The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals

The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals

The “Nucleotide-binding domain and Leucine-rich Repeat” (NLR) genes are a family of intracellular pattern recognition receptors (PRR) that are a critical component of the metazoan innate immune system, involved in both defense against pathogenic microorganisms and in beneficial interactions with sym...

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Main Authors: Yuen, Benedict, Bayes, Joanne M., Degnan, Sandie M.
Format: Online
Language:English
Published: Oxford University Press 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879445/
id pubmed-3879445
recordtype oai_dc
spelling pubmed-38794452014-01-03 The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals Yuen, Benedict Bayes, Joanne M. Degnan, Sandie M. Discoveries The “Nucleotide-binding domain and Leucine-rich Repeat” (NLR) genes are a family of intracellular pattern recognition receptors (PRR) that are a critical component of the metazoan innate immune system, involved in both defense against pathogenic microorganisms and in beneficial interactions with symbionts. To investigate the origin and evolution of the NLR gene family, we characterized the full NACHT domain-containing gene complement in the genome of the sponge, Amphimedon queenslandica. As sister group to all animals, sponges are ideally placed to inform our understanding of the early evolution of this ancient PRR family. Amphimedon queenslandica has a large NACHT domain-containing gene complement that is dominated by bona fide NLRs (n = 135) with varied phylogenetic histories. Approximately half of these have a tripartite architecture that includes an N-terminal CARD or DEATH domain. The multiplicity of the A. queenslandica NLR genes and the high variability across the N- and C-terminal domains are consistent with involvement in immunity. We also provide new insight into the evolution of NLRs in invertebrates through comparative genomic analysis of multiple metazoan and nonmetazoan taxa. Specifically, we demonstrate that the NLR gene family appears to be a metazoan innovation, characterized by two major gene lineages that may have originated with the last common eumetazoan ancestor. Subsequent lineage-specific gene duplication, gene loss and domain shuffling all have played an important role in the highly dynamic evolutionary history of invertebrate NLRs. Oxford University Press 2014-01 2013-10-03 /pmc/articles/PMC3879445/ /pubmed/24092772 http://dx.doi.org/10.1093/molbev/mst174 Text en © The Author 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Yuen, Benedict
Bayes, Joanne M.
Degnan, Sandie M.
spellingShingle Yuen, Benedict
Bayes, Joanne M.
Degnan, Sandie M.
The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
author_facet Yuen, Benedict
Bayes, Joanne M.
Degnan, Sandie M.
author_sort Yuen, Benedict
title The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
title_short The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
title_full The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
title_fullStr The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
title_full_unstemmed The Characterization of Sponge NLRs Provides Insight into the Origin and Evolution of This Innate Immune Gene Family in Animals
title_sort characterization of sponge nlrs provides insight into the origin and evolution of this innate immune gene family in animals
description The “Nucleotide-binding domain and Leucine-rich Repeat” (NLR) genes are a family of intracellular pattern recognition receptors (PRR) that are a critical component of the metazoan innate immune system, involved in both defense against pathogenic microorganisms and in beneficial interactions with symbionts. To investigate the origin and evolution of the NLR gene family, we characterized the full NACHT domain-containing gene complement in the genome of the sponge, Amphimedon queenslandica. As sister group to all animals, sponges are ideally placed to inform our understanding of the early evolution of this ancient PRR family. Amphimedon queenslandica has a large NACHT domain-containing gene complement that is dominated by bona fide NLRs (n = 135) with varied phylogenetic histories. Approximately half of these have a tripartite architecture that includes an N-terminal CARD or DEATH domain. The multiplicity of the A. queenslandica NLR genes and the high variability across the N- and C-terminal domains are consistent with involvement in immunity. We also provide new insight into the evolution of NLRs in invertebrates through comparative genomic analysis of multiple metazoan and nonmetazoan taxa. Specifically, we demonstrate that the NLR gene family appears to be a metazoan innovation, characterized by two major gene lineages that may have originated with the last common eumetazoan ancestor. Subsequent lineage-specific gene duplication, gene loss and domain shuffling all have played an important role in the highly dynamic evolutionary history of invertebrate NLRs.
publisher Oxford University Press
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3879445/
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