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Pollen reverses decreased lifespan, altered nutritional metabolism and suppressed immunity in honey bees (Apis mellifera) treated with antibiotics.

Identifieur interne : 000259 ( Main/Exploration ); précédent : 000258; suivant : 000260

Pollen reverses decreased lifespan, altered nutritional metabolism and suppressed immunity in honey bees (Apis mellifera) treated with antibiotics.

Auteurs : Jianghong Li [États-Unis, République populaire de Chine] ; Matthew C. Heerman [États-Unis] ; Jay D. Evans [États-Unis] ; Robyn Rose [États-Unis] ; Wenfeng Li [États-Unis] ; Cristina Rodríguez-García [États-Unis] ; Gloria Degrandi-Hoffman [États-Unis] ; Yazhou Zhao [États-Unis, République populaire de Chine] ; Shaokang Huang [République populaire de Chine] ; Zhiguo Li [République populaire de Chine] ; Michele Hamilton [États-Unis] ; Yanping Chen

Source :

RBID : pubmed:30846535

Descripteurs français

English descriptors

Abstract

Nutrition is involved in regulating multiple aspects of honey bee biology such as caste, immunity, lifespan, growth and behavioral development. Deformed wing virus (DWV) is a major pathogenic factor which threatens honey bee populations, and its replication is regulated by the nutrition status and immune response of honey bees. The alimentary canal of the honey bee is home to a diverse microbial community that provides essential nutrients and serves to bolster immune responses. However, to what extent gut bacteria affect honey bee nutrition metabolism and immunity with respect to DWV has not been investigated fully. In this study, newly emerged worker bees were subjected to four diets that contained (1) pollen, (2) pollen and antibiotics, (3) neither pollen nor antibiotics or (4) antibiotics alone. The expression level of two nutrition genes target of rapamycin (tor) and insulin like peptide (ilp1), one nutritional marker gene vitellogenin (vg), five major royal jellyprotein genes (mrjp1-5), one antimicrobial peptide regulating gene relish (rel), and DWV virus titer and its replication intermediate, negative RNA strand, were determined by qRT-PCR from the honey bees at 7 days post-antibiotic treatment. Additionally, honey bee head mass and survival rate were measured. We observed that antibiotics decreased the expression of tor and rel, and increased DWV titer and its replication activity. Expression of ilp1, mrjp1-5 and vg, and honey bee head mass were also reduced compared with bees on a pollen diet. Antibiotics also caused a significant drop in survivorship, which could be rescued by addition of pollen to the diet. Of importance, pollen could partially rescue the loss of vg and mrjp2 while also increasing the head mass of antibiotic-treated bees. Our results illuminate the roles of bacteria in honey bee nutrition, metabolism and immunity, which confer the ability to inhibit virus replication, extend honey bee lifespan and improve overall health.

