Strong impact of orally administered BCR4 defensin on aphid survival, embryo development, and symbiotic cells in three Acyrthosiphon pisum parthenogenetic lines

Terrasson, Hugo;Gaget, Karen;Lapetoule, Garance;Rahioui, Isabelle;Da Silva, Pedro;et.al.
(2025) Journal of Pest Science — Vol. 98, n° 3, p. 1599-1612 (2025)

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Authors
  • Terrasson, Hugoorcid-logoINSA Lyon, INRAE, BF2I, UMR203, 69621, Villeurbanne, France
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  • Gaget, Karenorcid-logoINSA Lyon, INRAE, BF2I, UMR203, 69621, Villeurbanne, France
    Author
  • Lapetoule, GaranceINSA Lyon, INRAE, BF2I, UMR203, 69621, Villeurbanne, France
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  • Rahioui, IsabelleINSA Lyon, INRAE, BF2I, UMR203, 69621, Villeurbanne, France
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  • Da Silva, Pedroorcid-logoINSA Lyon, INRAE, BF2I, UMR203, 69621, Villeurbanne, France
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Abstract
Aphids are major crop pests capable of colonizing the main plants grown for human consumption. They have specialized cells, the bacteriocytes, which house the obligate symbiont Buchnera aphidicola that provide them with essential nutrients missing from their diet. Bacteriocyte-specific cysteine-rich peptides (BCRs) are encoded by a defensin gene family exclusively present in aphids and specifically expressed in bacteriocytes. One BCR family member, BCR4, has been shown to have insecticidal properties against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae). In the present study, we exposed the pea aphid to different doses of BCR4 and examined the impact on aphid survival, mass, anatomy, and fecundity, as well as on bacterial symbiosis. As different pea aphid lines with various symbiotic status may be differently affected by stress, we investigated the effect of BCR4 ingestion on three different A. pisum lines: LL01 and YR2-amp, that are mono-infected with B. aphidicola, and YR2-Ri, that is genetically identical to YR2-amp but also contains the extracellular facultative symbiont Regiella insecticola. Our results show a strong dose–response effect of BCR4 on LL01 survival and a more moderate effect on both YR2 lines, while an impact on the mass was observed in the three lines. Histological analyses revealed severe embryonic developmental defects due to the treatment. Finally, BCR4 treatment reduced symbiont quantity, with B. aphidicola being more affected than R. insecticola. This study supports the hypothesis that BCR4 could act as a key regulator of aphid symbiosis and development and highlights its potential as a candidate bioinsecticide for pest control.
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Citations

Terrasson, H., Gaget, K., Lapetoule, G., Rahioui, I., Renoz, F., Benhamou, S., Jouve, C., Sivignon, C., Duport, G., Aucagne, V., Simon, J.-C., Ribeiro Lopes, M., Calevro, F., & Da Silva, P. (2025). Strong impact of orally administered BCR4 defensin on aphid survival, embryo development, and symbiotic cells in three Acyrthosiphon pisum parthenogenetic lines. Journal of Pest Science, 98(3), 1599-1612. https://doi.org/10.1007/s10340-025-01923-0 (Original work published 2025)