Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (agrilus planipennis)

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Mittapalli, Omprakash ^a   Bai, Xiaodong ^a   Mamidala, Praveen ^a   Rajarapu, Swapna Priya ^a   Bonello, Pierluigi ^b   Herms, Daniel A ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN; CYTOCHROME P450; GLUCAN SYNTHASE; MESSENGER RNA; MOLECULAR MARKER; POLYGALACTURONASE; PROTEIN KINASE; TRANSCRIPTOME; TRYPSIN; INSECT PROTEIN;

AGRILUS PLANIPENNIS; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTHROPOD LARVA; ARTICLE; BEETLE; BORING SPECIES; CANADA; CELL WALL; CONTROLLED STUDY; ENZYME DEGRADATION; ENZYME STRUCTURE; EXOTIC SPECIES; EXPRESSED SEQUENCE TAG; FAT BODY; FRAXINUS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC DATABASE; METABOLIC REGULATION; MICROSATELLITE MARKER; MIDGUT; MOLECULAR DYNAMICS; NONHUMAN; PEST INSECT; PREDICTION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PYROSEQUENCING; SEQUENCE HOMOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES COMPARISON; SPECIES INVASION; TISSUE SPECIFICITY; TRANSCRIPTOMICS; UNITED STATES; ANIMAL; GENE EXPRESSION PROFILING; GENETICS;

AGRILUS PLANIPENNIS; FRAXINUS; HEXAPODA;

ANIMALS; BEETLES; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; INSECT PROTEINS;

EID: 78149463754     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013708     Document Type: Article

References (77)