DOI: 10.1242/jeb.202077
PubMed: 30846535


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<name sortKey="Rodriguez Garcia, Cristina" sort="Rodriguez Garcia, Cristina" uniqKey="Rodriguez Garcia C" first="Cristina" last="Rodríguez-García">Cristina Rodríguez-García</name>
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<name sortKey="Degrandi Hoffman, Gloria" sort="Degrandi Hoffman, Gloria" uniqKey="Degrandi Hoffman G" first="Gloria" last="Degrandi-Hoffman">Gloria Degrandi-Hoffman</name>
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<name sortKey="Zhao, Yazhou" sort="Zhao, Yazhou" uniqKey="Zhao Y" first="Yazhou" last="Zhao">Yazhou Zhao</name>
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<country xml:lang="fr">République populaire de Chine</country>
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<settlement type="city">Pékin</settlement>
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<term>Animal Nutritional Physiological Phenomena (MeSH)</term>
<term>Animals (MeSH)</term>
<term>Anti-Bacterial Agents (administration & dosage)</term>
<term>Bacteria (classification)</term>
<term>Bacteria (drug effects)</term>
<term>Bacteria (isolation & purification)</term>
<term>Bees (immunology)</term>
<term>Bees (microbiology)</term>
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<term>Female (MeSH)</term>
<term>Gastrointestinal Microbiome (drug effects)</term>
<term>Gene Expression (MeSH)</term>
<term>Head (anatomy & histology)</term>
<term>Penicillins (administration & dosage)</term>
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<term>RNA Viruses (growth & development)</term>
<term>Streptomycin (administration & dosage)</term>
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<term>Abeilles (immunologie)</term>
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<term>Antibactériens (administration et posologie)</term>
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<term>Bactéries (isolement et purification)</term>
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<term>Microbiome gastro-intestinal (effets des médicaments et des substances chimiques)</term>
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<term>Bacteria</term>
<term>Gastrointestinal Microbiome</term>
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<keywords scheme="MESH" qualifier="effets des médicaments et des substances chimiques" xml:lang="fr">
<term>Bactéries</term>
<term>Microbiome gastro-intestinal</term>
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<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>RNA Viruses</term>
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<term>Abeilles</term>
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<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Bees</term>
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<keywords scheme="MESH" qualifier="isolation & purification" xml:lang="en">
<term>Bacteria</term>
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<term>Bactéries</term>
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<term>Abeilles</term>
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<term>Bees</term>
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<term>Animal Nutritional Physiological Phenomena</term>
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<term>Diet</term>
<term>Female</term>
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<term>Pollen</term>
</keywords>
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<term>Animaux</term>
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<term>Expression des gènes</term>
<term>Femelle</term>
<term>Phénomènes physiologiques nutritionnels chez l'animal</term>
<term>Pollen</term>
<term>Régime alimentaire</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Nutrition is involved in regulating multiple aspects of honey bee biology such as caste, immunity, lifespan, growth and behavioral development. Deformed wing virus (DWV) is a major pathogenic factor which threatens honey bee populations, and its replication is regulated by the nutrition status and immune response of honey bees. The alimentary canal of the honey bee is home to a diverse microbial community that provides essential nutrients and serves to bolster immune responses. However, to what extent gut bacteria affect honey bee nutrition metabolism and immunity with respect to DWV has not been investigated fully. In this study, newly emerged worker bees were subjected to four diets that contained (1) pollen, (2) pollen and antibiotics, (3) neither pollen nor antibiotics or (4) antibiotics alone. The expression level of two nutrition genes
<i>target of rapamycin</i>
(
<i>tor</i>
) and
<i>insulin like peptide</i>
(
<i>ilp1</i>
), one nutritional marker gene
<i>vitellogenin</i>
(
<i>vg</i>
), five
<i>major royal jelly</i>
<i>protein</i>
genes (
<i>mrjp1</i>
-
<i>5</i>
), one antimicrobial peptide regulating gene
<i>relish</i>
(
<i>rel</i>
), and DWV virus titer and its replication intermediate, negative RNA strand, were determined by qRT-PCR from the honey bees at 7 days post-antibiotic treatment. Additionally, honey bee head mass and survival rate were measured. We observed that antibiotics decreased the expression of
<i>tor</i>
and
<i>rel</i>
, and increased DWV titer and its replication activity. Expression of
<i>ilp1</i>
,
<i>mrjp1</i>
-
<i>5</i>
and
<i>vg</i>
, and honey bee head mass were also reduced compared with bees on a pollen diet. Antibiotics also caused a significant drop in survivorship, which could be rescued by addition of pollen to the diet. Of importance, pollen could partially rescue the loss of
