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Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor.

Authors :
Guillaume Tetreau
Julien Dhinaut
Richard Galinier
Pascaline Audant-Lacour
Sébastien N Voisin
Karim Arafah
Manon Chogne
Frédérique Hilliou
Anaïs Bordes
Camille Sabarly
Philippe Chan
Marie-Laure Walet-Balieu
David Vaudry
David Duval
Philippe Bulet
Christine Coustau
Yannick Moret
Benjamin Gourbal
Source :
PLoS Pathogens, Vol 16, Iss 10, p e1008935 (2020)
Publication Year :
2020
Publisher :
Public Library of Science (PLoS), 2020.

Abstract

In a number of species, individuals exposed to pathogens can mount an immune response and transmit this immunological experience to their offspring, thereby protecting them against persistent threats. Such vertical transfer of immunity, named trans-generational immune priming (TGIP), has been described in both vertebrates and invertebrates. Although increasingly studied during the last decade, the mechanisms underlying TGIP in invertebrates are still elusive, especially those protecting the earliest offspring life stage, i.e. the embryo developing in the egg. In the present study, we combined different proteomic and transcriptomic approaches to determine whether mothers transfer a "signal" (such as fragments of infecting bacteria), mRNA and/or protein/peptide effectors to protect their eggs against two natural bacterial pathogens, namely the Gram-positive Bacillus thuringiensis and the Gram-negative Serratia entomophila. By taking the mealworm beetle Tenebrio molitor as a biological model, our results suggest that eggs are mainly protected by an active direct transfer of a restricted number of immune proteins and of antimicrobial peptides. In contrast, the present data do not support the involvement of mRNA transfer while the transmission of a "signal", if it happens, is marginal and only occurs within 24h after maternal exposure to bacteria. This work exemplifies how combining global approaches helps to disentangle the different scenarios of a complex trait, providing a comprehensive characterization of TGIP mechanisms in T. molitor. It also paves the way for future alike studies focusing on TGIP in a wide range of invertebrates and vertebrates to identify additional candidates that could be specific to TGIP and to investigate whether the TGIP mechanisms found herein are specific or common to all insect species.

Details

Language :
English
ISSN :
15537366 and 15537374
Volume :
16
Issue :
10
Database :
Directory of Open Access Journals
Journal :
PLoS Pathogens
Publication Type :
Academic Journal
Accession number :
edsdoj.120cb6a62f6644f0b989999b489aa1b0
Document Type :
article
Full Text :
https://doi.org/10.1371/journal.ppat.1008935