1. Yu Q, Lu C, Li W, Xiang Z, Zhang Z (2009) Annotation and expression of carboxylesterases in the silkworm Bombyx mori. BMC Genomics 10: 553-566.
2. Mittapalli O, Neal J, Shukle RH (2007) Antioxidant defense response in a galling insect. Proc Natl Acad Sci USA 104: 1889-1894.
3. Pauchet Y, Wilkinson P, Vogel H, Nelson DR, Reynolds SE, et al. (2010) Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol Biol 19: 61-75.
4. Tittiger C, Keeling CI, Blomquist GJ (2005) Some insights into the remarkable metabolism of the bark beetle midgut. Recent Adv. Phytochem 39: 57-78.
5. Felton GW, Duffey SS (1991) Protective action of midgut catalase in lepidopteran larvae against oxidative plant defenses. Journal of Chemical Ecology 17: 1715-1732.
6. Mittapalli O, Sardesai N, Giovanini MP, Williams CE, Shukle RH (2006a) Expression patterns of antibacterial genes in the Hessian fly. J Insect Physiol 52: 1143-1152.
7. Hou Y, Zhao P, Liu HL, Zou Y, Guan J, et al. (2007) Proteomics analysis of fat body from silkworm (Bombyx mori). Sheng Wu Gong Cheng Xue Bao 5: 867-872.
8. Arrese EL, Soulages JL (2009) Insect fat body: energy, metabolism and regulation. Annu. Rev Entomol 55: 207-225.
9. Liebherr JK, McHugh JV (2003) Coleoptera (beetles, weevils, fireflies). In: Resh VH, Carde RT, eds. Encyclopedia of insects. San Diego, CA: Academic Press. pp 209-203.
10. Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomol 51: 152-163.
11. Poland T, McCullough D (2006) Emerald ash borer: invasion of the urban forest and the threat to North Americás ash resource. J Forestry 104: 118-124.
12. Anulewicz AC, McCullough DG, Cappeart DL (2007) Emerald ash borer (Agrilus planipennis) density and canopy dieback in three North American ash species. Arbor Urban For 33: 338-349.
13. Smith A (2006) Effects of community structure on forest susceptibility and response to the emerald ash borer invasion of the Huron River Watershed in southeastern Michigan. Columbus: M.S. Thesis, The Ohio State University 122.
14. Herms DA, Stone AK, Chatfield JA (2003) Emerald ash borer: the beginning of the end of Ash in North America? In: Chatfield JA, Draper EA, Mathers HM, Dyke DE, Bennett PJ, Boggs JF, eds. 2004, Ornamental Plants: Annual Reports and Research Reviews 2003. pp 62-71. Ohio Agriculture Research and Development Center, Ohio State University Extension Special Circular 193.
15. Gandhi JKJ, Herms DA (2010) North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biol Invas 12: 1839-1846.
16. Burns RM, Honkala BH (1990) Silvics of North America. SDA Forest Service, Timber Management Research Agriculture Handbook 654, Washington, DC. Agriculture Handbook. pp 654 p. 877.
17. Liebhold AM, MacDonald WL, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci Mon 30: 1-49.
18. Akiyama K, Ohmomo S (2000) The buprestid beetles of the world. Iconic Series of Insects 4. Gekkan-Mushi Company, Ltd: Tokyo, Japan.
19. Schaefer PW (2005) Foreign exploration for emerald ash borer and its natural enemies. In: Mastro VC, Reardon R, eds. Proceedings of Emerald Ash Borer Research and Technology Development Meeting, USDA Forest Health Technology Enterprise Team Publication FHTET-2004-15. Morgantown, W.Va: USDA Forest Service. pp 67-68.
20. Bauer LS, Liu HP, Haack RA, Gao RT, Zhao TH, et al. (2005) Update on emerald ash borer natural enemies in Michigan and China. In: Mastro V, Reardon R, eds. Proceedings of the Emerald Ash Borer Research and Technology Meeting, Romulus, MI. USDA FS FHTET-2004-15. pp 71-72.
21. Yu CM (1992) Agrilus marcopoli Obenberger. In: Xiao G-R, ed. Forest Insects of China. 2nd Edition. Beijing, China: China Forestry Publishing House. Pp 400-401.
22. Haack RA, Jendek E, Liu H, Marchant KR, Petrice TR, et al. (2002) The emerald ash borer: A new exotic pest in North America. Michigan Entomological Soc Newsletter 47: 1-5.
23. Gould J, Tanner J, Winograd D, Lane S (2004) Initial studies on the laboratory rearing of emerald ash borer and foreign exploration for natural enemies. In: Mastro VC, Reardon R, eds. Proceedings of Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Health Technology EnterpriseTeam Publication FHTET-2004-15. MorgantownW.Va.: USDA Forest Service, 2005. pp 73-74.
24. Rebek EJ, Herms DA, Smitley DR (2008) Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environ Entomol 37: 242-246.
25. Eyles A, Jones W, Riedl K, Cipollini D, Schwartz S, et al. (2007) Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and two North American Ash species (F. americana and F. pennsylvanica). J Chem Ecol 33: 1430-1448.
26. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380.
27. Bentley DR (2006) Whole-genome re-sequencing. Curr Opin Genet Dev 16: 545-552.
28. Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92: 255-264.
29. Bai X, Zhang W, Ornates L, Jun T, Mittapalli O, et al. (2010) Combining nextgeneration sequencing strategies for rapid molecular resource development from an invasive aphid species, Aphis glycines. PLoS ONE 5: e11370.
30. Pauchet Y, Wilkinson P, van Munster M, Augustin S, Pauron D, et al. (2009) Pyrosequencing of the midgut transcriptome of the poplar leaf beetle Chrysomela tremulae reveals new gene families in Coleoptera. Insect Biochem Mol Biol 39: 403-413.
31. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949-955.
32. Elvin CM, Vuocolo T, Pearson RD, East IJ, Riding GA, et al. (1996) Characterization of a major peritrophic membrane protein, peritrophin- 44, from the larvae of Lucilia cuprina. J Biol Chem 271: 8925-8935.
33. Bhandary B, Rajarapu SP, Rivera-Vega L, Mittapalli O (2010) Analysis of gene expression in emerald ash borer (Agrilus planipennis) using quantitative real time- PCR. J Vis Exp;DOI 0.3791/1974.
34. Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42: 525-550.
35. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture and function. Ann Rev Entomol 54: 285-302.
