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<title xml:lang="en">Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity</title>
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<name sortKey="Anderson, Peter A" sort="Anderson, Peter A" uniqKey="Anderson P" first="Peter A." last="Anderson">Peter A. Anderson</name>
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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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<name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name>
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<nlm:aff id="aff1">School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience,
<institution>University of Queensland</institution>
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<title xml:lang="en" level="a" type="main">Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity</title>
<author>
<name sortKey="Ve, Thomas" sort="Ve, Thomas" uniqKey="Ve T" first="Thomas" last="Ve">Thomas Ve</name>
<affiliation>
<nlm:aff id="aff1">School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience,
<institution>University of Queensland</institution>
, Brisbane, QLD 4072,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Williams, Simon J" sort="Williams, Simon J" uniqKey="Williams S" first="Simon J." last="Williams">Simon J. Williams</name>
<affiliation>
<nlm:aff id="aff1">School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience,
<institution>University of Queensland</institution>
, Brisbane, QLD 4072,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Catanzariti, Ann Maree" sort="Catanzariti, Ann Maree" uniqKey="Catanzariti A" first="Ann-Maree" last="Catanzariti">Ann-Maree Catanzariti</name>
<affiliation>
<nlm:aff id="aff2">Plant Science Division, Research School of Biology,
<institution>Australian National University</institution>
, Canberra, ACT 0200,
<country>Australia</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rafiqi, Maryam" sort="Rafiqi, Maryam" uniqKey="Rafiqi M" first="Maryam" last="Rafiqi">Maryam Rafiqi</name>
<affiliation>
<nlm:aff id="aff2">Plant Science Division, Research School of Biology,
<institution>Australian National University</institution>
, Canberra, ACT 0200,
<country>Australia</country>
;</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="aff3">Institute of Phytopathology and Applied Zoology, Research Centre for BioSystems, Land Use, and Nutrition,
<institution>Justus Liebig University</institution>
, 35390 Giessen,
<country>Germany</country>
;</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Rahman, Motiur" sort="Rahman, Motiur" uniqKey="Rahman M" first="Motiur" last="Rahman">Motiur Rahman</name>
<affiliation>
<nlm:aff wicri:cut="; and" id="aff4">School of Biological Sciences,
<institution>Flinders University</institution>
, Adelaide, SA 5001,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
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<name sortKey="Ellis, Jeffrey G" sort="Ellis, Jeffrey G" uniqKey="Ellis J" first="Jeffrey G." last="Ellis">Jeffrey G. Ellis</name>
<affiliation>
<nlm:aff id="aff5">
<institution>Commonwealth Scientific and Industrial Research Organization Plant Industry</institution>
, Canberra, ACT 2601,
<country>Australia</country>
</nlm:aff>
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<name sortKey="Hardham, Adrienne R" sort="Hardham, Adrienne R" uniqKey="Hardham A" first="Adrienne R." last="Hardham">Adrienne R. Hardham</name>
<affiliation>
<nlm:aff id="aff2">Plant Science Division, Research School of Biology,
<institution>Australian National University</institution>
, Canberra, ACT 0200,
<country>Australia</country>
;</nlm:aff>
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<name sortKey="Jones, David A" sort="Jones, David A" uniqKey="Jones D" first="David A." last="Jones">David A. Jones</name>
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<nlm:aff id="aff2">Plant Science Division, Research School of Biology,
<institution>Australian National University</institution>
, Canberra, ACT 0200,
<country>Australia</country>
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<affiliation>
<nlm:aff wicri:cut="; and" id="aff4">School of Biological Sciences,
<institution>Flinders University</institution>
, Adelaide, SA 5001,
<country>Australia</country>
</nlm:aff>
</affiliation>
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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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<nlm:aff id="aff5">
<institution>Commonwealth Scientific and Industrial Research Organization Plant Industry</institution>
, Canberra, ACT 2601,
<country>Australia</country>
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<name sortKey="Kobe, Bostjan" sort="Kobe, Bostjan" uniqKey="Kobe B" first="Bostjan" last="Kobe">Bostjan Kobe</name>
<affiliation>
<nlm:aff id="aff1">School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience,
<institution>University of Queensland</institution>
, Brisbane, QLD 4072,
<country>Australia</country>
;</nlm:aff>
</affiliation>
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<series>
<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
<imprint>
<date when="2013">2013</date>
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<front>
<div type="abstract" xml:lang="en">
<title>Significance</title>
<p>Fungal and oomycete pathogens cause devastating diseases in crop plants and facilitate infection by delivering effector molecules into the plant cell. The secreted effector protein AvrM from flax rust, a fungal pathogen that infects flax plants, internalizes into host cells in the absence of the pathogen, binds to phosphoinositides, and is recognized directly by the resistance protein M in flax to initiate effector-triggered immunity. We describe the crystal structure of AvrM and identify functionally important surface regions in the protein, which advances our understanding of the molecular mechanisms underlying how effectors enter host cells and how they are detected by the plant immune system.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group>
<journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
<publisher>
<publisher-name>National Academy of Sciences</publisher-name>
</publisher>
</journal-meta>
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<article-id pub-id-type="pmid">24101475</article-id>
