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An xa5 Resistance Gene-Breaking Indian Strain of the Rice Bacterial Blight Pathogen Xanthomonas oryzae pv. oryzae Is Nearly Identical to a Thai Strain.

Identifieur interne : 000218 ( Main/Exploration ); précédent : 000217; suivant : 000219

An xa5 Resistance Gene-Breaking Indian Strain of the Rice Bacterial Blight Pathogen Xanthomonas oryzae pv. oryzae Is Nearly Identical to a Thai Strain.

Auteurs : Sara C D. Carpenter [États-Unis] ; Prashant Mishra [Inde] ; Chandrika Ghoshal [Inde] ; Prasanta K. Dash [Inde] ; Li Wang [États-Unis] ; Samriti Midha [Inde] ; Gouri S. Laha [Inde] ; Jagjeet S. Lore [Inde] ; Wichai Kositratana [Thaïlande] ; Nagendra K. Singh [Inde] ; Kuldeep Singh [Inde] ; Prabhu B. Patil [Inde] ; Ricardo Oliva [Philippines] ; Sujin Patarapuwadol [Thaïlande] ; Adam J. Bogdanove [États-Unis] ; Rhitu Rai [Inde]

Source :

RBID : pubmed:33193207

Abstract

The rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae (Xoo) constrains production in major rice growing countries of Asia. Xoo injects transcription activator-like effectors (TALEs) that bind to and activate host "susceptibility" (S) genes that are important for disease. The bacterial blight resistance gene xa5, which reduces TALE activity generally, has been widely deployed. However, strains defeating xa5 have been reported in India and recently also in Thailand. We completely sequenced and compared the genomes of one such strain from each country and examined the encoded TALEs. The two genomes are nearly identical, including the TALE genes, and belong to a previously identified, highly clonal lineage. Each strain harbors a TALE known to activate the major S gene SWEET11 strongly enough to be effective even when diminished by xa5. The findings suggest international migration of the xa5-compatible pathotype and highlight the utility of whole genome sequencing and TALE analysis for understanding and responding to breakdown of resistance.

DOI: 10.3389/fmicb.2020.579504
PubMed: 33193207
PubMed Central: PMC7610140


Affiliations:


