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1 September 2013 Cloning and Polymorphism Analysis of Glutamate-Gated Chloride Channel Gene of Laodelphax striatellus (Hemiptera: Delphacidae)
Yaoxue Dong, Yu Chen, Qi Wei, Jianya Su, Congfen Gao
Author Affiliations +

A glutamate-gated chloride channel (GluCl) gene encodes a transmembrane domain protein that is an important target for insecticides. In insects, the GluCl genes of Tribolium castaneum, Apis mellifera, Nasonia vitripennis, Drosophila melanogaster, Musca domestica, Lucilia cuprina, Aedes aegypti, Schistocerca gregaria, Plutella xylostella and Acyrthosiphon pisum were cloned, but not the corresponding gene of Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae), the small brown planthopper. In this study, the complete cDNA sequence of GluCl gene from L. striatellus was cloned and sequenced. The sequence includes 2,112 nucleotides, and the open reading frame ranges from 208 to 1,566 bp. The sequence encoded 452 amino acid residues. Alignment of the amino acid sequences of the GluCls between L. striatellus and other species indicated that the similarity of sequences was in the range of 48%–86%. The purified reverse transcription PCR product of GluCl coding sequence was cloned into a T-vector and then the sequence was analyzed. This analysis revealed polymorphism of GluCl gene among several strains, including a relatively susceptible strain, a fipronil resistant strain and a field strain of L. striatellus. Because the GluCls is an important target receptor, the GluCl gene in L. striatellus is worthy of further investigation.

The small brown planthopper (SBPH), Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae), has a wide distribution from south-east Asia to Siberia and Europe. As a pest of rice, wheat and corn, it causes serious damage to crops by the transmission of Rice stripe virus (RSV), Rice black streaked dwarf virus (RBSDV) and Maize rough dwarf virus (MRDV) (Kisimoto 1967; Fang et al. 2001). In China, the SBPH has been causing serious feeding damage or crop disease since 1999 and the density of the L. striatellus population increased dramatically from 1999 to 2008 (Liu et al. 2006). To control the pest, neonicotinoid and phenylpyrazole insecticides, such as imidacloprid and fipronil, have been widely used. Extensive use of fipronil against the rice planthopper, Nilaparvata lugens (Stål), has led to insecticide resistance problems in East and Southeast Asia (Matsumura & Otuka 2009; Matsumura et al. 2009; Zhao et al. 2011).

The glutamate-gated chloride channel (GluCl) is a member of the “Cys-loop” superfamily of ligand-gated ion channels. GluCls mediate synaptic inhibition in neurons and are expressed extra-junctionally in striated muscles. They may play key roles in regulating swallowing, locomotion, sensing, memory and juvenile hormone biosynthesis (Yates et al. 2003; Liu et al. 2005). Until now GluCl channels have been found only in invertebrates, and therefore they are ideal insecticide targets with high selectivity (Janssen et al. 2007). Most of the information about the GluCl channel has come from studies on model nematodes and model insects. All together several α subunits and β subunits of the channel are found in nematodes. One α subunit has been cloned from insects. The GluCl channels are most similar to GABA (γ-amino butyric acid) receptors with respect to their physiology and pharmacology. However, the amino acid sequences of GluCl channels are most similar to those of glycine receptor (Cully et al. 1996). The insecticides acting on GluCl channels are avermectin/milbemycin, fipronil, nodulisporic acid, a novelindole diterpene (Kane et al. 2000; Smith et al. 2000; Janssen et al. 2007).

Fipronil is a phenyl pyrazole insecticide introduced for pest control, and it is highly effective against both piercing sucking and chewing insects (Colliot et al. 1992; Moffat 1993). Fipronil is a potent blocker of the insect GABA-gated chloride channel or GABA receptor (Cole et al. 1993; Buckingham et al. 1994), and therefore it belongs to IRAC (Insecticide Resistance Action Committee) mode of action group 2B (IRAC 2006). Growing evidence indicates that fipronil may inhibit GluCls of invertebrates generally, because it does so in the nematode, Caenorhabditis elegans Maupas (Horoszok et al. 2001), in the American cockroach, Periplaneta americana (L.) (Ikeda et al. 2003) and the migratory locust, Locusta migratoria (L.) (Janssen et al. 2007).

