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Antennal Morphology and Localization of a Pheromone-Binding Protein of Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae)

  • Systematics, Morphology and Physiology
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Abstract

In the sensory system of insects, olfactory sensilla constitute important functional elements for discriminating odors. Therefore, we used light microscopy and scanning electron microscopy to investigate the morphology and distribution of sensilla in the antennae of Lobesia botrana (Denis & Schiffermüller). In addition, we studied the expression of the gene encoding for pheromone-binding protein 1 (LbotPBP1) by in situ hybridization. Lobesia botrana antennae are filiform and are subdivided into three segments: scape, pedicel, and flagellum. The number of flagellum and their overall length were significantly higher and longer in males than in females. Six morphological types of sensilla (trichodea, chaetica, coeloconica, auricillica, basiconica, and styloconica) were identified on the antennae of both sexes. Trichodea sensilla were the most abundant on the antennae of L. botrana, and three subtypes, discerned by their lengths, were observed. However, sensilla trichodea subtype III was only present in male antennae. Moreover, LbotPBP1 expression was restricted to this type of sensilla, thus confirming its olfactory role, specifically under the context of sexual pheromone perception.

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References

  • Albert PJ, Seabrook WD (1973) Morphology and histology of the antenna of the male eastern spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae). Can J Zool 51:443–448

    Article  Google Scholar 

  • Ansebo L, Ignell R, Löfqvist J, Hansson B (2005) Responses to sex pheromone and plant odours by olfactory receptor neurons housed in sensilla auricillica of the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). J Insect Physiol 51:1066–1074

    Article  CAS  PubMed  Google Scholar 

  • Arn H, Rauscher S, Guerin P, Buser HR (1988) Sex pheromone blends of three tortricid pests in European vineyards. Agric Ecosyst Environ 21:111–117

    Article  CAS  Google Scholar 

  • Binyameen M, Anderson P, Ignell R, Seada MA, Hansson BS, Schlyter F (2012) Spatial organization of antennal olfactory sensory neurons in the female Spodoptera littoralis moth: differences in sensitivity and temporal characteristics. Chem Senses 37:613–629

  • Callahan PS (1975) Insect antennae with special reference to the mechanism of scent detection and the evolution of sensilla. Int J Insect Morphol Embryol 4:381–430

    Article  Google Scholar 

  • Castrejón-Gómez VR, Nieto G, Valdes J, Castrejón F, Rojas J (2003) The antennal sensilla of Zamagiria dixolophella Dyar (Lepidoptera: Pyralidae). Ann Entomol Soc Am 96:672–678

    Article  Google Scholar 

  • Castrejón-Gómez VR, Valdez-Carrasco J (2008) Morphological characteristics of antennal sensilla in Talponia batesi (Lepidoptera: Tortricidae). Ann Entomol Soc Am 101:181–188

    Article  Google Scholar 

  • Den Otter CJ, Schuil HA, Sander-Van OOsten A (1978) Reception of host-plant odours and female sex pheromone in Adoxophyes orana (Lepidoptera: Tortricidae): electrophysiology and morphology. Entomol Exp Appl 24:370–378

    Article  Google Scholar 

  • Ebbinghausa D, Löselb PM, Lindemannb M, Scherkenbeckb J, Zebitza CPW (1997) Detection of major and minor sex pheromone components by the male codling moth Cydia pomonella (Lepidoptera: Tortricidae). J Insect Physiol 44:49–58

    Article  Google Scholar 

  • El-Sayed A, Godde J, Witzgall P, Arn H (1999) Characterization of pheromone blend for grapevine moth, Lobesia botrana by using flight track recording. J Chem Ecol 25:389–400

    Article  CAS  Google Scholar 

  • George JA, Nagy AL (1984) Morphology, distribution, and ultrastructural differences of sensilla trichodea and basiconica on the antennae of the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae). Int J Insect Morphol Embryol 13:157–170