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Le document en format XML

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<title xml:lang="en">An
<i>xa5</i>
Resistance Gene-Breaking Indian Strain of the Rice Bacterial Blight Pathogen
<i>Xanthomonas oryzae</i>
pv. oryzae Is Nearly Identical to a Thai Strain.</title>
<author>
<name sortKey="Carpenter, Sara C D" sort="Carpenter, Sara C D" uniqKey="Carpenter S" first="Sara C D" last="Carpenter">Sara C D. Carpenter</name>
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<name sortKey="Ghoshal, Chandrika" sort="Ghoshal, Chandrika" uniqKey="Ghoshal C" first="Chandrika" last="Ghoshal">Chandrika Ghoshal</name>
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<name sortKey="Wang, Li" sort="Wang, Li" uniqKey="Wang L" first="Li" last="Wang">Li Wang</name>
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<name sortKey="Laha, Gouri S" sort="Laha, Gouri S" uniqKey="Laha G" first="Gouri S" last="Laha">Gouri S. Laha</name>
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<name sortKey="Lore, Jagjeet S" sort="Lore, Jagjeet S" uniqKey="Lore J" first="Jagjeet S" last="Lore">Jagjeet S. Lore</name>
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<name sortKey="Kositratana, Wichai" sort="Kositratana, Wichai" uniqKey="Kositratana W" first="Wichai" last="Kositratana">Wichai Kositratana</name>
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<name sortKey="Singh, Nagendra K" sort="Singh, Nagendra K" uniqKey="Singh N" first="Nagendra K" last="Singh">Nagendra K. Singh</name>
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<name sortKey="Singh, Kuldeep" sort="Singh, Kuldeep" uniqKey="Singh K" first="Kuldeep" last="Singh">Kuldeep Singh</name>
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<name sortKey="Patil, Prabhu B" sort="Patil, Prabhu B" uniqKey="Patil P" first="Prabhu B" last="Patil">Prabhu B. Patil</name>
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<name sortKey="Oliva, Ricardo" sort="Oliva, Ricardo" uniqKey="Oliva R" first="Ricardo" last="Oliva">Ricardo Oliva</name>
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<name sortKey="Patarapuwadol, Sujin" sort="Patarapuwadol, Sujin" uniqKey="Patarapuwadol S" first="Sujin" last="Patarapuwadol">Sujin Patarapuwadol</name>
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<name sortKey="Rai, Rhitu" sort="Rai, Rhitu" uniqKey="Rai R" first="Rhitu" last="Rai">Rhitu Rai</name>
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<title xml:lang="en">An
<i>xa5</i>
Resistance Gene-Breaking Indian Strain of the Rice Bacterial Blight Pathogen
<i>Xanthomonas oryzae</i>
pv. oryzae Is Nearly Identical to a Thai Strain.</title>
<author>
<name sortKey="Carpenter, Sara C D" sort="Carpenter, Sara C D" uniqKey="Carpenter S" first="Sara C D" last="Carpenter">Sara C D. Carpenter</name>
<affiliation wicri:level="4">
<nlm:affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY</wicri:regionArea>
<placeName>
<region type="state">État de New York</region>
<settlement type="city">Ithaca (New York)</settlement>
</placeName>
<orgName type="university">Université Cornell</orgName>
</affiliation>
</author>
<author>
<name sortKey="Mishra, Prashant" sort="Mishra, Prashant" uniqKey="Mishra P" first="Prashant" last="Mishra">Prashant Mishra</name>
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<nlm:affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
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<wicri:noRegion>New Delhi</wicri:noRegion>
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<name sortKey="Ghoshal, Chandrika" sort="Ghoshal, Chandrika" uniqKey="Ghoshal C" first="Chandrika" last="Ghoshal">Chandrika Ghoshal</name>
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<nlm:affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi</wicri:regionArea>
<wicri:noRegion>New Delhi</wicri:noRegion>
</affiliation>
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<name sortKey="Dash, Prasanta K" sort="Dash, Prasanta K" uniqKey="Dash P" first="Prasanta K" last="Dash">Prasanta K. Dash</name>
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<nlm:affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi</wicri:regionArea>
<wicri:noRegion>New Delhi</wicri:noRegion>
</affiliation>
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<author>
<name sortKey="Wang, Li" sort="Wang, Li" uniqKey="Wang L" first="Li" last="Wang">Li Wang</name>
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<nlm:affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY</wicri:regionArea>
<placeName>
<region type="state">État de New York</region>
<settlement type="city">Ithaca (New York)</settlement>
</placeName>
<orgName type="university">Université Cornell</orgName>
</affiliation>
</author>
<author>
<name sortKey="Midha, Samriti" sort="Midha, Samriti" uniqKey="Midha S" first="Samriti" last="Midha">Samriti Midha</name>
<affiliation wicri:level="1">
<nlm:affiliation>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh</wicri:regionArea>
<wicri:noRegion>Chandigarh</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Laha, Gouri S" sort="Laha, Gouri S" uniqKey="Laha G" first="Gouri S" last="Laha">Gouri S. Laha</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, ICAR-Indian Institute of Rice Research, Hyderabad, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Department of Plant Pathology, ICAR-Indian Institute of Rice Research, Hyderabad</wicri:regionArea>
<wicri:noRegion>Hyderabad</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lore, Jagjeet S" sort="Lore, Jagjeet S" uniqKey="Lore J" first="Jagjeet S" last="Lore">Jagjeet S. Lore</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, Punjab Agricultural University, Ludhiana, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Department of Plant Pathology, Punjab Agricultural University, Ludhiana</wicri:regionArea>
<wicri:noRegion>Ludhiana</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Kositratana, Wichai" sort="Kositratana, Wichai" uniqKey="Kositratana W" first="Wichai" last="Kositratana">Wichai Kositratana</name>
<affiliation wicri:level="1">
