The genome- and transcriptome-wide analysis of innate immunity in the brown planthopper, Nilaparvata lugens

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Bao, Yan Yuan ^a   Qu, Lv Yu ^a   Zhao, Dong ^a   Chen, Li Bo ^a   Jin, Hong Yuan ^a   Xu, Liang Min ^a   Cheng, Jia An ^a   Zhang, Chuan Xi ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Gene expression; Genome; Hemimetabolous insect; Innate immunity; Nilaparvata lugens; Transcriptome

Indexed keywords

PATTERN RECOGNITION RECEPTOR; TRANSCRIPTOME;

ANIMAL TISSUE; ARTICLE; BETA GLUCAN RECOGNITION PROTEIN 1 GENE; BETA GLUCAN RECOGNITION PROTEIN 2 GENE; BETA GLUCAN RECOGNITION PROTEIN 3 GENE; BETA GLUCAN RECOGNITION PROTEIN 4 GENE; BETA GLUCAN RECOGNITION PROTEIN 5 GENE; BETA GLUCAN RECOGNITION PROTEIN 6 GENE; BETA GLUCAN RECOGNITION PROTEIN 7 GENE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC TRANSCRIPTION; GENOME ANALYSIS; IMMUNE RESPONSE GENE; INNATE IMMUNITY; INSECT DEVELOPMENT; INSECT GENETICS; INSECT GENOME; MALE; NILAPARVATA LUGENS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDOGLYCAN RECOGNITION PROTEIN LB GENE; PEPTIDOGLYCAN RECOGNITION PROTEIN LC GENE; PLANTHOPPER; SIGNAL TRANSDUCTION; SPECIES COMPARISON; SYMBIONT; VIRUS TRANSMISSION;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; GENOME, INSECT; HEMIPTERA; IMMUNITY, INNATE; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSCRIPTOME;

BACTERIA (MICROORGANISMS); HEXAPODA; NILAPARVATA LUGENS;

EID: 84874716210     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-160     Document Type: Article

References (75)

