Diversity and Variability of NOD-Like Receptors in Fungi
Identifieur interne : 001638 ( Pmc/Checkpoint ); précédent : 001637; suivant : 001639Diversity and Variability of NOD-Like Receptors in Fungi
Auteurs : Witold Dyrka [France] ; Marina Lamacchia [France] ; Pascal Durrens [France] ; Bostjan Kobe [Australie] ; Asen Daskalov [France] ; Matthieu Paoletti [France] ; David J. Sherman [France] ; Sven J. Saupe [France]Source :
- Genome Biology and Evolution [ 1759-6653 ] ; 2014.
Abstract
Nucleotide-binding oligomerization domain (NOD)-like receptors (NLRs) are intracellular receptors that control innate immunity and other biotic interactions in animals and plants. NLRs have been characterized in plant and animal lineages, but in fungi, this gene family has not been systematically described. There is however previous indications of the involvement of NLR-like genes in nonself recognition and programmed cell death in fungi. We have analyzed 198 fungal genomes for the presence of NLRs and have annotated a total of 5,616 NLR candidates. We describe their phylogenetic distribution, domain organization, and evolution. Fungal NLRs are characterized by a great diversity of domain organizations, suggesting frequently occurring combinatorial assortments of different effector, NOD and repeat domains. The repeat domains are of the WD, ANK, and TPR type; no LRR motifs were found. As previously documented for WD-repeat domains of fungal NLRs, TPR, and ANK repeats evolve under positive selection and show highly conserved repeats and repeat length polymorphism, suggesting the possibility of concerted evolution of these repeats. We identify novel effector domains not previously found associated with NLRs, whereas others are related to effector domains of plant or animals NLRs. In particular, we show that the HET domain found in fungal NLRs may be related to Toll/interleukin-1 receptor domains found in animal and plant immune receptors. This description of fungal NLR repertoires reveals both similarities and differences with plant and animals NLR collections, highlights the importance of domain reassortment and repeat evolution and provides a novel entry point to explore the evolution of NLRs in eukaryotes.
Url:
DOI: 10.1093/gbe/evu251
PubMed: 25398782
PubMed Central: 4986451
Affiliations:
- Australie, France
- Aquitaine, Aquitaine-Limousin-Poitou-Charentes, Nouvelle-Aquitaine
- Bordeaux, Talence
- Université de Bordeaux
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<front><div type="abstract" xml:lang="en"><p>Nucleotide-binding oligomerization domain (NOD)-like receptors (NLRs) are intracellular receptors that control innate immunity and other biotic interactions in animals and plants. NLRs have been characterized in plant and animal lineages, but in fungi, this gene family has not been systematically described. There is however previous indications of the involvement of NLR-like genes in nonself recognition and programmed cell death in fungi. We have analyzed 198 fungal genomes for the presence of NLRs and have annotated a total of 5,616 NLR candidates. We describe their phylogenetic distribution, domain organization, and evolution. Fungal NLRs are characterized by a great diversity of domain organizations, suggesting frequently occurring combinatorial assortments of different effector, NOD and repeat domains. The repeat domains are of the WD, ANK, and TPR type; no LRR motifs were found. As previously documented for WD-repeat domains of fungal NLRs, TPR, and ANK repeats evolve under positive selection and show highly conserved repeats and repeat length polymorphism, suggesting the possibility of concerted evolution of these repeats. We identify novel effector domains not previously found associated with NLRs, whereas others are related to effector domains of plant or animals NLRs. In particular, we show that the HET domain found in fungal NLRs may be related to Toll/interleukin-1 receptor domains found in animal and plant immune receptors. This description of fungal NLR repertoires reveals both similarities and differences with plant and animals NLR collections, highlights the importance of domain reassortment and repeat evolution and provides a novel entry point to explore the evolution of NLRs in eukaryotes.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Genome Biol Evol</journal-id>
<journal-id journal-id-type="iso-abbrev">Genome Biol Evol</journal-id>
<journal-id journal-id-type="publisher-id">gbe</journal-id>
<journal-id journal-id-type="hwp">gbe</journal-id>
<journal-title-group><journal-title>Genome Biology and Evolution</journal-title>
</journal-title-group>
<issn pub-type="epub">1759-6653</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25398782</article-id>
<article-id pub-id-type="pmc">4986451</article-id>
<article-id pub-id-type="doi">10.1093/gbe/evu251</article-id>
<article-id pub-id-type="publisher-id">evu251</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Diversity and Variability of NOD-Like Receptors in Fungi</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Dyrka</surname>
<given-names>Witold</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lamacchia</surname>
<given-names>Marina</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Durrens</surname>
