Genomic Insights into the Glutathione S-Transferase Gene Family of Two Rice Planthoppers, Nilaparvata lugens (Stål) and Sogatella furcifera (Horváth) (Hemiptera: Delphacidae)

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Zhou, Wen Wu ^a   Liang, Qing Mei ^a   Xu, Yi ^b   Gurr, Geoff M ^a,c   Bao, Yan Yuan ^a   Zhou, Xue Ping ^b   Zhang, Chuan Xi ^a   Cheng, Jiaan ^a   Zhu, Zeng Rong ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c CHARLES STURT UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BUPROFEZIN; CHLORPYRIFOS; CIPERMETHRIN; GLUTATHIONE TRANSFERASE; IMIDACLOPRID; INSECTICIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXON; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; GENOMICS; GLUTATHIONE S TRANSFERASE GENE; IMAGO; INSECT GENOME; INSECTICIDE RESISTANCE; INTRON; MALE; NIGSTE1 GENE; NIGSTM2 GENE; NILAPARVATA LUGENS; NONHUMAN; NUCLEOTIDE SEQUENCE; NYMPH; PLANTHOPPER; RNA INTERFERENCE; SOGATELLA FURCIFERA; UNINDEXED SEQUENCE; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; DATABASES, GENETIC; DRUG RESISTANCE; GENOMICS; GLUTATHIONE TRANSFERASE; HEMIPTERA; INSECTICIDES; MOLECULAR SEQUENCE DATA; NYMPH; ORGAN SPECIFICITY; ORYZA SATIVA; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; TRANSCRIPTOME;

EID: 84874003210     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056604     Document Type: Article

References (71)

1. Despres L, David JP, Gallet C, (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22: 298-307.
2. Enayati AA, Ranson H, Hemingway J, (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14: 3-8.
3. Li XC, Schuler MA, Berenbaum MR, (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231-253.
4. Skopelitou K, Muleta AW, Pavli O, Skaracis GN, Flemetakis E, et al. (2012) Overlapping protective roles for glutathione transferase gene family members in chemical and oxidative stress response in Agrobacterium tumefaciens. Funct Integr Genomics 12: 157-172.
5. Zou S, Meadows S, Sharp L, Jan LY, Jan YN, (2000) Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. Proc Natl Acad Sci U S A 97: 13726-13731.
6. Hayes JD, Pulford DJ, (1995) The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol 30: 445-600.
7. Ketterman AJ, Saisawang C, Wongsantichon J, (2011) Insect glutathione transferases. Drug Metab Rev 43: 253-265.
8. Friedman R, (2011) Genomic organization of the glutathione S-transferase family in insects. Mol Phylogenet Evol 61: 924-932.
9. Catindig JLA, Arida GS, Baehaki SE, Bentur JS, Cuong LQ,et al. (2009) Situation of planthoppers in Asia. In: Heong KL, Hardy B, editors. Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. Los Baños: International Rice Research Institute. pp. 191-220.
10. Zhou GH, Wen JJ, Cai DJ, Li P, Xu DL, et al. (2008) Southern rice black-streaked dwarf virus: A new proposed Fijivirus speices in the family Reoviridae. Chinese Sci Bull 53: 3677-3685.
11. Cheng JA (2009) Rice planthopper problems and relevant causes in China. In: Heong KL, Hardy B, editors. Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. Los Baños: International Rice Research Institute. pp. 157-178.
12. Kenmore PE (1991) Indonesia's integrated pest management-a model of Asia. FAO Rice IPM Programme. Manila, Philippines: FAO-Manila.
13. Yang ZF, Zhang FT, He Q, He GC, (2005) Tolerance genes in brown planthopper (Nilaparvata lugens Stål., Homoptera: Delphacidae) feeding on resistant rice plants. Arch Insect Biochem Mol Biol 59: 59-66.
14. Yao HW, Jiang CY, Ye GY, Cheng JA, (2002) Studies on cultivar-induced changes in insecticide susceptibility and its related enzyme activities of the white backed planthopper, Sogatella furcifera (Horváth) (Homoptera: Delphacidae). Insect Sci 9: 9-15.
15. Liu ZW, Han ZJ, (2006) Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stal. Pest Manag Sci 62: 279-282.
16. Vontas JG, Small GJ, Nikou DC, Ranson H, Hemingway J, (2002) Purification, molecular cloning and heterologous expression of a glutathione S-transferase involved in insecticide resistance from the rice brown planthopper, Nilaparvata lugens. Biochem J 362: 329-337.
17. Tang J, Li J, Shao Y, Yang BJ, Liu ZW, (2010) Fipronil resistance in the whitebacked planthopper (Sogatella furcifera): possible resistance mechanisms and cross-resistance. Pest Manag Sci 66: 121-125.
18. Zhou WW, Li XW, Quan YH, Cheng JA, Zhang CX, et al. (2012) Identification and expression profiles of nine glutathione S-transferase genes from an important rice phloem sap-sucker and virus vector Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae). Pest Manag Sci 68: 1296-1305.
