Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach

Emiliano Fratini, Marco Salvemini, Fabrizio Lombardo, Maurizio Muzzi, Marco Molfini, Silvia Gisondi, Elia Roma, Veronica D’Ezio, Tiziana Persichini, Tecla Gasperi, Paolo Mariottini, Andrea Di Giulio, Marco Alberto Bologna, Manuela Cervelli, Emiliano Mancini

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Abstract

Background: Meloidae (blister beetles) are known to synthetize cantharidin (CA), a toxic and defensive terpene mainly stored in male accessory glands (MAG) and emitted outward through reflex-bleeding. Recent progresses in understanding CA biosynthesis and production organ(s) in Meloidae have been made, but the way in which self-protection is achieved from the hazardous accumulation and release of CA in blister beetles has been experimentally neglected. To provide hints on this pending question, a comparative de novo assembly transcriptomic approach was performed by targeting two tissues where CA is largely accumulated and regularly circulates in Meloidae: the male reproductive tract (MRT) and the haemolymph. Differential gene expression profiles in these tissues were examined in two blister beetle species, Lydus trimaculatus (Fabricius, 1775) (tribe Lyttini) and Mylabris variabilis (Pallas, 1781) (tribe Mylabrini). Upregulated transcripts were compared between the two species to identify conserved genes possibly involved in CA detoxification and transport. Results: Based on our results, we hypothesize that, to avoid auto-intoxication, ABC, MFS or other solute transporters might sequester purported glycosylated CA precursors into MAG, and lipocalins could bind CA and mitigate its reactivity when released into the haemolymph during the autohaemorrhaging response. We also found an over-representation in haemolymph of protein-domains related to coagulation and integument repairing mechanisms that likely reflects the need to limit fluid loss during reflex-bleeding. Conclusions: The de novo assembled transcriptomes of L. trimaculatus and M. variabilis here provided represent valuable genetic resources to further explore the mechanisms employed to cope with toxicity of CA in blister beetle tissues. These, if revealed, might help conceiving safe and effective drug-delivery approaches to enhance the use of CA in medicine.

OriginalsprogEngelsk
Artikelnummer808
TidsskriftBMC Genomics
Vol/bind22
Antal sider24
ISSN1471-2164
DOI
StatusUdgivet - 2021

Bibliografisk note

Funding Information:
Thanks to all students and colleagues helping collecting specimens of blister beetles on field, and R. Poloni (Modena) for providing individuals of Mylabris variabilis from Abruzzo (Italy). We wish to thank A. Riccieri (Roma Tre University) for providing starting material to set-up RT-qPCR and M.V. Modica for her precious advice on data analysis workflow. We are sincerely grateful to Prof. W.D. Woggon (University of Basel) for sharing data and opinion on cantharidin biosynthesis and blister beetle defensive behaviour. We are also grateful to three anonymous reviewers, whose suggestions greatly improved the manuscript.

Funding Information:
This work was carried out in the frame of the project “CanBBio - Cantaridina: dalla Biodiversità alle Biotecnologie” (prot. n° 85–2017-14967) financed by Regione Lazio (Progetti Gruppi di ricerca – Conoscenza e Cooperazione per un Nuovo Modello di Sviluppo, L.R. Lazio 13/08) and co-funded by MIUR-Italy (Departments of Excellence, L. 232/2016, art.1: 314–337, awarded to Dept. of Science, University of Roma Tre, Rome Italy for 2018–2022).

Publisher Copyright:
© 2021, The Author(s).

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