Literature DB >> 33057453

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

Guillaume Tetreau1, Julien Dhinaut2, Richard Galinier1, Pascaline Audant-Lacour3, Sébastien N Voisin4, Karim Arafah4, Manon Chogne2, Frédérique Hilliou3, Anaïs Bordes1, Camille Sabarly2, Philippe Chan5, Marie-Laure Walet-Balieu5, David Vaudry5, David Duval1, Philippe Bulet4,6, Christine Coustau3, Yannick Moret2, Benjamin Gourbal1.   

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.

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Year:  2020        PMID: 33057453      PMCID: PMC7591081          DOI: 10.1371/journal.ppat.1008935

Source DB:  PubMed          Journal:  PLoS Pathog        ISSN: 1553-7366            Impact factor:   6.823


  80 in total

Review 1.  The prophenoloxidase-activating system in invertebrates.

Authors:  Lage Cerenius; Kenneth Söderhäll
Journal:  Immunol Rev       Date:  2004-04       Impact factor: 12.988

Review 2.  Anti-microbial peptides: from invertebrates to vertebrates.

Authors:  Philippe Bulet; Reto Stöcklin; Laure Menin
Journal:  Immunol Rev       Date:  2004-04       Impact factor: 12.988

3.  Immune competence in insect eggs depends on the extraembryonic serosa.

Authors:  Chris G C Jacobs; Maurijn van der Zee
Journal:  Dev Comp Immunol       Date:  2013-05-31       Impact factor: 3.636

4. 

Authors:  Alice Ewest
Journal:  Wilhelm Roux Arch Entwickl Mech Org       Date:  1937-12

Review 5.  The Ultimate qPCR Experiment: Producing Publication Quality, Reproducible Data the First Time.

Authors:  Sean C Taylor; Katia Nadeau; Meysam Abbasi; Claude Lachance; Marie Nguyen; Joshua Fenrich
Journal:  Trends Biotechnol       Date:  2019-01-14       Impact factor: 19.536

Review 6.  Immune memory in invertebrates.

Authors:  Barbara Milutinović; Joachim Kurtz
Journal:  Semin Immunol       Date:  2016-07-09       Impact factor: 11.130

7.  How plants and insects inherit immunity from their parents.

Authors:  Brian Owens
Journal:  Nature       Date:  2019-11       Impact factor: 49.962

8.  Primed for success: Oyster parents treated with poly(I:C) produce offspring with enhanced protection against Ostreid herpesvirus type I infection.

Authors:  Timothy J Green; Karla Helbig; Peter Speck; David A Raftos
Journal:  Mol Immunol       Date:  2016-09-09       Impact factor: 4.407

9.  Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum.

Authors:  Olivia Roth; Gerrit Joop; Hendrik Eggert; Jonas Hilbert; Jens Daniel; Paul Schmid-Hempel; Joachim Kurtz
Journal:  J Anim Ecol       Date:  2009-10-14       Impact factor: 5.091

10.  The maternal NF-kappaB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle.

Authors:  G Chen; K Handel; S Roth
Journal:  Development       Date:  2000-12       Impact factor: 6.868

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  1 in total

Review 1.  Response Mechanisms of Invertebrates to Bacillus thuringiensis and Its Pesticidal Proteins.

Authors:  Daniel Pinos; Ascensión Andrés-Garrido; Juan Ferré; Patricia Hernández-Martínez
Journal:  Microbiol Mol Biol Rev       Date:  2021-01-27       Impact factor: 11.056

  1 in total

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