19. Yang ZH, Nielsen R, (1998) Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 46: 409-418.
20. Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, et al. (2002) Evolution of supergene families associated with insecticide resistance. Science 298: 179-181.
21. Zou FM, Lou DS, Zhu YH, Wang SP, Jin BR, et al. (2011) Expression profiles of glutathione S-transferase genes in larval midgut of Bombyx mori exposed to insect hormones. Mol Biol Rep 38: 639-647.
22. Qin G, Jia M, Liu T, Xuan T, Yan Zhu K, et al. (2011) Identification and characterisation of ten glutathione S-transferase genes from oriental migratory locust, Locusta migratoria manilensis (Meyen). Pest Manag Sci 67: 697-704.
23. Feng QL, Davey KG, S D Pang A, Ladd TR, Retnakaran A, et al. (2001) Developmental expression and stress induction of glutathione Stransferase in the spruce budworm, Choristoneura fumiferana. J Insect Physiol 47: 1-10.
24. Pannabecker T, (1995) Physiology of the Malpighian Tubule. Annu Rev Entomol 40: 493-510.
25. Ortelli F, Rossiter LC, Vontas J, Ranson H, Hemingway J, (2003) Heterologous expression of four glutathione transferase genes genetically linked to a major insecticide-resistance locus from the malaria vector Anopheles gambiae. Biochem J 373: 957-963.
26. Hemingway J, Ranson H, (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45: 371-391.
27. Vontas JG, Small GJ, Hemingway J, (2001) Glutathione S-transferases as antioxidant defence agents confer pyrethroid resistance in Nilaparvata lugens. Biochem J 357: 65-72.
28. Singh SP, Coronella JA, Benes H, Cochrane BJ, Zimniak P, (2001) Catalytic function of Drosophila melanogaster glutathione S-transferase DmGSTS1-1 (GST-2) in conjugation of lipid peroxidation end products. Eur J Biochem 268: 2912-2923.
29. Wongtrakul J, Pongjaroenkit S, Leelapat P, Nachaiwieng W, Prapanthadara LA, et al. (2010) Expression and characterization of three new glutathione transferases, an epsilon (AcGSTE2-2), omega (AcGSTO1-1), and theta (AeGSTT1-1) from Anopheles cracens (Diptera: Culicidae), a major Thai malaria vector. J Med Entomol 47: 162-171.
30. Yamamoto K, Shigeoka Y, Aso Y, Banno Y, Kimura M, et al. (2009) Molecular and biochemical characterization of a Zeta-class glutathione S-transferase of the silkmoth. Pestic Biochem Phys 94: 30-35.
31. Liu SH, Ding ZP, Zhang CW, Yang BJ, Liu ZW, (2010) Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 40: 666-671.
32. Li J, Chen QH, Lin YJ, Jiang TR, Wu G, et al. (2011) RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion. Pest Manag Sci 67: 852-859.
33. Chen J, Zhang D, Yao Q, Zhang J, Dong X, et al. (2010) Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Mol Biol 19: 777-786.
34. Zha WJ, Peng XX, Chen RZ, Du B, Zhu LL, et al. (2011) Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. Plos One 6: e20504.
35. Ding JH, (1981) A review of studies on classification and species of the genus Nilaparvata distant (Homoptera: Delphacidae). Journal Nanjing Agr U 1: 78-85.
36. Asano K, Yamasaki M, Takuno S, Miura K, Katagiri S, et al. (2011) Artificial selection for a green revolution gene during japonica rice domestication. Proc Natl Acad Sci U S A 108: 11034-11039.
37. Fukumorita T, Chino M, (1982) Sugar, amino acid and inorganic contents in rice phloem sap. Plant Cell Physiol 23: 273-283.
38. Hayashi H, Chino M, (1985) Nitrate and other anions in the rice phloem sap. Plant Cell Physiol 26: 325-330.
39. Kawabe S, Fukumorita T, Chino M, (1980) Collection of rice phloem sap from stylets of homopterous insects severed by YAG laser. Plant Cell Physiol 21: 1319-1327.
40. Hayashi H, Chino M, (1990) Chemical composition of phloem sap from the uppermost internode of the rice plant. Plant Cell Physiol 31: 247-251.
41. Niranjan RBP, Prasad GB, Raghavendra K, (2011) In silico characterization and comparative genomic analysis of the Culex quinquefasciatus glutathione S-transferase (GST) supergene family. Parasitol Res 109: 1165-1177.
42. Vit P, Santiago B, (2008) Chemical composition of fresh bee pollen collected in the Misinta paramo from the Venezuelan Andes. Arch Latinoam Nutr 58: 411-415.
43. Nardini L, Christian RN, Coetzer N, Ranson H, Coetzee M, et al. (2012) Detoxification enzymes associated with insecticide resistance in laboratory strains of Anopheles arabiensis of different geographic origin. Parasit Vectors 5: 113.
44. Li X, Zhang X, Zhang J, Zhang X, Starkey SR, et al. (2009) Identification and characterization of eleven glutathione S-transferase genes from the aquatic midge Chironomus tentans (Diptera: Chironomidae). Insect Biochem Mol Biol 39: 745-754.
