
Dysdercus cingulatus Synthetic diet [8] erysimi Buchnera
(red cotton bug) aphidicola
Acyrthosiphon pisum Synthetic diet [30] (Q93T48)
(pea aphid) Lypaphis 55 NI [8]
erysimi
Dysdercus sp. 45 NI [8]
Aphis 66 NI [54]
d-endotoxins can be used together without interfering the craccivora
activity of each other [88]. Nephotettix Four proteins NI [78]
virescens from 30 to
66 kDa
M. persicae 40, 66 and NI [23]
4 Putative Receptors of Garlic Lectins in the Midgut 70 kDa
of Insects NI not identified

Binding of toxins to receptors in the insect gut is an

important step in toxicity. This also determines the speci-
ficity of a toxin to insect. Garlic lectins bind to several
proteins (cadherin-like proteins, glycosyl phosphatidyl-
inositol (GPI)-anchored aminopeptidase-N (APN), GPI-
anchored alkaline phosphatase (ALP), polycalins, sucrase,
cytochrome P450, symbionin and others) in the midgut
of insects (Table 2) through glycan mediated interactions
[9, 54, 84]. Most of these receptor proteins are membrane
bound enzymes. Some of them like ALP, APN and poly-
calins are earlier reported as receptors of d-endotoxins.
This is due to the lectin like structure of third domain of d-
endotoxins, which binds to specific sugar residues on
receptors [12, 79].
4.1 Cadherin like Protein
Cadherins belong to diverse superfamily of proteins with a
variety of functions, like cell adhesion, migration, cyto-
skeletal organization and morphogenesis [3, 36]. Cadherins
generally possess 534 calcium binding domains or cad-
herin repeats [3, 21, 61] and/or laminin, epidermal growth
factor-like repeats [60] and mucin domains [34]. Expres-
sion of cadherins is highly regulated temporally as well as
spatially and sometimes limited or unique to a particular
cell type. These are glycosylated proteins and usually
anchored on membranes by single trans-membrane
domain. But cadherins with seven-trans-membrane

