RNA-sequence analysis of gene expression from honeybees (Apis mellifera) infected with Nosema ceranae
Identifieur interne : 000125 ( Pmc/Checkpoint ); précédent : 000124; suivant : 000126RNA-sequence analysis of gene expression from honeybees (Apis mellifera) infected with Nosema ceranae
Auteurs : Bouabid Badaoui [Italie] ; André Fougeroux [France] ; Fabien Petit [France] ; Anna Anselmo [Italie] ; Chiara Gorni [Italie] ; Marco Cucurachi [Italie] ; Antonella Cersini [Italie] ; Anna Granato [Italie] ; Giusy Cardeti [Italie] ; Giovanni Formato [Italie] ; Franco Mutinelli [Italie] ; Elisabetta Giuffra [Italie] ; John L. Williams [Australie] ; Sara Botti [Italie]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
Honeybees (
Url:
DOI: 10.1371/journal.pone.0173438
PubMed: 28350872
PubMed Central: 5370102
Affiliations:
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Williams</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Davies Research Centre, University of Adelaide, Roseworthy, South Australia, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Davies Research Centre, University of Adelaide, Roseworthy, South Australia</wicri:regionArea><wicri:noRegion>South Australia</wicri:noRegion></affiliation></author><author><name sortKey="Botti, Sara" sort="Botti, Sara" uniqKey="Botti S" first="Sara" last="Botti">Sara Botti</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28350872</idno><idno type="pmc">5370102</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5370102</idno><idno type="RBID">PMC:5370102</idno><idno type="doi">10.1371/journal.pone.0173438</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">002971</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002971</idno><idno type="wicri:Area/Pmc/Curation">002821</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002821</idno><idno type="wicri:Area/Pmc/Checkpoint">000125</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000125</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">RNA-sequence analysis of gene expression from honeybees (<italic>Apis mellifera</italic>) infected with <italic>Nosema ceranae</italic></title><author><name sortKey="Badaoui, Bouabid" sort="Badaoui, Bouabid" uniqKey="Badaoui B" first="Bouabid" last="Badaoui">Bouabid Badaoui</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author><author><name sortKey="Fougeroux, Andre" sort="Fougeroux, Andre" uniqKey="Fougeroux A" first="André" last="Fougeroux">André Fougeroux</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Syngenta, Guyancourt, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Syngenta, Guyancourt</wicri:regionArea><wicri:noRegion>Guyancourt</wicri:noRegion><wicri:noRegion>Guyancourt</wicri:noRegion></affiliation></author><author><name sortKey="Petit, Fabien" sort="Petit, Fabien" uniqKey="Petit F" first="Fabien" last="Petit">Fabien Petit</name><affiliation wicri:level="3"><nlm:aff id="aff003"><addr-line>RNAGRO, TOURS, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>RNAGRO, TOURS</wicri:regionArea><placeName><region type="region">Centre-Val de Loire</region><region type="old region">Région Centre</region><settlement type="city">Tours</settlement></placeName></affiliation></author><author><name sortKey="Anselmo, Anna" sort="Anselmo, Anna" uniqKey="Anselmo A" first="Anna" last="Anselmo">Anna Anselmo</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author><author><name sortKey="Gorni, Chiara" sort="Gorni, Chiara" uniqKey="Gorni C" first="Chiara" last="Gorni">Chiara Gorni</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author><author><name sortKey="Cucurachi, Marco" sort="Cucurachi, Marco" uniqKey="Cucurachi M" first="Marco" last="Cucurachi">Marco Cucurachi</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author><author><name sortKey="Cersini, Antonella" sort="Cersini, Antonella" uniqKey="Cersini A" first="Antonella" last="Cersini">Antonella Cersini</name><affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Granato, Anna" sort="Granato, Anna" uniqKey="Granato A" first="Anna" last="Granato">Anna Granato</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua</wicri:regionArea><wicri:noRegion>Padua</wicri:noRegion></affiliation></author><author><name sortKey="Cardeti, Giusy" sort="Cardeti, Giusy" uniqKey="Cardeti G" first="Giusy" last="Cardeti">Giusy Cardeti</name><affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Formato, Giovanni" sort="Formato, Giovanni" uniqKey="Formato G" first="Giovanni" last="Formato">Giovanni Formato</name><affiliation