Use of chromatin remodeling ATPases as RNAi targets for parental control of western corn rootworm (Diabrotica virgifera virgifera) and Neotropical brown stink bug (Euschistus heros)

Insect Biochemistry and Molecular Biology

Volumn 71, Issue , 2016, Pages 58-71

  Fishilevich, Elane ^a   Vélez, Ana M ^b   Khajuria, Chitvan ^b   Frey, Meghan L F ^a   Hamm, Ronda L ^a   Wang, Haichuan ^b   Schulenberg, Greg A ^a   Bowling, Andrew J ^a   Pence, Heather E ^a   Gandra, Premchand ^a   Arora, Kanika ^a   Storer, Nicholas P ^a   Narva, Kenneth E ^a   Siegfried, Blair D ^c  

^a DOW AGROSCIENCES LLC   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Brahma; Chd1; Chromatin remodeling ATPase; Diabrotica; Iswi; Mi 2; Parental RNAi; Stink bug

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHROMATIN; INSECT PROTEIN; SMALL INTERFERING RNA;

ANIMAL; BEETLE; BIOLOGICAL PEST CONTROL; CHROMATIN; ENZYMOLOGY; FEMALE; FERTILITY; GENETICS; HETEROPTERA; INSECT CONTROL; MALE; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BEETLES; CHROMATIN; FEMALE; FERTILITY; HETEROPTERA; INSECT CONTROL; INSECT PROTEINS; MALE; PEST CONTROL, BIOLOGICAL; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84959322506     PISSN: 09651748     EISSN: 18790240     Source Type: Journal    
DOI: 10.1016/j.ibmb.2016.02.004     Document Type: Article

References (68)

