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Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus

Identifieur interne : 000076 ( France/Analysis ); précédent : 000075; suivant : 000077

Sex and parasites: genomic and transcriptomic analysis of Microbotryum lychnidis-dioicae, the biotrophic and plant-castrating anther smut fungus

Auteurs : Michael H. Perlin [États-Unis] ; Joelle Amselem [France] ; Eric Fontanillas [France] ; Su San Toh [États-Unis] ; Zehua Chen [États-Unis] ; Jonathan Goldberg [États-Unis] ; Sebastien Duplessis [France] ; Bernard Henrissat [France, Arabie saoudite] ; Sarah Young [États-Unis] ; Qiandong Zeng [États-Unis] ; Gabriela Aguileta [Espagne] ; Elsa Petit [France] ; Helene Badouin [France] ; Jared Andrews [États-Unis] ; Dominique Razeeq [États-Unis] ; Toni Gabald N [Espagne] ; Hadi Quesneville [France] ; Tatiana Giraud [France] ; Michael E. Hood [États-Unis] ; David J. Schultz [États-Unis] ; Christina A. Cuomo [États-Unis]

Source :

RBID : PMC:4469406

Abstract

Background

The genus Microbotryum includes plant pathogenic fungi afflicting a wide variety of hosts with anther smut disease. Microbotryum lychnidis-dioicae infects Silene latifolia and replaces host pollen with fungal spores, exhibiting biotrophy and necrosis associated with altering plant development.

Results

We determined the haploid genome sequence for M. lychnidis-dioicae and analyzed whole transcriptome data from plant infections and other stages of the fungal lifecycle, revealing the inventory and expression level of genes that facilitate pathogenic growth. Compared to related fungi, an expanded number of major facilitator superfamily transporters and secretory lipases were detected; lipase gene expression was found to be altered by exposure to lipid compounds, which signaled a switch to dikaryotic, pathogenic growth. In addition, while enzymes to digest cellulose, xylan, xyloglucan, and highly substituted forms of pectin were absent, along with depletion of peroxidases and superoxide dismutases that protect the fungus from oxidative stress, the repertoire of glycosyltransferases and of enzymes that could manipulate host development has expanded. A total of 14 % of the genome was categorized as repetitive sequences. Transposable elements have accumulated in mating-type chromosomal regions and were also associated across the genome with gene clusters of small secreted proteins, which may mediate host interactions.

Conclusions

The unique absence of enzyme classes for plant cell wall degradation and maintenance of enzymes that break down components of pollen tubes and flowers provides a striking example of biotrophic host adaptation.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1660-8) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12864-015-1660-8
PubMed: 26076695
PubMed Central: 4469406


Affiliations:


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PMC:4469406

Le document en format XML

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the biotrophic and plant-castrating anther smut fungus</title>
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<name sortKey="Perlin, Michael H" sort="Perlin, Michael H" uniqKey="Perlin M" first="Michael H" last="Perlin">Michael H. Perlin</name>
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<wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Biologie et gestion des risques en agriculture (BIOGER), Thiverval-Grignon</wicri:regionArea>
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<wicri:noRegion>Thiverval-Grignon</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Fontanillas, Eric" sort="Fontanillas, Eric" uniqKey="Fontanillas E" first="Eric" last="Fontanillas">Eric Fontanillas</name>
<affiliation wicri:level="4">
<nlm:aff id="Aff4">Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
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<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
<orgName type="university">Université Paris-Sud</orgName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff5">CNRS, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Toh, Su San" sort="Toh, Su San" uniqKey="Toh S" first="Su San" last="Toh">Su San Toh</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff1">Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, KY 40292 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kentucky</region>
</placeName>
<wicri:cityArea>Department of Biology, Program on Disease Evolution, University of Louisville, Louisville</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Chen, Zehua" sort="Chen, Zehua" uniqKey="Chen Z" first="Zehua" last="Chen">Zehua Chen</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff6">Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Goldberg, Jonathan" sort="Goldberg, Jonathan" uniqKey="Goldberg J" first="Jonathan" last="Goldberg">Jonathan Goldberg</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff6">Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sebastien" last="Duplessis">Sebastien Duplessis</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff7">INRA, UMR 1136, Interactions Arbres-Microorganismes, Champenoux, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INRA, UMR 1136, Interactions Arbres-Microorganismes, Champenoux</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Grand Est</region>
<region type="old region" nuts="2">Lorraine (région)</region>
<settlement type="city">Champenoux</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="Aff8">UMR 1136, Université de Lorraine, Interactions Arbres-Microorganismes, Vandoeuvre-lès-Nancy, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>UMR 1136, Université de Lorraine, Interactions Arbres-Microorganismes, Vandoeuvre-lès-Nancy</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Grand Est</region>
<region type="old region" nuts="2">Lorraine (région)</region>
<settlement type="city">Vandœuvre-lès-Nancy</settlement>
<settlement type="city" wicri:auto="agglo">Nancy</settlement>
</placeName>
<orgName type="university">Université de Lorraine</orgName>
</affiliation>
</author>
<author>
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff9">Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, 13288 Marseille, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, 13288 Marseille</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Marseille</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="Aff10">Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia</nlm:aff>
<country xml:lang="fr">Arabie saoudite</country>
<wicri:regionArea>Department of Biological Sciences, King Abdulaziz University, Jeddah</wicri:regionArea>
<wicri:noRegion>Jeddah</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Young, Sarah" sort="Young, Sarah" uniqKey="Young S" first="Sarah" last="Young">Sarah Young</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff6">Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Zeng, Qiandong" sort="Zeng, Qiandong" uniqKey="Zeng Q" first="Qiandong" last="Zeng">Qiandong Zeng</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff6">Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Aguileta, Gabriela" sort="Aguileta, Gabriela" uniqKey="Aguileta G" first="Gabriela" last="Aguileta">Gabriela Aguileta</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff11">Centre for Genomic Regulation (CRG), Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>Centre for Genomic Regulation (CRG), Barcelona</wicri:regionArea>
<placeName>
<settlement type="city">Barcelone</settlement>
<region nuts="2" type="region">Catalogne</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Petit, Elsa" sort="Petit, Elsa" uniqKey="Petit E" first="Elsa" last="Petit">Elsa Petit</name>
<affiliation wicri:level="4">
<nlm:aff id="Aff4">Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
<orgName type="university">Université Paris-Sud</orgName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff5">CNRS, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff9">Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, 13288 Marseille, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, 13288 Marseille</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
<settlement type="city">Marseille</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Badouin, Helene" sort="Badouin, Helene" uniqKey="Badouin H" first="Helene" last="Badouin">Helene Badouin</name>
<affiliation wicri:level="4">
<nlm:aff id="Aff4">Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
