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Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes

Identifieur interne : 000723 ( Pmc/Checkpoint ); précédent : 000722; suivant : 000724

Comparative genomics of Australian isolates of the wheat stem rust pathogen Puccinia graminis f. sp. tritici reveals extensive polymorphism in candidate effector genes

Auteurs : Narayana M. Upadhyaya [Australie] ; Diana P. Garnica [Australie] ; Haydar Karaoglu [Australie] ; Jana Sperschneider [Australie] ; Adnane Nemri [Australie] ; Bo Xu [Australie] ; Rohit Mago [Australie] ; Christina A. Cuomo [États-Unis] ; John P. Rathjen [Australie] ; Robert F. Park [Australie] ; Jeffrey G. Ellis [Australie] ; Peter N. Dodds [Australie]

Source :

RBID : PMC:4288056

Abstract

The wheat stem rust fungus Puccinia graminis f. sp. tritici (Pgt) is one of the most destructive pathogens of wheat. In this study, a draft genome was built for a founder Australian Pgt isolate of pathotype (pt.) 21-0 (collected in 1954) by next generation DNA sequencing. A combination of reference-based assembly using the genome of the previously sequenced American Pgt isolate CDL 75-36-700-3 (p7a) and de novo assembly were performed resulting in a 92 Mbp reference genome for Pgt isolate 21-0. Approximately 13 Mbp of de novo assembled sequence in this genome is not present in the p7a reference assembly. This novel sequence is not specific to 21-0 as it is also present in three other Pgt rust isolates of independent origin. The new reference genome was subsequently used to build a pan-genome based on five Australian Pgt isolates. Transcriptomes from germinated urediniospores and haustoria were separately assembled for pt. 21-0 and comparison of gene expression profiles showed differential expression in ∼10% of the genes each in germinated spores and haustoria. A total of 1,924 secreted proteins were predicted from the 21-0 transcriptome, of which 520 were classified as haustorial secreted proteins (HSPs). Comparison of 21-0 with two presumed clonal field derivatives of this lineage (collected in 1982 and 1984) that had evolved virulence on four additional resistance genes (Sr5, Sr11, Sr27, SrSatu) identified mutations in 25 HSP effector candidates. Some of these mutations could explain their novel virulence phenotypes.


Url:
DOI: 10.3389/fpls.2014.00759
PubMed: 25620970
PubMed Central: 4288056


Affiliations:


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PMC:4288056

Le document en format XML

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<italic>Puccinia graminis</italic>
f. sp.
<italic>tritici</italic>
reveals extensive polymorphism in candidate effector genes</title>
<author>
<name sortKey="Upadhyaya, Narayana M" sort="Upadhyaya, Narayana M" uniqKey="Upadhyaya N" first="Narayana M." last="Upadhyaya">Narayana M. Upadhyaya</name>
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<name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A." last="Cuomo">Christina A. Cuomo</name>
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</nlm:aff>
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<wicri:regionArea></wicri:regionArea>
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<name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N." last="Dodds">Peter N. Dodds</name>
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<p>The wheat stem rust fungus
<italic>Puccinia graminis</italic>
f. sp.
<italic>tritici</italic>
(
<italic>Pgt</italic>
) is one of the most destructive pathogens of wheat. In this study, a draft genome was built for a founder Australian
<italic>Pgt</italic>
isolate of pathotype (pt.) 21-0 (collected in 1954) by next generation DNA sequencing. A combination of reference-based assembly using the genome of the previously sequenced American
<italic>Pgt</italic>
isolate CDL 75-36-700-3 (p7a) and
<italic>de novo</italic>
assembly were performed resulting in a 92 Mbp reference genome for
<italic>Pgt</italic>
isolate 21-0. Approximately 13 Mbp of
<italic>de novo</italic>
assembled sequence in this genome is not present in the p7a reference assembly. This novel sequence is not specific to 21-0 as it is also present in three other
<italic>Pgt</italic>
rust isolates of independent origin. The new reference genome was subsequently used to build a pan-genome based on five Australian
<italic>Pgt</italic>
isolates. Transcriptomes from germinated urediniospores and haustoria were separately assembled for pt. 21-0 and comparison of gene expression profiles showed differential expression in ∼10% of the genes each in germinated spores and haustoria. A total of 1,924 secreted proteins were predicted from the 21-0 transcriptome, of which 520 were classified as haustorial secreted proteins (HSPs). Comparison of 21-0 with two presumed clonal field derivatives of this lineage (collected in 1982 and 1984) that had evolved virulence on four additional resistance genes (
<italic>Sr5</italic>
,
<italic>Sr11</italic>
,
<italic>Sr27</italic>
,
<italic>SrSatu</italic>
) identified mutations in 25 HSP effector candidates. Some of these mutations could explain their novel virulence phenotypes.</p>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id>
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<journal-title>Frontiers in Plant Science</journal-title>
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<issn pub-type="epub">1664-462X</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">25620970</article-id>
<article-id pub-id-type="pmc">4288056</article-id>
<article-id pub-id-type="doi">10.3389/fpls.2014.00759</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Plant Science</subject>
<subj-group>
<subject>Original Research Article</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Comparative genomics of Australian isolates of the wheat stem rust pathogen
<italic>Puccinia graminis</italic>
f. sp.
<italic>tritici</italic>
reveals extensive polymorphism in candidate effector genes</article-title>
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<contrib-group>
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<name>
<surname>Upadhyaya</surname>
<given-names>Narayana M.</given-names>
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<xref ref-type="aff" rid="aff1">
<sup>1</sup>
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<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/108904"></uri>
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<contrib contrib-type="author">
<name>
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<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/188732"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Karaoglu</surname>
<given-names>Haydar</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Sperschneider</surname>
<given-names>Jana</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/163492"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nemri</surname>
<given-names>Adnane</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/107927"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Xu</surname>
<given-names>Bo</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/188485"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mago</surname>
<given-names>Rohit</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/188476"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Cuomo</surname>
<given-names>Christina A.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>4</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/115286"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rathjen</surname>
<given-names>John P.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/27223"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Park</surname>
<given-names>Robert F.</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/185715"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ellis</surname>
<given-names>Jeffrey G.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/169013"></uri>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dodds</surname>
<given-names>Peter N.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/28215"></uri>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Agriculture Flagship, Commonwealth Scientific and Industrial Research Organization</institution>
<country>Canberra, ACT, Australia</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Research School of Biology, Australian National University</institution>
