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Comparative Analysis Highlights Variable Genome Content of Wheat Rusts and Divergence of the Mating Loci.

Identifieur interne : 000073 ( Main/Exploration ); précédent : 000072; suivant : 000074

Comparative Analysis Highlights Variable Genome Content of Wheat Rusts and Divergence of the Mating Loci.

Auteurs : Christina A. Cuomo [États-Unis] ; Guus Bakkeren [Canada] ; Hala Badr Khalil [Canada] ; Vinay Panwar [Canada] ; David Joly [Canada] ; Rob Linning [Canada] ; Sharadha Sakthikumar [États-Unis] ; Xiao Song [Canada] ; Xian Adiconis [États-Unis] ; Lin Fan [États-Unis] ; Jonathan M. Goldberg [États-Unis] ; Joshua Z. Levin [États-Unis] ; Sarah Young [États-Unis] ; Qiandong Zeng [États-Unis] ; Yehoshua Anikster [Israël] ; Myron Bruce [États-Unis] ; Meinan Wang [États-Unis] ; Chuntao Yin [États-Unis] ; Brent Mccallum [Canada] ; Les J. Szabo [États-Unis] ; Scot Hulbert [États-Unis] ; Xianming Chen [États-Unis] ; John P. Fellers [États-Unis]

Source :

RBID : pubmed:27913634

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English descriptors

Abstract

Three members of the Puccinia genus, Pucciniatriticina (Pt), Pstriiformis f.sp. tritici (Pst), and Pgraminis f.sp. tritici (Pgt), cause the most common and often most significant foliar diseases of wheat. While similar in biology and life cycle, each species is uniquely adapted and specialized. The genomes of Pt and Pst were sequenced and compared to that of Pgt to identify common and distinguishing gene content, to determine gene variation among wheat rust pathogens, other rust fungi, and basidiomycetes, and to identify genes of significance for infection. Pt had the largest genome of the three, estimated at 135 Mb with expansion due to mobile elements and repeats encompassing 50.9% of contig bases; in comparison, repeats occupy 31.5% for Pst and 36.5% for Pgt We find all three genomes are highly heterozygous, with Pst [5.97 single nucleotide polymorphisms (SNPs)/kb] nearly twice the level detected in Pt (2.57 SNPs/kb) and that previously reported for Pgt Of 1358 predicted effectors in Pt, 784 were found expressed across diverse life cycle stages including the sexual stage. Comparison to related fungi highlighted the expansion of gene families involved in transcriptional regulation and nucleotide binding, protein modification, and carbohydrate degradation enzymes. Two allelic homeodomain pairs, HD1 and HD2, were identified in each dikaryotic Puccinia species along with three pheromone receptor (STE3) mating-type genes, two of which are likely representing allelic specificities. The HD proteins were active in a heterologous Ustilago maydis mating assay and host-induced gene silencing (HIGS) of the HD and STE3 alleles reduced wheat host infection.

DOI: 10.1534/g3.116.032797
PubMed: 27913634
PubMed Central: PMC5295586


Affiliations:


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Le document en format XML

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<name sortKey="Wang, Meinan" sort="Wang, Meinan" uniqKey="Wang M" first="Meinan" last="Wang">Meinan Wang</name>
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<name sortKey="Yin, Chuntao" sort="Yin, Chuntao" uniqKey="Yin C" first="Chuntao" last="Yin">Chuntao Yin</name>
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<name sortKey="Szabo, Les J" sort="Szabo, Les J" uniqKey="Szabo L" first="Les J" last="Szabo">Les J. Szabo</name>
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<name sortKey="Chen, Xianming" sort="Chen, Xianming" uniqKey="Chen X" first="Xianming" last="Chen">Xianming Chen</name>
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<name sortKey="Fellers, John P" sort="Fellers, John P" uniqKey="Fellers J" first="John P" last="Fellers">John P. Fellers</name>
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<nlm:affiliation>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan, Kansas 66506 cuomo@broadinstitute.org Guus.Bakkeren@agr.gc.ca john.fellers@ars.usda.gov.</nlm:affiliation>
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<title xml:lang="en">Comparative Analysis Highlights Variable Genome Content of Wheat Rusts and Divergence of the Mating Loci.</title>
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<name sortKey="Sakthikumar, Sharadha" sort="Sakthikumar, Sharadha" uniqKey="Sakthikumar S" first="Sharadha" last="Sakthikumar">Sharadha Sakthikumar</name>
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<name sortKey="Song, Xiao" sort="Song, Xiao" uniqKey="Song X" first="Xiao" last="Song">Xiao Song</name>
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<name sortKey="Fan, Lin" sort="Fan, Lin" uniqKey="Fan L" first="Lin" last="Fan">Lin Fan</name>
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<nlm:affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</nlm:affiliation>
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<region type="state">Massachusetts</region>
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<name sortKey="Goldberg, Jonathan M" sort="Goldberg, Jonathan M" uniqKey="Goldberg J" first="Jonathan M" last="Goldberg">Jonathan M. Goldberg</name>
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<nlm:affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</nlm:affiliation>
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<name sortKey="Levin, Joshua Z" sort="Levin, Joshua Z" uniqKey="Levin J" first="Joshua Z" last="Levin">Joshua Z. Levin</name>
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<nlm:affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Massachusetts</region>
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<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
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<name sortKey="Young, Sarah" sort="Young, Sarah" uniqKey="Young S" first="Sarah" last="Young">Sarah Young</name>
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<nlm:affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
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<region type="state">Massachusetts</region>
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<author>
<name sortKey="Zeng, Qiandong" sort="Zeng, Qiandong" uniqKey="Zeng Q" first="Qiandong" last="Zeng">Qiandong Zeng</name>
<affiliation wicri:level="2">
<nlm:affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Massachusetts</region>
</placeName>
<wicri:cityArea>Broad Institute of MIT and Harvard, Cambridge</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Anikster, Yehoshua" sort="Anikster, Yehoshua" uniqKey="Anikster Y" first="Yehoshua" last="Anikster">Yehoshua Anikster</name>
<affiliation wicri:level="1">
<nlm:affiliation>The Institute for Cereal Crops Improvement, Tel Aviv University, Ramat Aviv 69978, Israel.</nlm:affiliation>
<country xml:lang="fr">Israël</country>
<wicri:regionArea>The Institute for Cereal Crops Improvement, Tel Aviv University, Ramat Aviv 69978</wicri:regionArea>
<wicri:noRegion>Ramat Aviv 69978</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Bruce, Myron" sort="Bruce, Myron" uniqKey="Bruce M" first="Myron" last="Bruce">Myron Bruce</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan, Kansas 66506.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kansas</region>
</placeName>
<wicri:cityArea>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Wang, Meinan" sort="Wang, Meinan" uniqKey="Wang M" first="Meinan" last="Wang">Meinan Wang</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Washington (État)</region>
</placeName>
<wicri:cityArea>Department of Plant Pathology, Washington State University, Pullman</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Yin, Chuntao" sort="Yin, Chuntao" uniqKey="Yin C" first="Chuntao" last="Yin">Chuntao Yin</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Washington (État)</region>
</placeName>
<wicri:cityArea>Department of Plant Pathology, Washington State University, Pullman</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Mccallum, Brent" sort="Mccallum, Brent" uniqKey="Mccallum B" first="Brent" last="Mccallum">Brent Mccallum</name>