    Article  Google Scholar 

  • González M (2010) Lobesia botrana: Polilla de la uva. Revista Enologia 2:1–5

    Google Scholar 

  • Gilligan TM, Epstein ME, Passoa SC, Powell JA, Sage OC, Brown JW (2011) Discovery of Lobesia botrana (Denis & Schiffermuller) in California: an invasive species new to North America (Lepidoptera: Tortricidae). Proc Entomol Soc Wash 113:14–30

    Article  Google Scholar 

  • Harari A, Steinitz H (2013) The evolution of female sex pheromones. Curr Zool 59:569–578

    Article  Google Scholar 

  • Harari A, Zahavi T, Steinitz H (2014) Female detection of the synthetic sex pheromone contributes to the efficacy of mating disruption of the European grapevine moth, Lobesia botrana. Pest Manag Sci 71:316–322

    Article  CAS  PubMed  Google Scholar 

  • Hunger T, Steinbrecht R (1998) Functional morphology of a double-walled multiporous olfactory sensillum: the sensillum coeloconicum of Bombyx mori (Insecta, Lepidoptera). Tissue Cell 30:14–29

    Article  CAS  PubMed  Google Scholar 

  • Ioriatti C, Anfora G, Angeli G, Mazzoni V, Trona F (2009) Effects of chlorantraniliprole on eggs and larvae of Lobesia botrana (Denis & Schiffermuller) (Lepidoptera: Tortricidae). Pest Manag Sci 65:717–722

    Article  CAS  PubMed  Google Scholar 

  • Ioriatti C, Anfora G, Tasin M, De Cristofaro A, Witzgall P, Lucchi A (2011) Chemical ecology and management of Lobesia botrana (Lepidoptera: Tortricidae). J Econ Entomol 104:1125–1137

    Article  CAS  PubMed  Google Scholar 

  • Kaissling KE (1986) Chemo-electrical transduction in insect olfactory receptors. Annu Rev Neurosci 9:121–145

    Article  CAS  PubMed  Google Scholar 

  • Koh Y, Park K, Boo K (1995) Antennal sensilla in adult Helicoverpa assulta (Lepidoptera: Noctuidae): morphology, distribution and ultrastructure. Ann Entomol Soc Am 88:519–530

    Article  Google Scholar 

  • Larsson M, Hallberg E, Kozlov M, Francke W, Hansson B, Löfstedt C (2002) Specialized olfactory receptor neurons mediating intra- and interspecific chemical communication in leafminer moths Eriocrania spp. (Lepidoptera: Eriocraniidae). J Exp Biol 205:989–998

    PubMed  Google Scholar 

  • Leal WS (2003) Proteins that make sense, in insect pheromone biochemistry and molecular biology. The biosynthesis and detection of pheromones and plant volatiles. In: Blomquist GJ. Academic Press, Vogt RG (Eds), pp 447–476

    Google Scholar 

  • Leal WS, Chen AM, Ishida Y, Chiang VP, Erickson ML, Morgan TL, Tsuruda JM (2005) Kinetics and molecular properties of pheromone binding and release. Proc Natl Acad Sci U S A 102:5385–5391

    Article  CAS  Google Scholar 

  • Ma M, Chang MM, Lu Y, Lei CL, Yang FL (2017) Ultrastructure of sensilla of antennae and ovipositor of Sitotroga cerealella (Lepidoptera: Gelechiidae), and location of female sex pheromone gland. Sci Rep 7:40637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moschos T, Souliotis C, Broumas T, Kapothanassi V (2004) Control of the European grapevine moth Lobesia botrana in Greece by the mating disruption technique: a three-year survey. Phytoparasitica 32:83–96

    Article  Google Scholar 

  • Mutis A, Palma R, Venthur H, Iturriaga-Vásquez P, Faundez-Parraguez M, Mella-Herrera R, Kontodimas D, Lobos C, Quiroz A (2014) Molecular characterization and in silico analysis of the pheromone-binding protein of the European grapevine moth Lobesia botrana (Denis & Schiffermüller) (Lepidoptera, Tortricidae). Neotrop Entomol 43:266–275