Polymorphisms, abundant in insect genes, result in a permanent changes in gene activity that determine amino acid substitutions. Three amino acid (AA) substitutions, E114G, V235A and L256F, in the AVR-14B in C. oncophora have been associated with resistance to ivermectin (IVM), whose main site of action is glutamategated chloride (GluCl) channels (Njue & Prichard 2004; Njue et al. 2004). In this study, the cDNA sequence of glutamate-gated chloride channel gene from L. Striatellus was cloned by molecular technology and then analysed. Subsequently, single nucleotide polymorphisms sites were detected by direct sequencing. Our purpose was to provide a foundation of theory and findings for the further study of the mechanism of Fipronil resistance.






The relatively susceptible strain (WX) of L. striatellus, which had been maintained in the laboratory for 8 years without exposure to insecticides, was collected from Wuxi, Jiangsu, China in 2005. A fipronil resistant strain (WX-F) was derived from the field-collected strain (WX) by 90 generations of continuous selection with fipronil using the rice seedling dip method. A field-collected L. striatellus strain (CX) collected from Changxing, Zhejiang, China in 2013, which since 2010 was exposed several insecticides but not to fipronil. All strains were reared on rice seedlings, seedlings were kept at 25 ± 1 °C, 70 ± 10% RH and 16:8 (L: D) h.

RNA Preparation and cDNA Synthesis

Total cellular RNA was isolated from 30 mg of L. striatellus adult tissue using the RNeasy Midi kit (QIAGEN, Hilden, Germany) by following the manufacturer's instructions. Single-stranded cDNA was synthesized from the total RNA with reverse transcriptase M-MLV and oligo (dT) 18. 5′-and 3′-RACE-ready cDNA were prepared according to the instructions of the Gene Racer Kit (Invitrogen).

Degenerate PCR Amplification

Degenerate primers targeting conserved gene regions were determined by alignment of published GluCl sequences from related species. Primers were synthesized by Invitrogen (Shanghai, China). The 3 degenerate primers used are shown in Table 1. Polymerase chain reaction (PCR) contained 2 µL of cDNA, 5 µL of 10 × standard PCR buffer, 4 µL of 25 mM Mg2+, 10 pmol of each primer, 1 µL of 10 mM dNTP, and 1 U Taq DNA polymerase. The initial step of the amplification reaction denaturation at 94 °C for 3min, followed by 30 cycles of 94 fi01_1168.gifC for 30 s, 55 °C for 30 s, 72 °C for 1 kb/min, and a final extension at 72 °C for 10 min. PCR products of the expected size were excised and purified by using the DNA agarose Gel Pur Kit (BIOMIGA, Nanjing, China) and cloned by using the pUCm-T vector system (Sangon, Shanghai, China). The second round of polymerase chain reaction was the same as the above. Primer-F and primer-R2 were used.

Cloning of the Full Length Fragment of the GluCl Gene by the RACE Technique

In order to amplify the GluCl gene of L. striatellus by means of degenerate primers, specific primers were designed and used to amplify the full length sequence. Primers used are shown in Table 2.

Analysis of the GluCl Gene Sequence with Online Tools

The cDNA sequences were analyzed with BioEdit software (Thompson et al. 1997). Sequences were aligned with ClustalX software, and then viewed with the Bioedit software (Thompson et al. 1997). The identity of the cDNA as GluCl was confirmed by similarity searches of GenBank using Blastx NR ( Multiple Sequences Alignment of the cDNA was accomplished by using bioedit and ClustalX softwares (Thompson et al. 1997). The trans-membrane helix was predicted using TMpred on-line tools ( A phylogenetic tree was constructed by the neighbor-joining method (1000 replicates; seed = 64,238) for 14 amino acid sequences of the GluCls of the various species using the MEGA 4.0 program.

