Silencing Abnormal Wing Disc Gene of the Asian Citrus Psyllid, Diaphorina citri Disrupts Adult Wing Development and Increases Nymph Mortality

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  El Shesheny, Ibrahim ^a,b   Hajeri, Subhas ^a   El Hawary, Ibrahim ^b   Gowda, Siddarame ^a   Killiny, Nabil ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b Tanta University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; MESSENGER RNA; NUCLEOSIDE DIPHOSPHATE KINASE;

ARTICLE; AWD GENE; BACTERIUM CARRIER; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIAPHORINA CITRI; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; INSECT CONTROL; INSECT DEVELOPMENT; INSECT GENOME; INSECTICIDAL ACTIVITY; METAMORPHOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; NYMPH; PHENOTYPE; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; WINGED INSECT;

AMINO ACID SEQUENCE; ANIMALS; CITRUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMIPTERA; HOST-PARASITE INTERACTIONS; INSECT CONTROL; INSECT PROTEINS; INSECT VECTORS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOSIDE-DIPHOSPHATE KINASE; NYMPH; PLANT DISEASES; PROTEIN CONFORMATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHIZOBIACEAE; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; WING;

BACTERIA (MICROORGANISMS); CANDIDATUS LIBERIBACTER ASIATICUS; CITRUS; DIAPHORINA CITRI; HEXAPODA; PSYLLIDAE;

EID: 84878447750     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065392     Document Type: Article

References (86)

