Molecular cloning and RNA interference-mediated functional characterization of a Halloween gene spook in the white-backed planthopper Sogatella furcifera

BMC Molecular Biology

Volumn 14, Issue , 2013, Pages

  Jia, Shuang ^a   Wan, Pin Jun ^a   Zhou, Li Tao ^a   Mu, Li Li ^a   Li, Guo Qing ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

Development; Ecdysteroidogenesis; Halloween gene; Lethality; RNA interference; Sogatella furcifera

Indexed keywords

CELL NUCLEUS RECEPTOR; DOUBLE STRANDED RNA; ECDYSONE RECEPTOR; INSECT PROTEIN; SFCYP307A1 PROTEIN; SFSPO PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; DEVELOPMENTAL STAGE; LETHALITY; MOLECULAR CLONING; NONHUMAN; NYMPH; PLANTHOPPER; PROTEIN EXPRESSION; PROTEIN MOTIF; RNA INTERFERENCE; SEQUENCE ANALYSIS; SOGATELLA FURCIFERA;

DIPTERA; HEMIPTERA; HEXAPODA; LEPIDOPTERA; ORTHOPTERA; SOGATELLA FURCIFERA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CLONING, MOLECULAR; CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; GENES, INSECT; GENES, LETHAL; HEMIPTERA; INSECT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, STEROID; RNA INTERFERENCE; SEQUENCE ALIGNMENT;

EID: 84883269788     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/1471-2199-14-19     Document Type: Article

References (63)