<orgName type="university">Université Paris-Sud</orgName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff5">CNRS, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Andrews, Jared" sort="Andrews, Jared" uniqKey="Andrews J" first="Jared" last="Andrews">Jared Andrews</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff1">Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, KY 40292 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kentucky</region>
</placeName>
<wicri:cityArea>Department of Biology, Program on Disease Evolution, University of Louisville, Louisville</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Razeeq, Dominique" sort="Razeeq, Dominique" uniqKey="Razeeq D" first="Dominique" last="Razeeq">Dominique Razeeq</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff1">Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, KY 40292 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kentucky</region>
</placeName>
<wicri:cityArea>Department of Biology, Program on Disease Evolution, University of Louisville, Louisville</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Gabald N, Toni" sort="Gabald N, Toni" uniqKey="Gabald N T" first="Toni" last="Gabald N">Toni Gabald N</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff11">Centre for Genomic Regulation (CRG), Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>Centre for Genomic Regulation (CRG), Barcelona</wicri:regionArea>
<placeName>
<settlement type="city">Barcelone</settlement>
<region nuts="2" type="region">Catalogne</region>
</placeName>
</affiliation>
<affiliation wicri:level="4">
<nlm:aff id="Aff12">Universitat Pompeu Fabra (UPF), Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>Universitat Pompeu Fabra (UPF), Barcelona</wicri:regionArea>
<placeName>
<settlement type="city">Barcelone</settlement>
<region nuts="2" type="region">Catalogne</region>
</placeName>
<orgName type="university">Université Pompeu Fabra</orgName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff13">Institució Catalana d’Estudis Avançats (ICREA), Barcelona, Spain</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea>Institució Catalana d’Estudis Avançats (ICREA), Barcelona</wicri:regionArea>
<placeName>
<settlement type="city">Barcelone</settlement>
<region nuts="2" type="region">Catalogne</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Quesneville, Hadi" sort="Quesneville, Hadi" uniqKey="Quesneville H" first="Hadi" last="Quesneville">Hadi Quesneville</name>
<affiliation wicri:level="3">
<nlm:aff id="Aff2">Institut National de la Recherche Agronomique (INRA), Unité de Recherche Génomique Info (URGI), Versailles, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité de Recherche Génomique Info (URGI), Versailles</wicri:regionArea>
<placeName>
<region type="region">Île-de-France</region>
<region type="old region">Île-de-France</region>
<settlement type="city">Versailles</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Giraud, Tatiana" sort="Giraud, Tatiana" uniqKey="Giraud T" first="Tatiana" last="Giraud">Tatiana Giraud</name>
<affiliation wicri:level="4">
<nlm:aff id="Aff4">Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Ecologie, Systématique et Evolution, Bâtiment 360, Université Paris-Sud, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
<orgName type="university">Université Paris-Sud</orgName>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="Aff5">CNRS, F-91405 Orsay, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>CNRS, F-91405 Orsay</wicri:regionArea>
<placeName>
<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Orsay</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Hood, Michael E" sort="Hood, Michael E" uniqKey="Hood M" first="Michael E." last="Hood">Michael E. Hood</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff14">Department of Biology, Amherst College, Amherst, MA 01002 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Department of Biology, Amherst College, Amherst</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Schultz, David J" sort="Schultz, David J" uniqKey="Schultz D" first="David J." last="Schultz">David J. Schultz</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff1">Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, KY 40292 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kentucky</region>
</placeName>
<wicri:cityArea>Department of Biology, Program on Disease Evolution, University of Louisville, Louisville</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A." last="Cuomo">Christina A. Cuomo</name>
<affiliation wicri:level="2">
<nlm:aff id="Aff6">Broad Institute of MIT and Harvard, Cambridge, MA 02142 USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
</analytic>
<series>
<title level="j">BMC Genomics</title>
<idno type="eISSN">1471-2164</idno>
<imprint>
<date when="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>The genus
<italic>Microbotryum</italic>
includes plant pathogenic fungi afflicting a wide variety of hosts with anther smut disease.
<italic>Microbotryum lychnidis-dioicae</italic>
infects
<italic>Silene latifolia</italic>
and replaces host pollen with fungal spores, exhibiting biotrophy and necrosis associated with altering plant development.</p>
</sec>
<sec>
<title>Results</title>
<p>We determined the haploid genome sequence for
<italic>M. lychnidis-dioicae</italic>