1. Allen M.L., Walker W.B. Saliva of Lygus lineolaris digests double stranded ribonucleic acids. J. insect Physiol. 2012, 58:391-396.
2. Armstrong J.A., Papoulas O., Daubresse G., Sperling A.S., Lis J.T., Scott M.P., Tamkun J.W. The Drosophila BRM complex facilitates global transcription by RNA polymerase II. EMBO J. 2002, 21:5245-5254.
3. Baum J.A., Roberts J.K. Chapter five - progress towards RNAi-mediated insect pest management. Advances in Insect Physiology 2014, 249-295. Academic Press. S.D. Tarlochan, S.G. Sarjeet (Eds.).
4. Baum J.A., Bogaert T., Clinton W., Heck G.R., Feldmann P., Ilagan O., Johnson S., Plaetinck G., Munyikwa T., Pleau M., Vaughn T., Roberts J. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 2007, 25:1322-1326.
5. Boisson B., Jacques J.C., Choumet V., Martin E., Xu J., Vernick K., Bourgouin C. Gene silencing in mosquito salivary glands by RNAi. FEBS Lett. 2006, 580:1988-1992.
6. Bouazoune K., Brehm A. ATP-dependent chromatin remodeling complexes in Drosophila. Chromosome Res. Int. J. Mol. Supramol. Evol. Aspects Chromosome Biol. 2006, 14:433-449.
7. Branson T.F., Jackson J.J. An improved diet for adult Diabrotica virgifera virgifera (Coleoptera, Chrysomelidae). J. Kans. Entomol. Soc. 1988, 61:353-355.
8. Branson T.F., Johnson R.D. Adult Western Corn Rootworms: Oviposition, Fecundity, and Longevity in the Laboratory 1973.
9. Brizuela B.J., Elfring L., Ballard J., Tamkun J.W., Kennison J.A. Genetic analysis of the brahma gene of Drosophila melanogaster and polytene chromosome subdivisions 72AB. Genetics 1994, 137:803-813.
10. Bucher G., Scholten J., Klingler M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. CB 2002, 12:R85-R86.
11. Campbell L.A., Meinke L.J. Fitness of Diabrotica barberi, Diabrotica longicornis, and their hybrids (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 2010, 103:925-935.
12. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
13. Coleman A.D., Wouters R.H., Mugford S.T., Hogenhout S.A. Persistence and transgenerational effect of plant-mediated RNAi in aphids. J. Exp. Bot. 2015, 66:541-548.
14. Cote J., Quinn J., Workman J.L., Peterson C.L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Sci. (New York, N.Y.) 1994, 265:53-60.
15. Coupe R.H., Capel P.D. Trends in pesticide use on soybean, corn, and cotton since the introduction of major genetically modified crops in the United States. Pest Manag. Sci. 2015, 2015/07/22 ed.
16. de la Serna I.L., Ohkawa Y., Imbalzano A.N. Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat. Rev. Genet. 2006, 7:461-473.
17. Deuring R., Fanti L., Armstrong J.A., Sarte M., Papoulas O., Prestel M., Daubresse G., Verardo M., Moseley S.L., Berloco M., Tsukiyama T., Wu C., Pimpinelli S., Tamkun J.W. The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo. Mol. Cell 2000, 5:355-365.
18. Dietzl G., Chen D., Schnorrer F., Su K.C., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
19. Durr H., Korner C., Muller M., Hickmann V., Hopfner K.P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005, 121:363-373.
20. Eisen J.A., Sweder K.S., Hanawalt P.C. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 1995, 23:2715-2723.
21. Elfring L.K., Deuring R., McCallum C.M., Peterson C.L., Tamkun J.W. Identification and characterization of Drosophila relatives of the yeast transcriptional activator SNF2/SWI2. Mol. Cell. Biol. 1994, 14:2225-2234.
22. Eyun S.I., Wang H.C., Pauchet Y., Ffrench-Constant R.H., Benson A.K., Valencia-Jimenez A., Moriyama E.N., Siegfried B.D. Molecular evolution of glycoside hydrolase genes in the western corn rootworm (Diabrotica virgifera virgifera). Plos One 2014, 9:e94052.
23. Finn R.D., Bateman A., Clements J., Coggill P., Eberhardt R.Y., Eddy S.R., Heger A., Hetherington K., Holm L., Mistry J., Sonnhammer E.L., Tate J., Punta M. Pfam: the protein families database. Nucleic Acids Res. 2014, 42:D222-D230.
24. Fortes P., Magro S.R., Panizzi A.R., Parra J.R. Development of a dry artificial diet for Nezara viridula (L.) and Euschistus heros (Fabricius) (Heteroptera: Pentatomidae). Neotropical Entomol. 2006, 35:567-572.