123
442
domains [89] or GPI-anchor has also been reported [98].
Cadherins are primarily characterized as receptor of
d-endotoxins [35, 43, 90] which consisted of a signal
peptide, 12 cadherin repeats, a membrane proximal extra-
cellular domain, a transmembrane domain and a small
cytoplasmic domain [91]. Similar domain organization has
been reported for cadherin receptors of d-endotoxins in
insects [64]. However, garlic leaf lectin interact wih BM1
type of cadherin in H. armigera [84] which is different
from the d-endotoxin specific cadherins. BM1 cadherin
consists of additional leminin G and EGF domains with
cadherin repeats.
4.2 Glycosylphosphatidyl-Inositol (GPI)-Anchored
Aminopeptidase-N (APN)
APNs are also a family of proteins which cleave peptide
bonds from the N-terminus of proteins to release amino
acids. These are known for variety of functions in different
species and work along with endopeptidases and carb-
oxypeptidases for proteins digestion in insect gut [101].
These belong to the gluc-zincins subfamily of zinc binding
metalloprotease/peptidase superfamily [41]. Enzymes of
this family contain a zincin motif (HEXXH; where X can
be any amino acid) and a conserved glutamic acid residue
at 24th position downstream of the first histidine. First
glutamic acid residue is important for enzyme catalysis,
while histidines and last glutamic acid residue serve as zinc
ligands. The enzyme also consists of another highly con-
served GAMEN motif which forms the part of active site
[52]. APNs are about one thousand amino acid residues
long proteins and post translational modification in various
ways produces 70170 kDa mature proteins. Several forms
of APNs have been isolated and characterized. Presence of
N- or O-linked glycosylation has also been reported [2, 12,
49]. N-terminal signal peptide directs APNs to the outer
surface of the cytoplasmic membrane where they bind to
the membrane by GPI anchor [19, 50, 53, 82]. Angelucci
et al. [2] have reported seven APN genes in H. armigera,
four among them interact with Cry1Ac d-endotoxin. It is
noteworthy that APNs have been comprehensively studied
as receptors of d-endotoxins [2, 44, 49, 87].
Fitches et al. [30] observed the interaction of garlic bulb
lectin with the membrane bound alanyl aminopeptidase N
of Acyrthosiphon pisum. APN2 of H. armigera interacts
with garlic leaf lectin [84] which is well known receptor of
d-endotoxins. It is suspected that lectins inhibit the APN
activity, which results in toxicity. However, we observed
that the garlic leaf lectin does not inhibit the APN activity
[88]. Since the exact mechanism is not known, APNs are
expected to involve in the transport of garlic lectins to the
haemolymph, as observed for GNA [67].
123
S. K. Upadhyay, P. K. Singh
4.3 GPI-Anchored Alkaline Phosphatase (ALP)
ALPs are also a family of proteins and function as a
receptor of d-endotoxins in H. armigera [87], M. sexta
[58], H. virescens [45, 46, 51] and others. Glycan mediated
binding of ALPs to d-endotoxins has been demonstrated
[79]. Garlic leaf lectin also binds to ALP of H. armigera
[84] and inhibits the phophatase activity like Cry1Ac
[79, 88]. Inhibition in enzyme activity might play some
role in insecticidal activity. Like APNs, ALPs are also
expected to involve in internalization of lectin. Interference
in ALP activity in haemolymph or other tissue might also
contributed in toxicity.
4.4 Other Proteins
Garlic leaf lectin also interacts with polycalins which
consist of multiple lipocalin domains [84]. Mauchamp
et al. [57] isolated this protein for the first time from
Bombyx mori but now it is reported in other insects like H.
armigera also [2, 56]. Alternative splicing in the transcript
generates different form of polycalins which enhances their
diversity and binding specificities. These proteins generally
consist of signal peptide, GPI anchor attachment and sev-
eral potential sites for glycosylation. Some of the sequen-
ces of polycalins match with d-endotoxin binding proteins
[42, 64]. Polycalins have been reported as receptor of
Cry1Ac in H. armigera [2, 56].
Fitches et al. [30] reported the interaction of garlic bulb
lectin with sucrase in gut of aphid A. pisum. Gut sucrase is
involved in carbon nutrition and osmoregulation. It is
localized in the aphids distal midgut and mediates the
hydrolysis of sucrose into glucose and fructose [6, 17].
Most of the fructose and some glucose utilized in respira-
tion and anabolism [6]. Remaining glucose used in trans-
glucosidation via a gut transglucosidase activity and
incorporated into glucose-dominated oligosaccharides of
20 hexose units, which later on annulled in the aphids
honeydews [6, 76, 100]. The transglucosidation of glucose
reduces the osmotic pressure of the gut contents and hon-
eydew becomes isosmotic to the aphid body fluids [20, 26,
103]. A chemical inhibitor of sucrase decreases the mean
aphid survival to 2.8 days [47]. Binding of lectins might
interfere in sucrase activity, which results in toxicity. The
observation supports the acute toxicity of lectins to insects
at higher doses [29, 30].
Garlic leaf lectin also interacts with Cytochrome P450
(CYP315A1) in H. armigera [84]. Cytochrome P450 is a
member of highly conserved halloween gene family in
insects and involved in the biosynthesis of the insect
molting hormone, 20-hydroxyecdysone (20E) [33, 7274,
102]. Ecdysones play major role in life cycle (embryonic,
larval, pupal and adult development and reproduction) of
Receptors of Garlic