1. Iga M, Kataoka H. Recent studies on insect hormone metabolic pathways mediated by cytochrome P450 enzymes. Biol Pharm Bull 2012, 35(6):838-843. 10.1248/bpb.35.838, 22687472.
2. Behmer ST, David Nes W. Insect sterol nutrition and physiology: a global overview. Advances in insect physiology 2003, 31:1-72.
3. Chen CC, Cheng LL, Hou RF. Studies on the intracellular yeast-like symbiote in the brown planthopper, Nilaparvata lugens Stal. J Appl Entomol 1981, 92:440-449.
4. Pang K, Dong S-Z, Hou Y, Bian Y-L, Yang K, Yu X-P. Cultivation, identification and quantification of one species of yeast-like symbiotes, Candida, in the rice brown planthopper, Nilaparvata lugens. Insect Sci 2012, 19(4):477-484.
5. Dong SZ, Pang K, Bai X, Yu XP, Hao PY. Identification of two species of yeast-like symbiotes in the brown planthopper, Nilaparvata lugens. Curr Microbiol 2011, 62(4):1133-1138. 10.1007/s00284-010-9830-z, 21153730.
6. Noda H, Saito T. The role of intracelular yeastlike symbiotes in the development of Laodelphax striatellus (Homoptera: Delphacidae). Appl Environ Microbiol 1979, 14:453-458.
7. Noda H, Saito T. Histological and histochemical observation of intracellular yeastlike symbiotes in the fat body of the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Applied Entomology and Zoology 1977, 12:134-141.
8. Noda H. Preliminary histological observation and population dynamics of intracellular yeast-like symbiotes in the smaller brown planthopper, Laodelphax striatellus (Homoptera: Delphacidae). Applied Entomology and Zoology 1974, 9:275-277.
9. Noda H, Wada K, Saito T. Sterols in Laodelphax striatellus with special reference to the intracellular yeastlike symbiotes as a sterol source. J Insect Physiol 1979, 25(5):443-447.
10. Eya BK, Kenny PT, Tamura SY, Ohnishi M, Naya Y, Nakanishi K, Sugiura M. Chemical association in symbiosis, Sterol donors in planthoppers. J Chem Ecol 1989, 15(1):373-380.
11. Wetzel JM, Ohnishi M, Fujita T, Nakanishi K, Naya Y, Noda H, Sugiura M. Diversity in steroidogenesis of symbiotic microorganisms from planthoppers. J Chem Ecol 1992, 18(11):2083-2094.
12. Noda H, Koizumi Y. Sterol biosynthesis by symbiotes: cytochrome P450 sterol C-22 desaturase genes from yeastlike symbiotes of rice planthoppers and anobiid beetles. Insect Biochem Mol Biol 2003, 33(6):649-658. 10.1016/S0965-1748(03)00056-0, 12770582.
13. Yoshiyama T, Namiki T, Mita K, Kataoka H, Niwa R. Neverland is an evolutionally conserved Rieske-domain protein that is essential for ecdysone synthesis and insect growth. Development 2006, 133:2565-2574. 10.1242/dev.02428, 16763204.
14. Yoshiyama-Yanagawa T, Enya S, Shimada-Niwa Y, Yaguchi S, Haramoto Y, Matsuya T, Shiomi K, Sasakura Y, Takahashi S, Asashima M. The conserved rieske oxygenase DAF-36/neverland is a novel cholesterol-metabolizing enzyme. J Biol Chem 2011, 286(29):25756-25762. 10.1074/jbc.M111.244384, 3138242, 21632547.
15. Gilbert LI, Warren JT. A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam Horm 2005, 73:31-57.
16. Namiki T, Niwa R, Sakudoh T, Shirai K, Takeuchi H, Kataoka H. Cytochrome P450 CYP307A1/Spook: a regulator for ecdysone synthesis in insects. Biochemical and Biophysical Research Communication 2005, 337:367-374.
17. Ono H, Rewitz KF, Shinoda T, Itoyama K, Petryk A, Rybczynski R, Jarcho M, Warren JT, Marqués G, Shimell MJ. Spook and Spookier code for stage-specific components of the ecdysone biosynthetic pathway in Diptera. Dev Biol 2006, 298(2):555-570. 10.1016/j.ydbio.2006.07.023, 16949568.
18. Ou Q, Magico A, King-Jones K. Nuclear receptor DHR4 controls the timing of steroid hormone pulses during Drosophila development. PLoS Biol 2011, 9(9):e1001160. 10.1371/journal.pbio.1001160, 3181225, 21980261.
19. Ono H, Morita S, Asakura I, Nishida R. Conversion of 3-oxo steroids into ecdysteroids triggers molting and expression of 20E-inducible genes in Drosophila melanogaster. Biochem Biophys Res Commun 2012, 421(3):561-566. 10.1016/j.bbrc.2012.04.045, 22525676.
20. Luan J-B, Ghanim M, Liu S-S, Czosnek H. Silencing the ecdysone synthesis and signaling pathway genes disrupts nymphal development in the whitefly. Insect Biochem Mol Biol 2013, 43(8):740-746. 10.1016/j.ibmb.2013.05.012, 23748027.
