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EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

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EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

Auteurs : Yidan Liu ; Congcong Zhang [République populaire de Chine] ; Dinghe Wang [République populaire de Chine] ; Wei Su ; Linchuan Liu [République populaire de Chine] ; Muyang Wang [République populaire de Chine] ; Jianming Li [République populaire de Chine]

Source :

Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2015.

RBID : PMC:4593087

Abstract

Significance

Endoplasmic reticulum (ER)-associated degradation (ERAD) is a well-studied cellular process in yeast and mammalian systems. Recent molecular and genetic studies in the reference plant Arabidopsis have revealed that ERAD also is conserved in plants. Here we report that an Arabidopsis ERAD process for degrading misfolded/mutant receptor-like kinases requires a plant-specific protein, ethyl methanesulfonate-mutagenized brassinosteroid-insensitive 1 suppressor 7 (EBS7), that is localized to the ER membrane and is induced by ER stress. Our biochemical studies suggest that EBS7 functions as a key regulator of this Arabidopsis ERAD process by maintaining the protein stability of its core component, a membrane-anchored E3 ligase, Arabidopsis thaliana HMG-CoA reductase degradation 1a (AtHrd1a).

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4593087

DOI: 10.1073/pnas.1511724112
PubMed: 26371323
PubMed Central: 4593087

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<author><name sortKey="Liu, Yidan" sort="Liu, Yidan" uniqKey="Liu Y" first="Yidan" last="Liu">Yidan Liu</name>
<affiliation><nlm:aff id="aff1">Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Congcong" sort="Zhang, Congcong" uniqKey="Zhang C" first="Congcong" last="Zhang">Congcong Zhang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Wang, Dinghe" sort="Wang, Dinghe" uniqKey="Wang D" first="Dinghe" last="Wang">Dinghe Wang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Su, Wei" sort="Su, Wei" uniqKey="Su W" first="Wei" last="Su">Wei Su</name>
<affiliation><nlm:aff id="aff1">Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
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<author><name sortKey="Liu, Linchuan" sort="Liu, Linchuan" uniqKey="Liu L" first="Linchuan" last="Liu">Linchuan Liu</name>
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, Shanghai 201602,<country>China</country>
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<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Wang, Muyang" sort="Wang, Muyang" uniqKey="Wang M" first="Muyang" last="Wang">Muyang Wang</name>
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, Shanghai 201602,<country>China</country>
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<country xml:lang="fr">République populaire de Chine</country>
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<author><name sortKey="Li, Jianming" sort="Li, Jianming" uniqKey="Li J" first="Jianming" last="Li">Jianming Li</name>
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, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
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<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
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</title>
<author><name sortKey="Liu, Yidan" sort="Liu, Yidan" uniqKey="Liu Y" first="Yidan" last="Liu">Yidan Liu</name>
<affiliation><nlm:aff id="aff1">Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Zhang, Congcong" sort="Zhang, Congcong" uniqKey="Zhang C" first="Congcong" last="Zhang">Congcong Zhang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<author><name sortKey="Wang, Dinghe" sort="Wang, Dinghe" uniqKey="Wang D" first="Dinghe" last="Wang">Dinghe Wang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Su, Wei" sort="Su, Wei" uniqKey="Su W" first="Wei" last="Su">Wei Su</name>
<affiliation><nlm:aff id="aff1">Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Liu, Linchuan" sort="Liu, Linchuan" uniqKey="Liu L" first="Linchuan" last="Liu">Linchuan Liu</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wang, Muyang" sort="Wang, Muyang" uniqKey="Wang M" first="Muyang" last="Wang">Muyang Wang</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Li, Jianming" sort="Li, Jianming" uniqKey="Li J" first="Jianming" last="Li">Jianming Li</name>
<affiliation><nlm:aff id="aff1">Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</nlm:aff>
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<affiliation wicri:level="1"><nlm:aff id="aff2">Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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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>
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<front><div type="abstract" xml:lang="en"><title>Significance</title>
<p>Endoplasmic reticulum (ER)-associated degradation (ERAD) is a well-studied cellular process in yeast and mammalian systems. Recent molecular and genetic studies in the reference plant <italic>Arabidopsis</italic>
 have revealed that ERAD also is conserved in plants. Here we report that an <italic>Arabidopsis</italic>
 ERAD process for degrading misfolded/mutant receptor-like kinases requires a plant-specific protein, ethyl methanesulfonate-mutagenized brassinosteroid-insensitive 1 suppressor 7 (EBS7), that is localized to the ER membrane and is induced by ER stress. Our biochemical studies suggest that EBS7 functions as a key regulator of this <italic>Arabidopsis</italic>
 ERAD process by maintaining the protein stability of its core component, a membrane-anchored E3 ligase, <italic>Arabidopsis thaliana</italic>
 HMG-CoA reductase degradation 1a (AtHrd1a).</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>
<article-meta><article-id pub-id-type="pmid">26371323</article-id>
<article-id pub-id-type="pmc">4593087</article-id>
<article-id pub-id-type="publisher-id">201511724</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1511724112</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>EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in <italic>Arabidopsis</italic>