    Article  CAS  PubMed  Google Scholar 

  • Ndomo-Moualeu A, Ulrichs C, Radek R, Adler C (2014) Structure and distribution of antennal sensilla in the Indianmeal moth, Plodia interpunctella (Hübner, 1813) (Lepidoptera: Pyralidae). J Stored Prod Res 59:66–75

    Article  Google Scholar 

  • Odendaal FJ, Ehrlich PR, Thomas FC (1985) Structure and function of the antennae of Euphydryas editha (Lepidoptera, Nymphalidae). J Morphol 184:3–22

    Article  Google Scholar 

  • Palanaswamy P, Seabrook WD (1978) Behavioural responses of the female eastern spruce budworm Choristoneura fumiferana (Lepidoptera: Tortricidae) to the sex pheromone of her own species. J Chem Ecol 4:649–655

    Article  CAS  Google Scholar 

  • Pelosi P, Mastrogiacomo R, Iovinella I, Tuccori E, Persaud C (2014) Structure and biotechnological applications of odorant-binding proteins. Appl Microbiol Biotechnol 98:61–70

    Article  CAS  PubMed  Google Scholar 

  • Roh HS, Park KCh OHW, Park CG (2016) Morphology and distribution of antennal sensilla of two tortricid moths, Cydia pomonella and C. succedana (Lepidoptera). Micros Res Tech 79:1069–1081

    Article  Google Scholar 

  • Roh GH, Park KCh OHW, Park CG (2018) Species- and sex-specific distribution of antennal olfactory sensilla in two tortricid moths, Epiphyas postvittana and Planotortrix octo. Micron 106:7–20

    Article  PubMed  Google Scholar 

  • Rojas V, Jiménez H, Palma-Millanao R, González-González A, Machuca J, Godoy R, Ceballos R, Mutis A, Venthur H (2018) Analysis of the grapevine moth Lobesia botrana antennal transcriptome and expression of odorant-binding and chemosensory proteins. Comp Biochem Physiol Part D Genomics Proteomics 27:1–12

    Article  CAS  PubMed  Google Scholar 

  • Romero-López A, Morón M (2013) Sexual dimorphism in antennae of Mexican species of Phyllophaga (Coleoptera: Scarabaeoidea: Melolonthidae). Biochemistry, Genetics and Molecular Biology. In: Moriyama H (Ed) London, InTech. 17-34

  • Seada M (2015) Antennal morphology and sensillum distribution of female cotton leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae). J Basic Appl Zool 68:10–18

    Article  Google Scholar 

  • Shields VDC, Hildebrand JG (1999) Fine structure of antennal sensilla of the female sphinx moth, Manduca sexta (Lepidoptera: Sphingidae). II. Auriculate, coeloconic, and styliform complex sensilla. Can J Zool 77:302–313

    Article  Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122

    Article  Google Scholar 

  • Tanaka S, Yukuhiro F, Wakamura S (2006) Sexual dimorphism in body dimensions and antennal sensilla in the white grub beetle, Dasylepida ishigakiensis (Coleoptera: Scarabaeidae). Appl Entomol Zool 41:455–461

    Article  Google Scholar 

  • Trona F, Anfora G, Balkenius A, Bengtsson M, Tasin M, Knight A, Janz N, Witzgall P, Ignell R (2013) Neural coding merges sex and habitat chemosensory signals in an insect herbivore. Proc R Soc Lond B Biol Sci 280:20130267. https://doi.org/10.1098/rspb.2013.0267

    Article  CAS  Google Scholar 

  • Wall C (1978) Morphology and histology of the antenna of Cydia nigricana (F) (Lepidoptera: Tortricidae). Int J Insect Morphol Embryol 7:237–250