insects [75]. Cytochrome P450 is a cytosolic protein and
therefore cannot function as an extracellular receptor. It is
possible that lectins first accumulate into the haemolymph
and then interact with Cytochrome P450. This results delay
in larval development and premature death of insect.
Severe growth retardation has been reported in several
insects after lectin ingestion [85].
Banerjee et al. [9] reported symbionin (SymL) in Lipaphis
erysimi as a receptor of garlic leaf lectin. Buchnera aphidi-
cola, a bacterial endosymbiont of aphid encodes this protein
[1, 25, 106]. It is a glycoprotein and its carbohydrate moiety
plays critical role in binding to the lectin [9]. Symbionin is
found in haemolymph only and therefore cannot function as
receptor. Antibiotic treatment of pea aphids reduced the
amount of symbionin in heamolymph but do not change
sensitivity of the insect with garlic lectins [30]. Rice brown
plant hopper maintains yeast as its endosymbiont which does
not produce symbionin and yet sensitive to garlic lectins
[66]. These studies establish that the interaction with sym-
bionin is not necessary for the insecticidal activity of garlic
lectins, this might play some other role.
Several other proteins of various sizes have been
reported from different insects, which show interaction
with garlic lectins [8, 23, 78]. In-depth studies are required
to identify and characterize such proteins and elucidate
their contribution in the toxicity of garlic lectins to insects.
5 Role of Glycans in Receptors-Lectins Interaction
and Insecticidal Action
Lectins interact non-covalently with carbohydrate moieties
of glycosylated proteins and display high affinity and
specificity for their ligands. Glycan binding ability of lec-
tins has been established by several methods like inhibition
of agglutination, enzyme-linked lectin adsorbent assay,
surface plasmon resonance (SPR), isothermal titration
calorimetry and glycan array [7, 11, 18, 85]. X-ray dif-
fraction experiments, used for the three-dimensional
structures analysis of several plant lectins, have also con-
tributed in the study [15]. Co-crystallization of lectins has
given the information about their interactions with simple
and complex carbohydrate moities and enlightened the
amino acids residues involved in the interaction. Lectins
have been classified as glucose/mannose, N-acetylgluco-
samine, galactose/N-acetylgalactosamine and fucose-bind-
ing, according to their specificity. Van Damme et al. [93]
have constituted a new group of lectins which are isolated
from monocotyledonous plants and show very high man-
nose specificity. Lectins interact with the insects intestinal
epithelial cells or peritrophic membrane and/or glycosyl-
ated digestive enzymes [30, 63, 84]. However, the exact
mechanism of insecticidal action is unknown. Lectins
443
exhibiting similar glycan specificity; might have different
effect on closely related insects [13]. Similarly, one lectin
might cause different effect on closely related insects.
Garlic lectins show the glycan mediated interaction with
several putative receptors in the midgut of insects [9, 54,
84]. Interactions with the digestive and moulting enzymes
are also carbohydrate mediated [30, 84]. This shows that
carbohydrate affinity of lectin plays critical role not only in
other known biological functions but also in the insect
specificity and insecticidal activity [13, 96].
6 Mode of Insecticidal Action
Study on the mechanism of insecticidal action of lectins
was initiated nearly 25 year ago. Gatehouse et al. [31]
proposed that lectins inhibit the nutrient absorption or
cause severe disruption of the epithelial cells in midgut by
stimulating endocytosis. This results in disorganization and
elongation of the striated brush border microvilli which
leads to the swelling of epithelial cells and complete clo-
sure of the gut lumen [28, 37, 38, 67]. Powell et al. [67]
reported the transportation of lectin across the midgut
epithelial barrier after binding to the midgut glycoproteins
and disruption in the microvilli of striated brush border
region. Sauvion et al. [80] reported the interaction of a
lectin with glycosylated receptors on the surface of stom-
ach epithelial cells which cause interference in normal
metabolism and cell functions leading to the rapid feedback
response on feeding behaviour. These results suggest that
each lectin has different mode of action for different insects
at the cellular level. Insecticidal actions of garlic lectins to
homopteran and lepidopteran insects have been described
in detail (Fig. 2).
6.1 Insecticidal Action Against Lepidopteran Insects
A hypothetical mode of insecticidal action of garlic lectins
against lepidopteran insects is described (Fig 2a).
According to published literature and our own observation,
the garlic lectins interact with several glycosylated BBMV
proteins like Cadherin, APN, ALP, polycalins and others in
the midgut peritropic membrane [84]. Since most of them
are reported as receptor for d-endotoxins, there is possi-
bility that a few or all functions as receptor for garlic
lectins also. Binding of lectins to the midgut proteins affect
the nutrient absorption. This might be due to the inhibition
of digestive and other related enzymes. Further, garlic
lectins are resistant to the midgut proteases and transported
to haemolymph. Where, these lectins interact with a
Cytochrome P450 and interfere in larval development. This
results in severe growth retardation and premature death
[84].
123
444 S. K. Upadhyay, P. K. Singh