Analysis of cDNA Polymorphism of GluCl from 3 Strains of L. striatellus

There is a phenomenon of single nucleotide polymorphism (SNP) in the open reading frame of GluCla of L. striatellus, moreover, some animo acids are changed because of SNP. To explore this phenomenon in-depth, the full-length GluCl coding sequence of individual L. striatellus adults from the original WX strain, the fipronil resistant WX-F strain and the field CX strain were cloned by the RNA prep MicroKit (BIOTEKE) in accordance with its instructions. Thereafter we used Phanta Super Fidelity DNA Polymerase (Vazyme) to minimize the probability of mismatches during PCR. We used 5′-CAGCGCAGCCCAACTAACCACC-3′ as the Specific Forward Primer (F5) and 5′-AGCTGTTGTGTTGCGAGTCGCCC-3′ as the Specific Reverse Primer (R5).





Cloning the Full Length cDNA of the GluCl Gene of L. striatellus

The full-length cDNA of L. striatellus was amplified with the degenerate primers (Table 1) and the specific primers (Table 2). The cloned sequence included 2,112 nucleotides (GenBank accession JF430868), and the open reading frame ranged from 208 to 1566 bp, which encoded 452 amino acid residues. This gene was designated as LsGIuCl. This L. striatellus transcript was the most similar to the reported GluCl-like transcript of Lucilia cuprina (81%), followed by those of Musca domestica (80%), Drosophila melanogaster (80%–83%), Aedes aegypti (86%),Tribolium castaneum (84%–86%), Plutella xylostella (84%), Nasonia. vitripennis (83%–84%), Apis mellifera (82%), Acyrthosiphon pisum (79%), Tetranychus urticae (64%), Riphicephalus sanguineus (68%), Haemonchus contortus (45%–46%) and Caenorhabditis elegans (48%–51%) (Table 3). Furthermore, according to the analysis with TMpred on-line tools, the GluCl gene included 2 pairs of cysteine residues (enclosed in the black boxes Fig. 1) within the N-terminal region and the 4 proposed trans-membrane regions (M1–4: underlined in Fig. 1) in the C-terminal region.

Phylogenetic Relations of Various Invertebrates Based on Their GluCl Genes

A phylogenetic tree was generated using 14 amino acid sequences of GluCl genes from 14 invertebrate species (Fig. 2). From the phylogenetic tree branches, we may find that Class Insecta, Class Arachnida (mites, ticks, spiders, etc.) and Class Secernetea (nematodes) belong to 1 group, and that the GluCl genes of the various different species in these Classes share a high degree of similarity. This suggests that GluCl genes have had a long common evolutionary history. Thus, it is reasonable to deduce that the GluCl genes might have evolved from an ancient ancestral gene, and might be generally distributed in a wide range of organisms.




Analysis of cDNA Polymorphism of GluCl from 3 Strains of L. striatellus

The ORF of the GluCl gene was cloned from the DNA of 10 L. striatellus individuals of each strain, i.e., the susceptible strain in laboratory, the fipronil-resistant strain, and the field strain . Upon comparing 30 sequences of the SS (the relatively fipronil-susceptible strain), the RS (the fipronil-resistant strain) and the field strain, we discovered notable polymorphisms involving 80 base substitutions, and these were predominantly C-T nucleotide substitutions. All single nucleotide substitutions (SNPs) led to 20 amino acid replacements within the GluCl subunit. These amino acid substitutions involved 20 loci of GluCl gene of the 3 strains, i.e., I31K, D63A, V68I, I73L, S79A, K80T, etc. By comparing and analyzing cDNA sequences of the GluCl gene of the 3 strains, we found 2 loci with amino acid substitutions (A294D ,G298D) located between the M2–M3 trans membrane domain, 3 loci with amino acid substitutions (R352C,A364V, K378S) located between the M3–M4 trans membrane domain, the remaining loci determining amino acid substitutions at the hydrophilic N-terminus extracellular region (Table 4).