<affiliation wicri:level="1">
<nlm:affiliation>Agriculture and Agri-Food Canada, Morden Research and Development Centre, Manitoba R6M 1Y5, Canada.</nlm:affiliation>
<country xml:lang="fr">Canada</country>
<wicri:regionArea>Agriculture and Agri-Food Canada, Morden Research and Development Centre, Manitoba R6M 1Y5</wicri:regionArea>
<wicri:noRegion>Manitoba R6M 1Y5</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Szabo, Les J" sort="Szabo, Les J" uniqKey="Szabo L" first="Les J" last="Szabo">Les J. Szabo</name>
<affiliation wicri:level="2">
<nlm:affiliation>Cereal Disease Laboratory, United States Department of Agriculture-Agricultural Research Service, St. Paul, Minnesota 55108.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Minnesota</region>
</placeName>
<wicri:cityArea>Cereal Disease Laboratory, United States Department of Agriculture-Agricultural Research Service, St. Paul</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Hulbert, Scot" sort="Hulbert, Scot" uniqKey="Hulbert S" first="Scot" last="Hulbert">Scot Hulbert</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Washington (État)</region>
</placeName>
<wicri:cityArea>Department of Plant Pathology, Washington State University, Pullman</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Chen, Xianming" sort="Chen, Xianming" uniqKey="Chen X" first="Xianming" last="Chen">Xianming Chen</name>
<affiliation wicri:level="2">
<nlm:affiliation>Wheat Health, Genetics, and Quality Research Unit, United States Department of Agriculture-Agricultural Research Service, Pullman, Washington 99164.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Washington (État)</region>
</placeName>
<wicri:cityArea>Wheat Health, Genetics, and Quality Research Unit, United States Department of Agriculture-Agricultural Research Service, Pullman</wicri:cityArea>
</affiliation>
</author>
<author>
<name sortKey="Fellers, John P" sort="Fellers, John P" uniqKey="Fellers J" first="John P" last="Fellers">John P. Fellers</name>
<affiliation wicri:level="2">
<nlm:affiliation>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan, Kansas 66506 cuomo@broadinstitute.org Guus.Bakkeren@agr.gc.ca john.fellers@ars.usda.gov.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<placeName>
<region type="state">Kansas</region>
</placeName>
<wicri:cityArea>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan</wicri:cityArea>
</affiliation>
</author>
</analytic>
<series>
<title level="j">G3 (Bethesda, Md.)</title>
<idno type="eISSN">2160-1836</idno>
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<term>Basidiomycota (genetics)</term>
<term>Basidiomycota (pathogenicity)</term>
<term>Genes, Mating Type, Fungal (genetics)</term>
<term>Genome, Fungal (MeSH)</term>
<term>Life Cycle Stages (genetics)</term>
<term>Molecular Sequence Annotation (MeSH)</term>
<term>Plant Diseases (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Polymorphism, Single Nucleotide (MeSH)</term>
<term>Receptors, Pheromone (genetics)</term>
<term>Sequence Analysis, DNA (MeSH)</term>
<term>Triticum (genetics)</term>
<term>Triticum (growth & development)</term>
<term>Triticum (microbiology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de séquence d'ADN (MeSH)</term>
<term>Annotation de séquence moléculaire (MeSH)</term>
<term>Basidiomycota (génétique)</term>
<term>Basidiomycota (pathogénicité)</term>
<term>Gènes fongiques du type conjugant (génétique)</term>
<term>Génome fongique (MeSH)</term>
<term>Maladies des plantes (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Polymorphisme de nucléotide simple (MeSH)</term>
<term>Récepteurs aux phéromones (génétique)</term>
<term>Triticum (croissance et développement)</term>
<term>Triticum (génétique)</term>
<term>Triticum (microbiologie)</term>
<term>Étapes du cycle de vie (génétique)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Receptors, Pheromone</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Basidiomycota</term>
<term>Genes, Mating Type, Fungal</term>
<term>Life Cycle Stages</term>
<term>Plant Diseases</term>
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Basidiomycota</term>
<term>Gènes fongiques du type conjugant</term>
<term>Maladies des plantes</term>
<term>Récepteurs aux phéromones</term>
<term>Triticum</term>
<term>Étapes du cycle de vie</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
<term>Triticum</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogenicity" xml:lang="en">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" qualifier="pathogénicité" xml:lang="fr">
<term>Basidiomycota</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Genome, Fungal</term>
<term>Molecular Sequence Annotation</term>
<term>Polymorphism, Single Nucleotide</term>
<term>Sequence Analysis, DNA</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de séquence d'ADN</term>
<term>Annotation de séquence moléculaire</term>
<term>Génome fongique</term>
<term>Polymorphisme de nucléotide simple</term>
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<front>
<div type="abstract" xml:lang="en">Three members of the
<i>Puccinia</i>
genus,
