The Mediterranean fruit fly, Ceratitis capitata (medfly), is an extremely invasive agricultural pest due to its extremely wide host range and its ability to adapt to a broad range of climatic conditions and habitats. Chemosensory behaviour plays an important role in many crucial stages in the life of this insect, such as the detection of pheromone cues during mate pursuit and odorants during host plant localisation. Thus, the analysis of the chemosensory gene repertoire is an important step for the interpretation of the biology of this species and consequently its invasive potential. Moreover, these genes may represent ideal targets for the development of novel, effective control methods and pest population monitoring systems. Expressed sequence tag libraries from C. capitata adult heads, embryos, male accessory glands and testes were screened for sequences encoding putative odorant binding proteins (OBPs). A total of seventeen putative OBP transcripts were identified, corresponding to 13 Classic, three Minus-C and one Plus-C subfamily OBPs. The tissue distributions of the OBP transcripts were assessed by RT-PCR and a subset of five genes with predicted proteins sharing high sequence similarities and close phylogenetic affinities to Drosophila melanogaster pheromone binding protein related proteins (PBPRPs) were characterised in greater detail. Real Time quantitative PCR was used to assess the effects of maturation, mating and time of day on the transcript abundances of the putative PBPRP genes in the principal olfactory organs, the antennae, in males and females. The results of the present study have facilitated the annotation of OBP genes in the recently released medfly genome sequence and represent a significant contribution to the characterisation of the medfly chemosensory repertoire. The identification of these medfly OBPs/PBPRPs permitted evolutionary and functional comparisons with homologous sequences from other tephritids of the genera Bactrocera and Rhagoletis.
References
[1]
Malacrida AR, Gomulski LM, Bonizzoni M, Bertin S, Gasperi G, et al. (2007) Globalization and fruitfly invasion and expansion: the medfly paradigm. Genetica 131: 1–9.
[2]
Diaz-Fleischer F, Papaj DR, Prokopy RJ, Norrbom AL, Aluja M (2000) Evolution of fruit fly oviposition behavior. In: M A, Norrbom AL, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton, Florida, USA: CRC Press. 811–841.
[3]
Drew RAI, Yuval B (2000) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom A, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton, Florida, USA: CRC Press. 731–749.
[4]
Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293: 161–163.
[5]
Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58: 373–391.
[6]
Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63: 1658–1676.
[7]
Leal WS, Nikonova L, Peng G (1999) Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Lett 464: 85–90.
[8]
Tegoni M, Campanacci V, Cambillau C (2004) Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem Sci 29: 257–264.
[9]
Zhou JJ (2010) Odorant-Binding Proteins in Insects. Vitamins and Hormones 83: 241–272.
[10]
Vieira FG, Rozas J (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.
[11]
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.
[12]
Valenzuela JG, Charlab R, Gonzalez EC, de Miranda-Santos IK, Marinotti O, et al. (2002) The D7 family of salivary proteins in blood sucking diptera. Insect Molecular Biology 11: 149–155.
[13]
Zhou JJ, Huang W, Zhang GA, Pickett JA, Field LM (2004) “Plus-C” odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 327: 117–129.
[14]
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.
[15]
Zhou JJ, He XL, Pickett JA, Field LM (2008) Identification of odorant-binding proteins of the yellow fever mosquito Aedes aegypti: genome annotation and comparative analyses. Insect Molecular Biology 17: 147–163.
[16]
Gong DP, Zhang HJ, Zhao P, Xia QY, Xiang ZH (2009) The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics 10: 332.
[17]
Xu P, Atkinson R, Jones DN, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45: 193–200.
[18]
Laughlin JD, Ha TS, Jones DN, Smith DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133: 1255–1265.
[19]
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: e118.
[20]
Foret 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: 1404–1413.
Takemori N, Yamamoto MT (2009) Proteome mapping of the Drosophila melanogaster male reproductive system. Proteomics 9: 2484–2493.