<article-id pub-id-type="pmc">3808616</article-id>
<article-id pub-id-type="publisher-id">201307614</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1307614110</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Plant Biology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity</article-title>
<alt-title alt-title-type="short">Structure of the flax-rust effector AvrM</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Ve</surname>
<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Williams</surname>
<given-names>Simon J.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Catanzariti</surname>
<given-names>Ann-Maree</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rafiqi</surname>
<given-names>Maryam</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Rahman</surname>
<given-names>Motiur</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Ellis</surname>
<given-names>Jeffrey G.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hardham</surname>
<given-names>Adrienne R.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jones</surname>
<given-names>David A.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Anderson</surname>
<given-names>Peter A.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Dodds</surname>
<given-names>Peter N.</given-names>
</name>
<xref ref-type="aff" rid="aff5">
<sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kobe</surname>
<given-names>Bostjan</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>1</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
School of Chemistry and Molecular Biosciences, Australian Infectious Diseases Research Centre and Institute for Molecular Bioscience,
<institution>University of Queensland</institution>
, Brisbane, QLD 4072,
<country>Australia</country>
;</aff>
<aff id="aff2">
<sup>b</sup>
Plant Science Division, Research School of Biology,
<institution>Australian National University</institution>
, Canberra, ACT 0200,
<country>Australia</country>
;</aff>
<aff id="aff3">
<sup>c</sup>
Institute of Phytopathology and Applied Zoology, Research Centre for BioSystems, Land Use, and Nutrition,
<institution>Justus Liebig University</institution>
, 35390 Giessen,
<country>Germany</country>
;</aff>
<aff id="aff4">
<sup>d</sup>
School of Biological Sciences,
<institution>Flinders University</institution>
, Adelaide, SA 5001,
<country>Australia</country>
; and</aff>
<aff id="aff5">
<sup>e</sup>
<institution>Commonwealth Scientific and Industrial Research Organization Plant Industry</institution>
, Canberra, ACT 2601,
<country>Australia</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>1</sup>
To whom correspondence should be addressed. E-mail:
<email>b.kobe@uq.edu.au</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Brian J. Staskawicz, University of California, Berkeley, CA, and approved September 14, 2013 (received for review April 23, 2013)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: T.V., S.J.W., A.-M.C., M. Rafiqi, J.G.E., A.R.H., D.A.J., P.A.A., P.N.D., and B.K. designed research; T.V., S.J.W., A.-M.C., and M. Rahman performed research; T.V., S.J.W., A.-M.C., M. Rafiqi, P.A.A., P.N.D., and B.K. analyzed data; and T.V. and B.K. wrote the paper.</p>
</fn>
<fn fn-type="conflict">
<p>The authors declare no conflict of interest.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>22</day>
<month>10</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>7</day>
<month>10</month>
<year>2013</year>
</pub-date>
<volume>110</volume>
<issue>43</issue>
<fpage>17594</fpage>
<lpage>17599</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201307614.pdf"></self-uri>
<abstract abstract-type="executive-summary">
<title>Significance</title>
<p>Fungal and oomycete pathogens cause devastating diseases in crop plants and facilitate infection by delivering effector molecules into the plant cell. The secreted effector protein AvrM from flax rust, a fungal pathogen that infects flax plants, internalizes into host cells in the absence of the pathogen, binds to phosphoinositides, and is recognized directly by the resistance protein M in flax to initiate effector-triggered immunity. We describe the crystal structure of AvrM and identify functionally important surface regions in the protein, which advances our understanding of the molecular mechanisms underlying how effectors enter host cells and how they are detected by the plant immune system.</p>
</abstract>
<abstract>
<p>Fungal and oomycete pathogens cause some of the most devastating diseases in crop plants, and facilitate infection by delivering a large number of effector molecules into the plant cell. AvrM is a secreted effector protein from flax rust (
<italic>Melampsora lini</italic>
) that can internalize into plant cells in the absence of the pathogen, binds to phosphoinositides (PIPs), and is recognized directly by the resistance protein M in flax (
<italic>Linum usitatissimum</italic>
), resulting in effector-triggered immunity. We determined the crystal structures of two naturally occurring variants of AvrM, AvrM-A and avrM, and both reveal an L-shaped fold consisting of a tandem duplicated four-helix motif, which displays similarity to the WY domain core in oomycete effectors. In the crystals, both AvrM variants form a dimer with an unusual nonglobular shape. Our functional analysis of AvrM reveals that a hydrophobic surface patch conserved between both variants is required for internalization into plant cells, whereas the C-terminal coiled-coil domain mediates interaction with M. AvrM binding to PIPs is dependent on positive surface charges, and mutations that abrogate PIP binding have no significant effect on internalization, suggesting that AvrM binding to PIPs is not essential for transport of AvrM across the plant membrane. The structure of AvrM and the identification of functionally important surface regions advance our understanding of the molecular mechanisms underlying how effectors enter plant cells and how they are detected by the plant immune system.</p>
</abstract>
<kwd-group>
<kwd>innate immunity</kwd>
<kwd>plant cell internalization</kwd>
<kwd>plant disease resistance</kwd>
<kwd>avirulence protein</kwd>
<kwd>lipid binding</kwd>
</kwd-group>
<counts>
<page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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