(A) Ingestion of garlic (Allium (B) Ingestion of garlic (Allium

sativum) lectins sativum) lectins

Glycan mediated interaction of garlic lectins to
the midgut brush border membrane vesicle (BBMV)
proteins [as cadherin like proteins, aminopeptidases
(APN), alkaline phosphatases (ALP), Polycalins and
others]
Inhibition in nutrient absorption and alteration
in the enzyme activity of ALP and APN which
leads to physiological disorders.
Carbohydrate mediated binding of
garlic lectins to the mouth parts
sensory receptor of insects
Disruption in membrane integrity
and food detection ability of
insects
Death of insects due to starvation
Carbohydrate mediated binding of
garlic lectins to the proteins like
aminopeptidases (APN), sucrase
and others in midgut epithelial
cells of insects
Inhibition in nutrient absorption and alteration
in the enzyme activity of APN and sucrase,
leads to the physiological disorders

Inhibition in sucrase Internalization of lectins

activity might cause in haemolymph shows
Internalization of garlic lectins in osmotic imbalance stability against gut
haemolymph, show stability against gut between gut and proteases
proteases haemolymph

Interaction with proteins

Interaction of garlic lectins with Cyt p450 in midgut Transfer of body fluid to like symbionin and
microsomes or fat body and might interfere in molting gut and insects appear others
and development of insects. These might also inhibit the shrivel and finally dead
ALP activity in haemolymph and other tissue

Death of insects by
unknown mechanism
Severe growth retardation and/or death of
insects by unknown mechanism

Fig. 2 a A hypothetical mechanism of insecticidal action of garlic insecticidal action of garlic lectin against Homopteran insects,
lectins against lepidopteran insects, summarized from the several summarized from the several studies in different experimental
studies in different experimental conditions reported in literature conditions reported in literature (cited in the text and tables)
(cited in the text and tables). b A hypothetical mechanism of

6.2 Insecticidal Action Against Homopteran Insects
Insecticidal action of garlic lectins against homopteran
insects slightly differ from the lepidopteran insects
(Fig. 2b). Garlic lectins bind to the sensory receptors of
mouth parts which reduce the food detection ability of
insects resulting in starvation and eventually death [39, 80].
Subsequently, lectins enter into the insect gut and interact
with glycosylated gut proteins like APN, sucrase and others
in midgut epithelial cells [30]. These result in inhibition in
nutrient absorption. Further, garlic lectins might alter the
enzyme activity of APN and sucrase, which ultimately
disturb the physiology of insects. Inhibition of sucrase
activity has been correlated with the osmotic imbalance in
aphid gut leading to insect mortality [30, 47]. Similar to
lepidopteran insects, garlic lectins get accumulated in the
haemolymph and ovarioles [29]. Accumulation in ovarioles
might be responsible for the loss in fecundity. The role of
garlic lectins in the haemolymph and mechanism of tox-
icity is need be elucidated in detail in future.
lepidopteran insect pests. Due to the edible source of origin
garlic lectins are supposed to be biosafe. The insecticidal
action of garlic lectins is a multi-step process that involves
the interaction with several glycosylated receptor proteins in
midgut of insects. This results in inhibition in nutrient
absorption leading to mortality. Garlic lectins get accumu-
lated into the haemolymph and ovarioles and interfere in the
development and reproduction. Although, several reports on
the receptors of garlic lectins have been summarised in this
review, still detail study on their interaction with lectins and
post interaction processes will be imperative in order to
understand the insecticidal mechanism. In addition, the
identification of binding epitopes will be helpful in engi-
neering the lectins for more specificity, higher toxicity and
delay the resistance development in insects.
Acknowledgment Authors are grateful to the Council of Scientific
and Industrial Research, Government of India for funding the
research. SKU is thankful to CSIR for senior research fellowship and
G B Technical University, Lucknow, UP, India for Ph.D. registration.