and analyzed whole transcriptome data from plant infections and other stages of the fungal lifecycle, revealing the inventory and expression level of genes that facilitate pathogenic growth. Compared to related fungi, an expanded number of major facilitator superfamily transporters and secretory lipases were detected; lipase gene expression was found to be altered by exposure to lipid compounds, which signaled a switch to dikaryotic, pathogenic growth. In addition, while enzymes to digest cellulose, xylan, xyloglucan, and highly substituted forms of pectin were absent, along with depletion of peroxidases and superoxide dismutases that protect the fungus from oxidative stress, the repertoire of glycosyltransferases and of enzymes that could manipulate host development has expanded. A total of 14 % of the genome was categorized as repetitive sequences. Transposable elements have accumulated in mating-type chromosomal regions and were also associated across the genome with gene clusters of small secreted proteins, which may mediate host interactions.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>The unique absence of enzyme classes for plant cell wall degradation and maintenance of enzymes that break down components of pollen tubes and flowers provides a striking example of biotrophic host adaptation.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12864-015-1660-8) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
<back>
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</author>
<author>
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<name sortKey="Huerta Cepas, J" uniqKey="Huerta Cepas J">J Huerta-Cepas</name>
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</TEI>
<affiliations>
<list>
<country>
<li>Arabie saoudite</li>
<li>Espagne</li>
<li>France</li>
<li>États-Unis</li>
</country>
<region>
<li>Catalogne</li>
<li>Grand Est</li>
<li>Kentucky</li>
<li>Lorraine (région)</li>
<li>Massachusetts</li>
<li>Provence-Alpes-Côte d'Azur</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Barcelone</li>
<li>Champenoux</li>
<li>Marseille</li>
<li>Nancy</li>
<li>Orsay</li>
<li>Vandœuvre-lès-Nancy</li>
<li>Versailles</li>
</settlement>
<orgName>
<li>Université Paris-Sud</li>
<li>Université Pompeu Fabra</li>
<li>Université de Lorraine</li>
</orgName>
</list>
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<country name="États-Unis">
<region name="Kentucky">
<name sortKey="Perlin, Michael H" sort="Perlin, Michael H" uniqKey="Perlin M" first="Michael H" last="Perlin">Michael H. Perlin</name>
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<name sortKey="Andrews, Jared" sort="Andrews, Jared" uniqKey="Andrews J" first="Jared" last="Andrews">Jared Andrews</name>
<name sortKey="Chen, Zehua" sort="Chen, Zehua" uniqKey="Chen Z" first="Zehua" last="Chen">Zehua Chen</name>
<name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A." last="Cuomo">Christina A. Cuomo</name>
<name sortKey="Goldberg, Jonathan" sort="Goldberg, Jonathan" uniqKey="Goldberg J" first="Jonathan" last="Goldberg">Jonathan Goldberg</name>
<name sortKey="Hood, Michael E" sort="Hood, Michael E" uniqKey="Hood M" first="Michael E." last="Hood">Michael E. Hood</name>
<name sortKey="Razeeq, Dominique" sort="Razeeq, Dominique" uniqKey="Razeeq D" first="Dominique" last="Razeeq">Dominique Razeeq</name>
<name sortKey="Schultz, David J" sort="Schultz, David J" uniqKey="Schultz D" first="David J." last="Schultz">David J. Schultz</name>
<name sortKey="Toh, Su San" sort="Toh, Su San" uniqKey="Toh S" first="Su San" last="Toh">Su San Toh</name>
<name sortKey="Young, Sarah" sort="Young, Sarah" uniqKey="Young S" first="Sarah" last="Young">Sarah Young</name>
<name sortKey="Zeng, Qiandong" sort="Zeng, Qiandong" uniqKey="Zeng Q" first="Qiandong" last="Zeng">Qiandong Zeng</name>
</country>
<country name="France">
<region name="Île-de-France">
<name sortKey="Amselem, Joelle" sort="Amselem, Joelle" uniqKey="Amselem J" first="Joelle" last="Amselem">Joelle Amselem</name>
</region>
<name sortKey="Amselem, Joelle" sort="Amselem, Joelle" uniqKey="Amselem J" first="Joelle" last="Amselem">Joelle Amselem</name>
<name sortKey="Badouin, Helene" sort="Badouin, Helene" uniqKey="Badouin H" first="Helene" last="Badouin">Helene Badouin</name>
<name sortKey="Badouin, Helene" sort="Badouin, Helene" uniqKey="Badouin H" first="Helene" last="Badouin">Helene Badouin</name>
<name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sebastien" last="Duplessis">Sebastien Duplessis</name>
<name sortKey="Duplessis, Sebastien" sort="Duplessis, Sebastien" uniqKey="Duplessis S" first="Sebastien" last="Duplessis">Sebastien Duplessis</name>
<name sortKey="Fontanillas, Eric" sort="Fontanillas, Eric" uniqKey="Fontanillas E" first="Eric" last="Fontanillas">Eric Fontanillas</name>
<name sortKey="Fontanillas, Eric" sort="Fontanillas, Eric" uniqKey="Fontanillas E" first="Eric" last="Fontanillas">Eric Fontanillas</name>
<name sortKey="Giraud, Tatiana" sort="Giraud, Tatiana" uniqKey="Giraud T" first="Tatiana" last="Giraud">Tatiana Giraud</name>
<name sortKey="Giraud, Tatiana" sort="Giraud, Tatiana" uniqKey="Giraud T" first="Tatiana" last="Giraud">Tatiana Giraud</name>
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
<name sortKey="Petit, Elsa" sort="Petit, Elsa" uniqKey="Petit E" first="Elsa" last="Petit">Elsa Petit</name>
<name sortKey="Petit, Elsa" sort="Petit, Elsa" uniqKey="Petit E" first="Elsa" last="Petit">Elsa Petit</name>
<name sortKey="Petit, Elsa" sort="Petit, Elsa" uniqKey="Petit E" first="Elsa" last="Petit">Elsa Petit</name>
<name sortKey="Quesneville, Hadi" sort="Quesneville, Hadi" uniqKey="Quesneville H" first="Hadi" last="Quesneville">Hadi Quesneville</name>
</country>
<country name="Arabie saoudite">
<noRegion>
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
</noRegion>
</country>
<country name="Espagne">
<region name="Catalogne">
<name sortKey="Aguileta, Gabriela" sort="Aguileta, Gabriela" uniqKey="Aguileta G" first="Gabriela" last="Aguileta">Gabriela Aguileta</name>
</region>
<name sortKey="Gabald N, Toni" sort="Gabald N, Toni" uniqKey="Gabald N T" first="Toni" last="Gabald N">Toni Gabald N</name>
<name sortKey="Gabald N, Toni" sort="Gabald N, Toni" uniqKey="Gabald N T" first="Toni" last="Gabald N">Toni Gabald N</name>
<name sortKey="Gabald N, Toni" sort="Gabald N, Toni" uniqKey="Gabald N T" first="Toni" last="Gabald N">Toni Gabald N</name>
</country>
</tree>
</affiliations>
</record>

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