<country>Canberra, ACT, Australia</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Plant Breeding Institute, Faculty of Agriculture and Environment, The University of Sydney</institution>
<country>Narellan, NSW, Australia</country>
</aff>
<aff id="aff4">
<sup>4</sup>
<institution>Genome Sequencing and Analysis Program, Broad Institute of MIT and Harvard</institution>
<country>Cambridge, MA, USA</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by:
<italic>David L. Joly, Université de Moncton, Canada</italic>
</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by:
<italic>Nils Rostoks, University of Latvia, Latvia; Nicolas Feau, University of British Columbia, Canada</italic>
</p>
</fn>
<corresp id="fn001">*Correspondence:
<italic>Peter N. Dodds and Narayana M. Upadhyaya, Agriculture Flagship, Commonwealth Scientific and Industrial Research Organization, Cnr. Barry Drive and Clunies Ross Street, Black Mountain, Acton, Canberra, ACT 2601, Australia e-mail:
<email xlink:type="simple">peter.dodds@csiro.au</email>
;
<email xlink:type="simple">Narayana.upadhyaya@csiro.au</email>
</italic>
</corresp>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Plant-Microbe Interaction, a section of the journal Frontiers in Plant Science.</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>08</day>
<month>1</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection">
<year>2014</year>
</pub-date>
<volume>5</volume>
<elocation-id>759</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>5</month>
<year>2014</year>
</date>
<date date-type="accepted">
<day>09</day>
<month>12</month>
<year>2014</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2015 Upadhyaya, Garnica, Karaoglu, Sperschneider, Nemri, Xu, Mago, Cuomo, Rathjen, Park, Ellis and Dodds.</copyright-statement>
<copyright-year>2015</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/">
<license-p> This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract>
<p>The wheat stem rust fungus
<italic>Puccinia graminis</italic>
f. sp.
<italic>tritici</italic>
(
<italic>Pgt</italic>
) is one of the most destructive pathogens of wheat. In this study, a draft genome was built for a founder Australian
<italic>Pgt</italic>
isolate of pathotype (pt.) 21-0 (collected in 1954) by next generation DNA sequencing. A combination of reference-based assembly using the genome of the previously sequenced American
<italic>Pgt</italic>
isolate CDL 75-36-700-3 (p7a) and
<italic>de novo</italic>
assembly were performed resulting in a 92 Mbp reference genome for
<italic>Pgt</italic>
isolate 21-0. Approximately 13 Mbp of
<italic>de novo</italic>
assembled sequence in this genome is not present in the p7a reference assembly. This novel sequence is not specific to 21-0 as it is also present in three other
<italic>Pgt</italic>
rust isolates of independent origin. The new reference genome was subsequently used to build a pan-genome based on five Australian
<italic>Pgt</italic>
isolates. Transcriptomes from germinated urediniospores and haustoria were separately assembled for pt. 21-0 and comparison of gene expression profiles showed differential expression in ∼10% of the genes each in germinated spores and haustoria. A total of 1,924 secreted proteins were predicted from the 21-0 transcriptome, of which 520 were classified as haustorial secreted proteins (HSPs). Comparison of 21-0 with two presumed clonal field derivatives of this lineage (collected in 1982 and 1984) that had evolved virulence on four additional resistance genes (
<italic>Sr5</italic>
,
<italic>Sr11</italic>
,
<italic>Sr27</italic>
,
<italic>SrSatu</italic>
) identified mutations in 25 HSP effector candidates. Some of these mutations could explain their novel virulence phenotypes.</p>
</abstract>
<kwd-group>
<kwd>haustoria</kwd>
<kwd>avirulence</kwd>
<kwd>resistance</kwd>
<kwd>secreted proteins</kwd>
<kwd>effectors</kwd>
</kwd-group>
<counts>
<fig-count count="5"></fig-count>
<table-count count="3"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="51"></ref-count>
<page-count count="13"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations>
<list>
<country>
<li>Australie</li>
<li>États-Unis</li>
</country>
</list>
<tree>
<country name="Australie">
<noRegion>
<name sortKey="Upadhyaya, Narayana M" sort="Upadhyaya, Narayana M" uniqKey="Upadhyaya N" first="Narayana M." last="Upadhyaya">Narayana M. Upadhyaya</name>
</noRegion>
<name sortKey="Dodds, Peter N" sort="Dodds, Peter N" uniqKey="Dodds P" first="Peter N." last="Dodds">Peter N. Dodds</name>
<name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G." last="Ellis">Jeffrey G. Ellis</name>
<name sortKey="Garnica, Diana P" sort="Garnica, Diana P" uniqKey="Garnica D" first="Diana P." last="Garnica">Diana P. Garnica</name>
<name sortKey="Karaoglu, Haydar" sort="Karaoglu, Haydar" uniqKey="Karaoglu H" first="Haydar" last="Karaoglu">Haydar Karaoglu</name>
<name sortKey="Mago, Rohit" sort="Mago, Rohit" uniqKey="Mago R" first="Rohit" last="Mago">Rohit Mago</name>
<name sortKey="Nemri, Adnane" sort="Nemri, Adnane" uniqKey="Nemri A" first="Adnane" last="Nemri">Adnane Nemri</name>
<name sortKey="Park, Robert F" sort="Park, Robert F" uniqKey="Park R" first="Robert F." last="Park">Robert F. Park</name>
<name sortKey="Rathjen, John P" sort="Rathjen, John P" uniqKey="Rathjen J" first="John P." last="Rathjen">John P. Rathjen</name>
<name sortKey="Sperschneider, Jana" sort="Sperschneider, Jana" uniqKey="Sperschneider J" first="Jana" last="Sperschneider">Jana Sperschneider</name>
<name sortKey="Xu, Bo" sort="Xu, Bo" uniqKey="Xu B" first="Bo" last="Xu">Bo Xu</name>
</country>
<country name="États-Unis">
<noRegion>
<name sortKey="Cuomo, Christina A" sort="Cuomo, Christina A" uniqKey="Cuomo C" first="Christina A." last="Cuomo">Christina A. Cuomo</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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