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Constitutive heterologous overexpression of a TIR-NB-ARC-LRR gene encoding a putative disease resistance protein from wild Chinese Vitis pseudoreticulata in Arabidopsis and tobacco enhances resistance to phytopathogenic fungi and bacteria.

Identifieur interne : 000340 ( Main/Exploration ); précédent : 000339; suivant : 000341

Constitutive heterologous overexpression of a TIR-NB-ARC-LRR gene encoding a putative disease resistance protein from wild Chinese Vitis pseudoreticulata in Arabidopsis and tobacco enhances resistance to phytopathogenic fungi and bacteria.

Auteurs : Zhifeng Wen [République populaire de Chine] ; Liping Yao [République populaire de Chine] ; Stacy D. Singer [Canada] ; Hanif Muhammad [République populaire de Chine] ; Zhi Li [République populaire de Chine] ; Xiping Wang [République populaire de Chine]

Source :

RBID : pubmed:28131063

Descripteurs français

English descriptors

Abstract

Plants use resistance (R) proteins to detect pathogen effector proteins and activate their innate immune response against the pathogen. The majority of these proteins contain an NB-ARC (nucleotide-binding adaptor shared by APAF-1, R proteins, and CED-4) domain along with a leucine-rich repeat (LRR), and some also bear a toll interleukin 1 receptor (TIR) domain. In this study, we characterized a gene encoding a TIR-NB-ARC-LRR R protein (VpTNL1) (GenBank accession number KX649890) from wild Chinese grapevine Vitis pseudoreticulata accession "Baihe-35-1", which was identified previously from a transcriptomic analysis of leaves inoculated with powdery mildew (PM; Erysiphe necator (Schw.)). The VpTNL1 transcript was found to be highly induced in V. pseudoreticulata following inoculation with E. necator, as well as treatment with salicylic acid (SA). Sequence analysis demonstrated that the deduced amino acid sequence contained a TIR domain at the N-terminus, along with an NB-ARC and four LRRs domains within the C-terminus. Constitutive expression of VpTNL1 in Arabidopsis thaliana resulted in either a wild-type or dwarf phenotype. Intriguingly, the phenotypically normal transgenic lines displayed enhanced resistance to Arabidopsis PM, Golovinomyces cichoracearum, as well as to the virulent bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Similarly, constitutive expression of VpTNL1 in Nicotiana tabacum was found to confer enhanced resistance to tobacco PM, Erysiphe cichoacearum DC. Subsequent isolation of the VpTNL1 promoter and deletion analysis indicated that TC-rich repeats and TCA elements likely play an important role in its response to E. necator and SA treatment, respectively. Taken together, these results indicate that VpTNL1 contributes to PM resistance in grapevine and provide an interesting gene target for the future amelioration of grape via breeding and/or biotechnology.

