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

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...

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Main Authors: 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
Format: Article
Language:English
Published: BMC 2021-11-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-021-08118-8
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author 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
author_facet 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
author_sort Emiliano Fratini
collection DOAJ
description 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.
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spelling doaj.art-45494e0c09fb41a3b44e684c4063333b2022-12-21T20:37:52ZengBMCBMC Genomics1471-21642021-11-0122112410.1186/s12864-021-08118-8Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approachEmiliano Fratini0Marco Salvemini1Fabrizio Lombardo2Maurizio Muzzi3Marco Molfini4Silvia Gisondi5Elia Roma6Veronica D’Ezio7Tiziana Persichini8Tecla Gasperi9Paolo Mariottini10Andrea Di Giulio11Marco Alberto Bologna12Manuela Cervelli13Emiliano Mancini14Department of Sciences, University of Roma TreDepartment of Biology, University of Naples Federico IIDepartment of Public Health and Infectious Diseases, Sapienza UniversityDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Biology and Biotechnologies “Charles Darwin”, Sapienza UniversityDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Sciences, University of Roma TreDepartment of Biology and Biotechnologies “Charles Darwin”, Sapienza UniversityAbstract 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.https://doi.org/10.1186/s12864-021-08118-8CantharidinBlister beetleToxic terpeneReflex-bleedingAutohaemorrhagingClotting
spellingShingle 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
Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
BMC Genomics
Cantharidin
Blister beetle
Toxic terpene
Reflex-bleeding
Autohaemorrhaging
Clotting
title Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
title_full Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
title_fullStr Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
title_full_unstemmed Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
title_short Unraveling the role of male reproductive tract and haemolymph in cantharidin-exuding Lydus trimaculatus and Mylabris variabilis (Coleoptera: Meloidae): a comparative transcriptomics approach
title_sort unraveling the role of male reproductive tract and haemolymph in cantharidin exuding lydus trimaculatus and mylabris variabilis coleoptera meloidae a comparative transcriptomics approach
topic Cantharidin
Blister beetle
Toxic terpene
Reflex-bleeding
Autohaemorrhaging
Clotting
url https://doi.org/10.1186/s12864-021-08118-8
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