References
7 Conclusion
1. Andersson JO (2000) Curr Biol 10:R866R868
2. Angelucci C, Barrett-Wilt GA, Hunt DF, Akhurst RJ, East PD,
Garlic lectins are promising candidate molecules for the Gordon KH, Campbell PM (2008) Insect Biochem Mol Biol
development of transgenic crops to control homopteran and 38:685696

123
Receptors of Garlic
3. Angst BD, Marcozzi C, Magee AI (2001) J Cell Sci 114:
629641
4. Arenas I, Bravo A, Soberon M, Gomez I (2010) J Biol Chem
285:1249712503
5. Arora A, Sharma HC, Dreissche EV, Sharma KK (2005) SAT
eJournal/ejournal.icrisat.org. 1:13
6. Ashford DA, Smith WA, Douglas AE (2000) J Insect Physiol
46:335341
7. Bachhawat K, Thomas CJ, Amutha B, Krishnasastryi MV, Khan
MI, Surolia A (2001) J Biol Chem 276:55415546
8. Bandyopadhyay S, Roy A, Das S (2001) Plant Sci 161:
10251033
9. Banerjee S, Hess D, Majumder P, Roy D, Das S (2004) J Biol
Chem 279:2378223789
10. Bharathi Y, VijayaKumar S, Pasalu IC, Balachandran SM,
Reddy VD, Rao KV (2011) J Biotechnol 152:6371
11. Blixt O, Head S, Mondala T, Scanlan C, Huflejt ME, Alvarez R,
Bryan MC, Fazio F, Calarese D, Stevens J, Razi N, Stevens DJ,
Skehel JJ, Van Die I, Burton DR, Wilson IA, Cummings R,
Bovin N, Wong CH, Paulson JC (2004) Proc Natl Acad Sci USA
101:1703317038
12. Burton SL, Ellar DJ, Li J, Derbyshire DJ (1999) J Mol Biol
287:10111022
13. Carlini CR, Grossi-de-Sab (2002) Toxicon 40:15151539
14. Chakraborti D, Sarkar A, Mondal HA, Das S (2009) Transgenic
Res 18:529544
15. Chandra NR, Ramachandraiah G, Bachhawat K, Dam TK,
Surolia A, Vijayan M (1999) J Mol Biol 285:11571168
16. Chen SJ, Chen NT, Wang SH, Hsu JC, Ding WH, Kuo-Huang
LL, Huang RN (2009) Pest Manag Sci 65:923930
17. Cristofoletti PT, Ribeiro AF, Deraison C, Rahbe0 Y, Terra WR
(2003) J Insect Physiol 49:1124
18. Dam TK, Bachhawat K, Rani PG, Surolia A (1998) J Biol Chem
273:55285535
19. Denolf P, Hendrickx K, Van Damme J, Jansens S, Peferoen M,
Degheele D, Van Rie J (1997) Eur J Biochem 248:748761
20. Downing N (1978) J Exp Biol 77:247250
21. Dunne J, Hanby AM, Poulsom R, Jones TA, Sheer D, Chin WG,
Da SM, Zhao Q, Beverley PC, Owen MJ (1995) Genomics
30:207223
22. Dutt U (2007) Environment News Service, 21 August,
(countercurrents.org)
23. Dutta IP, Majumdar P, Saha P, Ray K, Das S (2005) Plant Sci
169:9961007
24. Dutta I, Saha P, Majumder P, Sarkar A, Chakraborti D, Banerjee
S, Das S (2005) Plant Biotech J 3:601611
25. Filichkin SA, Brumfield S, Filichkin TP, Young MJ (1997)
J Virol 71:569577