DOI: 10.1016/j.plaphy.2017.01.017
PubMed: 28131063


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<term>Amino Acid Sequence (MeSH)</term>
<term>Arabidopsis (genetics)</term>
<term>Arabidopsis (microbiology)</term>
<term>Ascomycota (drug effects)</term>
<term>Ascomycota (physiology)</term>
<term>Base Sequence (MeSH)</term>
<term>Cloning, Molecular (MeSH)</term>
<term>Disease Resistance (drug effects)</term>
<term>Disease Resistance (genetics)</term>
<term>Genes, Plant (MeSH)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Proteins (chemistry)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Plants, Genetically Modified (MeSH)</term>
<term>Promoter Regions, Genetic (genetics)</term>
<term>Proteins (chemistry)</term>
<term>Proteins (genetics)</term>
<term>Proteins (metabolism)</term>
<term>Pseudomonas (drug effects)</term>
<term>Pseudomonas (physiology)</term>
<term>Salicylic Acid (pharmacology)</term>
<term>Sequence Alignment (MeSH)</term>
<term>Tobacco (drug effects)</term>
<term>Tobacco (genetics)</term>
<term>Tobacco (microbiology)</term>
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<term>Acide salicylique (pharmacologie)</term>
<term>Alignement de séquences (MeSH)</term>
<term>Arabidopsis (génétique)</term>
<term>Arabidopsis (microbiologie)</term>
<term>Ascomycota (effets des médicaments et des substances chimiques)</term>
<term>Ascomycota (physiologie)</term>
<term>Clonage moléculaire (MeSH)</term>
<term>Gènes de plante (MeSH)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Phylogenèse (MeSH)</term>
<term>Protéines (composition chimique)</term>
<term>Protéines (génétique)</term>
<term>Protéines (métabolisme)</term>
<term>Protéines végétales (composition chimique)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Pseudomonas (effets des médicaments et des substances chimiques)</term>
<term>Pseudomonas (physiologie)</term>
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<term>Résistance à la maladie (effets des médicaments et des substances chimiques)</term>
<term>Résistance à la maladie (génétique)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Séquence nucléotidique (MeSH)</term>
<term>Tabac (effets des médicaments et des substances chimiques)</term>
<term>Tabac (génétique)</term>
<term>Tabac (microbiologie)</term>
<term>Vitis (génétique)</term>
<term>Végétaux génétiquement modifiés (MeSH)</term>
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<term>Plant Proteins</term>
<term>Proteins</term>
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<keywords scheme="MESH" qualifier="composition chimique" xml:lang="fr">
<term>Protéines</term>
<term>Protéines végétales</term>
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<term>Disease Resistance</term>
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<term>Disease Resistance</term>
<term>Plant Diseases</term>
<term>Plant Proteins</term>
<term>Promoter Regions, Genetic</term>
<term>Proteins</term>
<term>Tobacco</term>
<term>Vitis</term>
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<term>Arabidopsis</term>
<term>Maladies des plantes</term>
<term>Protéines</term>
<term>Protéines végétales</term>
<term>Régions promotrices (génétique)</term>
<term>Résistance à la maladie</term>
<term>Tabac</term>
<term>Vitis</term>
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<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Plant Proteins</term>
<term>Proteins</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Arabidopsis</term>
<term>Maladies des plantes</term>
<term>Tabac</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Arabidopsis</term>
<term>Plant Diseases</term>
<term>Tobacco</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Protéines</term>
<term>Protéines végétales</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Acide salicylique</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Salicylic Acid</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Ascomycota</term>
<term>Pseudomonas</term>
</keywords>
<keywords scheme="MESH" qualifier="physiology" xml:lang="en">
<term>Ascomycota</term>
<term>Pseudomonas</term>
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<term>Phylogenèse</term>
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<div type="abstract" xml:lang="en">Plants use resistance (R) proteins to detect pathogen effector proteins and activate their innate immune response against the pathogen. The majority of these proteins contain an NB-ARC (nucleotide-binding adaptor shared by APAF-1, R proteins, and CED-4) domain along with a leucine-rich repeat (LRR), and some also bear a toll interleukin 1 receptor (TIR) domain. In this study, we characterized a gene encoding a TIR-NB-ARC-LRR R protein (VpTNL1) (GenBank accession number KX649890) from wild Chinese grapevine Vitis pseudoreticulata accession "Baihe-35-1", which was identified previously from a transcriptomic analysis of leaves inoculated with powdery mildew (PM; Erysiphe necator (Schw.)). The VpTNL1 transcript was found to be highly induced in V. pseudoreticulata following inoculation with E. necator, as well as treatment with salicylic acid (SA). Sequence analysis demonstrated that the deduced amino acid sequence contained a TIR domain at the N-terminus, along with an NB-ARC and four LRRs domains within the C-terminus. Constitutive expression of VpTNL1 in Arabidopsis thaliana resulted in either a wild-type or dwarf phenotype. Intriguingly, the phenotypically normal transgenic lines displayed enhanced resistance to Arabidopsis PM, Golovinomyces cichoracearum, as well as to the virulent bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Similarly, constitutive expression of VpTNL1 in Nicotiana tabacum was found to confer enhanced resistance to tobacco PM, Erysiphe cichoacearum DC. Subsequent isolation of the VpTNL1 promoter and deletion analysis indicated that TC-rich repeats and TCA elements likely play an important role in its response to E. necator and SA treatment, respectively. Taken together, these results indicate that VpTNL1 contributes to PM resistance in grapevine and provide an interesting gene target for the future amelioration of grape via breeding and/or biotechnology.</div>
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<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.plaphy.2017.01.017</ELocationID>
<Abstract>