1. Dudley R, Byrnes G, Yanoviak SP, Borrell B, Brown RM, et al. (2007) Gliding and the Functional Origins of Flight: Biomechanical Novelty or Necessity? Annu Rev Ecol Evol Syst 38: 179-201.
2. Lewin R, (1985) On the Origin of Insect Wings: Experimental data on thermoregulation and aerodynamics give the first quantitative test of a popular hypothesis for the evolution of flight in insects. Science 230: 428-429.
3. Romoser W, Stoffolano J G (1998) The Science of Entomology. McGraw-Hill Companies Inc., Boston, MA., 326 p.
4. Baldassari N, Baronio P, Němec V, Rejzek M, Wimmer Z, (1997) Control of Cacopsylla (Psylla) pyri (L.) (Stenorhyncha, Psyllidae) by juvenile hormone analogues. J Appl Ent 121: 343-351.
5. Goberdhan DC, Paricio N, Goodman EC, Mlodzik M, Wilson C, (1999) Drosophila tumor suppressor PTEN controls cell size and number by antagonizing the Chico/PI3-kinase signaling pathway. Genes Dev 13: 3244-3258.
6. Timmons L, Shearn A, (2000) Role of AWD/nucleoside diphosphate kinase in Drosophila development. J. Bioenerg Biomembr 32: 293-300.
7. Matsunaga TM, Fujiwara H, (2002) Identification and characterization of genes abnormally expressed in wing-deficient mutant (flagella) of the silkworm, Bombyx mori. Insect Biochem Mol Biol 32: 691-699.
8. Dewey EM, McNabb SL, Ewer J, Kuo GR, Takanishi CL, et al. (2004) Identification of the gene encoding bursicon, an insect neuropeptide responsible for cuticle sclerotization and wing spreading. Curr Biol 14: 1208-1213.
9. Huang J, Zhang Y, Li M, Wang S, Liu W, et al. (2007) RNA interference-mediated silencing of the bursicon gene induces defects in wing expansion of silkworm. FEBS Lett 581: 697-701.
10. Koyama T, Syropyatova MO, Riddiford LM, (2008) Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone. Dev Biol 324: 258-265.
11. Sato K, Matsunaga TM, Futahashi R, Kojima T, Mita K, et al. (2008) Positional Cloning of a Bombyx wingless locus flagellos (fl) reveals a crucial role for fringe That Is Specific for Wing Morphogenesis. Genetics 179: 875-885.
12. Cohen B, McGuffin ME, Pfeifle C, Segal D, Cohen SM, (1992) apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6: 715-729.
13. Konopova B, Smykal V, Jindra M, (2011) Common and Distinct Roles of Juvenile Hormone Signaling Genes in Metamorphosis of Holometabolous and Hemimetabolous Insects. PLoS One 6: e28728.
14. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry- 5th Edition. WH Freeman and Company. 476 p.
15. Zhao XN, Tong DF, Jiang CY, Zhang YZ, (2009) Expression and purification of abnormal wing disc gene from silkworm, Bombyx mori. Bull [in Chinese] Sericulture 40: 20-25.
16. Jiang DF, Liu YQ, Li XS, Shi SL, (2010) Characterization of the Antheraea pernyi abnormal wing disc gene that may contribute to its temperature tolerance. African J Biotech 9: 7372-7378.
17. Rosengard AM, Krutzsch HC, Shearn A, Biggs JR, Barker E, et al. (1989) Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development. Nature 342: 177-180.
18. Biggs J, Hersperger E, Steeg PS, Liotta LA, Shearn A, (1990) A Drosophila gene that is homologous to a mammalian gene associated with tumor metastasis codes for a nucleoside diphosphate kinase. Cell 63: 933-940.
19. Whyard S, Singh AD, Wong S, (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem Mol Biol 39: 824-832.
20. Izant J, Weintraub H, (1984) Inhibition of thymidine kinase gene expression by antisense RNA: a molecular approach to genetic analysis. Cell 36: 1007-1015.
21. Fire A, Albertson D, Harrison S, Moerman D, (1991) Production of antisenseRNA leads to effective and specific inhibition of gene expression in C. elegans muscle. Development 113: 503-514.
22. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-810.
23. Chen X, Tian H, Zou L, Tang B, Hu J, et al. (2008) Disruption of Spodoptera exigua larval development by silencing chitin synthase gene A with RNA interference. Bull Entomol Res 98: 613-619.
24. Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, et al. (2011) RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57: 231-245.
25. Rajagopal R, Sivakumar S, Agrawal N, Malhotra P, Bhatnagar RK, (2002) Silencing of midgut aminopeptidase N of Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J Biol Chem. 277: 46849-46851.
26. Bautista MA, Miyata T, Miura K, Tanaka T, (2009) RNA interference-mediated knockdown of a cytochrome P450, CYP6BG1, from the diamondback moth, Plutella xylostella, reduces larval resistance to permethrin. Insect Biochem Mol Biol 39: 38-46.
27. Yang Y, Zhu YC, Ottea J, Husseneder C, Leonard BR, et al. (2010) Molecular characterization and RNA interference of three midgut aminopeptidase N isozymes from Bacillus thuringiensis-susceptible and-resistant strains of sugarcane borer, Diatraea saccharalis. Insect Biochem Mol Biol. 40: 592-603.
28. Masumoto M, Yaginuma T, Niimi T, (2009) Functional analysis of Ultra bithorax in the silkworm, Bombyx mori, using RNAi. Dev Genes Evol 219: 437-444.
29. Tomita S, Kikuchi A, (2009) Abd-B suppresses lepidopteran proleg development in posterior abdomen. Dev Biol 328: 403-409.