45. Nair PMG, Choi J, (2011) Identification, characterization and expression profiles of Chironomus riparius glutathione S-transferase (GST) genes in response to cadmium and silver nanoparticles exposure. Aquat Toxicol 101: 550-560.
46. Singh M, Silva E, Schulze S, Sinclair DA, Fitzpatrick KA, et al. (2000) Cloning and characterization of a new theta-class glutathione-S-transferase (GST) gene, gst-3, from Drosophila melanogaster. Gene 247: 167-173.
47. Lougarre A, Bride JM, Fournier D, (1999) Is the insect glutathione S-transferase I gene family intronless. Insect Mol Biol 8: 141-143.
48. Ding Y, Ortelli F, Rossiter LC, Hemingway J, Ranson H, (2003) The Anopheles gambiae glutathione transferase supergene family: annotation, phylogeny and expression profiles. BMC Genomics 4: 35.
49. Fedorov A, Roy S, Fedorova L, Gilbert W, (2003) Mystery of intron gain. Genome Res 13: 2236-2241.
50. Otuka A, Watanabe T, Suzuki Y, Matsumura M, Furuno A, et al. (2005) A migration analysis of the rice planthopper Nilaparvata lugens from the Philippines to East Asia with three-dimensional computer simulations. Popul Ecol 47: 143-150.
51. Sezer M, Butlin RK, (1998) The genetic basis of host plant adaptation in the brown planthopper (Nilaparvata lugens). Heredity 80: 499-508.
52. Morgenstern R (2005) Microsomal glutathione transferase 1. Gluthione Transferases and Gamma-Glutamyl Transpeptidases. In: Sies H, Packer L, editors. Methods in enzymology, Volume 401. Waltham, MA: Academic Press. pp. 136-146.
53. Aigaki T, Toba G, (2000) Disruption of the Microsomal glutathione S-transferase-like gene reduces life span of Drosophila melanogaster. Gene 253: 179-187.
54. Hemingway J, Karunaratne SHPP, Claridge MF, (1999) Insecticide resistance spectrum and underlying resistance mechanisms in tropical populations of the brown planthopper (Nilaparvata lugens) collected from rice and the wild grass Leersia hexandra. Int J Pest Manage 45: 215-223.
55. Lumjuan N, Rajatileka S, Changsom D, Wicheer J, Leelapat P, et al. (2011) The role of the Aedes aegypti Epsilon glutathione transferases in conferring resistance to DDT and pyrethroid insecticides. Insect Biochem Mol Biol 41: 203-209.
56. Bass C, Hebsgaard MB, Hughes J, (2012) Genomic resources for the brown planthopper, Nilaparvata lugens: Transcriptome pyrosequencing and microarray design. Insect Sci 19: 1-12.
57. Noda H, Kawai S, Koizumi Y, Matsui K, Zhang Q, et al. (2008) Annotated ESTs from various tissues of the brown planthopper Nilaparvata lugens: A genomic resource for studying agricultural pests. BMC Genomics 9.
58. Xue J, Bao YY, Li BL, Cheng YB, Peng ZY, et al. (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS One 5: e14233.
59. Xu Y, Zhou WW, Zhou YJ, Wu JX, Zhou XP, (2012) Transcriptome and Comparative Gene Expression Analysis of Sogatella furcifera (Horváth) in Response to Southern Rice Black-Streaked Dwarf Virus. PLoS One 7: e36238.
60. Nagata T, Masuda T, Moriya S, (1979) Development of insecticide resistance in the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Appl Entomol Zool 14: 264-269.
61. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
62. Liu SH, Ding ZP, Zhang CW, Yang BJ, Liu ZW, (2010) Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 40: 666-671.
63. Meng JY, Zhang CY, Zhu F, Wang XP, Lei CL, (2009) Ultraviolet light-induced oxidative stress: effects on antioxidant response of Helicoverpa armigera adults. J Insect Physiol 55: 588-592.
64. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, et al. (2000) The genome sequence of Drosophila melanogaster. Science 287: 2185-2195.
65. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.
66. Ranson H, Strode C, Wondji CS, David JP, Hawkes NJ, et al. (2008) Genomic analysis of detoxification genes in the mosquito Aedes aegypti. Insect Biochem Mol Biol 38: 113-123.
67. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931-949.
68. Oakeshott JG, Johnson RM, Berenbaum MR, Ranson H, Cristino AS, et al. (2010) Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Mol Biol 19: 147-163.
69. Kim HS, Murphy T, Xia J, Caragea D, Park Y, et al. (2010) BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res 38: D437-442.
70. Yu QY, Lu C, Li B, Fang SM, Zuo WD, et al. (2008) Identification, genomic organization and expression pattern of glutathione S-transferase in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38: 1158-1164.
71. Ramsey JS, Rider DS, Walsh TK, De Vos M, Gordon KHJ, et al. (2010) Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Mol Biol 19: 155-164.