GluCls were first identified in arthropods as extra-junctional glutamate receptors (H-receptors) that hyperpolarized the membrane potential of locust (S. gregaria) leg muscle (Gration et al. 1979; Patlak et al. 1979; Dudel et al. 1989), and later they were cloned from the soil nematode, Caenorhabditis elegans (Cully et al. 1994). GluCls are activated by the glutamate analog, ibotenic acid, and are inhibited weakly by the ligand-gated chloride channel blocker, picrotoxin (Smith et al. 1999; Raymond et al. 2000; Horoszok et al. 2001). Until now the glutamate-gated chloride channel has been described only in invertebrates, and it is an important target for the development of insecticides with high selective toxicity to arthopods (Cully et al. 1996; Raymond & Sattelle, 2002).

Insect glutamate-gated chloride channels, along with GABA-gated chloride channel, are important targets for the action of certain insecticides (Bloomquist 2001). In this study, the GluCl gene in the L. striatellus was cloned successfully, then submitted to GenBank and given the registration number, JF430868. Thus the GluCl gene of the L. striatellus probably will be of great fundamental importance for further research.

Fipronil was designated as a new GABA-gated chloride channel blocker and introduced into pest control, for instance against the Colorado potato beetle, Leptinotarsa decemlineata Say (Chrysomelidae), and against important crop and stored product pests in various Orders and families (Moffat 1993; Smith & Lockwood 2003). The blocking action of fipronil on GluCl channels was demonstrated in Xenopus sp. (Anura: Pipidae) oocytes transfected with GluCls (Horoszok et al. 2001), and a similar degree of blocking was observed on chloride currents induced by glutamate and ibotenate in the dorsal unpaired median (DUM) neurons of the cockroach, Periplaneta americana, and the grasshopper, Melanoplus sanguinipes (F.) (Smith et al. 1999; Raymond et al. 2000; Ikeda et al. 2003). The blocking effect of fipronil on GluCls was previously proposed to explain part of the toxicity of this insecticide, which is widely used in pest control to eradicate dieldrin-resistant insects (Horoszok et al. 2001; Smith & Lockwood 2003; Tingle et al. 2003; Zhao et al. 2004).

This study revealed substantial polymorphism of GluCl gene in L. striatellus. The relatively fipronil-susceptible strain (WX) of L. striatellus and the fipronil-resistant strain (WX-F), which had been continuously selected with fipronil for 90 generations, were collected in Wuxi, Jiangsu, China, they each have a uniform genetic background. By comparing and analyzing amino acid sequences of GluCla, we discovered 7 loci determining amino acid substitutions in the WX and WX-F strains, 2 loci unique to the WX-F strain, and 5 loci unique to the WX strain. In addition, we analyzed polymorphism in the L. striatellus field strain, which had a genetic background different from the SS (the relatively fipronil-susceptible) strain and the RS (fipronil-resistant) strain. There were 6 other amino acid replacements in the field strain besides the above loci, and no sharp contrast between the WX and the CX strains. Most of these polymorphism sites exist in an extracellular region. It was reported that 3 amino acid (AA) substitutions, E114G, V235A and L256F in the AVR-14B of GluClα of C. oncophora, which is associated with IVM resistance, also exist in an extracellular region (Njue & Prichard 2004; Njue et al. 2004). There is no published report linking fipronil-resistance to specific polymorphisms in the glutamate-gated chloride channel. Our comparison of the full-length GluCl coding sequence in the susceptible and resistant L. striatellus strains did not show definitive evidence linking nucleic acid sequences to fipronil-resistance in this study. This important problem awaits further study.

Fig. 1.