wicri:level="3"><nlm:aff id="aff004"><addr-line>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Mutinelli, Franco" sort="Mutinelli, Franco" uniqKey="Mutinelli F" first="Franco" last="Mutinelli">Franco Mutinelli</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua</wicri:regionArea><wicri:noRegion>Padua</wicri:noRegion></affiliation></author><author><name sortKey="Giuffra, Elisabetta" sort="Giuffra, Elisabetta" uniqKey="Giuffra E" first="Elisabetta" last="Giuffra">Elisabetta Giuffra</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author><author><name sortKey="Williams, John L" sort="Williams, John L" uniqKey="Williams J" first="John L." last="Williams">John L. Williams</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Davies Research Centre, University of Adelaide, Roseworthy, South Australia, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Davies Research Centre, University of Adelaide, Roseworthy, South Australia</wicri:regionArea><wicri:noRegion>South Australia</wicri:noRegion></affiliation></author><author><name sortKey="Botti, Sara" sort="Botti, Sara" uniqKey="Botti S" first="Sara" last="Botti">Sara Botti</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi</wicri:regionArea><wicri:noRegion>Lodi</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Honeybees (<italic>Apis mellifera</italic>) are constantly subjected to many biotic stressors including parasites. This study examined honeybees infected with <italic>Nosema ceranae</italic> (<italic>N</italic>. <italic>ceranae</italic>). <italic>N</italic>. <italic>ceranae</italic> infection increases the bees energy requirements and may contribute to their decreased survival. RNA-seq was used to investigate gene expression at days 5, 10 and 15 Post Infection (P.I) with <italic>N</italic>. <italic>ceranae</italic>. The expression levels of genes, isoforms, alternative transcription start sites (TSS) and differential promoter usage revealed a complex pattern of transcriptional and post-transcriptional gene regulation suggesting that bees use a range of tactics to cope with the stress of <italic>N</italic>. <italic>ceranae</italic> infection. <italic>N</italic>. <italic>ceranae</italic> infection may cause reduced immune function in the bees by: (i)disturbing the host amino acids metabolism (ii) down-regulating expression of antimicrobial peptides (iii) down-regulation of cuticle coatings and (iv) down-regulation of odorant binding proteins.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Higes, M" uniqKey="Higes M">M Higes</name></author><author><name sortKey="Meana, A" uniqKey="Meana A">A Meana</name></author><author><name sortKey="Bartolome, C" uniqKey="Bartolome C">C Bartolome</name></author><author><name sortKey="Botias, C" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28350872</article-id><article-id pub-id-type="pmc">5370102</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0173438</article-id><article-id pub-id-type="publisher-id">PONE-D-15-32809</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Invertebrates</subject><subj-group><subject>Arthropoda</subject><subj-group><subject>Insects</subject><subj-group><subject>Hymenoptera</subject><subj-group><subject>Bees</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Gene Expression</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Gene Expression</subject><subj-group><subject>Gene Regulation</subject><subj-group><subject>Post-Transcriptional Gene Regulation</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Invertebrates</subject><subj-group><subject>Arthropoda</subject><subj-group><subject>Insects</subject><subj-group><subject>Hymenoptera</subject><subj-group><subject>Bees</subject><subj-group><subject>Honey Bees</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Gene expression</subject><subj-group><subject>DNA transcription</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Genetics</subject><subj-group><subject>Gene Expression</subject><subj-group><subject>Gene Regulation</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Parasitic Diseases</subject></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>RNA-sequence analysis of gene expression from honeybees (<italic>Apis mellifera</italic>) infected with <italic>Nosema ceranae</italic></article-title><alt-title alt-title-type="running-head">Gene expression from honeybees infected with <italic>Nosema