<nlm:affiliation>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, Thailand.</nlm:affiliation>
<country xml:lang="fr">Thaïlande</country>
<wicri:regionArea>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom</wicri:regionArea>
<wicri:noRegion>Nakhon Pathom</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Singh, Nagendra K" sort="Singh, Nagendra K" uniqKey="Singh N" first="Nagendra K" last="Singh">Nagendra K. Singh</name>
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<nlm:affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi</wicri:regionArea>
<wicri:noRegion>New Delhi</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Singh, Kuldeep" sort="Singh, Kuldeep" uniqKey="Singh K" first="Kuldeep" last="Singh">Kuldeep Singh</name>
<affiliation wicri:level="1">
<nlm:affiliation>ICAR-National Bureau of Plant Genetic Resources, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>ICAR-National Bureau of Plant Genetic Resources, New Delhi</wicri:regionArea>
<wicri:noRegion>New Delhi</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Patil, Prabhu B" sort="Patil, Prabhu B" uniqKey="Patil P" first="Prabhu B" last="Patil">Prabhu B. Patil</name>
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<nlm:affiliation>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh</wicri:regionArea>
<wicri:noRegion>Chandigarh</wicri:noRegion>
</affiliation>
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<author>
<name sortKey="Oliva, Ricardo" sort="Oliva, Ricardo" uniqKey="Oliva R" first="Ricardo" last="Oliva">Ricardo Oliva</name>
<affiliation wicri:level="1">
<nlm:affiliation>Rice Breeding Platform, International Rice Research Institute, Los Banos, Philippines.</nlm:affiliation>
<country xml:lang="fr">Philippines</country>
<wicri:regionArea>Rice Breeding Platform, International Rice Research Institute, Los Banos</wicri:regionArea>
<wicri:noRegion>Los Banos</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Patarapuwadol, Sujin" sort="Patarapuwadol, Sujin" uniqKey="Patarapuwadol S" first="Sujin" last="Patarapuwadol">Sujin Patarapuwadol</name>
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<nlm:affiliation>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, Thailand.</nlm:affiliation>
<country xml:lang="fr">Thaïlande</country>
<wicri:regionArea>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom</wicri:regionArea>
<wicri:noRegion>Nakhon Pathom</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Bogdanove, Adam J" sort="Bogdanove, Adam J" uniqKey="Bogdanove A" first="Adam J" last="Bogdanove">Adam J. Bogdanove</name>
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<nlm:affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY</wicri:regionArea>
<placeName>
<region type="state">État de New York</region>
<settlement type="city">Ithaca (New York)</settlement>
</placeName>
<orgName type="university">Université Cornell</orgName>
</affiliation>
</author>
<author>
<name sortKey="Rai, Rhitu" sort="Rai, Rhitu" uniqKey="Rai R" first="Rhitu" last="Rai">Rhitu Rai</name>
<affiliation wicri:level="1">
<nlm:affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</nlm:affiliation>
<country xml:lang="fr">Inde</country>
<wicri:regionArea>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi</wicri:regionArea>
<wicri:noRegion>New Delhi</wicri:noRegion>
</affiliation>
</author>
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<series>
<title level="j">Frontiers in microbiology</title>
<idno type="ISSN">1664-302X</idno>
<imprint>
<date when="2020" type="published">2020</date>
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<front>
<div type="abstract" xml:lang="en">The rice bacterial blight pathogen
<i>Xanthomonas oryzae</i>
pv. oryzae (
<i>Xoo</i>
) constrains production in major rice growing countries of Asia.
<i>Xoo</i>
injects transcription activator-like effectors (TALEs) that bind to and activate host "susceptibility" (
<i>S</i>
) genes that are important for disease. The bacterial blight resistance gene
<i>xa</i>
5, which reduces TALE activity generally, has been widely deployed. However, strains defeating
<i>xa</i>
5 have been reported in India and recently also in Thailand. We completely sequenced and compared the genomes of one such strain from each country and examined the encoded TALEs. The two genomes are nearly identical, including the TALE genes, and belong to a previously identified, highly clonal lineage. Each strain harbors a TALE known to activate the major
<i>S</i>
gene
<i>SWEET11</i>
strongly enough to be effective even when diminished by
<i>xa</i>
5. The findings suggest international migration of the
<i>xa5</i>
-compatible pathotype and highlight the utility of whole genome sequencing and TALE analysis for understanding and responding to breakdown of resistance.</div>
</front>
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<Title>Frontiers in microbiology</Title>
<ISOAbbreviation>Front Microbiol</ISOAbbreviation>
</Journal>
<ArticleTitle>An
<i>xa5</i>
Resistance Gene-Breaking Indian Strain of the Rice Bacterial Blight Pathogen
<i>Xanthomonas oryzae</i>
pv. oryzae Is Nearly Identical to a Thai Strain.</ArticleTitle>
<Pagination>
<MedlinePgn>579504</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.579504</ELocationID>
<Abstract>
<AbstractText>The rice bacterial blight pathogen
<i>Xanthomonas oryzae</i>
pv. oryzae (
<i>Xoo</i>
) constrains production in major rice growing countries of Asia.
<i>Xoo</i>
injects transcription activator-like effectors (TALEs) that bind to and activate host "susceptibility" (
<i>S</i>
) genes that are important for disease. The bacterial blight resistance gene
<i>xa</i>
5, which reduces TALE activity generally, has been widely deployed. However, strains defeating
<i>xa</i>
5 have been reported in India and recently also in Thailand. We completely sequenced and compared the genomes of one such strain from each country and examined the encoded TALEs. The two genomes are nearly identical, including the TALE genes, and belong to a previously identified, highly clonal lineage. Each strain harbors a TALE known to activate the major
<i>S</i>