[23]
Scolari F, Gomulski LM, Ribeiro JM, Siciliano P, Meraldi A, et al. (2012) Transcriptional profiles of mating-responsive genes from testes and male accessory glands of the Mediterranean fruit fly, Ceratitis capitata. PLoS One 7: e46812.
[24]
Eberhard W (2000) Sexual behavior and sexual selection in the Mediterranean fruit fly, Ceratitis capitata (Dacinae: Ceratitidini). In: Aluja M, Norrbom A, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton, Florida, USA: CRC Press. 457–489.
[25]
Yuval B, Hendrichs J (2000) Behavior of flies in the genus Ceratitis (Dacinae: Ceratitidini). In: Aluja M, Norrbom A, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton: CRC Press. 429–458.
[26]
Shelly T, Edu J, Pahio E (2012) Mate Choice by Lekking Males: Evidence From the Mediterranean Fruit Fly From Field Cage Trials (Diptera: Tephritidae). Annals of the Entomological Society of America 105: 368–376.
[27]
Sivinski J, Aluja M, Dodson GN, Freidberg A, Headrick DH, et al. (2000) Topics in the evolution of sexual behavior in the Tephritidae. In: Aluja M, Norrbom A, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton, Florida, USA: CRC Press. 751–792.
[28]
Whittier TS, Kaneshiro KY, Prescott LD (1992) Mating-Behavior of Mediterranean Fruit-Flies (Diptera, Tephritidae) in a Natural-Environment. Annals of the Entomological Society of America 85: 214–218.
[29]
Briceno RD, Eberhard WG, Vilardi JC, Liedo P, Shelly TE (2002) Variation in the intermittent buzzing songs of male medflies (Diptera : Tephritidae) associated with geography, mass-rearing, and courtship success. Florida Entomologist 85: 32–40.
[30]
Baker R, Herbert RH, Grant GG (1985) Isolation and identification of the sex-pheromone of the Mediterranean fruit fly, Ceratitis capitata (Wied). J Chem Soc Chem Commun 12: 824–825.
[31]
Flath RA, Jang EB, Light DM, Mon TR, Carvalho L, et al. (1993) Volatile Pheromonal Emissions from the Male Mediterranean Fruit-Fly - Effects of Fly Age and Time of Day. J Agric Food Chem 41: 830–837.
[32]
Cosse AA, Todd JL, Millar JG, Martinez LA, Baker TC (1995) Electroantennographic and coupled gas chromatographic electroantennographic responses of the Mediterranean fruit fly, Ceratitis capitata, to male-produced volatiles and mango odor. J Chem Ecol 21: 1823–1836.
[33]
Alfaro C, Vacas S, Zarzo M, Navarro-Llopis V, Primo J (2011) Solid phase microextraction of volatile emissions of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae): influence of fly sex, age, and mating status. J Agric Food Chem 59: 298–306.
[34]
Vanickova L, do Nascimento RR, Hoskovec M, Jezkova Z, Brizova R, et al. (2012) Are the wild and laboratory insect populations different in semiochemical emission? The case of the medfly sex pheromone. J Agric Food Chem 60: 7168–7176.
[35]
Gomulski LM, Dimopoulos G, Xi Z, Soares MB, Bonaldo MF, et al. (2008) Gene discovery in an invasive tephritid model pest species, the Mediterranean fruit fly, Ceratitis capitata. BMC Genomics 9: 243.
[36]
Gomulski LM, Dimopoulos G, Xi Z, Scolari F, Gabrieli P, et al. (2012) Transcriptome profiling of sexual maturation and mating in the Mediterranean fruit fly, Ceratitis capitata. PLoS One 7: e30857.
[37]
Sirot LK, Poulson RL, McKenna MC, Girnary H, Wolfner MF, et al. (2008) Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 38: 176–189.
[38]
Zhou S, Stone EA, Mackay TF, Anholt RR (2009) Plasticity of the chemoreceptor repertoire in Drosophila melanogaster. PLoS Genet 5: e1000681.
[39]
South A, Sirot LK, Lewis SM (2011) Identification of predicted seminal fluid proteins in Tribolium castaneum. Insect Molecular Biology 20: 447–456.