26. Fisher DB (2000) In: Gruissem W, Jones RL, Buchanan BB
(eds) Long distance transport. American Society of Plant
Physiologists, Rockville, pp 730784
27. Fitches E, Gatehouse AMR, Gatehouse JA (1997) J Insect
Physiol 43:727739
28. Fitches E, Ilett C, Gatehouse AMR, Gatehouse LN, Greene R,
Edwards JP, Gatehouse JA (2001) J Insect Physiol 47:
13891398
29. Fitches E, Philip J, Hinchliffe G, Vercruysse L, Chougule N,
Gatehouse JA (2008) Insect Sci 15:483495
30. Fitches E, Wiles D, Douglas AE, Hinchliffe G, Audsley N,
Gatehouse JA (2008) Insect Biochem Mol Biol 38:905915
31. Gatehouse AMR, Dewey FM, Dove J, Fenton KA, Pusztai A
(1984) J Sci Food Agric 35:373380
32. Gatehouse AMR, Powell KS, Van Damme EJM, Peumans W,
Gatehouse JA (1995) In: Pusztai AJ, Bardocz S (eds) Lectins:
biomedical perspectives. Taylor & Francis, London, pp 3557
33. Gilbert LI, Warren JT (2005) Vitam Horm 73:3157
445
34. Goldberg M, Peshkovsky C, Shifteh A, Al-Awqati Q (2000)
J Biol Chem 275:2462224629
35. Gomez I, Sanchez J, Miranda R, Bravo A, Sanchez M (2002)
FEBS Lett 513:242246
36. Gumbiner BM (1996) Cell 84:345357
37. Habibi J, Backus EA, Czapla TC (1998) Cell Tissue Res
294:561571
38. Habibi J, Backus EA, Huesing JE (2000) J Insect Physiol 46:
611619
39. Harper MS, Hopkins TL, Czapla TH (1998) Tissue Cell 30:
166176
40. Hilder VA, Powell KS, Gatehouse AMR, Gatehouse JA, Gate-
house LN, Shi Y, Hamilton WDO, Merryweather A, Newell CA,
Timans JC (1995) Transgenic Res 4:1825
41. Hooper NM (1994) FEBS Lett 354:16
42. Hossain DM, Shitomi Y, Moriyama K, Higuchi M, Hayakawa T,
Mitsui T, Sato R, Hori H (2004) Appl Environ Microbiol
70:46044612
43. Hua G, Zhang R, Abdullah MA, Adang MJ (2008) Biochemistry
47:51015110
44. Ingle SS, Trivedi N, Prasad R, Kuruvilla J, Rao KK, Chhatpar
HS (2001) Curr Microbiol 43:255259
45. Jurat-Fuentes JL, Adang MJ (2004) Euro J Biochem 271:3127
3135
46. Jurat-Fuentes JL, Adang MJ (2007) J Invert Pathol 95:187191
47. Karley AJ, Ashford DA, Minto LB, Pritchard J, Douglas AE
(2005) J Insect Physiol 51:13131319
48. Kaur M, Singh K, Rup PJ, Kamboj SS, Saxena AK, Sharma M,
Bhagat M, Sood SK, Singh J (2006) J Biochem Mol Biol
39:432440
49. Knight PJ, Crickmore N, Ellar DJ (1994) Mol Microbiol
11:429436
50. Knight PJ, Knowles BH, Ellar DJ (1995) J Biol Chem 270:
1776517770
51. Krishnamoorthy M, Jurat-Fuentes JL, McNall RJ, Andacht T,
Adang MJ (2007) Insect Biochem Mol Biol 37:189201
52. Laustsen PG, Vang S, Kristensen T (2001) Eur J Biochem
268:98104
53. Lu YJ, Adang MJ (1996) Insect Biochem Mol Biol 26:3340
