ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis
Autophagy is a conserved pathway for bulk degradationof cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the func...
Gespeichert in:
| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2017-01, Vol.114 (3), p.E426-E435 |
|---|---|
| Hauptverfasser: | , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | E435 |
|---|---|
| container_issue | 3 |
| container_start_page | E426 |
| container_title | Proceedings of the National Academy of Sciences - PNAS |
| container_volume | 114 |
| creator | Zhuang, Xiaohong Chung, Kin Pan Cui, Yong Lin, Weili Gao, Caiji Kang, Byung-Ho Jiang, Liwen |
| description | Autophagy is a conserved pathway for bulk degradationof cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the functional relationship between ATG9 vesicles and the phagophore is controversial in different systems, and the molecular function of ATG9 remains unknown in plants. Here, we demonstrate that ATG9 is essential for endoplasmic reticulum (ER)-derived autophagosome formation in plants. Through a combination of genetic, in vivo imaging and electron tomography approaches, we show that Arabidopsis ATG9 deficiency leads to a drastic accumulation of autophagosome-related tubular structures in direct membrane continuity with the ER upon autophagic induction. Dynamic analyses demonstrate a transient membrane association between ATG9 vesicles and the autophagosomal membrane during autophagy. Furthermore, trafficking of ATG18a is compromised in atg9 mutants during autophagy by forming extended tubules in a phosphatidylinositol 3-phosphate–dependent manner. Taken together, this study provides evidence for a pivotal role of ATG9 in regulating autophagosome progression from the ER membrane in Arabidopsis. |
| doi_str_mv | 10.1073/pnas.1616299114 |
| format | Article |
| fullrecord | <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5255614</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26479019</jstor_id><sourcerecordid>26479019</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-7d30192a092879ff3e2ce17c08cc35f5217cde21a6066fea0827276efca3902e3</originalsourceid><addsrcrecordid>eNpdkc1P3DAQxa2Kqiy0556KIvXCJTC2468L0mrVUiSkXoCrZbyTXa-SONgJEv99jZZCy2lGer95mqdHyFcKZxQUPx8Hl8-opJIZQ2nzgSwoGFrLxsABWQAwVeuGNYfkKOcdABih4RM5ZBoEZ8wsyN3y5tJUCTdz5ybMlZunOG7dJubYYzWmuEmYc4hD1abYV9MWKxzWcexc7oMvh1Pwczf3VRiqZXL3oWg55M_kY-u6jF9e5jG5_fnjZvWrvv59ebVaXte-afhUqzUHapgDw7QybcuReaTKg_aei1awsq-RUSdByhYdaKaYkth6xw0w5MfkYu87zvc9rj0OU3KdHVPoXXqy0QX7vzKErd3ERyuYEJI2xeD0xSDFhxnzZPuQPXadGzDO2VIthNJSGSjo93foLs5pKPEKJSnnErQq1Pme8inmnLB9fYaCfe7MPndm3zorFyf_Znjl_5ZUgG97YJenmN502ZS3qOF_AC54nbk</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1861336087</pqid></control><display><type>article</type><title>ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis</title><source>Jstor Complete Legacy</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Zhuang, Xiaohong ; Chung, Kin Pan ; Cui, Yong ; Lin, Weili ; Gao, Caiji ; Kang, Byung-Ho ; Jiang, Liwen</creator><creatorcontrib>Zhuang, Xiaohong ; Chung, Kin Pan ; Cui, Yong ; Lin, Weili ; Gao, Caiji ; Kang, Byung-Ho ; Jiang, Liwen</creatorcontrib><description>Autophagy is a conserved pathway for bulk degradationof cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the functional relationship between ATG9 vesicles and the phagophore is controversial in different systems, and the molecular function of ATG9 remains unknown in plants. Here, we demonstrate that ATG9 is essential for endoplasmic reticulum (ER)-derived autophagosome formation in plants. Through a combination of genetic, in vivo imaging and electron tomography approaches, we show that Arabidopsis ATG9 deficiency leads to a drastic accumulation of autophagosome-related tubular structures in direct membrane continuity with the ER upon autophagic induction. Dynamic analyses demonstrate a transient membrane association between ATG9 vesicles and the autophagosomal membrane during autophagy. Furthermore, trafficking of ATG18a is compromised in atg9 mutants during autophagy by forming extended tubules in a phosphatidylinositol 3-phosphate–dependent manner. Taken together, this study provides evidence for a pivotal role of ATG9 in regulating autophagosome progression from the ER membrane in Arabidopsis.