25. Fortes P., Salvador G., Consoli F.L. Ovary development and maturation in Nezara viridula (L.) (Hemiptera: Pentatomidae). Neotropical Entomol. 2011, 40:89-96.
26. Futahashi R., Tanaka K., Matsuura Y., Tanahashi M., Kikuchi Y., Fukatsu T. Laccase2 is required for cuticular pigmentation in stinkbugs. Insect Biochem. Mol. Biol. 2011, 41:191-196.
27. Gassmann A.J., Petzold-Maxwell J.L., Keweshan R.S., Dunbar M.W. Field-evolved resistance to Bt maize by western corn rootworm. Plos One 2011, 6:e22629.
28. Gassmann A.J., Petzold-Maxwell J.L., Keweshan R.S., Dunbar M.W. Western corn rootworm and Bt maize: challenges of pest resistance in the field. GM crops food 2012, 3:235-244.
29. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., etal Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29. 644-U130.
30. Gray M.E., Sappington T.W., Miller N.J., Moeser J., Bohn M.O. Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu. Rev. Entomol. 2009, 54:303-321.
31. Grune T., Brzeski J., Eberharter A., Clapier C.R., Corona D.F., Becker P.B., Muller C.W. Crystal structure and functional analysis of a nucleosome recognition module of the remodeling factor ISWI. Mol. Cell 2003, 12:449-460.
32. Hassan A.H., Prochasson P., Neely K.E., Galasinski S.C., Chandy M., Carrozza M.J., Workman J.L. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 2002, 111:369-379.
33. He J., Xuan T., Xin T., An H., Wang J., Zhao G., Li M. Evidence for chromatin-remodeling complex PBAP-controlled maintenance of the Drosophila ovarian germline stem cells. Plos One 2014, 9:e103473.
34. Hill R.E. Mating, oviposition patterns, fecundity and longevity of the western corn rootworm. J. Econ. Entomol. 1975, 68:311-315.
35. Ho L., Crabtree G.R. Chromatin remodelling during development. Nature 2010, 463:474-484.
36. JMP®, 2007. Version 11 pro, in: Inc., S.I. (Ed.), Cary, NC.
37. Kehle J., Beuchle D., Treuheit S., Christen B., Kennison J.A., Bienz M., Muller J. dMi-2, a hunchback-interacting protein that functions in polycomb repression. Sci. (New York, N.Y.) 1998, 282:1897-1900.
38. Khajuria C., Velez A.M., Rangasamy M., Wang H., Fishilevich E., Frey M.L., Carneiro N.P., Gandra P., Narva K.E., Siegfried B.D. Parental RNA interference of genes involved in embryonic development of the western corn rootworm, Diabrotica virgifera virgifera LeConte. Insect Biochem. Mol. Biol. 2015, 63:54-62.
39. Klowden M.J. Chapter 4-reproductive systems. Physiological Systems in Insects 2008, 181-238. Academic Press, San Diego. second ed. M.J. Klowden (Ed.).
40. Koch R.L., Pahs T. Species composition, abundance, and seasonal dynamics of stink bugs (Hemiptera: Pentatomidae) in Minnesota soybean fields. Environ. Entomol. 2014, 43:883-888.
41. Levine E., OloumiSadeghi H. Western corn rootworm (Coleoptera: Chrysomelidae) larval injury to corn grown for seed production following soybeans grown for seed production. J. Econ. Entomol. 1996, 89:1010-1016.
42. Liu P.Z., Kaufman T.C. Hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Dev. Camb. Engl. 2004, 131:1515-1527.
43. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001, 25:402-408.
44. Mao J., Zeng F. Feeding-based RNA interference of a gap gene is lethal to the pea aphid, Acyrthosiphon pisum. Plos One 2012, 7:e48718.
45. Mao J., Liu C., Zeng F. Hunchback is required for abdominal identity suppression and germband growth in the parthenogenetic embryogenesis of the pea aphid, Acyrthosiphon pisum. Arch. Insect Biochem. Physiol. 2013, 84:209-221.
46. Marfella C.G., Imbalzano A.N. The Chd family of chromatin remodelers. Mutat. Res. 2007, 618:30-40.
47. Marra M.C., Piggott N.E., Goodwin B.K. The impact of corn rootworm protected biotechnology traits in the United States. AgBioForum 2012, 15:217-230.
48. McDaniel I.E., Lee J.M., Berger M.S., Hanagami C.K., Armstrong J.A. Investigations of CHD1 function in transcription and development of Drosophila melanogaster. Genetics 2008, 178:583-587.
49. McPherson R.M., McPherson J.E. Stink Bugs of Economic Importance in America North of Mexico 2000, CRC Press, Boca Raton, FL.