ceranae</italic></alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-6808-1765</contrib-id><name><surname>Badaoui</surname><given-names>Bouabid</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="author-notes" rid="currentaff001"><sup>¤a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Fougeroux</surname><given-names>André</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Petit</surname><given-names>Fabien</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Anselmo</surname><given-names>Anna</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gorni</surname><given-names>Chiara</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cucurachi</surname><given-names>Marco</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cersini</surname><given-names>Antonella</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Granato</surname><given-names>Anna</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cardeti</surname><given-names>Giusy</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Formato</surname><given-names>Giovanni</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mutinelli</surname><given-names>Franco</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Giuffra</surname><given-names>Elisabetta</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="author-notes" rid="currentaff002"><sup>¤b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Williams</surname><given-names>John L.</given-names></name><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Botti</surname><given-names>Sara</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Parco Tecnologico Padano - CERSA, Integrative Biology Group, Lodi, Italy</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Syngenta, Guyancourt, France</addr-line></aff><aff id="aff003"><label>3</label><addr-line>RNAGRO, TOURS, France</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Istituto Zooprofilattico Sperimentale del Lazio e della Toscana, Roma, Italy</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro, Padua, Italy</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Davies Research Centre, University of Adelaide, Roseworthy, South Australia, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Rueppell</surname><given-names>Olav</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of North Carolina at Greensboro, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>Andrea Fougeroux was employed by Syngenta during the course of the study. Fabien Petit acted as a contractor to Syngenta during the course of the study. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> BB SB EG.</p></list-item><list-item><p><bold>Data curation:</bold> BB AA MC.</p></list-item><list-item><p><bold>Formal analysis:</bold> BB SB AF FP CG AC AG GC GF FM.</p></list-item><list-item><p><bold>Funding acquisition:</bold> EG SB.</p></list-item><list-item><p><bold>Investigation:</bold> BB SB AF FP CG AC AG GC GF FM.</p></list-item><list-item><p><bold>Methodology:</bold> BB SB AF FP CG AC AG GC GF FM EG.</p></list-item><list-item><p><bold>Project administration:</bold> EG SB BB.</p></list-item><list-item><p><bold>Resources:</bold> SB AF FP CG AC AG GC GF FM.</p></list-item><list-item><p><bold>Software:</bold> BB AA MC.</p></list-item><list-item><p><bold>Supervision:</bold> SB.</p></list-item><list-item><p><bold>Validation:</bold> BB SB AF FP CG AC AG GC GF FM.</p></list-item><list-item><p><bold>Visualization:</bold> BB JLW.</p></list-item><list-item><p><bold>Writing – original draft:</bold> BB SB.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> BB JLW.</p></list-item></list></p></fn><fn fn-type="current-aff" id="currentaff001"><label>¤a</label><p>Current address: Mohamed V University in Rabat, Science Faculty, Rabat, Morocco</p></fn><fn fn-type="current-aff" id="currentaff002"><label>¤b</label><p>Current address: INRA - laboratory of Animal Genetics and Integrative Biology Team Genetics, Domaine de Vilvert, Jouy-en-Josas, France</p></fn><corresp id="cor001">* E-mail: <email>sara.botti@ptp.it</email></corresp></author-notes><pub-date pub-type="epub"><day>28</day><month>3</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>3</issue><elocation-id>e0173438</elocation-id><history><date date-type="received"><day>2</day><month>9</month><year>2015</year></date><date date-type="accepted"><day>22</day><month>2</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Badaoui et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Badaoui et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0173438.pdf"></self-uri><abstract><p>Honeybees (<italic>Apis mellifera</italic>) are constantly subjected to many biotic stressors including