Alignment of the GluCla subunit amino acid sequences from Lucilia cuprina, Musca domestica, Drosophila melanogaster, Aedes aegypti, Plutella xylostella, Tribolium castaneum, Apis mellifera, Nasonia vitripennis, Acyrthosiphon pisum and Laodelphax striatellus. These include the signature pairs of cysteine residues (enclosed in the black boxes at the third row) within the N-terminal region and the 4 proposed transmembrane regions (M1–4: underlined) in the C-terminal region. A second pair of N-terminal cysteine residues is enclosed by the black boxes at the fourth row.





Fig. 2.

A phylogenetic tree constructed by neighbor-joining method (1000 replicates; seed = 64238) for amino acid sequences of GluCls from 14 species using MEGA 4.0 program. Bootstrap values are shown at the branching points. Scale bar indicates the number of changes inferred as having occurred along each branch. GenBank accession codes: LcGluCl (Lucilia cuprina; AF081674); MdGluCl (Musca domestica; AB177546); DmGluCl (Drosophila melanogaster, DQ665648); AaGluCl (Aedes aegypti, XM001662847); TcGluCl (Tribolium castaneum, EF545123); PxGluCl (Plutella xylostella, GQ221939); LsGluCl (Laodelphax Striatellus, JF430868); NvGluCl (Nasonia vitripennis, FJ851100), AmGluCl (Apis niellifera, DQ667186); ApGluCl (Acyrthosiphon pisum, XM 001943378); TuGluCl (Tetranychus urticae, JQ738193); RsGluCl (Rhipicephalus sanguineus, GQ215234); CeGluCl (Caenorhabditis elegans, CEU14524); HcGluCl (Haemonchus contortus, AF119791).



We gratefully acknowledge that this work was funded by the Natural Science Foundation of China (31171184).



S. D. Buckingham , A. M. Hosie , R. L. Roush , and D. B. Sattelle 1994. Actions of agonists and convulsant antagonists on a Drosophila melanogaster GABA receptor (Rdl) homo-oligomer expressed in Xenopus oocytes. Neurosci. Letters 181(1–2): 137–140. Google Scholar


J. R. Bloomquist 2001. GABAand glutamate receptors as biochemical sites for insecticide action, pp. 17–41 In I. Ishaaya [ed.], Biochemical Sites of Insecticide Action and Resistance. Springer-Verlag, Berlin. Google Scholar


T. A. Cleland 1996. Inhibitory glutamate receptor channels. Molecular Neurobiol. 13:97–136. Google Scholar


L. M. Cole , R. A. Nicholson , and J. E. Casida 1993. Action of phenylpyrazole insecticides at the GABA gated chloride channel. Pesticide Biochem. Physiol. 46: 47–54. Google Scholar


F. K. Colliot , A Kukorowski, D. W. Hawkins , and D. A. Roberts 1992. Fipronil: a new soil and foliar broad spectrum insecticide, pp. 29–34 In Proc. Brighton Crop Prot. Conference: Pests and Diseases, British Crop Protection Council, Farnham, UK. Google Scholar


D. F. Cully , D. K Vassilatis , and K. K. Liu 1994. Cloning of an avermectin - sensitive glutamate-gated chloride channel from Caenorhabditis elegans. Nature 371: 707–711. Google Scholar


D. F. Cully , H. Wilkinson , and D. K. Vassilatis 1996. Molecular biology and electrophysiology of glutamate-gated chloride channels of invertebrates. Parasitol. 113(Suppl): 191–200. Google Scholar


J. Dudel , C. Franke , H. Hatt , and P. N. R. Usherwood 1989. Chloride channels gated by extra junctional glutamate receptors (H-receptors) on Locust leg muscle. Brain Res. 481: 215–220. Google Scholar


S. Fang , J. Yu , J. Feng , C. Han , D. Li , and Y. Liu 2001. Identification of rice black-streaked dwarf fijivirus in maize with rough dwarf disease in China. Virology 146 (1): 167–170. Google Scholar


K. A. Gration , R. B. Clark , and P. N. Usherwood 1979. Three types of L-glutamate receptor on junctional membrane of Locust muscle fibres. Brain Res. 171:360–364. Google Scholar