30. Liu W, Yang F, Jia S, Miao X, Huang Y, (2008) Cloning and characterization of Bmrunt from the silkworm Bombyx mori during embryonic development. Arch Insect Biochem Physiol 69: 47-59.
31. Dai H, Ma L, Wang J, Jiang R, Wang Z, et al. (2008) Knockdown of ecdysis-triggering hormone gene with a binary UAS/GAL4 RNA interference system leads to lethal ecdysis deficiency in silkworm. Acta Biochim Biophys Sin (Shanghai) 40: 790-795.
32. Hossain M, Shimizu S, Matsuki M, Imamura M, Sakurai S, et al. (2008) Expression of 20-hydroxyecdysone-induced genes in the silkworm brain and their functional analysis in post-embryonic development. Insect Biochem Mol Biol 38: 1001-1007.
33. Tsuzuki S, Sekiguchi S, Kamimura M, Kiuchi M, Hayakawa Y, (2005) A cytokine secreted from the suboesophageal body is essential for morphogenesis of the insect head. Mech Dev 122: 189-197.
34. Khajuria C, Buschman LL, Chen MS, Muthukrishnan S, Zhu KY, (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem Mol Biol 40: 621-629.
35. Chen J, Tang B, Chen H, Yao Q, Huang X, et al. (2010) Different Functions of the Insect Soluble and Membrane-Bound Trehalase Genes in Chitin Biosynthesis Revealed by RNA Interference. PLoS One 5: e10133.
36. 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.
37. Turner CT, Davy MW, MacDiarmid RM, Plummer KM, Birch NP, et al. (2006) RNA interference in the light brown apple moth, Epiphyas postvittana (Walker) induced by double-stranded RNA feeding. Insect Mol Biol 15: 383-391.
38. Ohnishi A, Hashimoto K, Imai K, Matsumoto S, (2009) Functional characterization of the Bombyx mori fatty acid transport protein (BmFATP) within the silk moth pheromone gland. J Biol Chem 28: 5128-5136.
39. Hull JJ, Lee JM, Kajigaya R, Matsumoto S, (2009) Bombyx mori homologs of STIM1 and Orai1 are essential components of the signal transduction cascade that regulates sex pheromone production. J Biol Chem 6: 31200-31213.
40. Takahashi T, Hamada A, Miyawaki K, Matsumoto Y, Mito T, et al. (2009) Systemic RNA interference for the study of learning and memory in an insect. J Neurosci Methods 179: 9-15.
41. Kumar M, Gupta GP, Rajam MV, (2009) Silencing of acetylcholinesterase gene of Helicoverpa armigera by siRNA affects larval growth and its life cycle J Insect Physiol. 55: 273-278.
42. Tang B, Wang S, Zhang F, (2010) Two storage hexamerins from the beet armyworm Spodoptera exigua: Cloning, characterization and the effect of gene silencing on survival. BMC Mol Biol 11: 65.
43. Li X, Zhang M, Zhang H, (2011) RNA Interference of Four Genes in Adult Bactrocera dorsalis by Feeding Their dsRNAs. PLoS One 6: e17788.
44. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P,et al. (2007) Control of coleopteran insect pests through RNA interference. Nat Biotech 25: 1322 - 1326.
45. Rangasamy M, Siegfried BD, (2012) Validation of RNA interference in western corn rootworm Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) adults. Pest Manag Sci 68: 587-591.
46. Zhou X, Wheeler MM, Oi FM, Scharf ME, (2008) RNA interference in the termite, Reticulitermes flavipes through ingestion of double-stranded RNA. Insect Biochem Mol Biol 38: 805-815.
47. Zhang J, Liu X, Zhang J, Li D, Sun Y, et al. (2010) Silencing of two alternative splicing-derived mRNA variants of chitin synthase 1 gene by RNAi is lethal to the oriental migratory locust, Locusta migratoria manilensis (Meyen). Insect Biochem Mol Biol 40: 824-833.
48. Araujo RN, Santos A, Pinto FS, Gontijo NF, Lehane MJ, et al. (2006) RNA interference of the salivary gland nitrophorin 2 in the triatomine bug Rhodnius prolixus (Hemiptera: Reduviidae) by dsRNA ingestion or injection. Insect Biochem Mol Biol 36: 683-693.
49. Zha W, Peng X, Chen R, Du B, Zhu L, et al. (2011) Knockdown of Midgut Genes by dsRNA-Transgenic Plant-Mediated RNA Interference in the Hemipteran Insect Nilaparvata lugens. PLoS One 6: e20504.
50. Wang Y, Fan HW, Huang HJ, Xue J, Wu WJ, et al. (2012) Chitin synthase 1 gene and its two alternative splicing variants from two sap-sucking insects, Nilaparvata lugens and Laodelphax striatellus (Hemiptera: Delphacidae). Insect Biochem Mol Biol 42: 637-646.
51. Ghanim M, Kontsedalov S, Czosnek H, (2007) Tissue-specific gene silencing by RNA interference in the whitefly Bemisia tabaci (Gennadius). Insect Biochem Mol Biol 37: 732-738.
52. Wuriyanghan H, Rosa C, Falk BW, (2011) Oral Delivery of Double-Stranded RNAs and siRNAs induces RNAi effects in the Potato/Tomato Psyllid, Bactericerca cockerelli. PLoS One 6: e27736.
53. Pitino M, Coleman AD, Maffei ME, Ridout CJ, Hogenhout SA, (2011) Silencing of Aphid genes by dsRNA feeding from plants. PLoS One 6: e25709.
54. Halbert SE, Manjunath KL, (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. Fla Entomol 87: 330-353.
55. Teixeira DC, Saillard C, Eveillard S, Danet JL, da Costa PI, et al. (2005) Candidatus Liberibacter americanus, associated with citrus huanglongbing (greening disease) in SaoPaulo State, Brazil. Int J Syst Evol Microbiol 55: 1857-1862.