<i>vg</i>
and
<i>mrjp2</i>
while also increasing the head mass of antibiotic-treated bees. Our results illuminate the roles of bacteria in honey bee nutrition, metabolism and immunity, which confer the ability to inhibit virus replication, extend honey bee lifespan and improve overall health.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">30846535</PMID>
<DateCompleted>
<Year>2020</Year>
<Month>06</Month>
<Day>16</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>06</Month>
<Day>16</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">1477-9145</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>222</Volume>
<Issue>Pt 7</Issue>
<PubDate>
<Year>2019</Year>
<Month>04</Month>
<Day>05</Day>
</PubDate>
</JournalIssue>
<Title>The Journal of experimental biology</Title>
<ISOAbbreviation>J Exp Biol</ISOAbbreviation>
</Journal>
<ArticleTitle>Pollen reverses decreased lifespan, altered nutritional metabolism and suppressed immunity in honey bees (
<i>Apis mellifera</i>
) treated with antibiotics.</ArticleTitle>
<ELocationID EIdType="pii" ValidYN="Y">jeb202077</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1242/jeb.202077</ELocationID>
<Abstract>
<AbstractText>Nutrition is involved in regulating multiple aspects of honey bee biology such as caste, immunity, lifespan, growth and behavioral development. Deformed wing virus (DWV) is a major pathogenic factor which threatens honey bee populations, and its replication is regulated by the nutrition status and immune response of honey bees. The alimentary canal of the honey bee is home to a diverse microbial community that provides essential nutrients and serves to bolster immune responses. However, to what extent gut bacteria affect honey bee nutrition metabolism and immunity with respect to DWV has not been investigated fully. In this study, newly emerged worker bees were subjected to four diets that contained (1) pollen, (2) pollen and antibiotics, (3) neither pollen nor antibiotics or (4) antibiotics alone. The expression level of two nutrition genes
<i>target of rapamycin</i>
(
<i>tor</i>
) and
<i>insulin like peptide</i>
(
<i>ilp1</i>
), one nutritional marker gene
<i>vitellogenin</i>
(
<i>vg</i>
), five
<i>major royal jelly</i>
<i>protein</i>
genes (
<i>mrjp1</i>
-
<i>5</i>
), one antimicrobial peptide regulating gene
<i>relish</i>
(
<i>rel</i>
), and DWV virus titer and its replication intermediate, negative RNA strand, were determined by qRT-PCR from the honey bees at 7 days post-antibiotic treatment. Additionally, honey bee head mass and survival rate were measured. We observed that antibiotics decreased the expression of
<i>tor</i>
and
<i>rel</i>
, and increased DWV titer and its replication activity. Expression of
<i>ilp1</i>
,
<i>mrjp1</i>
-
<i>5</i>
and
<i>vg</i>
, and honey bee head mass were also reduced compared with bees on a pollen diet. Antibiotics also caused a significant drop in survivorship, which could be rescued by addition of pollen to the diet. Of importance, pollen could partially rescue the loss of
<i>vg</i>
and
<i>mrjp2</i>
while also increasing the head mass of antibiotic-treated bees. Our results illuminate the roles of bacteria in honey bee nutrition, metabolism and immunity, which confer the ability to inhibit virus replication, extend honey bee lifespan and improve overall health.</AbstractText>
<CopyrightInformation>© 2019. Published by The Company of Biologists Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Jianghong</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>College of Bee Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Heerman</LastName>
<ForeName>Matthew C</ForeName>
<Initials>MC</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Evans</LastName>
<ForeName>Jay D</ForeName>
<Initials>JD</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rose</LastName>
<ForeName>Robyn</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>USDA APHIS, Plant Protection and Quarantine, 4700 River Rd, Riverdale, MD 20737, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Wenfeng</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rodríguez-García</LastName>
<ForeName>Cristina</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">0000-0002-0257-2745</Identifier>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>DeGrandi-Hoffman</LastName>
<ForeName>Gloria</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Carl Hayden Bee Research Center, 2000 East Allen Road, Tucson, AZ 85719, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zhao</LastName>
<ForeName>Yazhou</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institute of Apicultural Research, Chinese Academy of Agriculture Sciences, Beijing 100081, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Huang</LastName>
<ForeName>Shaokang</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>College of Bee Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Zhiguo</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>College of Bee Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hamilton</LastName>
<ForeName>Michele</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Yanping</ForeName>
<Initials>Y</Initials>
<Identifier Source="ORCID">0000-0002-5224-1100</Identifier>
<AffiliationInfo>
<Affiliation>USDA-ARS Bee Research Laboratory, Building 306, BARC-East, Beltsville, MD 20705, USA judy.chen@ars.usda.gov.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
<PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2019</Year>
<Month>04</Month>