[40]
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.
[41]
Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868–877.
[42]
Nielsen H, Engelbrecht J, Brunak S, vonHeijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10: 1–6.
[43]
Saul SH (1982) Rearing methods for the medfly, Ceratitis capitata. Ann Entomol Soc Am 75: 480–483.
[44]
Taylor PW, Yuval B (1999) Postcopulatory sexual selection in Mediterranean fruit flies: advantages for large and protein-fed males. Animal Behaviour 58: 247–254.
[45]
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511–518.
[46]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
[47]
Zheng W, Peng W, Zhu C, Zhang Q, Saccone G, et al. (2013) Identification and Expression Profile Analysis of Odorant Binding Proteins in the Oriental Fruit Fly Bactrocera dorsalis. Int J Mol Sci 14: 14936–14949.
[48]
Ramsdell KM, Lyons-Sobaski SA, Robertson HM, Walden KK, Feder JL, et al. (2010) Expressed sequence tags from cephalic chemosensory organs of the northern walnut husk fly, Rhagoletis suavis, including a putative canonical odorant receptor. J Insect Sci 10: 51.
[49]
Schwarz D, Robertson HM, Feder JL, Varala K, Hudson ME, et al. (2009) Sympatric ecological speciation meets pyrosequencing: sampling the transcriptome of the apple maggot Rhagoletis pomonella. BMC Genomics 10: 633.
[50]
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365–386.
[51]
Baruffi L, Damiani G, Guglielmino CR, Bandi C, Malacrida AR, et al. (1995) Polymorphism within and between Populations of Ceratitis-Capitata - Comparison between Rapd and Multilocus Enzyme Electrophoresis Data. Heredity (Edinb) 74: 425–437.
[52]
Mott R (1997) EST_GENOME: a program to align spliced DNA sequences to unspliced genomic DNA. Comput Appl Biosci 13: 477–478.
[53]
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
[54]
Sidák Z (1967) Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association: 626–633.
[55]
Papadopoulos NT, Katsoyannos BI, Kouloussis NA, Economopoulos AP, Carrey JR (1998) Effect of adult age, food, and time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males. Entomologia Experimentalis Et Applicata 89: 175–182.
[56]
Pelosi P, Maida R (1995) Odorant-binding proteins in insects. Comp Biochem Physiol B Biochem Mol Biol 111: 503–514.
[57]
Pikielny CW, Hasan G, Rouyer F, Rosbash M (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12: 35–49.
[58]
Lagarde A, Spinelli S, Qiao H, Tegoni M, Pelosi P, et al. (2011) Crystal structure of a novel type of odorant-binding protein from Anopheles gambiae, belonging to the C-plus class. Biochem J 437: 423–430.
[59]
Bigiani A, Scalera G, Crnjar R, Barbarossa IT, Magherini PC, et al. (1989) Distribution and functions of the antennal olfactory sensilla in Ceratitis capitata Wied. (Diptera, Trypetidae). Bolletino di Zoologia 56: 305–311.
[60]
Sanchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity (Edinb) 103: 208–216.
[61]
Ayala FJ, Barrio E, Kwiatowski J (1996) Molecular clock or erratic evolution? A tale of two genes. Proc Natl Acad Sci U S A 93: 11729–11734.
[62]
Anholt RR, Williams TI (2010) The soluble proteome of the Drosophila antenna. Chem Senses 35: 21–30.
[63]
Arya GH, Weber AL, Wang P, Magwire MM, Negron YL, et al. (2010) Natural variation, functional pleiotropy and transcriptional contexts of odorant binding protein genes in Drosophila melanogaster. Genetics 186: 1475–1485.
[64]
Zucoloto FS (1990) Effects of flavour and nutritional value on diet selection by Ceratitis capitata larvae (Diptera: Tephritidae). Journal of Physiological Entomology 37: 21–25.
[65]
Nakagawa S, Farias GJ, Suda D, Chambers DL (1973) Mating behavior of the Mediterranean fruit fly following excision of the antennae. Journal of Economic Entomology 66: 583–584.