<i>Puccinia</i>
<i>triticina</i>
(
<i>Pt</i>
),
<i>P</i>
<i>striiformis</i>
f.sp.
<i>tritici</i>
(
<i>Pst</i>
), and
<i>P</i>
<i>graminis</i>
f.sp.
<i>tritici</i>
(
<i>Pgt</i>
), cause the most common and often most significant foliar diseases of wheat. While similar in biology and life cycle, each species is uniquely adapted and specialized. The genomes of
<i>Pt</i>
and
<i>Pst</i>
were sequenced and compared to that of
<i>Pgt</i>
to identify common and distinguishing gene content, to determine gene variation among wheat rust pathogens, other rust fungi, and basidiomycetes, and to identify genes of significance for infection.
<i>Pt</i>
had the largest genome of the three, estimated at 135 Mb with expansion due to mobile elements and repeats encompassing 50.9% of contig bases; in comparison, repeats occupy 31.5% for
<i>Pst</i>
and 36.5% for
<i>Pgt</i>
We find all three genomes are highly heterozygous, with
<i>Pst</i>
[5.97 single nucleotide polymorphisms (SNPs)/kb] nearly twice the level detected in
<i>Pt</i>
(2.57 SNPs/kb) and that previously reported for
<i>Pgt</i>
Of 1358 predicted effectors in
<i>Pt</i>
, 784 were found expressed across diverse life cycle stages including the sexual stage. Comparison to related fungi highlighted the expansion of gene families involved in transcriptional regulation and nucleotide binding, protein modification, and carbohydrate degradation enzymes. Two allelic homeodomain pairs, HD1 and HD2, were identified in each dikaryotic
<i>Puccinia</i>
species along with three pheromone receptor (
<i>STE3</i>
) mating-type genes, two of which are likely representing allelic specificities. The HD proteins were active in a heterologous
<i>Ustilago maydis</i>
mating assay and host-induced gene silencing (HIGS) of the HD and
<i>STE3</i>
alleles reduced wheat host infection.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">27913634</PMID>
<DateCompleted>
<Year>2017</Year>
<Month>11</Month>
<Day>22</Day>
</DateCompleted>
<DateRevised>
<Year>2020</Year>
<Month>03</Month>
<Day>06</Day>
</DateRevised>
<Article PubModel="Electronic">
<Journal>
<ISSN IssnType="Electronic">2160-1836</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>7</Volume>
<Issue>2</Issue>
<PubDate>
<Year>2017</Year>
<Month>02</Month>
<Day>09</Day>
</PubDate>
</JournalIssue>
<Title>G3 (Bethesda, Md.)</Title>
<ISOAbbreviation>G3 (Bethesda)</ISOAbbreviation>
</Journal>
<ArticleTitle>Comparative Analysis Highlights Variable Genome Content of Wheat Rusts and Divergence of the Mating Loci.</ArticleTitle>
<Pagination>
<MedlinePgn>361-376</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1534/g3.116.032797</ELocationID>
<Abstract>
<AbstractText>Three members of the
<i>Puccinia</i>
genus,
<i>Puccinia</i>
<i>triticina</i>
(
<i>Pt</i>
),
<i>P</i>
<i>striiformis</i>
f.sp.
<i>tritici</i>
(
<i>Pst</i>
), and
<i>P</i>
<i>graminis</i>
f.sp.
<i>tritici</i>
(
<i>Pgt</i>
), cause the most common and often most significant foliar diseases of wheat. While similar in biology and life cycle, each species is uniquely adapted and specialized. The genomes of
<i>Pt</i>
and
<i>Pst</i>
were sequenced and compared to that of
<i>Pgt</i>
to identify common and distinguishing gene content, to determine gene variation among wheat rust pathogens, other rust fungi, and basidiomycetes, and to identify genes of significance for infection.
<i>Pt</i>
had the largest genome of the three, estimated at 135 Mb with expansion due to mobile elements and repeats encompassing 50.9% of contig bases; in comparison, repeats occupy 31.5% for
<i>Pst</i>
and 36.5% for
<i>Pgt</i>
We find all three genomes are highly heterozygous, with
<i>Pst</i>
[5.97 single nucleotide polymorphisms (SNPs)/kb] nearly twice the level detected in
<i>Pt</i>
(2.57 SNPs/kb) and that previously reported for
<i>Pgt</i>
Of 1358 predicted effectors in
<i>Pt</i>
, 784 were found expressed across diverse life cycle stages including the sexual stage. Comparison to related fungi highlighted the expansion of gene families involved in transcriptional regulation and nucleotide binding, protein modification, and carbohydrate degradation enzymes. Two allelic homeodomain pairs, HD1 and HD2, were identified in each dikaryotic
<i>Puccinia</i>
species along with three pheromone receptor (
<i>STE3</i>
) mating-type genes, two of which are likely representing allelic specificities. The HD proteins were active in a heterologous
<i>Ustilago maydis</i>
mating assay and host-induced gene silencing (HIGS) of the HD and
<i>STE3</i>
alleles reduced wheat host infection.</AbstractText>
<CopyrightInformation>Copyright © 2017 Cuomo et al.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Cuomo</LastName>
<ForeName>Christina A</ForeName>
<Initials>CA</Initials>
<Identifier Source="ORCID">0000-0002-5778-960X</Identifier>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142 cuomo@broadinstitute.org Guus.Bakkeren@agr.gc.ca john.fellers@ars.usda.gov.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bakkeren</LastName>
<ForeName>Guus</ForeName>
<Initials>G</Initials>
