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Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins.

Identifieur interne : 000C46 ( Main/Exploration ); précédent : 000C45; suivant : 000C47

Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins.

Auteurs : Emily E. Helliwell [États-Unis] ; Julio Vega-Arreguín [États-Unis] ; Zi Shi [États-Unis] ; Bryan Bailey [États-Unis] ; Shunyuan Xiao [États-Unis] ; Siela N. Maximova [États-Unis] ; Brett M. Tyler [États-Unis] ; Mark J. Guiltinan [États-Unis]

Source :

RBID : pubmed:26214158

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English descriptors

Abstract

The internalization of some oomycete and fungal pathogen effectors into host plant cells has been reported to be blocked by proteins that bind to the effectors' cell entry receptor, phosphatidylinositol-3-phosphate (PI3P). This finding suggested a novel strategy for disease control by engineering plants to secrete PI3P-binding proteins. In this study, we tested this strategy using the chocolate tree Theobroma cacao. Transient expression and secretion of four different PI3P-binding proteins in detached leaves of T. cacao greatly reduced infection by two oomycete pathogens, Phytophthora tropicalis and Phytophthora palmivora, which cause black pod disease. Lesion size and pathogen growth were reduced by up to 85%. Resistance was not conferred by proteins lacking a secretory leader, by proteins with mutations in their PI3P-binding site, or by a secreted PI4P-binding protein. Stably transformed, transgenic T. cacao plants expressing two different PI3P-binding proteins showed substantially enhanced resistance to both P. tropicalis and P. palmivora, as well as to the fungal pathogen Colletotrichum theobromicola. These results demonstrate that secretion of PI3P-binding proteins is an effective way to increase disease resistance in T. cacao, and potentially in other plants, against a broad spectrum of pathogens.

DOI: 10.1111/pbi.12436
PubMed: 26214158


Affiliations:


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Le document en format XML

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<keywords scheme="KwdEn" xml:lang="en">
<term>Amino Acid Sequence (MeSH)</term>
<term>Cacao (genetics)</term>
<term>Cacao (microbiology)</term>
<term>Colletotrichum (physiology)</term>
<term>Disease Resistance (MeSH)</term>
<term>Gene Expression Regulation, Plant (MeSH)</term>
<term>Mutant Proteins (chemistry)</term>
<term>Mutant Proteins (metabolism)</term>
<term>Phosphate-Binding Proteins (chemistry)</term>
<term>Phosphate-Binding Proteins (metabolism)</term>
<term>Phosphatidylinositol Phosphates (metabolism)</term>
<term>Phytophthora (pathogenicity)</term>
<term>Phytophthora (physiology)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Leaves (microbiology)</term>
<term>Plant Proteins (chemistry)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Protein Domains (MeSH)</term>
<term>RNA, Messenger (genetics)</term>
<term>RNA, Messenger (metabolism)</term>
<term>Reproducibility of Results (MeSH)</term>
<term>Transformation, Genetic (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>ARN messager (génétique)</term>
<term>ARN messager (métabolisme)</term>
<term>Cacaoyer (génétique)</term>
<term>Cacaoyer (microbiologie)</term>
<term>Colletotrichum (physiologie)</term>
<term>Domaines protéiques (MeSH)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Phosphates phosphatidylinositol (métabolisme)</term>
<term>Phytophthora (pathogénicité)</term>
<term>Phytophthora (physiologie)</term>
<term>Protéines de liaison aux phosphates (composition chimique)</term>
<term>Protéines de liaison aux phosphates (métabolisme)</term>
<term>Protéines mutantes (composition chimique)</term>
<term>Protéines mutantes (métabolisme)</term>
<term>Protéines végétales (composition chimique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Reproductibilité des résultats (MeSH)</term>
<term>Régulation de l'expression des gènes végétaux (MeSH)</term>
<term>Résistance à la maladie (MeSH)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Transformation génétique (MeSH)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en">
<term>Mutant Proteins</term>
<term>Phosphate-Binding Proteins</term>
<term>Plant Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Protéines de liaison aux phosphates</term>
<term>Protéines mutantes</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Cacao</term>
<term>RNA, Messenger</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>ARN messager</term>
<term>Cacaoyer</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Mutant Proteins</term>
<term>Phosphate-Binding Proteins</term>
<term>Phosphatidylinositol Phosphates</term>
<term>Plant Proteins</term>
<term>RNA, Messenger</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Cacaoyer</term>
<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Cacao</term>
<term>Plant Diseases</term>
<term>Plant Leaves</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>ARN messager</term>
<term>Phosphates phosphatidylinositol</term>
<term>Protéines de liaison aux phosphates</term>
<term>Protéines mutantes</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Colletotrichum</term>
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Colletotrichum</term>
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Amino Acid Sequence</term>
<term>Disease Resistance</term>
<term>Gene Expression Regulation, Plant</term>
<term>Plants, Genetically Modified</term>
<term>Protein Domains</term>
<term>Reproducibility of Results</term>
<term>Transformation, Genetic</term>
</keywords>
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<term>Domaines protéiques</term>
<term>Reproductibilité des résultats</term>
<term>Régulation de l'expression des gènes végétaux</term>
<term>Résistance à la maladie</term>
<term>Séquence d'acides aminés</term>
<term>Transformation génétique</term>
<term>Végétaux génétiquement modifiés</term>
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<front>
<div type="abstract" xml:lang="en">The internalization of some oomycete and fungal pathogen effectors into host plant cells has been reported to be blocked by proteins that bind to the effectors' cell entry receptor, phosphatidylinositol-3-phosphate (PI3P). This finding suggested a novel strategy for disease control by engineering plants to secrete PI3P-binding proteins. In this study, we tested this strategy using the chocolate tree Theobroma cacao. Transient expression and secretion of four different PI3P-binding proteins in detached leaves of T. cacao greatly reduced infection by two oomycete pathogens, Phytophthora tropicalis and Phytophthora palmivora, which cause black pod disease. Lesion size and pathogen growth were reduced by up to 85%. Resistance was not conferred by proteins lacking a secretory leader, by proteins with mutations in their PI3P-binding site, or by a secreted PI4P-binding protein. Stably transformed, transgenic T. cacao plants expressing two different PI3P-binding proteins showed substantially enhanced resistance to both P. tropicalis and P. palmivora, as well as to the fungal pathogen Colletotrichum theobromicola. These results demonstrate that secretion of PI3P-binding proteins is an effective way to increase disease resistance in T. cacao, and potentially in other plants, against a broad spectrum of pathogens.</div>
</front>
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<Month>12</Month>
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<Title>Plant biotechnology journal</Title>
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<ArticleTitle>Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins.</ArticleTitle>
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<ELocationID EIdType="doi" ValidYN="Y">10.1111/pbi.12436</ELocationID>
<Abstract>
<AbstractText>The internalization of some oomycete and fungal pathogen effectors into host plant cells has been reported to be blocked by proteins that bind to the effectors' cell entry receptor, phosphatidylinositol-3-phosphate (PI3P). This finding suggested a novel strategy for disease control by engineering plants to secrete PI3P-binding proteins. In this study, we tested this strategy using the chocolate tree Theobroma cacao. Transient expression and secretion of four different PI3P-binding proteins in detached leaves of T. cacao greatly reduced infection by two oomycete pathogens, Phytophthora tropicalis and Phytophthora palmivora, which cause black pod disease. Lesion size and pathogen growth were reduced by up to 85%. Resistance was not conferred by proteins lacking a secretory leader, by proteins with mutations in their PI3P-binding site, or by a secreted PI4P-binding protein. Stably transformed, transgenic T. cacao plants expressing two different PI3P-binding proteins showed substantially enhanced resistance to both P. tropicalis and P. palmivora, as well as to the fungal pathogen Colletotrichum theobromicola. These results demonstrate that secretion of PI3P-binding proteins is an effective way to increase disease resistance in T. cacao, and potentially in other plants, against a broad spectrum of pathogens.</AbstractText>