54. Majumder P, Banerjee S, Das S (2004) Glycoconjugate J 20:
525530
55. Majumder P, Mondal HA, Das S (2005) J Agric Food Chem
53:67256729
56. Malik K, Mahmood T, Riazuddin S (2001) J Biol Sci 1:782784
57. Mauchamp B, Royer C, Garel A, Jalabert A, Rocha MD, Grenier
AM, Labas V, Vinh J, Mita K, Kadono K, Chavancy G (2006)
Insect Biochem Mol Biol 36:623633
58. McNall RJ, Adang MJ (2003) Insect Biochem Mol Biol
33:9991010
59. Mondal HA, Chakraborti D, Majumder P, Roy P, Roy A,
Bhattacharya SG, Das S (2011) PLoS ONE 6:e27716
60. Nakayama M, Nakajima D, Nagase T, Nomura N, Seki N, Ohara
O (1998) Genomics 51:2734
61. Nollet F, Kools P, Roy VF (2000) J Mol Biol 299:551572
62. Ohizumi Y, Gaidamashvili M, Ohwada S, Matsuda K, Komi-
nami J, Nakamura-Tsuruta S, Hirabayashi J, Naganuma T, Og-
awa T, Muramoto K (2009) J Agric Food Chem 57:28962902
63. Peumans WJ, Van Damme EJM (1995) Plant Physiol
109:347352
64. Pigott CR, Ellar DJ (2007) Microbiol Mol Biol Rev 71:255281
65. Powell KS (2001) Entomol Exp Appl 99:7178
66. Powell KS, Gatehouse AMR, Hilder VA, van Damme EJM,
Peumans WJ, Boonjawat J, Horsham K, Gatehouse JA (1995)
Entomol Exp Appl 75:6165
67. Powell KS, Spence J, Bharathi M, Gatehouse JA, Gatehouse
AMR (1998) J Insect Physiol 44:529539
123
446
68. Ramachandraiah G, Chandra NR (2000) Proteins Struc Func
Genet 39:358364
69. Ramachandraiah G, Chandra NR, Surolia A, Vijayan M (2002)
Acta Cryst D58:414420
70. Ramachandraiah G, Chandra NR, Surolia A, Vijayan M (2003)
Glycobiology 13:765775
71. Rao KV, Rathore KS, Hodges TK, Fu X, Stoger E, Sudhakar D,
Williams S, Christou P, Bharathi M, Bown DP, Powell KS,
Spence J, Gatehouse AM, Gatehouse JA (1998) Plant J
15:469477
72. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI (2006) Insect
Biochem Mol Biol 36:188199
73. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI (2006) Mol
Cell Endocrinol 247:166174
74. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI (2006) Bio-
chem Soc Trans 34:12561260
75. Rewitz KF, Connor MB, Gilbert LI (2007) Insect Biochem Mol
Biol 37:741753
76. Rhodes JD, Croghan PC, Dixon AFG (1997) Physiol Entomol
22:373379
77. Sadeghi A, Smagghe G, Broeders S, Hernalsteens JP, DeGreve
H, Peumans WJ, VanDamme EJ (2008) Transgenic Res 17:918
78. Saha P, Dasgupta I, Das S (2006) Plant Mol Biol 62:735752
79. Sarkar A, Hess D, Mondal HA, Banerjee S, Sharma HC, Das S
(2009) J Prot Res 8:18381848
80. Sauvion N, Charles H, Febvay G, Rahbe Y (2004) Entomol Exp
Appl 110:3144