<Identifier Source="ORCID">0000-0002-3065-6989</Identifier>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Summerland Research and Development Centre, British Columbia V0H 1Z0, Canada cuomo@broadinstitute.org Guus.Bakkeren@agr.gc.ca john.fellers@ars.usda.gov.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Khalil</LastName>
<ForeName>Hala Badr</ForeName>
<Initials>HB</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Summerland Research and Development Centre, British Columbia V0H 1Z0, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Panwar</LastName>
<ForeName>Vinay</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Morden Research and Development Centre, Manitoba R6M 1Y5, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Joly</LastName>
<ForeName>David</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Summerland Research and Development Centre, British Columbia V0H 1Z0, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Linning</LastName>
<ForeName>Rob</ForeName>
<Initials>R</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Summerland Research and Development Centre, British Columbia V0H 1Z0, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sakthikumar</LastName>
<ForeName>Sharadha</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Song</LastName>
<ForeName>Xiao</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Summerland Research and Development Centre, British Columbia V0H 1Z0, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Adiconis</LastName>
<ForeName>Xian</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fan</LastName>
<ForeName>Lin</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Goldberg</LastName>
<ForeName>Jonathan M</ForeName>
<Initials>JM</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Levin</LastName>
<ForeName>Joshua Z</ForeName>
<Initials>JZ</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Young</LastName>
<ForeName>Sarah</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Zeng</LastName>
<ForeName>Qiandong</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Anikster</LastName>
<ForeName>Yehoshua</ForeName>
<Initials>Y</Initials>
<AffiliationInfo>
<Affiliation>The Institute for Cereal Crops Improvement, Tel Aviv University, Ramat Aviv 69978, Israel.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bruce</LastName>
<ForeName>Myron</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan, Kansas 66506.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Meinan</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yin</LastName>
<ForeName>Chuntao</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McCallum</LastName>
<ForeName>Brent</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Agriculture and Agri-Food Canada, Morden Research and Development Centre, Manitoba R6M 1Y5, Canada.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Szabo</LastName>
<ForeName>Les J</ForeName>
<Initials>LJ</Initials>
<AffiliationInfo>
<Affiliation>Cereal Disease Laboratory, United States Department of Agriculture-Agricultural Research Service, St. Paul, Minnesota 55108.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hulbert</LastName>
<ForeName>Scot</ForeName>
<Initials>S</Initials>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Washington State University, Pullman, Washington 99164.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Chen</LastName>
<ForeName>Xianming</ForeName>
<Initials>X</Initials>
<AffiliationInfo>
<Affiliation>Wheat Health, Genetics, and Quality Research Unit, United States Department of Agriculture-Agricultural Research Service, Pullman, Washington 99164.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Fellers</LastName>
<ForeName>John P</ForeName>
<Initials>JP</Initials>
<Identifier Source="ORCID">0000-0003-3872-2909</Identifier>
<AffiliationInfo>
<Affiliation>Department of Plant Pathology, Hard Winter Wheat Genetics Research Unit, United States Department of Agriculture-Agricultural Research Service, Manhattan, Kansas 66506 cuomo@broadinstitute.org Guus.Bakkeren@agr.gc.ca john.fellers@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>2017</Year>
<Month>02</Month>
<Day>09</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>G3 (Bethesda)</MedlineTA>
<NlmUniqueID>101566598</NlmUniqueID>
<ISSNLinking>2160-1836</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D043563">Receptors, Pheromone</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000472" MajorTopicYN="N">pathogenicity</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D049770" MajorTopicYN="N">Genes, Mating Type, Fungal</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016681" MajorTopicYN="Y">Genome, Fungal</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008018" MajorTopicYN="N">Life Cycle Stages</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D058977" MajorTopicYN="N">Molecular Sequence Annotation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010935" MajorTopicYN="N">Plant Diseases</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020641" MajorTopicYN="N">Polymorphism, Single Nucleotide</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D043563" MajorTopicYN="N">Receptors, Pheromone</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
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