The evolution of the metazoan Toll receptor family and its expression during protostome development
Background: Toll-like receptors (TLRs) play a crucial role in immunity and development. They contain leucine-rich repeat domains, one transmembrane domain, and one Toll/IL-1 receptor domain. TLRs have been classified into V-type/scc and P-type/mcc TLRs, based on differences in the leucine-rich repea...
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ftunivbergen:oai:bora.uib.no:11250/2834084 2023-05-15T15:59:03+02:00 The evolution of the metazoan Toll receptor family and its expression during protostome development Alcalde, Andrea Orus Lu, Tsai-Ming Børve, Aina Hejnol, Andreas 2021 application/pdf https://hdl.handle.net/11250/2834084 https://doi.org/10.1186/s12862-021-01927-1 eng eng BMC urn:issn:2730-7182 https://hdl.handle.net/11250/2834084 https://doi.org/10.1186/s12862-021-01927-1 cristin:1963926 BMC Ecology and Evolution. 2021, 21, 208. Navngivelse 4.0 Internasjonal http://creativecommons.org/licenses/by/4.0/deed.no Copyright 2021 the authors 208 BMC Ecology and Evolution 21 Journal article Peer reviewed 2021 ftunivbergen https://doi.org/10.1186/s12862-021-01927-1 2023-03-14T17:43:04Z Background: Toll-like receptors (TLRs) play a crucial role in immunity and development. They contain leucine-rich repeat domains, one transmembrane domain, and one Toll/IL-1 receptor domain. TLRs have been classified into V-type/scc and P-type/mcc TLRs, based on differences in the leucine-rich repeat domain region. Although TLRs are widespread in animals, detailed phylogenetic studies of this gene family are lacking. Here we aim to uncover TLR evolution by conducting a survey and a phylogenetic analysis in species across Bilateria. To discriminate between their role in development and immunity we furthermore analyzed stage-specific transcriptomes of the ecdysozoans Priapulus caudatus and Hypsibius exemplaris, and the spiralians Crassostrea gigas and Terebratalia transversa. Results: We detected a low number of TLRs in ecdysozoan species, and multiple independent radiations within the Spiralia. V-type/scc and P-type/mcc type-receptors are present in cnidarians, protostomes and deuterostomes, and therefore they emerged early in TLR evolution, followed by a loss in xenacoelomorphs. Our phylogenetic analysis shows that TLRs cluster into three major clades: clade α is present in cnidarians, ecdysozoans, and spiralians; clade β in deuterostomes, ecdysozoans, and spiralians; and clade γ is only found in spiralians. Our stage-specific transcriptome and in situ hybridization analyses show that TLRs are expressed during development in all species analyzed, which indicates a broad role of TLRs during animal development. Conclusions: Our findings suggest that a clade α TLR gene (TLR-Ca) and a clade β/γ TLR gene (TLR-Cβ/γ) were already present in the cnidarian-bilaterian common ancestor. However, although TLR-Ca was conserved in cnidarians, TLR-Cβ/γ was lost during the early evolution of these taxa. Moreover, TLR-Cβ/γ duplicated to generate TLR-Cβ and TLR-Cγ in the lineage to the last common protostome-deuterostome ancestor. TLR-Ca, TLR-Cβ and TLR-Cγ further expanded generating the three major TLR clades. While all three ... Article in Journal/Newspaper Crassostrea gigas University of Bergen: Bergen Open Research Archive (BORA-UiB) BMC Ecology and Evolution 21 1 |
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Open Polar |
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University of Bergen: Bergen Open Research Archive (BORA-UiB) |
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ftunivbergen |
language |
English |
description |
Background: Toll-like receptors (TLRs) play a crucial role in immunity and development. They contain leucine-rich repeat domains, one transmembrane domain, and one Toll/IL-1 receptor domain. TLRs have been classified into V-type/scc and P-type/mcc TLRs, based on differences in the leucine-rich repeat domain region. Although TLRs are widespread in animals, detailed phylogenetic studies of this gene family are lacking. Here we aim to uncover TLR evolution by conducting a survey and a phylogenetic analysis in species across Bilateria. To discriminate between their role in development and immunity we furthermore analyzed stage-specific transcriptomes of the ecdysozoans Priapulus caudatus and Hypsibius exemplaris, and the spiralians Crassostrea gigas and Terebratalia transversa. Results: We detected a low number of TLRs in ecdysozoan species, and multiple independent radiations within the Spiralia. V-type/scc and P-type/mcc type-receptors are present in cnidarians, protostomes and deuterostomes, and therefore they emerged early in TLR evolution, followed by a loss in xenacoelomorphs. Our phylogenetic analysis shows that TLRs cluster into three major clades: clade α is present in cnidarians, ecdysozoans, and spiralians; clade β in deuterostomes, ecdysozoans, and spiralians; and clade γ is only found in spiralians. Our stage-specific transcriptome and in situ hybridization analyses show that TLRs are expressed during development in all species analyzed, which indicates a broad role of TLRs during animal development. Conclusions: Our findings suggest that a clade α TLR gene (TLR-Ca) and a clade β/γ TLR gene (TLR-Cβ/γ) were already present in the cnidarian-bilaterian common ancestor. However, although TLR-Ca was conserved in cnidarians, TLR-Cβ/γ was lost during the early evolution of these taxa. Moreover, TLR-Cβ/γ duplicated to generate TLR-Cβ and TLR-Cγ in the lineage to the last common protostome-deuterostome ancestor. TLR-Ca, TLR-Cβ and TLR-Cγ further expanded generating the three major TLR clades. While all three ... |
format |
Article in Journal/Newspaper |
author |
Alcalde, Andrea Orus Lu, Tsai-Ming Børve, Aina Hejnol, Andreas |
spellingShingle |
Alcalde, Andrea Orus Lu, Tsai-Ming Børve, Aina Hejnol, Andreas The evolution of the metazoan Toll receptor family and its expression during protostome development |
author_facet |
Alcalde, Andrea Orus Lu, Tsai-Ming Børve, Aina Hejnol, Andreas |
author_sort |
Alcalde, Andrea Orus |
title |
The evolution of the metazoan Toll receptor family and its expression during protostome development |
title_short |
The evolution of the metazoan Toll receptor family and its expression during protostome development |
title_full |
The evolution of the metazoan Toll receptor family and its expression during protostome development |
title_fullStr |
The evolution of the metazoan Toll receptor family and its expression during protostome development |
title_full_unstemmed |
The evolution of the metazoan Toll receptor family and its expression during protostome development |
title_sort |
evolution of the metazoan toll receptor family and its expression during protostome development |
publisher |
BMC |
publishDate |
2021 |
url |
https://hdl.handle.net/11250/2834084 https://doi.org/10.1186/s12862-021-01927-1 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
208 BMC Ecology and Evolution 21 |
op_relation |
urn:issn:2730-7182 https://hdl.handle.net/11250/2834084 https://doi.org/10.1186/s12862-021-01927-1 cristin:1963926 BMC Ecology and Evolution. 2021, 21, 208. |
op_rights |
Navngivelse 4.0 Internasjonal http://creativecommons.org/licenses/by/4.0/deed.no Copyright 2021 the authors |
op_doi |
https://doi.org/10.1186/s12862-021-01927-1 |
container_title |
BMC Ecology and Evolution |
container_volume |
21 |
container_issue |
1 |
_version_ |
1766394824995373056 |