36. Hemingway J, Karunaratne SH (1998) Mosquito carboxylesterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Med Vet Entomol 12: 1-12.
37. Yu Q, Lu C, Li W, Xiang Z, Zhang Z (2009) Annotation and expression of carboxylesterases in the silkworm, Bombyx mori. BMC Genomics 10: 553.
38. Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol 44: 507-5033.
39. Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24: 181-185.
40. Hartman JJ, Mahr J, McNally K, Okawa K, Iwamatsu A, et al. (1998) Katanin, a microtubule-severing protein, Is a novel AAA ATPase that targets to the centrosome using a WD-40 containing subunit. Cell 93: 277-287.
41. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 15: 1185-11895.
42. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, et al. (2007) A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in Zebrafish. Cell 129: 69-82.
43. Wang G, Reinke V (2008) A C. elegans Piwi, PRG-1, Regulates 21U-RNAs during spermatogenesis. Curr Biol 18: 861-867.
44. Chuma S, Hosokawa M, Kitamura K, Kasai S, Fujioka M, et al. (2006) Tdrd1/ Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc Natl Acad Sci U S A 103: 15894-15899.
45. Kim VN (2006) Small RNAs just got bigger: Piwi-interacting RNAs (piRNAs) in mammalian testes. Genes Dev 20: 1993-1997.
46. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103.
47. Werck-Reichhart, Feyereisen R. (2000) Cytochromes P450: A success story. Genome Biol 1: 3003.1-3003.9.
48. Feyereisen R (2006) Evolution of insect P450. Biochem Soc Trans 34: 1252-1255.
49. Mittapalli O, Neal JJ, Shukle RH (2005) Differential expression of two cytochrome p450 genes in compatible and incompatible hessian fly/wheat interactions. Insect Biochem Mol Biol 35: 981-989.
50. Berenbaum MR, Cohen MB, Schuler MA (1992) Cytochrome P450 monooxygenase genes in oligophagous Lepidoptera. In: Mullin CA, Scott JG, eds. ACS Symposium Series 505. Washington, DC. pp 114-124.
51. 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 Biotechnol 25: 1307-1313.
52. Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, et al. (2006) A deficit of toxification enzymes: pesticide sensitivity and enviornmental response in the honeybee. Insect Mol Biol 15: 615-636.
53. Yang Y, Chen S, Wu S, Yue L, Wu Y (2006) Constitutive overexpression of multiple cytochrome P450 genes associated with pyrethroid resistance in Helicoverpa armigera. J Econ Entomol 99: 1784-1789.
54. Snyder MJ, Stevens JL, Andersen JF, Feyereisen R (1995) Expression of cytochrome P450 genes of the CYP4 family in midgut and fat body of the tobacco hornworm, Manduca sexta. Arch Biochem Biophys 321: 13-20.
55. Scharf ME, Parimi S, Meinke LJ, Chandler LD, Siegfried BD (2001) Expression and induction of three family 4 cytochrome P450 (CYP4) genes identified from insecticide-resistant and susceptible western corn rootworms, Diabrotica virgifera virgifera. Insect Mol Biol 10: 139-146.
56. Davies L, Williams DR, Aguiar-Santana IA, Pedersen J, Turner PC, et al. (2006) Expression and down-regulation of cytochrome P450 genes of the CYP4 family by ecdysteroid agonists in Spodoptera littoralis and Drosophila melanogaster. Insect Biochem Mol Biol 36: 801-807.
57. Rewitz KF, Rybczynski R, Warren JT, Gilbert LI (2006) Identification, characterization and developmental expression of Halloween genes encoding P450 enzymes mediating ecdysone biosynthesis in the tobacco hornworm, Manduca sexta. Insect Biochem Mol Biol 36: 188-199.
58. Bogwitz MR, Chung H, Magoc L, Rigby S, Wong W, et al. (2005) CYP12A4 confers lufenuron resistance in a natural population of Drosophila melanogaster. Proc Natl Acad Sci U S A 102: 12807-12812.
59. Vasemagi A, Nilsson J, Primmer CR (2005) Expressed Sequence Tag-Linked Microsatellites as a Source of Gene-Associated Polymorphisms for Detecting Signatures of Divergent Selection in Atlantic Salmon (Salmo salar L.). Mol Biol Evol 22: 1067-1076.
60. Vasanthakumar A, Handelsman J, Schloss PD, Bauer LS, Raffa KF (2008) Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environ Entomol 37: 1344-1353.
61. Bishop JG, Ripoll DR, Bashir S, Damasceno CMB, Seeds JD, et al. (2005) Selection on glycine b-1,3-endoglucanase genes differentially inhibited by a Phytophthora glucanase inhibitor protein. Genetics 169: 1009-1019.
62. Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144: 1063-1073.
63. Werren JH, Windsor DM (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc Lond B Biol Sci 267: 1277-1285.
64. Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9: 393-405.
65. Salzberg SL, Hotopp JC, Delcher AL, Pop M, Smith DR, et al. (2005) Serendipitous discovery of Wolbachia genomes in multiple Drosophila species. Genome Biol 6: R23.1-R23.8.
66. Heddi A, Grenier AM, Khatchadourian C, Charles H, Nardon P (1999) Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and Wolbachia. Proc Natl Acad Sci U S A 96: 6814-6819.
67. Zimmer C (2001) Wolbachia: A Tale of Sex and Survival. Science 292: 1093-1095.
68. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
69. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36: 281-288.
70. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
71. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
72. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, et al. (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36: 3420-3435.
73. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36: D480-D484.
74. Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28: 27-30.
75. Thurston MI, Field D (2005) Msatfinder: detection and characterisation of microsatellites. Available: http://www.genomics.ceh.ac.uk/msatfinder/.
76. Nakabachi A, Shigenobu S, Sakazume N, Shiraki T, Hayashizaki Y, et al. (2005) Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc Natl Acad SciUS A 12: 5477-5482.
77. Pfaffl WM (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29: 2002-2007.