L. Horoszok , V. Raymond , D. B. Sattelle , and A. J. Wolstenholme 2001. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxin-insensitive, L-glutamate-gated chloride channel subunit from Caenorhabditis elegans. J. Pharmacol. 132: 1247–1254. Google Scholar


T. Ikeda , X. Zhao , Y. Kono , J. Z. Yeh , and T. Naeahashi 2003. Fipronil modulation of glutamate-induced chloride currents in cockroach thoracic ganglion neurons, Neurotoxicol. 23: 807–815. Google Scholar


IRAC (INSECTICIDE RESISTANCE ACTION GROUP). 2006. IRAC mode of action classification, version 5.2. Revised and re-issued September 2006.  Google Scholar


D. Janssen , C. Derst , R. Buckinx , J. Vanden Eynden , J. M. Rigo , and E. Van Kerkhove 2007. Dorsal unpaired median neurons of Locusta migratoria express ivermectin-and fipronil-sensitive glutamate-gated chloride channels. J. Neurophysiol. 97: 2642–2650. Google Scholar


N. S. Kane , B. Hirschberg , S. Qian , D. Hunt , B. Thomas , R. Brochu , S. W. Ludmerer , Y. Zheng , M. Smith , J. P. Arena , C. J. Cohen , D. Schmatz , J. Warmke , and D. F. Cully 2000. Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. PNAS 97: 13949–13954. Google Scholar


R. Kisimoto 1967. Genetic variation in the ability of a planthopper vector; Laodelphax striatellus (Fallén) to acquire the rice stripevirus. Virology 32(1): 144–152. Google Scholar


H. P. Liu , S. C. Lin , and C. Y. Lin 2005. Glutamategated chloride channels inhibit juvenile hormone biosynthesis in the cockroach, Diploptera punctata. Insect Biochem. Mol. Biol. 35: 1260–1268. Google Scholar


X. D. Liu , B. P. Zhai , and C. M. Liu 2006. Outbreak reasons of Laodelphax striatellus population. Chinese Bull. Entomol. 43: 141–146. In Chinese with English summary. Google Scholar


M. Matsumura , and A. Otuka 2009. Current status of insecticide resistance in Asian rice planthoppers. Plant Prot. 63: 745–748. Google Scholar


M. Matsumura , H. Takeuchi , M. Satoh , S. Sanada-Morimura , A. Otuka , T. Watanabe , and D. V. Thanh 2009. Current status of insecticide resistance in rice planthoppers in Asia, pp. 233–244 In K. L. Heong and B. Hardy [eds.], Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Banos, The Philippines. Google Scholar


A. S. Moffat 1993. New chemicals seek to outwit insect pests. Science 261: 550–551. Google Scholar


A. I. Njue , and R. K. Prichard 2004. Genetic variability of glutamate-gated chloride channel genes in ivermectin-susceptible and -resistant strains of Cooperia oncophora. Parasitology 129: 741–751. Google Scholar


A. I. Njue , J. Hayashi , I. Kinne , X. P. Feng , and R. K. Prichard 2004. Mutations in the extracellular domains of glutamate-gated chloride channel alpha 3 and beta subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity. J. Neurochem. 89: 1137–1147. Google Scholar


Y. Ozoe , M. Asahi , F. Ozoe , K. Nakahira , and Mita . 2010. The antiparasitic isoxazoline A1443 is a potent blocker of insect ligand-gated chloride channels. Biochem. and Biophy Res. Commun. 391: 744–749. Google Scholar


J. B. Patlak , K. A. Gration , and P. N. Usherwood 1979. Single glutamate-activated channels in locust muscle. Nature 278(5705): 643–645. Google Scholar


V. Raymond , D. B. Sattelle , and B. Lapied 2000. Coexistence in DUM neurons of two GluCl channels that differ in their Picrotoxin sensitivity. Neuroreport 11: 2695–2701. Google Scholar