56. Bové JM, (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88: 7-37.
57. Wang Z, Yin Y, Hu H, Yuan Q, Peng G, et al. (2006) Development and application of molecular-based diagnosis for Candidatus Liberibacter asiaticus, the causal pathogen of citrus huanglongbing. Plant Pathol 55: 630-638.
58. Batool A, Iftikhar Y, Mughal SM, Khan MM, Jaskani MJ, et al. (2007) Citrus greening disease- A major cause of citrus decline in the world- A review. Hortic Sci (Parague) 34: 159-166.
59. Manjunath KL, Halbert SE, Ramadugu C, Webb S, Lee RF, (2008) Detection of Candidatus Liberibacter asiaticus in Diaphorina citri and its importance in the management of citrus huanglongbing in Florida. Phytopathology 98: 387-396.
60. Hodges AW, Spreen TH (2012) Economic Impacts of Citrus Greening (HLB) in Florida, 2006/07-2010/11. Available: http://edis-ifas.ufl/fe903. Accessed 20 January 2013.
61. Halbert SE (2005) Pest Alert: Citrus Greening/Huanglongbing. Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Available: http://www.doacs.state.fl.us/pi/chrp/greening/citrusgreeningalert.html. Accessed 21 January 2013.
62. Garnier M, Jagoueix-Eveillard S, Cornje HF, Le Roux PR, Bové JM, (2000) Genomic characterization of a Liberibacter present in an ornamental rutaceous tree, Calodendrum capense, in the Western Cape province of South Africa. Proposal of 'Candidatus Liberibacter africanus subsp. capensis'. Int J Syst Evol Microbiol 50: 2119-2125.
63. Skelley LH, Hoy MA, (2004) A synchronous rearing method for the Asian citrus psyllid and its parasitoids in quarantine. Biol. Control 29: 14-23.
64. Mead FW, Fasulo TR (1998) Asian Citrus Psyllid, Diaphorina citri Kuwayama (Insecta: Hemiptera: Psyllidae). Available: http://edis.ifas.ufl.edu/pdffiles/IN/IN16000.pdf. Accessed 22 January 2013.
65. Grafton-Cardwell EE, Godfrey KE, Rogers ME, Childers CC, Stansly PA (2005) Available: Asian citrus psyllid. http://ccpp.ucr.edu/news/PsyllidbrochureAug05.pdf. Accessed 22 January 2013.
66. Rogers ME, Stansly PA (2007) Biology and management of the Asian citrus psyllid, Diaphorina citri Kuwayama, in Florida Citrus. EDIS. Available: http://edis.ifas.ufl.edu/IN668.pdf. Accessed 23 January 2013.
67. Majumdar A, Nesbitt N, Fadamiro H. (2009) Asian Citrus Psyllid. ANR-1341, Alabama Cooperative Extension System. Available: http://www.aces.edu/pubs/docs/A/ANR-1341.pdf. Accessed 23 January 2013.
68. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics. 23: 2947-2948.
69. Combet C, Jambon M, Deléage G, Geourjon C, (2002) Geno3D: automatic comparative molecular modelling of protein. Bioinformatics. 18: 213-214.
70. Morera S, Lacombe ML, Xu Y, LeBras G, Janin J, (1995) X-ray structure of human nucleoside diphosphate kinase B complexed with GDP at 2 A resolution. Structure. 15: 1307-1314.
71. Lascu L, Giartosio A, Ransac S, Erent M, (2000) Quaternary structure of nucleoside diphosphate kinases. J Bioenerg Biomembr. 32: 227-36.
72. Tian H, Peng H, Yao Q, Chen H, Xie Q, et al. (2009) Developmental Control of a lepidopteran pest Spodoptera exigua by ingestion of bacteria expressing dsRNA of a non-Midgut gene. PLoS One 4: e6225.
73. Dearolf CR, Hersperger E, Shearn A, (1988) Developmental consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev Biol 129: 159-168.
74. Dearolf CR, Tripoulas N, Biggs J, Shearn A, (1988) Molecular consequences of awdb3, a cell-autonomous lethal mutation of Drosophila induced by hybrid dysgenesis. Dev Biol 129: 169-178.
75. Liu S, Ding Z, Zhang C, Yang B, Liu Z, (2010) Gene knockdown by intro-thoracic injection of double-stranded RNA in the brown planthopper, Nilaparvata lugens. Insect Biochem Mol Biol 40: 666-671.
76. Sivakumar S, Rajagopal R, Venkatesh GR, Srivastava A, Bhatmagar RK, (2007) Knockdown of aminopeptidase-N from Helicoverpa armigera larvae and in transfected Sf21 cells by RNA interference reveals its functional interaction with Bacillus thuringiensis insecticidal protein Cry1Ac. J Biol Chem 282: 7312-7319.
77. Boucias DG (1998) Principles of insect pathology. Springer press; 1999 edition. 565 p.
78. Nation JL (2001) Insect physiology and biochemistry. CRC Press, 496 p.
79. Wikipedians B (2011) Introduction to Insects. Pedia Press. 266 p.
80. Klowden MJ, Marc (2007) Physiological Systems in Insects. Academic Press; 2nd edition 688 p.
81. Matsumura F (1975) Toxicology of insecticides. Plenum Press, New York, USA.
82. Noble-Nesbitt J, (1970) Structural aspects of penetration through insect cuticles. J Pestic Sci 1: 204-208.
83. White IM, Hodkinson ID, (1985) Nymphal taxonomy and systematics of Psylloidea (Homoptera) Bull Br Mus Nat Hist Entomol. 50: 153-301.
84. Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, et al. (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14: 453-463.
85. Boisson B, Jacques JC, Choumet V, Martin E, Xu J, et al. (2006) Gene silencing in mosquito salivary glands by RNAi. FEBS Lett 580: 1988-1992.
86. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, et al. (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotech 25: 1307-1313.