gene
<i>SWEET11</i>
strongly enough to be effective even when diminished by
<i>xa</i>
5. The findings suggest international migration of the
<i>xa5</i>
-compatible pathotype and highlight the utility of whole genome sequencing and TALE analysis for understanding and responding to breakdown of resistance.</AbstractText>
<CopyrightInformation>Copyright © 2020 Carpenter, Mishra, Ghoshal, Dash, Wang, Midha, Laha, Lore, Kositratana, Singh, Singh, Patil, Oliva, Patarapuwadol, Bogdanove and Rai.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Carpenter</LastName>
<ForeName>Sara C D</ForeName>
<Initials>SCD</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Mishra</LastName>
<ForeName>Prashant</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ghoshal</LastName>
<ForeName>Chandrika</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dash</LastName>
<ForeName>Prasanta K</ForeName>
<Initials>PK</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Li</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Midha</LastName>
<ForeName>Samriti</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Laha</LastName>
<ForeName>Gouri S</ForeName>
<Initials>GS</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, ICAR-Indian Institute of Rice Research, Hyderabad, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lore</LastName>
<ForeName>Jagjeet S</ForeName>
<Initials>JS</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Punjab Agricultural University, Ludhiana, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kositratana</LastName>
<ForeName>Wichai</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, Thailand.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Singh</LastName>
<ForeName>Nagendra K</ForeName>
<Initials>NK</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Singh</LastName>
<ForeName>Kuldeep</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>ICAR-National Bureau of Plant Genetic Resources, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Patil</LastName>
<ForeName>Prabhu B</ForeName>
<Initials>PB</Initials>
<AffiliationInfo>
<Affiliation>Bacterial Genomics and Evolution Laboratory, CSIR-Institute of Microbial Technology, Chandigarh, India.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Oliva</LastName>
<ForeName>Ricardo</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Rice Breeding Platform, International Rice Research Institute, Los Banos, Philippines.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Patarapuwadol</LastName>
<ForeName>Sujin</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Faculty of Agriculture at Kamphaeng Saen, Kasetsart University, Nakhon Pathom, Thailand.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bogdanove</LastName>
<ForeName>Adam J</ForeName>
<Initials>AJ</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, United States.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rai</LastName>
<ForeName>Rhitu</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Plant Pathogen Interaction, ICAR-National Institute for Plant Biotechnology, New Delhi, India.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2020</Year>
<Month>10</Month>
<Day>21</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>Switzerland</Country>
<MedlineTA>Front Microbiol</MedlineTA>
<NlmUniqueID>101548977</NlmUniqueID>
<ISSNLinking>1664-302X</ISSNLinking>
</MedlineJournalInfo>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">SWEET genes</Keyword>
<Keyword MajorTopicYN="N">bacterial blight of rice</Keyword>
<Keyword MajorTopicYN="N">single molecule real-time sequencing</Keyword>
<Keyword MajorTopicYN="N">susceptibility genes</Keyword>
<Keyword MajorTopicYN="N">transcription activator-like effectors</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
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<PubMedPubDate PubStatus="received">
<Year>2020</Year>
<Month>07</Month>
<Day>02</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2020</Year>
<Month>08</Month>
<Day>31</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2020</Year>
<Month>11</Month>
<Day>16</Day>
<Hour>8</Hour>
<Minute>47</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2020</Year>
<Month>11</Month>
<Day>17</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2020</Year>
<Month>11</Month>
<Day>17</Day>
<Hour>6</Hour>
<Minute>1</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>epublish</PublicationStatus>
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<affiliations>
<list>
<country>
<li>Inde</li>
<li>Philippines</li>
<li>Thaïlande</li>
<li>États-Unis</li>
</country>
<region>
<li>État de New York</li>
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</orgName>
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<name sortKey="Bogdanove, Adam J" sort="Bogdanove, Adam J" uniqKey="Bogdanove A" first="Adam J" last="Bogdanove">Adam J. Bogdanove</name>
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</country>
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<noRegion>
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<name sortKey="Laha, Gouri S" sort="Laha, Gouri S" uniqKey="Laha G" first="Gouri S" last="Laha">Gouri S. Laha</name>
<name sortKey="Lore, Jagjeet S" sort="Lore, Jagjeet S" uniqKey="Lore J" first="Jagjeet S" last="Lore">Jagjeet S. Lore</name>
<name sortKey="Midha, Samriti" sort="Midha, Samriti" uniqKey="Midha S" first="Samriti" last="Midha">Samriti Midha</name>
<name sortKey="Patil, Prabhu B" sort="Patil, Prabhu B" uniqKey="Patil P" first="Prabhu B" last="Patil">Prabhu B. Patil</name>
<name sortKey="Rai, Rhitu" sort="Rai, Rhitu" uniqKey="Rai R" first="Rhitu" last="Rai">Rhitu Rai</name>
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<name sortKey="Singh, Nagendra K" sort="Singh, Nagendra K" uniqKey="Singh N" first="Nagendra K" last="Singh">Nagendra K. Singh</name>
</country>
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</noRegion>
<name sortKey="Patarapuwadol, Sujin" sort="Patarapuwadol, Sujin" uniqKey="Patarapuwadol S" first="Sujin" last="Patarapuwadol">Sujin Patarapuwadol</name>
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