V. Raymond , and D. B. Sattelle 2002. Novel animalhealth drug targets from ligand-gated chloride channels. Natl. Rev. Drug Discovery 1: 427–436. Google Scholar


D. I. Smith , and J. A. Lockwood 2003. Horizontal and trophic transfer of diflubenzuron and fipronil among grasshoppers (Melanoplus sanguinipes) and between grass-hoppers and darkling beetles (Tenebrionidae). Arch. Environ. Contam. Toxicol. 44: 377–382. Google Scholar


M. M. Smith , B. S. Thomas , V. A. Warren , R. Brochu , I. Dick , and B. Hirschberg 1999. Fipronil blocks invertebrate ligand-gated chloride channels. Soc. Neurosci. Abstr. 25: 1483. Google Scholar


M. M. Smith , V. A. Warren , B.S. Thomas , R. M. Brochu , E. A. Ertel , S. Rohrer , J. Schaeffer , D. Schmatz , B. R. Petuch , Y. S. Tang , P. T. Meinke , G J Kaczorowski , G. J. , and C. J. Cohen 2000. Nodulisporic acid opens insect glutamate-gated chloride channels: Identification of a new high affinity modulator. Biochem. 39: 5543–5554. Google Scholar


M. Sunesen , L. P. De Carvalho , V. Dufresne , R. GrailHe , N. Savatier-Duclert , G. Gibor A. Peretz , B. Attali , J.-P. Chanceux , and Y. Paas 2006. Mechanism of Cl- selection by a glutamate-gated chloride (GluCl) receptor revealed through mutations in the selectivity filter. J. Biol. Chem. 281(21): 14875–14881. Google Scholar


J. D. Thompson , T. J. Gibson , F. Plewniak , F. Jeanmougin , and D. G. Higgins 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876–4882. Google Scholar


C. C. Tingle , J. A. Rother , C. F. Dewhurst , S. Lauer , and W. J. King 2003. Fipronil: environmental fate, ecotoxicology, and human health concerns. Rev. Environ. Contam. Toxicol. 176: 1–66. Google Scholar


D. K. Vassilatis , K. O. Elliston , P. S. Paress , M. Hamelin , J. P. Arena , J. M. Schaeffer , L. H. T. Van Der Ploeg , and D. F. Cully 1997. Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate- gated chloride channels, J. Molec. Evol. 44: 501–508. Google Scholar


D. M. Yates , V. Portillo , and A. J. Wolstenholme 2003. The avermectin receptor of Haemonchus contortus and Caenorhabditis elegans. Intl. J. Parasitol. 33: 1183–1193. Google Scholar


X. Zhao , J. Z. Yeh , V. L. Salgado , and T. Narahashi 2004. Fipronil is a potent open channel blocker of glutamate-activated chloride channels in cockroach neurons. J. Pharmacol. Exp. Ther. 310: 192–201. Google Scholar


Xinghua Zhao , Ning Zuoping , He Yueping , Shen Jinliang , Su Jianya , Gao Congfen , and Zhu Yucehng . 2011. Differential resistance and crossresistance to three phenylpyrazole insecticides in the planthopper Nilaparvata lugens (Hemiptera: Delphacidae). J. Econ. Entomol. 104(4): 1364–1368. Google Scholar


X. Zhao , V. L. Salgado , J. Z. Yeh , and T. Narahashi 2004. Kinetic and pharmacological characterization of desensitizing and non-desensitizing glutamategated chloride channels in cockroach neurons, Neurotoxicol. 25: 967–980. Google Scholar
Yaoxue Dong, Yu Chen, Qi Wei, Jianya Su, and Congfen Gao "Cloning and Polymorphism Analysis of Glutamate-Gated Chloride Channel Gene of Laodelphax striatellus (Hemiptera: Delphacidae)," Florida Entomologist 96(3), 1168-1174, (1 September 2013).
Published: 1 September 2013
cDNA clone
clon de ADNc polimorfismo
Laodelphax striatellus
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