<CopyrightInformation>© 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Helliwell</LastName>
<ForeName>Emily E</ForeName>
<Initials>EE</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Science and Huck Institute of Life Sciences, The Pennsylvania State University, University Park, PA, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Center for Genome Research and Biocomputing, and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Vega-Arreguín</LastName>
<ForeName>Julio</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Virginia Bioinformatics Institute and Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Shi</LastName>
<ForeName>Zi</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Science and Huck Institute of Life Sciences, The Pennsylvania State University, University Park, PA, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bailey</LastName>
<ForeName>Bryan</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>United States Department of Agriculture, Agricultural Research Service, Beltsville, MD, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xiao</LastName>
<ForeName>Shunyuan</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Institute for Bioscience and Biotechnology Research & Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Maximova</LastName>
<ForeName>Siela N</ForeName>
<Initials>SN</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Science and Huck Institute of Life Sciences, The Pennsylvania State University, University Park, PA, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tyler</LastName>
<ForeName>Brett M</ForeName>
<Initials>BM</Initials>
<AffiliationInfo>
<Affiliation>Center for Genome Research and Biocomputing, and Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Virginia Bioinformatics Institute and Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guiltinan</LastName>
<ForeName>Mark J</ForeName>
<Initials>MJ</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Science and Huck Institute of Life Sciences, The Pennsylvania State University, University Park, PA, USA.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<DataBankList CompleteYN="Y">
<DataBank>
<DataBankName>GENBANK</DataBankName>
<AccessionNumberList>
<AccessionNumber>AAG01896.1</AccessionNumber>
<AccessionNumber>AAG15199.1</AccessionNumber>
<AccessionNumber>D50050</AccessionNumber>
<AccessionNumber>KF018690.1</AccessionNumber>
<AccessionNumber>NP_001235232.1</AccessionNumber>
<AccessionNumber>P32912.1</AccessionNumber>
</AccessionNumberList>
</DataBank>
</DataBankList>
<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>2015</Year>
<Month>07</Month>
<Day>27</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>England</Country>
<MedlineTA>Plant Biotechnol J</MedlineTA>
<NlmUniqueID>101201889</NlmUniqueID>
<ISSNLinking>1467-7644</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D050505">Mutant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D028044">Phosphate-Binding Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D018129">Phosphatidylinositol Phosphates</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D012333">RNA, Messenger</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C055525">phosphatidylinositol 3-phosphate</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002099" MajorTopicYN="N">Cacao</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020231" MajorTopicYN="N">Colletotrichum</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="Y">Disease Resistance</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D050505" MajorTopicYN="N">Mutant Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D028044" MajorTopicYN="N">Phosphate-Binding Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018129" MajorTopicYN="N">Phosphatidylinositol Phosphates</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010838" MajorTopicYN="N">Phytophthora</DescriptorName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018515" MajorTopicYN="N">Plant Leaves</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000072417" MajorTopicYN="N">Protein Domains</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012333" MajorTopicYN="N">RNA, Messenger</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015203" MajorTopicYN="N">Reproducibility of Results</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014170" MajorTopicYN="N">Transformation, Genetic</DescriptorName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Theobroma cacao</Keyword>
<Keyword MajorTopicYN="N">disease resistance</Keyword>
<Keyword MajorTopicYN="N">effectors</Keyword>
<Keyword MajorTopicYN="N">fungi</Keyword>
<Keyword MajorTopicYN="N">oomycetes</Keyword>
<Keyword MajorTopicYN="N">phosphatidylinositol-3-phosphate-binding protein</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2014</Year>
<Month>03</Month>
<Day>12</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2015</Year>
<Month>06</Month>
<Day>15</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2015</Year>
<Month>06</Month>
<Day>16</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2015</Year>
<Month>7</Month>
<Day>28</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2015</Year>
<Month>7</Month>
<Day>28</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2016</Year>
<Month>12</Month>
<Day>15</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">26214158</ArticleId>
<ArticleId IdType="doi">10.1111/pbi.12436</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>États-Unis</li>
</country>
<region>
<li>Maryland</li>
<li>Oregon</li>
<li>Pennsylvanie</li>
<li>Virginie</li>
</region>
<settlement>
<li>College Park (Maryland)</li>
<li>University Park (Pennsylvanie)</li>
</settlement>
<orgName>
<li>Université d'État de Pennsylvanie</li>
<li>Université du Maryland</li>
</orgName>
</list>
<tree>
<country name="États-Unis">
<region name="Pennsylvanie">
<name sortKey="Helliwell, Emily E" sort="Helliwell, Emily E" uniqKey="Helliwell E" first="Emily E" last="Helliwell">Emily E. Helliwell</name>
</region>
<name sortKey="Bailey, Bryan" sort="Bailey, Bryan" uniqKey="Bailey B" first="Bryan" last="Bailey">Bryan Bailey</name>
<name sortKey="Guiltinan, Mark J" sort="Guiltinan, Mark J" uniqKey="Guiltinan M" first="Mark J" last="Guiltinan">Mark J. Guiltinan</name>
<name sortKey="Helliwell, Emily E" sort="Helliwell, Emily E" uniqKey="Helliwell E" first="Emily E" last="Helliwell">Emily E. Helliwell</name>
<name sortKey="Maximova, Siela N" sort="Maximova, Siela N" uniqKey="Maximova S" first="Siela N" last="Maximova">Siela N. Maximova</name>
<name sortKey="Shi, Zi" sort="Shi, Zi" uniqKey="Shi Z" first="Zi" last="Shi">Zi Shi</name>
<name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name>
<name sortKey="Tyler, Brett M" sort="Tyler, Brett M" uniqKey="Tyler B" first="Brett M" last="Tyler">Brett M. Tyler</name>
<name sortKey="Vega Arreguin, Julio" sort="Vega Arreguin, Julio" uniqKey="Vega Arreguin J" first="Julio" last="Vega-Arreguín">Julio Vega-Arreguín</name>
<name sortKey="Xiao, Shunyuan" sort="Xiao, Shunyuan" uniqKey="Xiao S" first="Shunyuan" last="Xiao">Shunyuan Xiao</name>
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