1. Wilkinson T, Ishikawa H. On the functional significance of symbiotic microorganisms in the Homoptera: a comparative study of Acyrthosiphon pisum and Nilaparvata lugens. Physiol Entomol 2001, 26(1):86-93.
2. Tang M, Lv L, Jing S, Zhu L, He G. Bacterial symbionts of the brown planthopper, Nilaparvata lugens (Homoptera: Delphacidae). Appl Environ Microbiol 2010, 76(6):1740-1745.
3. Jena KK, Kim SM. Current status of brown planthopper (BPH) resistance and genetics. Rice 2010, 3(2):161-171.
4. Nakashima N, Kawahara N, Omura T, Noda H. Characterization of a novel satellite virus and a strain of Himetobi P virus (Dicistroviridae) from the brown planthopper, Nilaparvata lugens. J Invertebr Pathol 2006, 91(1):53-56.
5. Wang Y, Jehle JA. Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: new insights on an old topic. J Invertebr Pathol 2009, 101(3):187-193.
6. Xue J, Bao YY, Li B, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA. Transcriptome analysis of the brown planthopper nilaparvata lugens. PLoS One 2010, 5(12):e14233.
7. Bao YY, Wang Y, Wu WJ, Zhao D, Xue J, Zhang BQ, Shen ZC, Zhang CX. De novo intestine-specific transcriptome of the brown planthopper Nilaparvata lugens revealed potential functions in digestion, detoxification and immune response. Genomics 2012, 99(4):256-264.
8. Yoshida H, Kinoshita K, Ashida M. Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. J Biol Chem 1996, 271(23):13854-13860.
9. Morishima I, Yamada K, Ueno T. Bacterial peptidoglycan as elicitor of antibacterial protein synthesis in larvae of the silkworm, Bombyx mori. Insect Biochem Mol Biol 1992, 22(4):363-367.
10. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, Lee WJ, Mengin-Lecreulx D, Lemaitre B. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 2003, 4(5):478-484.
11. Liu C, Xu Z, Gupta D, Dziarski R. Peptidoglycan recognition proteins. A novel family of four human innate immunity pattern recognition molecules. J Biol Chem 2001, 276(37):34686-34694.
12. Mellroth P, Karlsson J, Steiner H. A scavenger function for a DrosophilaPeptidoglycan recognition protein. J Biol Chem 2003, 278(9):7059-7064.
13. Werner T, Liu G, Kang D, Ekengren S, Steiner H, Hultmark D. A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci 2000, 97(25):13772-13777.
14. Gelius E, Persson C, Karlsson J, Steiner H. A mammalian peptidoglycan recognition protein with N-acetylmuramoyl-alanine amidase activity. Biochem Biophys Res Commun 2003, 306(4):988-994.
15. Royet J, Dziarski R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nat Rev Microbiol 2007, 5(4):264-277.
16. Zaidman-Rémy A, Hervé M, Poidevin M, Pili-Floury S, Kim MS, Blanot D, Oh BH, Ueda R, Mengin-Lecreulx D, Lemaitre B. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 2006, 24(4):463-473.
17. Steiner H. Peptidoglycan recognition proteins: on and off switches for innate immunity. Immunol Rev 2004, 198(1):83-96.
18. Ramsey JS, Rider DS, Walsh TK, De Vos M, Gordon K, Ponnala L, Macmil S, Roe B, Jander G. Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Mol Biol 2010, 19:155-164.
19. Zaidman-Rémy A, Poidevin M, Hervé M, Welchman DP, Paredes JC, Fahlander C, Steiner H, Mengin-Lecreulx D, Lemaitre B. Drosophila immunity: analysis of PGRP-SB1 expression. Enzymatic Activity and Function. PLoS One 2011, 6(2):e17231.
20. Mellroth PS. H: PGRP-SB1: An N-acetylmuramoyll-alanineamidase with antibacterialactivity. Biochem Biophys Res Commun 2006, 350(4):994-999.
21. Kim MS, Byun M, Oh BH. Crystal structure of peptidoglycan recognition protein LB from Drosophila melanogaster. Nat Immunol 2003, 4(8):787-793.
22. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV. Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Sci STKE 2002, 296(5566):359.
23. Ochiai M, Ashida M. Purification of a beta-1, 3-glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm. Bombyx mori. J Biol Chem 1988, 263(24):12056.
24. Kim YS, Ryu JH, Han SJ, Choi KH, Nam KB, Jang IH, Lemaitre B, Brey PT, Lee WJ. Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and β-1, 3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J Biol Chem 2000, 275(42):32721-32727.
25. Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N, Yoshiyama M, Kaneko Y, Iwasaki T. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 2008, 38(12):1087-1110.
26. Gobert V, Gottar M, Matskevich AA, Rutschmann S, Royet J, Belvin M, Hoffmann JA, Ferrandon D. Dual activation of the Drosophila toll pathway by two pattern recognition receptors. Sci STKE 2003, 302(5653):2126.
27. Ferrandon D, Imler JL, Hetru C, Hoffmann JA. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 2007, 7(11):862-874.
28. Gottar M, Gobert V, Matskevich AA, Reichhart JM, Wang C, Butt TM, Belvin M, Hoffmann JA, Ferrandon D. Dual detection of fungal infections in drosophila via recognition of glucans and sensing of virulence factors. Cell 2006, 127(7):1425-1437.
29. Hoffmann JA. The immune response of Drosophila. Nature 2003, 426(6962):33-38.
30. Ochiai M, Ashida M. A pattern-recognition protein for β-1, 3-glucan. The binding domain and the cDNA cloning of beta-1,3-glucan recognition protein from the silkworm, bombyx mori. J Biol Chem 2000, 275(7):4995-5002.
31. Takahasi K, Ochiai M, Horiuchi M, Kumeta H, Ogura K, Ashida M, Inagaki F. Solution structure of the silkworm βGRP/GNBP3 N-terminal domain reveals the mechanism for β-1, 3-glucan-specific recognition. Proc Natl Acad Sci 2009, 106(28):11679-11684.
32. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 2007, 25:697-743.
33. Cherry S, Silverman N. Host-pathogen interactions in drosophila: new tricks from an old friend. Nat Immunol 2006, 7(9):911-917.
34. Hoffmann JA, Reichhart JM. Drosophila innate immunity: an evolutionary perspective. Nat Immunol 2002, 3(2):121-126.
35. Gregorio DE, Spellman PT, Tzou P, Rubin GM, Lemaitre B. The Toll and Imd pathways are the major regulators of the immune response in Drosophila. EMBO J 2002, 21(11):2568-2579.
36. Hashimoto C, Hudson KL, Anderson KV. The Toll gene of drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 1988, 52(2):269-279.
37. Xu Y, Tao X, Shen B, Horng T, Medzhitov R, Manley JL, Tong L. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 2000, 408(6808):111-115.
38. Cheng TC, Zhang YL, Liu C, Xu PZ, Gao Z, Xia QY, Xiang ZH. Identification and analysis of Toll-related genes in the domesticated silkworm, Bombyx mori. Dev Comp Immunol 2008, 32(5):464-475.
39. Söderhäll I, Wu C, Novotny M, Lee BL, Söderhäll K. A novel protein acts as a negative regulator of prophenoloxidase activation and melanization in the freshwater crayfish Pacifastacus leniusculus. J Biol Chem 2009, 284(10):6301-6310.
40. Cerenius L, Kawabata S, Lee BL, Nonaka M, Soderhall K. Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 2010, 35(10):575-583.
41. Kanost M, Clarke T. Proteases. Comprehensive molecular insect science 2005, 4:247-266.
42. Jiang H, Wang Y, Yu XQ, Zhu Y, Kanost M. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1 J and serine proteinase homologs. Insect Biochem Mol Biol 2003, 33(10):1049-1060.
43. Bao Y, Yamano Y, Morishima I. β-1, 3-Glucan inducible expression of prophenoloxidase-activating proteinase from eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol B Biochem Mol Biol 2007, 147(1):45-48.
44. Jiang H, Kanost MR. The clip-domain family of serine proteinases in arthropods. Insect Biochem Mol Biol 2000, 30(2):95.
45. Satoh D, Horii A, Ochiai M, Ashida M. Prophenoloxidase-activating enzyme of the silkworm, Bombyx mori. J Biol Chem 1999, 274(11):7441-7453.
46. Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 2008, 29(6):263-271.
47. De Gregorio E, Han SJ, Lee WJ, Baek MJ, Osaki T, Kawabata SI, Lee BL, Iwanaga S, Lemaitre B, Brey PT. An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev Cell 2002, 3(4):581-592.
48. Kanost MR, Jiang H, Yu XQ. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 2004, 198(1):97-105.
49. Tong Y, Kanost MR. Manduca sexta serpin-4 and serpin-5 inhibit the prophenol oxidase activation pathway. J Biol Chem 2005, 280(15):14923-14931.
50. Tong Y, Jiang H, Kanost MR. Identification of plasma proteases inhibited by Manduca sexta serpin-4 and serpin-5 and their association with components of the prophenol oxidase activation pathway. J Biol Chem 2005, 280(15):14932-14942.
51. Aggarwal K, Silverman N. Positive and negative regulation of the Drosophila immune response. BMB Rep 2008, 41(4):267-277.