</article-title>
<alt-title alt-title-type="short">Plant-specific ERAD component</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Yidan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Congcong</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Dinghe</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Su</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Linchuan</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Muyang</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Jianming</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>2</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
Department of Molecular, Cellular, and Developmental Biology,<institution>University of Michigan</institution>
, Ann Arbor,<addr-line>MI</addr-line>
 48109;</aff>
<aff id="aff2"><sup>b</sup>
Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences,<institution>The Chinese Academy of Sciences</institution>
, Shanghai 201602,<country>China</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>2</sup>
To whom correspondence should be addressed. Email: <email>jian@umich.edu</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by Natasha V. Raikhel, Center for Plant Cell Biology, Riverside, CA, and approved August 12, 2015 (received for review June 19, 2015)</p>
</fn>
<fn fn-type="con"><p>Author contributions: Y.L. and J.L. designed research; Y.L., C.Z., D.W., W.S., and L.L. performed research; D.W., W.S., and M.W. contributed new reagents/analytic tools; Y.L., C.Z., D.W., L.L., M.W., and J.L. analyzed data; and Y.L., C.Z., and J.L. wrote the paper.</p>
</fn>
<fn fn-type="present-address" id="fn1"><p><sup>1</sup>
Present address: The State Key Laboratory of Genetic Engineering and Institute of Plant Biology, School of Life Sciences, Fudan University, Shanghai 200433, China.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>29</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>14</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>14</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the 
 							. </pmc-comment>
      <volume>112</volume>
<issue>39</issue>
<fpage>12205</fpage>
<lpage>12210</lpage>
<permissions><license license-type="open-access"><license-p>Freely available online through the PNAS open access option.</license-p>
</license>
</permissions>
<self-uri xlink:title="pdf" xlink:href="pnas.201511724.pdf"></self-uri>
<abstract abstract-type="executive-summary"><title>Significance</title>
<p>Endoplasmic reticulum (ER)-associated degradation (ERAD) is a well-studied cellular process in yeast and mammalian systems. Recent molecular and genetic studies in the reference plant <italic>Arabidopsis</italic>
 have revealed that ERAD also is conserved in plants. Here we report that an <italic>Arabidopsis</italic>
 ERAD process for degrading misfolded/mutant receptor-like kinases requires a plant-specific protein, ethyl methanesulfonate-mutagenized brassinosteroid-insensitive 1 suppressor 7 (EBS7), that is localized to the ER membrane and is induced by ER stress. Our biochemical studies suggest that EBS7 functions as a key regulator of this <italic>Arabidopsis</italic>
 ERAD process by maintaining the protein stability of its core component, a membrane-anchored E3 ligase, <italic>Arabidopsis thaliana</italic>
 HMG-CoA reductase degradation 1a (AtHrd1a).</p>
</abstract>
<abstract><p>Endoplasmic reticulum (ER)-associated degradation (ERAD) is an essential part of an ER-localized protein quality-control system for eliminating terminally misfolded proteins. Recent studies have demonstrated that the ERAD machinery is conserved among yeast, animals, and plants; however, it remains unknown if the plant ERAD system involves plant-specific components. Here we report that the <italic>Arabidopsis ethyl methanesulfonate-mutagenized brassinosteroid-insensitive 1 suppressor 7</italic>
 (<italic>EBS7</italic>
) gene encodes an ER membrane-localized ERAD component that is highly conserved in land plants. Loss-of-function <italic>ebs7</italic>
 mutations prevent ERAD of brassinosteroid insensitive 1-9 (bri1-9) and bri1-5, two ER-retained mutant variants of the cell-surface receptor for brassinosteroids (BRs). As a result, the two mutant receptors accumulate in the ER and consequently leak to the plasma membrane, resulting in the restoration of BR sensitivity and phenotypic suppression of the <italic>bri1-9</italic>
 and <italic>bri1-5</italic>
 mutants. EBS7 accumulates under ER stress, and its mutations lead to hypersensitivity to ER and salt stresses. EBS7 interacts with the ER membrane-anchored ubiquitin ligase <italic>Arabidopsis thaliana</italic>
 HMG-CoA reductase degradation 1a (AtHrd1a), one of the central components of the <italic>Arabidopsis</italic>
 ERAD machinery, and an <italic>ebs7</italic>
 mutation destabilizes AtHrd1a to reduce polyubiquitination of bri1-9. Taken together, our results uncover a plant-specific component of a plant ERAD pathway and also suggest its likely biochemical function.</p>
</abstract>
<kwd-group><kwd>brassinosteroid receptor BRI1</kwd>
<kwd>ERAD</kwd>
<kwd>EMS-mutagenized bri1 suppressor</kwd>
<kwd>ubiquitin ligase E3</kwd>
<kwd>unfolded protein response</kwd>
</kwd-group>
<funding-group><award-group id="gs1"><funding-source id="sp1">University of Michigan (U-M)<named-content content-type="funder-id">100007270</named-content>
</funding-source>
<award-id rid="sp1">OVPRE-U032381</award-id>
</award-group>
<award-group id="gs2"><funding-source id="sp2">Chinese Academy of Sciences (CAS)<named-content content-type="funder-id">501100002367</named-content>
</funding-source>
<award-id rid="sp2">2012CSP004</award-id>
</award-group>
</funding-group>
<counts><page-count count="6"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>

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EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

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Abstract

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