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The Drosophila odorant-binding protein 28a is involved in the detection of the floral odour ß-ionone

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Abstract

Odorant-binding proteins (OBPs) are small soluble proteins that are thought to transport hydrophobic odorants across the aqueous sensillar lymph to olfactory receptors. A recent study revealed that OBP28a, one of the most abundant Drosophila OBPs, is not required for odorant transport, but acts in buffering rapid odour variation in the odorant environment. To further unravel and decipher its functional role, we expressed recombinant OBP28a and characterized its binding specificity. Using a fluorescent binding assay, we found that OBP28a binds a restricted number of floral-like chemicals, including ß-ionone, with an affinity in the micromolar range. We solved the X-ray crystal structure of OBP28a, which showed extensive conformation changes upon ligand binding. Mutant flies genetically deleted for the OBP28a gene showed altered responses to ß-ionone at a given concentration range, supporting its essential role in the detection of specific compounds present in the natural environment of the fly.

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Abbreviations

OBPs:

Odorant-binding proteins

OSNs:

Olfactory-sensory neurons

Ors:

Odorant receptors

cVA:

Cis-vaccenyl acetate

RPLC:

Reverse-phase liquid chromatography

CD:

Circular dichroism

SEC:

Size-exclusion chromatography

MALS:

Multi-angle laser light scattering

1PE:

Pentaethylene glycol

NPN:

N-phenyl-1-naphthylamine

SSR:

Single-sensillum recording

lmadPBP:

Pheromone-binding protein from Leucophaea maderae

dmelOBP76a:

Odorant-binding protein 76a from D. melanogaster

amelASP1:

Pheromone-binding protein 1 from Apis mellifera

amelOBP14:

Odorant-binding protein 14 from Apis mellifera

bmorPBP:

Pheromone-binding protein from Bombyx mori

agamOBP1:

Odorant-binding protein 1 from Anopheles gambiae

cquiOBP1:

Odorant-binding protein 1 from Culex pipiens quinquefasciatus

BMGY:

Buffered minimal glycerol

YNB:

Yeast nitrogen base

BMM:

Buffered minimal methanol

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Acknowledgements

We thank Dr. J. R. Carlson for Drosophila lines; Dr. C. Everaerts for help with the statistics; and Dr. T. Tanimura for discussion and critical reading. The ESRF is acknowledged for access to beamlines via its in-house research program. Mass spectrometry experiments were performed by the Plateforme d’Analyse Protéomique de Paris Sud-Ouest (PAPPSO, Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France).

Funding

This work was partly supported by grants from the Institut National de la Recherche Agronomique, of the Centre National de la Recherche Scientifique, of the Université de Bourgogne-Franche Comté, the Bourgogne-Franche Comté Regional Council (PARI 2010–2011–2012, AGRALE1 Project), and a postdoctoral fellowship from the Bourgogne Regional Council (D.G.). Fellowship for PhD to K.R. (INRA + Bourgogne-Franche Comté Regional Council).

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  1. Daniel Gonzalez and Karen Rihani have contributed equally to this work.

Authors and Affiliations

  1. AgroSup Dijon, CNRS, INRA, Université de Bourgogne-Franche Comté, Centre des Sciences du Goût et de l’Alimentation, 21000, Dijon, France

    Daniel Gonzalez, Karen Rihani, Fabrice Neiers, Nicolas Poirier, Stéphane Fraichard, Jean-François Ferveur & Loïc Briand

  2. European Synchrotron Radiation Facility, 38043, Grenoble, France

    Guillaume Gotthard

  3. Sorbonne Université, INRA, CNRS, IRD, UPEC, Institut d’Ecologie et des Sciences de l’Environnement de Paris, 75005, Paris, France

    Thomas Chertemps & Martine Maïbèche

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Contributions

JFF and LB designed the research. DG, KR, FN, NP, SF, GG, and TC performed the research. DG, KR, FN, SF, GG, TC, and MM analysed the data. The manuscript was written by DG, KR, JFF, and LB. All authors read and approved the final manuscript.

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Correspondence to Loïc Briand.

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Gonzalez, D., Rihani, K., Neiers, F. et al. The Drosophila odorant-binding protein 28a is involved in the detection of the floral odour ß-ionone. Cell. Mol. Life Sci. 77, 2565–2577 (2020). https://doi.org/10.1007/s00018-019-03300-4

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