parasites. This study examined honeybees infected with <italic>Nosema ceranae</italic> (<italic>N</italic>. <italic>ceranae</italic>). <italic>N</italic>. <italic>ceranae</italic> infection increases the bees energy requirements and may contribute to their decreased survival. RNA-seq was used to investigate gene expression at days 5, 10 and 15 Post Infection (P.I) with <italic>N</italic>. <italic>ceranae</italic>. The expression levels of genes, isoforms, alternative transcription start sites (TSS) and differential promoter usage revealed a complex pattern of transcriptional and post-transcriptional gene regulation suggesting that bees use a range of tactics to cope with the stress of <italic>N</italic>. <italic>ceranae</italic> infection. <italic>N</italic>. <italic>ceranae</italic> infection may cause reduced immune function in the bees by: (i)disturbing the host amino acids metabolism (ii) down-regulating expression of antimicrobial peptides (iii) down-regulation of cuticle coatings and (iv) down-regulation of odorant binding proteins.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>Eureka-Eurostars Project Application</institution></funding-source><award-id>E!5069 NewBone</award-id></award-group><funding-statement>Funded by Eureka-Eurostars Project Application E!5069 NewBone. Andrea Fougeroux was employed by Syngenta during the course of the study. Syngenta provided support in the form of salary for author AF, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific role of this author is articulated in the ‘author contributions’ section.</funding-statement></funding-group><counts><fig-count count="3"></fig-count><table-count count="0"></table-count><page-count count="17"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>The data may be found at the SRA database at the following URL: <ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/bioproject/PRJNA378655/">https://www.ncbi.nlm.nih.gov/bioproject/PRJNA378655/</ext-link> and accession number PRJNA378655.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>The data may be found at the SRA database at the following URL: <ext-link ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/bioproject/PRJNA378655/">https://www.ncbi.nlm.nih.gov/bioproject/PRJNA378655/</ext-link> and accession number PRJNA378655.</p></notes></front></pmc><affiliations><list><country><li>Australie</li><li>France</li><li>Italie</li></country><region><li>Centre-Val de Loire</li><li>Latium</li><li>Région Centre</li></region><settlement><li>Rome</li><li>Tours</li></settlement></list><tree><country name="Italie"><noRegion><name sortKey="Badaoui, Bouabid" sort="Badaoui, Bouabid" uniqKey="Badaoui B" first="Bouabid" last="Badaoui">Bouabid Badaoui</name></noRegion><name sortKey="Anselmo, Anna" sort="Anselmo, Anna" uniqKey="Anselmo A" first="Anna" last="Anselmo">Anna Anselmo</name><name sortKey="Botti, Sara" sort="Botti, Sara" uniqKey="Botti S" first="Sara" last="Botti">Sara Botti</name><name sortKey="Cardeti, Giusy" sort="Cardeti, Giusy" uniqKey="Cardeti G" first="Giusy" last="Cardeti">Giusy Cardeti</name><name sortKey="Cersini, Antonella" sort="Cersini, Antonella" uniqKey="Cersini A" first="Antonella" last="Cersini">Antonella Cersini</name><name sortKey="Cucurachi, Marco" sort="Cucurachi, Marco" uniqKey="Cucurachi M" first="Marco" last="Cucurachi">Marco Cucurachi</name><name sortKey="Formato, Giovanni" sort="Formato, Giovanni" uniqKey="Formato G" first="Giovanni" last="Formato">Giovanni Formato</name><name sortKey="Giuffra, Elisabetta" sort="Giuffra, Elisabetta" uniqKey="Giuffra E" first="Elisabetta" last="Giuffra">Elisabetta Giuffra</name><name sortKey="Gorni, Chiara" sort="Gorni, Chiara" uniqKey="Gorni C" first="Chiara" last="Gorni">Chiara Gorni</name><name sortKey="Granato, Anna" sort="Granato, Anna" uniqKey="Granato A" first="Anna" last="Granato">Anna Granato</name><name sortKey="Mutinelli, Franco" sort="Mutinelli, Franco" uniqKey="Mutinelli F" first="Franco" last="Mutinelli">Franco Mutinelli</name></country><country name="France"><noRegion><name sortKey="Fougeroux, Andre" sort="Fougeroux, Andre" uniqKey="Fougeroux A" first="André" last="Fougeroux">André Fougeroux</name></noRegion><name sortKey="Petit, Fabien" sort="Petit, Fabien" uniqKey="Petit F" first="Fabien" last="Petit">Fabien Petit</name></country><country name="Australie"><noRegion><name sortKey="Williams, John L" sort="Williams, John L" uniqKey="Williams J" first="John L." last="Williams">John L. 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