52. Gandhe AS, John SH, Nagaraju J. Noduler, a novel immune up-regulated protein mediates nodulation response in insects. J Immunol 2007, 179(10):6943.
53. Zhu Y, Johnson TJ, Myers AA, Kanost MR. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect Biochem Mol Biol 2003, 33(5):541-559.
54. Shin SW, Park SS, Park DS, Kim MG, Kim SC, Brey PT, Park HY. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochem Mol Biol 1998, 28(11):827-837.
55. Bao Y, Mega K, Yamano Y, Morishima I. cDNA cloning and expression of bacteria-induced Hdd11 gene from eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol C Toxicol Pharmacol 2003, 136(4):337-342.
56. Veiga AB, Ribeiro JM, Guimaraes JA, Francischetti IM. A catalog for the transcripts from the venomous structures of the caterpillar Lonomia obliqua: identification of the proteins potentially involved in the coagulation disorder and hemorrhagic syndrome. Gene 2005, 355:11-27.
57. Bao Y, Xue J, Wu W, Wang Y, Lv Z, Zhang C. An immune-induced reeler protein is involved in the Bombyx mori melanization cascade. Insect Biochem Mol Biol 2011, 41(9):696.
58. Callewaert L, Michiels CW. Lysozymes in the animal kingdom. J Biosci 2010, 35(1):127-160.
59. Zou H, Song L, Xu W, Yang G. Molecular cloning and characterization analysis of cDNA encoding g-type lysozyme from scallop (Argopecten irradians). High Tech Lett 2005, 15:101-106.
60. Zhao J, Song L, Li C, Zou H, Ni D, Wang W, Xu W. Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol Immunol 2007, 44(6):1198-1208.
61. Irwin DM, Gong ZM. Molecular evolution of vertebrate goose-type lysozyme genes. J Mol Evol 2003, 56(2):234-242.
62. Nilsen I, Myrnes B, Edvardsen R, Chourrout D. Urochordates carry multiple genes for goose-type lysozyme and no genes for chicken-or invertebrate-type lysozymes. Cell Mol Life Sci 2003, 60(10):2210-2218.
63. Li B, Calvo E, Marinotti O, James AA, Paskewitz SM. Characterization of the c-type lysozyme gene family in Anopheles gambiae. Gene 2005, 360(2):131-139.
64. Paskewitz S, Li B, Kajla M. Cloning and molecular characterization of two invertebrate-type lysozymes from Anopheles gambiae. Insect Mol Biol 2008, 17(3):217-225.
65. Ito Y, Yoshikawa A, Hotani T, Fukuda S, Sugimura K, Imoto T. Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur J Biochem 1999, 259(1-2):456-461.
66. Itoh N, Takahashi KG. cDNA cloning and in situ hybridization of a novel lysozyme in the Pacific oyster, Crassostrea gigas. Comp Biochem Physiol B Biochem Mol Biol 2007, 148(2):160-166.
67. Xue QG, Itoh N, Schey K, Li YL, Cooper R, La Peyre J. A new lysozyme from the eastern oyster (Crassostrea virginica) indicates adaptive evolution of i-type lysozymes. Cell Mol Life Sci 2007, 64(1):82-95.
68. Olsen OM, Nilsen IW, Sletten K, Myrnes B. Multiple invertebrate lysozymes in blue mussel (Mytilus edulis). Comp Biochem Physiol B Biochem Mol Biol 2003, 136(1):107-115.
69. Zavalova L, Baskova I, Lukyanov S, Sass A, Snezhkov E, Akopov S, Artamonova I, Archipova V, Nesmeyanov V, Kozlov D. Destabilase from the medicinal leech is a representative of a novel family of lysozymes. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology 2000, 1478(1):69-77.
70. Touch V, Hayakawa S, Saitoh K. Relationships between conformational changes and antimicrobial activity of lysozyme upon reduction of its disulfide bonds. Food Chem 2004, 84(3):421-428.
71. Zavalova L, Yudina T, Artamonova I, Baskova I. Antibacterial non-glycosidase activity of invertebrate destabilase-lysozyme and of its helical amphipathic peptides. Chemotherapy 2006, 52(3):158-160.
72. Cong L, Yang X, Wang X, Tada M, Lu M, Liu H, Zhu B. Characterization of an i-type lysozyme gene from the sea cucumber Stichopus japonicus, and enzymatic and nonenzymatic antimicrobial activities of its recombinant protein. J Biosci Bioeng 2009, 107(6):583-588.
73. Consortium IAG. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 2010, 8(2):e1000313.
74. Kocks C, Cho JH, Nehme N, Ulvila J, Pearson AM, Meister M, Strom C, Conto SL, Hetru C, Stuart LM. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in drosophila. Cell 2005, 123(2):335-346.
75. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25(24):4876-4882.