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Applied Entomology and Zoology

, Volume 49, Issue 1, pp 89–95 | Cite as

Identification of odorant-binding protein genes expressed in the antennae and the legs of the onion fly, Delia antiqua (Diptera: Anthomyiidae)

  • Shinya Ohta
  • Yousuke Seto
  • Koichiro Tamura
  • Yukio Ishikawa
  • Takashi MatsuoEmail author
Original Research Paper

Abstract

The onion fly, Delia antiqua (Meigen), is a pest specialized to the onion, Allium cepa L., and some other Allium plants. Host odorants play an important role in the attraction of D. antiqua adults and stimulation of oviposition in females. Odorant-binding proteins (OBPs) may serve as a first step in the perception of these chemical cues. In this study, to identify all OBP genes expressed in the chemosensory tissues in D. antiqua, RNA-seq analysis was carried out. In addition to the seven OBP genes previously identified, we found eight novel OBPs. Comparisons with Drosophila melanogaster Meigen OBP genes revealed that these 15 D. antiqua OBPs cover the structural variety observed in D. melanogaster OBPs, including Plus C and Minus C OBPs. These results suggest that a relatively large repertoire of chemosensory genes is maintained even in a specialist feeder.

Keywords

RNA-seq Oligophagous insect Evolution of chemosensory genes 

Notes

Acknowledgments

This work was supported by JSPS KAKENHI Grant Number 24380030 to TM.

References

  1. Dindonis LL, Miller JR (1980) Onion fly trap catch as affected by release rates of n-dipropyl disulfide from polyethylene enclosures. J Chem Ecol 7:411–418CrossRefGoogle Scholar
  2. Forêt S, Maleszka R (2006) Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera). Genome Res 16:1401–1413. doi: 10.1101/gr.5075706 Google Scholar
  3. Galindo K, Smith DP (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159:1059–1072PubMedGoogle Scholar
  4. Gaunt MW, Miles MA (2002) An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19:748–761PubMedCrossRefGoogle Scholar
  5. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 15:644–652. doi: 10.1038/nbt.1883 CrossRefGoogle Scholar
  6. Graham LA, Davies PL (2002) The odorant-binding proteins of Drosophila melanogaster: annotation and characterization of a divergent gene family. Gene 292:43–55. doi: 10.1186/gb-2007-8-11-r235 PubMedCrossRefGoogle Scholar
  7. Harada E, Haba D, Aigaki T, Matsuo T (2008) Behavioral analyses of mutants for two odorant-binding protein genes, Obp57d and Obp57e, in Drosophila melanogaster. Genes Genetic Syst 83:257–264. doi: 10.1266/ggs.83.257 CrossRefGoogle Scholar
  8. Harada E, Nakagawa J, Asano T, Taoka M, Sorimachi H, Ito Y, Aigaki T, Matsuo T (2012) Functional evolution of duplicated odorant-binding protein genes, Obp57d and Obp57e, in Drosophila. PLoS ONE 7:e29710. doi: 10.1371/journal.pone.0029710 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12:1357–1369. doi: 10.1101/gr.239402 PubMedCrossRefGoogle Scholar
  10. Ishikawa Y, Ikeshoji T, Matsumoto Y (1978) A propylthio moiety essential to oviposition attractant and stimulant of onion fly, Heylemya antiqua Meigen. Appl Entomol Zool 13:115–122Google Scholar
  11. Ishikawa Y, Mochizuki A, Ikeshoji T, Matsumoto Y (1983) Mass-rearing of the onion and seed-corn flies, Hylemya antiqua and Hylemya platura (Diptera, Anthomyiidae), on an artificial diet with antibiotics. Appl Entomol Zool 18:62–69Google Scholar
  12. Kopp A, Barmina O, Hamilton AM, Higgins L, McIntyre LM, Jones CD (2008) Evolution of gene expression in the Drosophila olfactory system. Mol Biol Evol 25:1081–1092. doi: 10.1093/molbev/msn055 PubMedCrossRefGoogle Scholar
  13. Matsuo T (2008a) Genes for host-plant selection in Drosophila. J Neurogenet 22:195–210. doi: 10.1080/01677060802298483 PubMedCrossRefGoogle Scholar
  14. Matsuo T (2008b) Rapid evolution of two odorant-binding protein genes, Obp57d and Obp57e, in the Drosophila melanogaster species group. Genetics 178:1061–1072. doi: 10.1534/genetics.107.079046 PubMedCrossRefGoogle Scholar
  15. Matsuo T (2012) Contribution of olfactory and gustatory sensations of octanoic acid in the oviposition behavior of Drosophila melanogaster (Diptera: Drosophilidae). Appl Entomol Zool 47:137–142. doi: 10.1007/s13355-012-0100-3 CrossRefGoogle Scholar
  16. Matsuo T, Sugaya S, Yasukawa J, Aigaki T, Fuyama Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biol 5:985–996. doi: 10.1371/journal.pbio.0050118 CrossRefGoogle Scholar
  17. Mitaka H, Matsuo T, Miura N, Ishikawa Y (2011) Identification of odorant-binding protein genes from antennal expressed sequence tags of the onion fly, Delia antiqua. Mol Biol Rep 38:1787–1792. doi: 10.1007/s11033-010-0293-x PubMedCrossRefGoogle Scholar
  18. Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63:1658–1676. doi: 10.1007/s00018-005-5607-0 PubMedCrossRefGoogle Scholar
  19. Petersen TN, Brunak S, Heijne GH, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. doi: 10.1038/nmeth.1701 PubMedCrossRefGoogle Scholar
  20. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  21. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 PubMedCrossRefGoogle Scholar
  22. Vieira FG, Rozas Julio (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490. doi: 10.1093/gbe/evr033 PubMedCentralPubMedCrossRefGoogle Scholar
  23. Vieira FG, Sanchez-Gracia A, Rozas J (2007) Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution. Genome Biol 8:R235. doi: 10.1186/gb-2007-8-11-r235 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Wiegmann BM, Yeates DK, Thorne JL, Kishino H (2003) Time flies, a new molecular time-scale for brachyceran fly evolution without a clock. Syst Biol 52:745–756PubMedCrossRefGoogle Scholar
  25. Xu PX, Zwiebel LJ, Smith DP (2003) Identification of a distinct family of genes encoding atypical odorant-binding proteins in the malaria vector mosquito, Anopheles gambiae. Insect Mol Biol 12:549–560. doi: 10.1046/j.1365-2583.2003.00440.x PubMedCrossRefGoogle Scholar
  26. Zhang J, Rosenberg HF, Nei M (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95:3708–3713PubMedCrossRefGoogle Scholar
  27. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166Google Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2013

Authors and Affiliations

  • Shinya Ohta
    • 1
  • Yousuke Seto
    • 2
  • Koichiro Tamura
    • 2
    • 3
  • Yukio Ishikawa
    • 1
  • Takashi Matsuo
    • 1
    Email author
  1. 1.Department of Agricultural and Environmental BiologyThe University of TokyoTokyoJapan
  2. 2.Department of Biological SciencesTokyo Metropolitan UniversityTokyoJapan
  3. 3.Research Center for Genomics and BioinformaticsTokyo Metropolitan UniversityTokyoJapan

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