The evolution of the metazoan Toll receptor family and its expression during protostome development

Abstract 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-ri...

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Autores principales:	Andrea Orús-Alcalde, Tsai-Ming Lu, Aina Børve, Andreas Hejnol
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Toll receptor Toll-like receptor Innate immunity Development Metazoan evolution Gene duplication Ecology QH540-549.5 Evolution QH359-425
Acceso en línea:	https://doaj.org/article/79226820f72f4047b391fd5afe0fd698
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spelling	oai:doaj.org-article:79226820f72f4047b391fd5afe0fd6982021-11-28T12:04:06ZThe evolution of the metazoan Toll receptor family and its expression during protostome development10.1186/s12862-021-01927-12730-7182https://doaj.org/article/79226820f72f4047b391fd5afe0fd6982021-11-01T00:00:00Zhttps://doi.org/10.1186/s12862-021-01927-1https://doaj.org/toc/2730-7182Abstract 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 clades radiated in several spiralian lineages, specific TLRs clades have been presumably lost in other lineages. Furthermore, the expression of the majority of these genes during protostome ontogeny suggests a likely role in development.Andrea Orús-AlcaldeTsai-Ming LuAina BørveAndreas HejnolBMCarticleToll receptorToll-like receptorInnate immunityDevelopmentMetazoan evolutionGene duplicationEcologyQH540-549.5EvolutionQH359-425ENBMC Ecology and Evolution, Vol 21, Iss 1, Pp 1-21 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Toll receptor Toll-like receptor Innate immunity Development Metazoan evolution Gene duplication Ecology QH540-549.5 Evolution QH359-425
spellingShingle	Toll receptor Toll-like receptor Innate immunity Development Metazoan evolution Gene duplication Ecology QH540-549.5 Evolution QH359-425 Andrea Orús-Alcalde Tsai-Ming Lu Aina Børve Andreas Hejnol The evolution of the metazoan Toll receptor family and its expression during protostome development
description	Abstract 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 clades radiated in several spiralian lineages, specific TLRs clades have been presumably lost in other lineages. Furthermore, the expression of the majority of these genes during protostome ontogeny suggests a likely role in development.
format	article
author	Andrea Orús-Alcalde Tsai-Ming Lu Aina Børve Andreas Hejnol
author_facet	Andrea Orús-Alcalde Tsai-Ming Lu Aina Børve Andreas Hejnol
author_sort	Andrea Orús-Alcalde
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://doaj.org/article/79226820f72f4047b391fd5afe0fd698
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The evolution of the metazoan Toll receptor family and its expression during protostome development

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