50. Meinke L.J., Siegfried B.D., Wright R.J., Chandler L.D. Adult susceptibility of Nebraska western corn rootworm (Coleoptera: Chrysomelidae) populations to selected insecticides. J. Econ. Entomol. 1998, 91:594-600.
51. Paim R.M., Araujo R.N., Lehane M.J., Gontijo N.F., Pereira M.H. Long-term effects and parental RNAi in the blood feeder Rhodnius prolixus (Hemiptera; Reduviidae). Insect Biochem. Mol. Biol. 2013, 43:1015-1020.
52. Perrimon N. Creating mosaics in Drosophila. Int. J. Dev. Biol. 1998, 42:243-247.
53. Pilkay G. Ecology and Management of Stink Bugs (Hemiptera: Pentatomidae) in Southeastern Farmscapes 2013, All Dissertations. Paper 1146.
54. Pilkay G.L., Reay-Jones F.P.F., Toews M.D., Greene J.K., Bridges W.C. Spatial and temporal dynamics of stink bugs in Southeastern farmscapes. J. Insect. Sci. 2015, 2015/04/07 ed.
55. Pitino M., Coleman A.D., Maffei M.E., Ridout C.J., Hogenhout S.A. Silencing of aphid genes by dsRNA feeding from plants. Plos One 2011, 6:e25709.
56. Rangasamy M., Siegfried B.D. Validation of RNA interference in western corn rootworm Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) adults. Pest Manag. Sci. 2012, 68:587-591.
57. Roignant J.Y., Carre C., Mugat B., Szymczak D., Lepesant J.A., Antoniewski C. Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. Rna 2003, 9:299-308.
58. Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 2012, 9:671-675.
59. Shukla J.N., Palli S.R. Production of all female progeny: evidence for the presence of the male sex determination factor on the Y chromosome. J. Exp. Biol. 2014, 217:1653-1655.
60. Silva F.A., Calizotti G.S., Panizzi A.R. Survivorship and egg production of phytophagous pentatomids in laboratory rearing. Neotropical Entomol. 2011, 40:35-38.
61. Sosa-Gomez D.R., Da Silva J.J., Lopes Ide O., Corso I.C., Almeida A.M., De Moraes G.C., Baur M.E. Insecticide susceptibility of Euschistus heros (Heteroptera:Pentatomidae) in Brazil. J. Econ. Entomol. 2009, 102:1209-1216.
62. Temple J.H., Davis J.A., Micinski S., Hardke J.T., Price P., Leonard B.R. Species composition and seasonal abundance of stink bugs (Hemiptera: Pentatomidae) in Louisiana soybean. Environ. Entomol. 2013, 42:648-657.
63. Terenius O., Papanicolaou A., Garbutt J.S., Eleftherianos I., Huvenne H., Kanginakudru S., Albrechtsen M., An C., Aymeric J.L., Barthel A., Bebas P., Bitra K., Bravo A., Chevalier F., Collinge D.P., Crava C.M., de Maagd R.A., Duvic B., Erlandson M., Faye I., Felfoldi G., Fujiwara H., Futahashi R., Gandhe A.S., Gatehouse H.S., Gatehouse L.N., Giebultowicz J.M., Gomez I., Grimmelikhuijzen C.J., Groot A.T., Hauser F., Heckel D.G., Hegedus D.D., Hrycaj S., Huang L., Hull J.J., Iatrou K., Iga M., Kanost M.R., Kotwica J., Li C., Li J., Liu J., Lundmark M., Matsumoto S., Meyering-Vos M., Millichap P.J., Monteiro A., Mrinal N., Niimi T., Nowara D., Ohnishi A., Oostra V., Ozaki K., Papakonstantinou M., Popadic A., Rajam M.V., Saenko S., Simpson R.M., Soberon M., Strand M.R., Tomita S., Toprak U., Wang P., Wee C.W., Whyard S., Zhang W., Nagaraju J., Ffrench-Constant R.H., Herrero S., Gordon K., Swevers L., Smagghe G. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. insect Physiol. 2011, 57:231-245.
64. Tomoyasu Y., Miller S.C., Tomita S., Schoppmeier M., Grossmann D., Bucher G. Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol. 2008, 9. R10-R10.
65. Wang D., Liu Q., Li X., Sun Y., Wang H., Xia L. Double-stranded RNA in the biological control of grain aphid (Sitobion avenae F.). Funct. Integr. genomics 2015, 15:211-223.
66. Whyard S., Singh A.D., Wong S. Ingested double-stranded RNAs can act as species-specific insecticides. Insect Biochem. Mol. Biol. 2009, 39:824-832.
67. Wynant N., Verlinden H., Breugelmans B., Simonet G., Vanden Broeck J. Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria. Insect Biochem. Mol. Biol. 2012, 42:911-917.
68. Zhang J., Khan S.A., Hasse C., Ruf S., Heckel D.G., Bock R. Pest control. Full crop protection from an insect pest by expression of long double-stranded RNAs in plastids. Sci. (New York, N.Y.) 2015, 347:991-994.