81. Smeets K, Van Damme EJM, Verhaert P, Barre A, Rouge P,
Van Leuven F, Peumans WJ (1997) Plant Mol Biol 33:223234
82. Takesue S, Yokota K, Miyajima S, Taguchi R, Ikezawa H,
Takesue Y (1992) Comp Biochem Physiol B 102:711
83. Upadhyay SK, Chandrashekar K, Thakur N, Verma PC, Borgio
JF, Singh PK, Tuli R (2011) J Biosci 36:153161
84. Upadhyay SK, Mishra M, Singh H, Ranjan A, Chandrashekar K,
Verma PC, Singh PK, Tuli R (2010) Proteomics 10:44314440
85. Upadhyay SK, Saurabh S, Rai P, Singh R, Chandrashekar K,
Verma PC, Singh PK, Tuli R (2010) J Biotechnol 146:18
86. Upadhyay SK, Saurabh S, Singh R, Rai P, Dubey NK,
Chandrashekar K, Negi KS, Singh PK, Tuli R (2011c) Protein J.
doi:10.1007/s10930-011-9342-0
123
S. K. Upadhyay, P. K. Singh
87. Upadhyay SK, Singh P K (2011b) Biotechnol Lett. doi:
10.1007/s10529-011-0665-x
88. Upadhyay SK, Singh S, Chandrashekar K, Tuli R, Singh P K
(2012) Appl Microbiol Biotechnol. doi: 10.1007/s00253-
011-3547-1
89. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwarz
TL, Takeichi M, Uemura T (1999) Cell 98:585595
90. Vadlamudi RK, Ji TH, Bulla LA Jr (1993) J Biol Chem
268:1233412340
91. Vadlamudi RK, Weber E, Ji I, Ji TH, Bulla LA Jr (1995) J Biol
Chem 270:54905494
92. Van Damme EJM, Barre A, Rouge P, Peumans WJ (2004)
Trends Plant Sci 9:484489
93. Van Damme EJM, Lannoo N, Peumans WJ (2008) Adv Bot Res
48:107209
94. Van Damme EJM, Peumans WJ, Barre A, Rouge P (1998) CRC
Crit Rev Plant Sci 17:575692
95. Van Damme EJM, Smeets K, Torrekens S, Van Leuven F,
Goldstein IJ, Peumans WJ (1992) Eur J Biochem 206:413420
96. Van Driessche E, Fischer J, Beeckmans S, Bog-Hanse TC
(1996) Lectins, biology, biochemistry, clinical biochemistry,
Textop, Denmark, vol 11
97. Vasconcelos IM, Oliveira JTA (2004) Toxicon 44:385403
98. Vestal DJ, Ranscht B (1992) J Cell Biol 119:451461
99. Virla EG, Casuso M, Frias EA (2010) Crop protection
29:635638
100. Walters FS, Mullin CA (1988) Arch Insect Biochem Physiol
9:3546
101. Wang P, Zhang X, Zhang J (2005) Insect Biochem Mol Biol
35:611620
102. Warren JT, Petryk A, Marques G, Parvy JP, Shinoda T, Itoyama
K, Kobayashi J, Jarcho M, Li Y, OConnor MB, Dauphin-
Villemant C, Gilbert LI (2004) Insect Biochem Mol Biol
34:9911010
103. Wilkinson TL, Ashford DA, Pritchard J, Douglas AE (1997) J
Exp Biol 200:21372143
104. Wolfersberger MG (1984) Am Zool 24:187197
105. Yarasi B, Sadumpati V, Immanni CP, Vudem DR, Khareedu VR
(2008) BMC Plant Biol 8:102
106. Young MJ, Filichkin SA (1999) Trends Microbiol 7:346347