<Day>05</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>J Exp Biol</MedlineTA>
<NlmUniqueID>0243705</NlmUniqueID>
<ISSNLinking>0022-0949</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D000900">Anti-Bacterial Agents</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010406">Penicillins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>Y45QSO73OB</RegistryNumber>
<NameOfSubstance UI="D013307">Streptomycin</NameOfSubstance>
</Chemical>
</ChemicalList>
<SupplMeshList>
<SupplMeshName Type="Organism" UI="C000623733">Deformed wing virus</SupplMeshName>
</SupplMeshList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000824" MajorTopicYN="N">Animal Nutritional Physiological Phenomena</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000900" MajorTopicYN="N">Anti-Bacterial Agents</DescriptorName>
<QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001419" MajorTopicYN="N">Bacteria</DescriptorName>
<QualifierName UI="Q000145" MajorTopicYN="N">classification</QualifierName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000302" MajorTopicYN="Y">isolation & purification</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001516" MajorTopicYN="N">Bees</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000821" MajorTopicYN="N">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004032" MajorTopicYN="N">Diet</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000069196" MajorTopicYN="N">Gastrointestinal Microbiome</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015870" MajorTopicYN="N">Gene Expression</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006257" MajorTopicYN="N">Head</DescriptorName>
<QualifierName UI="Q000033" MajorTopicYN="N">anatomy & histology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010406" MajorTopicYN="N">Penicillins</DescriptorName>
<QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011058" MajorTopicYN="Y">Pollen</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012328" MajorTopicYN="N">RNA Viruses</DescriptorName>
<QualifierName UI="Q000254" MajorTopicYN="N">growth & development</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013307" MajorTopicYN="N">Streptomycin</DescriptorName>
<QualifierName UI="Q000008" MajorTopicYN="N">administration & dosage</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">DWV</Keyword>
<Keyword MajorTopicYN="Y">Deformed wing virus</Keyword>
<Keyword MajorTopicYN="Y">Gut bacteria</Keyword>
<Keyword MajorTopicYN="Y">Immunity</Keyword>
<Keyword MajorTopicYN="Y">Nutrition metabolism</Keyword>
</KeywordList>
<CoiStatement>Competing interestsThe authors declare no competing or financial interests.</CoiStatement>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2018</Year>
<Month>11</Month>
<Day>21</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2019</Year>
<Month>02</Month>
<Day>25</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2019</Year>
<Month>3</Month>
<Day>9</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>6</Month>
<Day>17</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2019</Year>
<Month>3</Month>
<Day>9</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>epublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">30846535</ArticleId>
<ArticleId IdType="pii">jeb.202077</ArticleId>
<ArticleId IdType="doi">10.1242/jeb.202077</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>République populaire de Chine</li>
<li>États-Unis</li>
</country>
<region>
<li>Arizona</li>
<li>Fujian</li>
<li>Maryland</li>
</region>
<settlement>
<li>Fuzhou</li>
<li>Pékin</li>
</settlement>
</list>
<tree>
<noCountry>
<name sortKey="Chen, Yanping" sort="Chen, Yanping" uniqKey="Chen Y" first="Yanping" last="Chen">Yanping Chen</name>
</noCountry>
<country name="États-Unis">
<region name="Maryland">
<name sortKey="Li, Jianghong" sort="Li, Jianghong" uniqKey="Li J" first="Jianghong" last="Li">Jianghong Li</name>
</region>
<name sortKey="Degrandi Hoffman, Gloria" sort="Degrandi Hoffman, Gloria" uniqKey="Degrandi Hoffman G" first="Gloria" last="Degrandi-Hoffman">Gloria Degrandi-Hoffman</name>
<name sortKey="Evans, Jay D" sort="Evans, Jay D" uniqKey="Evans J" first="Jay D" last="Evans">Jay D. Evans</name>
<name sortKey="Hamilton, Michele" sort="Hamilton, Michele" uniqKey="Hamilton M" first="Michele" last="Hamilton">Michele Hamilton</name>
<name sortKey="Heerman, Matthew C" sort="Heerman, Matthew C" uniqKey="Heerman M" first="Matthew C" last="Heerman">Matthew C. Heerman</name>
<name sortKey="Li, Wenfeng" sort="Li, Wenfeng" uniqKey="Li W" first="Wenfeng" last="Li">Wenfeng Li</name>
<name sortKey="Rodriguez Garcia, Cristina" sort="Rodriguez Garcia, Cristina" uniqKey="Rodriguez Garcia C" first="Cristina" last="Rodríguez-García">Cristina Rodríguez-García</name>
<name sortKey="Rose, Robyn" sort="Rose, Robyn" uniqKey="Rose R" first="Robyn" last="Rose">Robyn Rose</name>
<name sortKey="Zhao, Yazhou" sort="Zhao, Yazhou" uniqKey="Zhao Y" first="Yazhou" last="Zhao">Yazhou Zhao</name>
</country>
<country name="République populaire de Chine">
<region name="Fujian">
<name sortKey="Li, Jianghong" sort="Li, Jianghong" uniqKey="Li J" first="Jianghong" last="Li">Jianghong Li</name>
</region>
<name sortKey="Huang, Shaokang" sort="Huang, Shaokang" uniqKey="Huang S" first="Shaokang" last="Huang">Shaokang Huang</name>
<name sortKey="Li, Zhiguo" sort="Li, Zhiguo" uniqKey="Li Z" first="Zhiguo" last="Li">Zhiguo Li</name>
<name sortKey="Zhao, Yazhou" sort="Zhao, Yazhou" uniqKey="Zhao Y" first="Yazhou" last="Zhao">Yazhou Zhao</name>
</country>
</tree>
</affiliations>
</record>

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