<given-names>Pascal</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kobe</surname>
<given-names>Bostjan</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Daskalov</surname>
<given-names>Asen</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Paoletti</surname>
<given-names>Matthieu</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sherman</surname>
<given-names>David J.</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Saupe</surname>
<given-names>Sven J.</given-names>
</name>
<xref ref-type="aff" rid="evu251-AFF2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="evu251-COR1">*</xref>
</contrib>
</contrib-group>
<aff id="evu251-AFF1"><sup>1</sup>
INRIA-Université Bordeaux-CNRS, MAGNOME, Talence, France</aff>
<aff id="evu251-AFF2"><sup>2</sup>
Institut de Biochimie et de Génétique Cellulaire, UMR 5095, CNRS-Université de Bordeaux, France</aff>
<aff id="evu251-AFF3"><sup>3</sup>
School of Chemistry and Molecular Biosciences, Institute for Molecular Bioscience and Centre for Infectious Disease Research, University of Queensland, Brisbane, Queensland, Australia</aff>
<author-notes><corresp id="evu251-COR1">*Corresponding author: E-mail: <email>sven.saupe@ibgc.cnrs.fr</email>
.</corresp>
<fn><p><bold>Associate editor</bold>
: Kenneth Wolfe</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>12</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>08</day>
<month>12</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>08</day>
<month>12</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>6</volume>
<issue>12</issue>
<fpage>3137</fpage>
<lpage>3158</lpage>
<history><date date-type="accepted"><day>6</day>
<month>11</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</copyright-statement>
<copyright-year>2014</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/" license-type="creative-commons"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Nucleotide-binding oligomerization domain (NOD)-like receptors (NLRs) are intracellular receptors that control innate immunity and other biotic interactions in animals and plants. NLRs have been characterized in plant and animal lineages, but in fungi, this gene family has not been systematically described. There is however previous indications of the involvement of NLR-like genes in nonself recognition and programmed cell death in fungi. We have analyzed 198 fungal genomes for the presence of NLRs and have annotated a total of 5,616 NLR candidates. We describe their phylogenetic distribution, domain organization, and evolution. Fungal NLRs are characterized by a great diversity of domain organizations, suggesting frequently occurring combinatorial assortments of different effector, NOD and repeat domains. The repeat domains are of the WD, ANK, and TPR type; no LRR motifs were found. As previously documented for WD-repeat domains of fungal NLRs, TPR, and ANK repeats evolve under positive selection and show highly conserved repeats and repeat length polymorphism, suggesting the possibility of concerted evolution of these repeats. We identify novel effector domains not previously found associated with NLRs, whereas others are related to effector domains of plant or animals NLRs. In particular, we show that the HET domain found in fungal NLRs may be related to Toll/interleukin-1 receptor domains found in animal and plant immune receptors. This description of fungal NLR repertoires reveals both similarities and differences with plant and animals NLR collections, highlights the importance of domain reassortment and repeat evolution and provides a novel entry point to explore the evolution of NLRs in eukaryotes.</p>
</abstract>
<kwd-group><kwd>NLR</kwd>
<kwd>fungi</kwd>
<kwd>NACHT</kwd>
<kwd>immunity</kwd>
</kwd-group>
<counts><page-count count="22"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>France</li>
</country>
<region><li>Aquitaine</li>
<li>Aquitaine-Limousin-Poitou-Charentes</li>
<li>Nouvelle-Aquitaine</li>
</region>
<settlement><li>Bordeaux</li>
<li>Talence</li>
</settlement>
<orgName><li>Université de Bordeaux</li>
</orgName>
</list>
<tree><country name="France"><region name="Aquitaine-Limousin-Poitou-Charentes"><name sortKey="Dyrka, Witold" sort="Dyrka, Witold" uniqKey="Dyrka W" first="Witold" last="Dyrka">Witold Dyrka</name>
</region>
<name sortKey="Daskalov, Asen" sort="Daskalov, Asen" uniqKey="Daskalov A" first="Asen" last="Daskalov">Asen Daskalov</name>
<name sortKey="Durrens, Pascal" sort="Durrens, Pascal" uniqKey="Durrens P" first="Pascal" last="Durrens">Pascal Durrens</name>
<name sortKey="Lamacchia, Marina" sort="Lamacchia, Marina" uniqKey="Lamacchia M" first="Marina" last="Lamacchia">Marina Lamacchia</name>
<name sortKey="Paoletti, Matthieu" sort="Paoletti, Matthieu" uniqKey="Paoletti M" first="Matthieu" last="Paoletti">Matthieu Paoletti</name>
<name sortKey="Saupe, Sven J" sort="Saupe, Sven J" uniqKey="Saupe S" first="Sven J." last="Saupe">Sven J. Saupe</name>
<name sortKey="Sherman, David J" sort="Sherman, David J" uniqKey="Sherman D" first="David J." last="Sherman">David J. Sherman</name>
</country>
<country name="Australie"><noRegion><name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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