<AbstractText>Plants use resistance (R) proteins to detect pathogen effector proteins and activate their innate immune response against the pathogen. The majority of these proteins contain an NB-ARC (nucleotide-binding adaptor shared by APAF-1, R proteins, and CED-4) domain along with a leucine-rich repeat (LRR), and some also bear a toll interleukin 1 receptor (TIR) domain. In this study, we characterized a gene encoding a TIR-NB-ARC-LRR R protein (VpTNL1) (GenBank accession number KX649890) from wild Chinese grapevine Vitis pseudoreticulata accession "Baihe-35-1", which was identified previously from a transcriptomic analysis of leaves inoculated with powdery mildew (PM; Erysiphe necator (Schw.)). The VpTNL1 transcript was found to be highly induced in V. pseudoreticulata following inoculation with E. necator, as well as treatment with salicylic acid (SA). Sequence analysis demonstrated that the deduced amino acid sequence contained a TIR domain at the N-terminus, along with an NB-ARC and four LRRs domains within the C-terminus. Constitutive expression of VpTNL1 in Arabidopsis thaliana resulted in either a wild-type or dwarf phenotype. Intriguingly, the phenotypically normal transgenic lines displayed enhanced resistance to Arabidopsis PM, Golovinomyces cichoracearum, as well as to the virulent bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Similarly, constitutive expression of VpTNL1 in Nicotiana tabacum was found to confer enhanced resistance to tobacco PM, Erysiphe cichoacearum DC. Subsequent isolation of the VpTNL1 promoter and deletion analysis indicated that TC-rich repeats and TCA elements likely play an important role in its response to E. necator and SA treatment, respectively. Taken together, these results indicate that VpTNL1 contributes to PM resistance in grapevine and provide an interesting gene target for the future amelioration of grape via breeding and/or biotechnology.</AbstractText>
<CopyrightInformation>Copyright © 2017 Elsevier Masson SAS. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Wen</LastName>
<ForeName>Zhifeng</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712100, China; Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi 712100, China; College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, Fujian 350002, China. Electronic address: zhifengwen@126.com.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yao</LastName>
<ForeName>Liping</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Horticultural Plant Biology and Metabolomics Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou 350002, China. Electronic address: lpy106080@163.com.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Singer</LastName>
<ForeName>Stacy D</ForeName>
<Initials>SD</Initials>
<AffiliationInfo>
<Affiliation>Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2P5, Canada. Electronic address: stacysinger@hotmail.com.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Muhammad</LastName>
<ForeName>Hanif</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712100, China; Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi 712100, China. Electronic address: mdhanif1716@yahoo.com.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Li</LastName>
<ForeName>Zhi</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712100, China; Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi 712100, China. Electronic address: lizhi@nwsuaf.edu.cn.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Xiping</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Crop Stress Biology in Arid Areas, College of Horticulture, Northwest A&F University, Yangling, Shaanxi 712100, China; Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi 712100, China. Electronic address: wangxiping@nwsuaf.edu.cn.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>01</Month>
<Day>17</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>France</Country>
<MedlineTA>Plant Physiol Biochem</MedlineTA>
<NlmUniqueID>9882449</NlmUniqueID>
<ISSNLinking>0981-9428</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011506">Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C107657">leucine-rich repeat proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>O414PZ4LPZ</RegistryNumber>
<NameOfSubstance UI="D020156">Salicylic Acid</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017360" MajorTopicYN="N">Arabidopsis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001203" MajorTopicYN="N">Ascomycota</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D003001" MajorTopicYN="N">Cloning, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D060467" MajorTopicYN="N">Disease Resistance</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D017343" MajorTopicYN="Y">Genes, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D030821" MajorTopicYN="N">Plants, Genetically Modified</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011401" MajorTopicYN="N">Promoter Regions, Genetic</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011506" MajorTopicYN="N">Proteins</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011549" MajorTopicYN="N">Pseudomonas</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020156" MajorTopicYN="N">Salicylic Acid</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016415" MajorTopicYN="N">Sequence Alignment</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D014026" MajorTopicYN="N">Tobacco</DescriptorName>
<QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D027843" MajorTopicYN="N">Vitis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">Disease resistance</Keyword>
<Keyword MajorTopicYN="N">Powdery mildew</Keyword>
<Keyword MajorTopicYN="N">Promoter analysis</Keyword>
<Keyword MajorTopicYN="N">VpTNL1</Keyword>
<Keyword MajorTopicYN="N">Wild Chinese vitis</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2016</Year>
<Month>09</Month>
<Day>30</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2017</Year>
<Month>01</Month>
<Day>13</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2017</Year>
<Month>01</Month>
<Day>14</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2017</Year>
<Month>1</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>5</Month>
<Day>2</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2017</Year>
<Month>1</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">28131063</ArticleId>
<ArticleId IdType="pii">S0981-9428(17)30025-6</ArticleId>
<ArticleId IdType="doi">10.1016/j.plaphy.2017.01.017</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>Canada</li>
<li>République populaire de Chine</li>
</country>
<region>
<li>Fujian</li>
</region>
<settlement>
<li>Fuzhou</li>
</settlement>
</list>
<tree>
<country name="République populaire de Chine">
<noRegion>
<name sortKey="Wen, Zhifeng" sort="Wen, Zhifeng" uniqKey="Wen Z" first="Zhifeng" last="Wen">Zhifeng Wen</name>
</noRegion>
<name sortKey="Li, Zhi" sort="Li, Zhi" uniqKey="Li Z" first="Zhi" last="Li">Zhi Li</name>
<name sortKey="Muhammad, Hanif" sort="Muhammad, Hanif" uniqKey="Muhammad H" first="Hanif" last="Muhammad">Hanif Muhammad</name>
<name sortKey="Wang, Xiping" sort="Wang, Xiping" uniqKey="Wang X" first="Xiping" last="Wang">Xiping Wang</name>
<name sortKey="Yao, Liping" sort="Yao, Liping" uniqKey="Yao L" first="Liping" last="Yao">Liping Yao</name>
</country>
<country name="Canada">
<noRegion>
<name sortKey="Singer, Stacy D" sort="Singer, Stacy D" uniqKey="Singer S" first="Stacy D" last="Singer">Stacy D. Singer</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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