    Article  Google Scholar 

  • Wee S, Oh H, Park K (2016) Antennal sensillum morphology and electrophysiological responses of olfactory receptor neurons in trichoid sensilla of the diamondback moth (Lepidoptera: Plutellidae). Fla Entomol 99:146–158

    Article  Google Scholar 

  • Witzgall P, Tasin M, Buser HR, Wegner-Kiss G, Mancebón VSM, Ioriatti C, Bäckman AC, Bengtsson M, Lehmann L, Francke W (2005) New pheromone components of the grapevine moth Lobesia botrana. J Chem Ecol 31:2923–2932

    Article  CAS  PubMed  Google Scholar 

  • Wojtasek H (2002) Molecular mechanisms of insect chemical communication: from pheromone biosynthesis to perception and degradation, Wydawn. Uniwersytetu Opolskiego, Poland

  • Zacharuk R (1980) Ultrastructure and function of insect chemosensilla. Annu Rev Entomol 25:27–47

    Article  Google Scholar 

  • Zar J (1999) Biostatistical analysis. Fourth Edition, Prentice Hall, New Jersey

  • Zhang Z, Li X, Chen L, Wang L, Lei C (2016) Morphology, distribution and abundance of antennal sensilla of the oyster mushroom fly, Coboldia fuscipes (Meigen) (Diptera: Scatopsidae). Rev Bras Entomol 60:8–14

    Article  Google Scholar 

  • Zheng H, Liu H, Guo S, Yan Y, Zong S, Zhang J (2014) Scanning electron microscopy study of the antennal sensilla of Catocala remissa. B Insectol 67:63–71

    Google Scholar 

  • Zhou JJ (2010) Odorant-Binding Proteins in Insects. In: Odorant-binding proteins in insects, 1st edn. Elsevier Inc. https://doi.org/10.1016/S0083-6729(10)83010-9

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Acknowledgments

This study was supported by FONDECYT project 11140668.

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Authors and Affiliations

  1. Carrera de Bioquímica, Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, La Araucanía, 4811230, Temuco, Chile

    R. Godoy, C. Aburto & P. Lizana

  2. Centro de Investigación Biotecnológica Aplicada al Medio Ambiente (CIBAMA), Universidad de La Frontera, Av. Francisco Salazar 01145, Casilla 54-D, Temuco, Chile

    R. Godoy, H. Venthur, L. Méndez, L. Bardehle, A. Quiroz & A. Mutis

  3. Laboratorio de Química Ecológica, Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Araucanía, Temuco, Chile

    H. Venthur, L. Bardehle, A. Quiroz & A. Mutis

  4. Instituto de Ciencias Biológicas, Millennium Nucleus Centre in Molecular Ecology and Evolutionary Applications in the Agroecosystems, Universidad de Talca, Talca, Chile

    R. Palma-Millanao

  5. Instituto de Investigaciones Agropecuarias (INIA Quilamapu), Chillán, Chile

    M. Panichini

  6. Doctorado en Ciencias de Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Temuco, Chile

    F. Moraga

  7. Scientific and Technological Bioresource Nucleus (BIOREN-UFRO), Universidad de La Frontera, Temuco, Chile

    L. Bardehle

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  1. R. Godoy
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  2. C. Aburto
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Contributions

AM, AQ, and RP planned, designed, and executed experimental work. PL, CA, FM, and HV executed experimental work with antennae. RG and AM performed in situ hybridization. MP, LB, and LM performed data analyses. AM, RG, and HV wrote the manuscript.

Corresponding author

Correspondence to A. Mutis.

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Edited by Roberto Romani – Univ of Perugia

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Godoy, R., Aburto, C., Lizana, P. et al. Antennal Morphology and Localization of a Pheromone-Binding Protein of Lobesia botrana (Denis & Schiffermüller) (Lepidoptera: Tortricidae). Neotrop Entomol 48, 422–432 (2019). https://doi.org/10.1007/s13744-018-0648-x

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