21. Hentze JL, Moeller ME, Jørgensen AF, Bengtsson MS, Bordoy AM, Warren JT, Gilbert LI, Andersen O, Rewitz KF. Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects. PLoS One 2013, 8(2):e55131. 10.1371/journal.pone.0055131, 3562185, 23383307.
22. Yamazaki Y, Kiuchi M, Takeuchi H, Kubo T. Ecdysteroid biosynthesis in workers of the European honeybee Apis mellifera L. Insect Biochem Mol Biol 2011, 41(5):283-293. 10.1016/j.ibmb.2011.01.005, 21277979.
23. Iga M, Smagghe G. Identification and expression profile of Halloween genes involved in ecdysteroid biosynthesis in Spodoptera littoralis. Peptides 2010, 31(3):456-467. 10.1016/j.peptides.2009.08.002, 19682519.
24. Zhou J, Zhang H, Li J, Sheng X, Zong S, Luo Y, Weng Q. Molecular cloning and expression profile of a Halloween gene encoding CYP307A1 from the seabuckthorn carpenterworm, Holcocerus hippophaecolus. J Insect Sci 2012, 13:56.
25. Marchal E, Badisco L, Verlinden H, Vandersmissen T, Van Soest S, Van Wielendaele P, Vanden Broeck J. Role of the Halloween genes, Spook and Phantom in ecdysteroidogenesis in the desert locust, Schistocerca gregaria. J Insect Physiol 2011, 57(9):1240-1248. 10.1016/j.jinsphys.2011.05.009, 21708158.
26. Christiaens O, Iga M, Velarde R, Rougé P, Smagghe G. Halloween genes and nuclear receptors in ecdysteroid biosynthesis and signalling in the pea aphid. Insect Mol Biol 2010, 19:187-200.
27. Tan A, Palli SR. Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 2008, 291(1):42-49. 2595142, 18583027.
28. Wu W-J, Wang Y, Huang H-J, Bao Y-Y, Zhang C-X. Ecdysone receptor controls wing morphogenesis and melanization during rice planthopper metamorphosis. J Insect Physiol 2012, 58(3):420-426. 10.1016/j.jinsphys.2012.01.012, 22326762.
29. Karim FD, Thummel C. Temporal coordination of regulatory gene expression by the steroid hormone ecdysone. EMBO J 1992, 11(11):4083-4093. 556918, 1382981.
30. Varghese J, Cohen SM. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Science 2007, 21(18):2277-2282.
31. Matusmura M, Sanada-Morimura S. Recent status of insecticide resistance in Asian rice planthoppers. Japan Agricultural Research Quarterly 2010, 44(3):225-230.
32. Zhang P, Mar TT, Liu W, Li L, Wang X. Simultaneous detection and differentiation of Rice black streaked dwarf virus (RBSDV) and Southern rice black streaked dwarf virus (SRBSDV) by duplex real time RT-PCR. Virol J 2013, 10(1):24. 10.1186/1743-422X-10-24, 3610162, 23331990.
33. Matsukura K, Towata T, Sakai J, Onuki M, Okuda M, Matsumura M. Dynamics of Southern rice black-streaked dwarf virus in rice and implication for virus acquisition. Phytopathology 2013,
34. Fujita D, Kohli A, Horgan FG. Rice resistance to planthoppers and leafhoppers. Crit Rev Plant Sci 2013, 32(3):162-191.
35. Xu Y, Zhou W, Zhou Y, Wu J, Zhou X. Transcriptome and comparative gene expression analysis of Sogatella furcifera (Horváth) in response to southern rice black-streaked dwarf virus. PLoS One 2012, 7(4):e36238. 10.1371/journal.pone.0036238, 3338671, 22558400.
36. Zha W, Peng X, Chen R, Du B, Zhu L, He G. Knockdown of midgut genes by dsRNA-transgenic plant-mediated RNA interference in the hemipteran insect Nilaparvata lugens. PLoS One 2011, 6(5):e20504. 10.1371/journal.pone.0020504, 3105074, 21655219.
37. Li J, Chen QH, Lin YJ, Jiang TR, Wu G, Hua HX. RNA interference in Nilaparvata lugens (Homoptera: Delphacidae) based on dsRNA ingestion. Pest Manag Sci 2011, 67(7):852-859. 10.1002/ps.2124, 21370391.
38. Chen J, Zhang D, Yao Q, Zhang J, Dong X, Tian H, Zhang W. Feeding-based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens. Insect Mol Biol 2010, 19(6):777-786. 10.1111/j.1365-2583.2010.01038.x, 20726907.
39. He P, Zhang J, Liu NY, Zhang YN, Yang K, Dong SL. Distinct expression profiles and different functions of odorant binding proteins in Nilaparvata lugens Stål. PLoS One 2011, 6(12):e28921. 10.1371/journal.pone.0028921, 3235172, 22174925.
40. Werck-Reichhart D, Feyereisen R. Cytochromes P450: a success story. Genome Biol 2000, 1(6):reviews 3003.3001-3009.
41. Petryk A, Warren JT, Marqués G, Jarcho MP, Gilbert LI, Kahler J, Parvy JP, Li Y, Dauphin-Villemant C, O'Connor MB. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc Natl Acad Sci USA 2003, 100(24):13773-13778. 10.1073/pnas.2336088100, 283497, 14610274.
42. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI. Developmental expression of Manduca shade, the P450 mediating the final step in molting hormone synthesis. Mol Cell Endocrinol 2006, 247(1-2):166-174.
43. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI. The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem Soc Trans 2006, 34:1256-1260. 10.1042/BST0341256, 17073797.
44. Yamazaki Y, Kiuchi M, Takeuchi H, Kubo T. Ecdysteroid biosynthesis in workers of the European honeybee Apis mellifera L. Insect Biochem Mol Biol 2011, 41:283-293. 10.1016/j.ibmb.2011.01.005, 21277979.
45. Rewitz K, Gilbert L. Daphnia Halloween genes that encode cytochrome P450s mediating the synthesis of the arthropod molting hormone: Evolutionary implications. BMC Evol Biol 2008, 8(1):60. 10.1186/1471-2148-8-60, 2276477, 18298845.
46. Warren JT, Petryk A, Marqués G, Parvy JP, Shinoda T, Itoyama K, Kobayashi J, Jarcho M, Li Y, O'Connor MB. Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: a P450 enzyme critical in ecdysone biosynthesis. Insect Biochem Mol Biol 2004, 34(9):991-1010. 10.1016/j.ibmb.2004.06.009, 15350618.
47. Kobayashi M, Uchida M, Kuriyama K. Elevation of 20-hydroxyecdysone level by buprofezin in Nilaparvata lugens Stål nymphs. Pestic Biochem Physiol 1989, 34(1):9-16.
48. Niwa R, Matsuda T, Yoshiyama T, Namiki T, Mita K, Fujimoto Y, Kataoka H. CYP306A1, a cytochrome P450 enzyme, is essential for ecdysteroid biosynthesis in the prothoracic glands of Bombyx and Drosophila. J Biol Chem 2004, 279(34):35942-35949. 10.1074/jbc.M404514200, 15197185.
49. Chávez VM, Marqués G, Delbecque JP, Kobayashi K, Hollingsworth M, Burr J, Natzle JE, O'Connor MB. The Drosophila disembodied gene controls late embryonic morphogenesis and codes for a cytochrome P450 enzyme that regulates embryonic ecdysone levels. Development 2000, 127(19):4115-4126.
50. Niwa R, Sakudoh T, Namiki T, Saida K, Fujimoto Y, Kataoka H. The ecdysteroidogenic P450 Cyp302a1/disembodied from the silkworm, Bombyx mori, is transcriptionally regulated by prothoracicotropic hormone. Insect Mol Biol 2005, 14(5):563-571. 10.1111/j.1365-2583.2005.00587.x, 16164612.
51. Warren JT, Petryk A, Marqués G, Jarcho M, Parvy JP, Dauphin-Villemant C, O'Connor MB, Gilbert LI. Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc Natl Acad Sci USA 2002, 99(17):11043-11048. 10.1073/pnas.162375799, 123207, 12177427.
52. Varghese J, Cohen SM. microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Science Signalling 2007, 21(18):2277-2282.
53. Tan AJ, Palli SR. Edysone receptor isoforms play distinct roles in controlling molting and metamorphosis in the red flour beetle, Tribolium castaneum. Mol Cell Endocrinol 2008, 291:42-49. 10.1016/j.mce.2008.05.006, 2595142, 18583027.
54. Wu WJ, Wang Y, Huang HJ, Bao YY, Zhang CX. Ecdysone receptor controls wing morphogenesis and melanization during rice planthopper metamorphosis. J Insect Physiol 2012, 58:420-426. 10.1016/j.jinsphys.2012.01.012, 22326762.
55. Miyake T, Haruyama H, Mitsui T, Sakurai A. Effects of a new juvenile hormone mimic, NC-170, on metamorphosis and diapause of the small brown planthopper, Laodelphax striatellus. J Pestic Sci 1992, 17(1):75-82.
56. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652. 10.1038/nbt.1883, 3571712, 21572440.
57. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132(3):365-386.
58. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
59. Fu Q, Zhang Z, Hu C, Lai F, Sun Z. A chemically defined diet enables continuous rearing of the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Applied Entomology and Zoology 2001, 36(1):111-116.
60. Sun HX, Hu XJ, Shu YH, Zhang GR. Observation on the antennal sensilla of Sogatella furcifera (Horváth) (Homoptera: Delphacidae) with scanning electron microscope. Acta Entomologica Sinica 2006, 49(2):349-354.
61. Ding JH, Hu CL, Fu Q, He JC, Xie MC. A colour atlas of commonly encountered delphacidae in china rice regions 2012, 10-26. HangZhou, China: HangZhou Science and Technology Press.
62. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45. 10.1093/nar/29.9.e45, 55695, 11328886.
63. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3:RESEARCH0034. 126239, 12184808.