Comparative and functional genomics of the ABC transporter superfamily across arthropods.


Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
19 Jul 2021
Historique:
received: 15 04 2021
accepted: 23 06 2021
entrez: 20 7 2021
pubmed: 21 7 2021
medline: 22 7 2021
Statut: epublish

Résumé

The ATP-binding cassette (ABC) transporter superfamily is comprised predominantly of proteins which directly utilize energy from ATP to move molecules across the plasma membrane. Although they have been the subject of frequent investigation across many taxa, arthropod ABCs have been less well studied. While the manual annotation of ABC transporters has been performed in many arthropods, there has so far been no systematic comparison of the superfamily within this order using the increasing number of sequenced genomes. Furthermore, functional work on these genes is limited. Here, we developed a standardized pipeline to annotate ABCs from predicted proteomes and used it to perform comparative genomics on ABC families across arthropod lineages. Using Kruskal-Wallis tests and the Computational Analysis of gene Family Evolution (CAFE), we were able to observe significant expansions of the ABC-B full transporters (P-glycoproteins) in Lepidoptera and the ABC-H transporters in Hemiptera. RNA-sequencing of epithelia tissues in the Lepidoptera Helicoverpa armigera showed that the 7 P-glycoprotein paralogues differ substantially in their tissue distribution, suggesting a spatial division of labor. It also seems that functional redundancy is a feature of these transporters as RNAi knockdown showed that most transporters are dispensable with the exception of the highly conserved gene Snu, which is probably due to its role in cuticular formation. We have performed an annotation of the ABC superfamily across > 150 arthropod species for which good quality protein annotations exist. Our findings highlight specific expansions of ABC transporter families which suggest evolutionary adaptation. Future work will be able to use this analysis as a resource to provide a better understanding of the ABC superfamily in arthropods.

Sections du résumé

BACKGROUND BACKGROUND
The ATP-binding cassette (ABC) transporter superfamily is comprised predominantly of proteins which directly utilize energy from ATP to move molecules across the plasma membrane. Although they have been the subject of frequent investigation across many taxa, arthropod ABCs have been less well studied. While the manual annotation of ABC transporters has been performed in many arthropods, there has so far been no systematic comparison of the superfamily within this order using the increasing number of sequenced genomes. Furthermore, functional work on these genes is limited.
RESULTS RESULTS
Here, we developed a standardized pipeline to annotate ABCs from predicted proteomes and used it to perform comparative genomics on ABC families across arthropod lineages. Using Kruskal-Wallis tests and the Computational Analysis of gene Family Evolution (CAFE), we were able to observe significant expansions of the ABC-B full transporters (P-glycoproteins) in Lepidoptera and the ABC-H transporters in Hemiptera. RNA-sequencing of epithelia tissues in the Lepidoptera Helicoverpa armigera showed that the 7 P-glycoprotein paralogues differ substantially in their tissue distribution, suggesting a spatial division of labor. It also seems that functional redundancy is a feature of these transporters as RNAi knockdown showed that most transporters are dispensable with the exception of the highly conserved gene Snu, which is probably due to its role in cuticular formation.
CONCLUSIONS CONCLUSIONS
We have performed an annotation of the ABC superfamily across > 150 arthropod species for which good quality protein annotations exist. Our findings highlight specific expansions of ABC transporter families which suggest evolutionary adaptation. Future work will be able to use this analysis as a resource to provide a better understanding of the ABC superfamily in arthropods.

Identifiants

pubmed: 34281528
doi: 10.1186/s12864-021-07861-2
pii: 10.1186/s12864-021-07861-2
pmc: PMC8290562
doi:

Substances chimiques

ATP-Binding Cassette Transporters 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

553

Informations de copyright

© 2021. The Author(s).

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Auteurs

Shane Denecke (S)

Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology Hellas, 100 N. Plastira Street, 700 13, Heraklion Crete, Greece. shane_denecke@imbb.forth.gr.

Ivan Rankić (I)

Department of Chemistry and Biochemistry, Mendel University in Brno, Zemedelska 1, 613 00, Brno, Czechia.

Olympia Driva (O)

Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology Hellas, 100 N. Plastira Street, 700 13, Heraklion Crete, Greece.

Megha Kalsi (M)

Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology Hellas, 100 N. Plastira Street, 700 13, Heraklion Crete, Greece.

Ngoc Bao Hang Luong (NBH)

Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology Hellas, 100 N. Plastira Street, 700 13, Heraklion Crete, Greece.

Benjamin Buer (B)

CropScience Division, Bayer AG, R&D Pest Control, D-40789, Monheim, Germany.

Ralf Nauen (R)

CropScience Division, Bayer AG, R&D Pest Control, D-40789, Monheim, Germany.

Sven Geibel (S)

CropScience Division, Bayer AG, R&D Pest Control, D-40789, Monheim, Germany.

John Vontas (J)

Institute of Molecular Biology & Biotechnology, Foundation for Research & Technology Hellas, 100 N. Plastira Street, 700 13, Heraklion Crete, Greece.
Laboratory of Pesticide Science, Department of Crop Science, Agricultural University of Athens, Athens, Greece.

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