[66]
Féron M (1962) L'instinct de reproduction chez la mouche mediterrannéene des fruits Ceratitis capitata. Comportement sexuel. Comportement de ponte. Rev Pathol Veg Entomol Agr Fr 41: 1–129.
[67]
Prokopy RJ, Hendrichs J (1979) Mating behaviour of Ceratitis capitata on field-caged host tree. Annals of the Entomological Society of America 72: 642–648.
[68]
McDonald PT (1987) Intragroup stimulation of pheromone release by male Mediterranean fruit flies. Annals of the Entomological Society of America 80: 17–20.
[69]
Light DM, Jang EB, Binder RG, Flath RA, Kint S (1999) Minor and intermediate components enhance attraction of female Mediterranean fruit flies to natural male odor pheromone and its synthetic major components. J Chem Ecol 25: 2757–2777.
[70]
Landolt PJ, Heath RR, Chambers DL (1992) Oriented Flight Responses of Female Mediterranean Fruit-Flies to Calling Males, Odor of Calling Males, and a Synthetic Pheromone Blend. Entomologia Experimentalis Et Applicata 65: 259–266.
[71]
Kaspi R, Mossinson S, Drezner T, Kamensky B, Yuval B (2002) Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiological Entomology 27: 29–38.
[72]
Fletcher BS (1989) Movements of Tephritid fruit flies. In: Robertson AS, Hooper G, editors. Fruit flies Their biology, natural enemies and control. Amsterdam, The Netherlands: Elsevier. 209–219.
[73]
Jang EB (1995) Effects of Mating and Accessory-Gland Injections on Olfactory-Mediated Behavior in the Female Mediterranean Fruit-Fly, Ceratitis-Capitata. Journal of Insect Physiology 41: 705–710.
[74]
Papadopoulos NT, Shelly TE, Niyazi N, Jang E (2006) Olfactory and behavioral mechanisms underlying enhanced mating competitiveness following exposure to ginger root oil and orange oil in males of the mediterranean fruit fly, Ceratitis capitata (Diptera : Tephritidae). Journal of Insect Behavior 19: 403–418.
[75]
Levinson H, Levinson A, Osterried E (2003) Orange-derived stimuli regulating oviposition in the Mediterranean fruit fly. Journal of Applied Entomology-Zeitschrift Fur Angewandte Entomologie 127: 269–275.
[76]
Papadopoulos NT, Liedo P, Muller HG, Wang JL, Molleman F, et al. (2010) Cost of reproduction in male medflies: The primacy of sexual courting in extreme longevity reduction. Journal of Insect Physiology 56: 283–287.
[77]
Shelly TE, Kennelly SS, McInnis DO (2002) Effect of adult diet on signaling activity, mate attraction, and mating success in male mediterranean fruit flies (Diptera : Tephritidae). Florida Entomologist 85: 150–155.
[78]
Kyriacou CP, Hall JC (1980) Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song. Proc Natl Acad Sci U S A 77: 6729–6733.
[79]
Sakai T, Ishida N (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci U S A 98: 9221–9225.
[80]
Emery P, Francis M (2008) Circadian rhythms: timing the sense of smell. Curr Biol 18: R569–571.
[81]
McDonald MJ, Rosbash M (2001) Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107: 567–578.
[82]
Ashburner M (1998) Speculations on the subject of alcohol dehydrogenase and its properties in Drosophila and other flies. Bioessays 20: 949–954.
[83]
Heath RR, Landolt PJ, Robacker DC, Dueben BD, Epsky ND (2000) Sexual pheromones of tephritid flies: clues to unravel phylogeny and behavior. In: Aluja M, Norrbom A, editors. Fruit flies (Tephritidae): phylogeny and evolution of behavior. Boca Raton, Florida, USA: CRC Press. 793–809.
[84]
Dyck VA, Hendrichs J, Robinson AS (2005) Sterile Insect Technique: Principles and practice in Area-wide Integrated Pest Management. DordrechtThe Netherlands: Springer. 787 p.
[85]
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18: 691–699.