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1616299114</identifier><identifier>PMID: 28053229</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Autophagy ; Biological Sciences ; Endoplasmic reticulum ; Flowers & plants ; Genetics ; Membranes ; PNAS Plus</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2017-01, Vol.114 (3), p.E426-E435</ispartof><rights>Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Jan 17, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-7d30192a092879ff3e2ce17c08cc35f5217cde21a6066fea0827276efca3902e3</citedby><cites>FETCH-LOGICAL-c443t-7d30192a092879ff3e2ce17c08cc35f5217cde21a6066fea0827276efca3902e3</cites><orcidid>0000-0003-2786-3095</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26479019$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26479019$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28053229$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhuang, Xiaohong</creatorcontrib><creatorcontrib>Chung, Kin Pan</creatorcontrib><creatorcontrib>Cui, Yong</creatorcontrib><creatorcontrib>Lin, Weili</creatorcontrib><creatorcontrib>Gao, Caiji</creatorcontrib><creatorcontrib>Kang, Byung-Ho</creatorcontrib><creatorcontrib>Jiang, Liwen</creatorcontrib><title>ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Autophagy is a conserved pathway for bulk degradationof cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the functional relationship between ATG9 vesicles and the phagophore is controversial in different systems, and the molecular function of ATG9 remains unknown in plants. Here, we demonstrate that ATG9 is essential for endoplasmic reticulum (ER)-derived autophagosome formation in plants. Through a combination of genetic, in vivo imaging and electron tomography approaches, we show that Arabidopsis ATG9 deficiency leads to a drastic accumulation of autophagosome-related tubular structures in direct membrane continuity with the ER upon autophagic induction. Dynamic analyses demonstrate a transient membrane association between ATG9 vesicles and the autophagosomal membrane during autophagy. Furthermore, trafficking of ATG18a is compromised in atg9 mutants during autophagy by forming extended tubules in a phosphatidylinositol 3-phosphate–dependent manner. Taken together, this study provides evidence for a pivotal role of ATG9 in regulating autophagosome progression from the ER membrane in Arabidopsis.</description><subject>Autophagy</subject><subject>Biological Sciences</subject><subject>Endoplasmic reticulum</subject><subject>Flowers & plants</subject><subject>Genetics</subject><subject>Membranes</subject><subject>PNAS Plus</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNpdkc1P3DAQxa2Kqiy0556KIvXCJTC2468L0mrVUiSkXoCrZbyTXa-SONgJEv99jZZCy2lGer95mqdHyFcKZxQUPx8Hl8-opJIZQ2nzgSwoGFrLxsABWQAwVeuGNYfkKOcdABih4RM5ZBoEZ8wsyN3y5tJUCTdz5ybMlZunOG7dJubYYzWmuEmYc4hD1abYV9MWKxzWcexc7oMvh1Pwczf3VRiqZXL3oWg55M_kY-u6jF9e5jG5_fnjZvWrvv59ebVaXte-afhUqzUHapgDw7QybcuReaTKg_aei1awsq-RUSdByhYdaKaYkth6xw0w5MfkYu87zvc9rj0OU3KdHVPoXXqy0QX7vzKErd3ERyuYEJI2xeD0xSDFhxnzZPuQPXadGzDO2VIthNJSGSjo93foLs5pKPEKJSnnErQq1Pme8inmnLB9fYaCfe7MPndm3zorFyf_Znjl_5ZUgG97YJenmN502ZS3qOF_AC54nbk</recordid><startdate>20170117</startdate><enddate>20170117</enddate><creator>Zhuang, Xiaohong</creator><creator>Chung, Kin Pan</creator><creator>Cui, Yong</creator><creator>Lin, Weili</creator><creator>Gao, Caiji</creator><creator>Kang, Byung-Ho</creator><creator>Jiang, Liwen</creator><general>National Academy of Sciences</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2786-3095</orcidid></search><sort><creationdate>20170117</creationdate><title>ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis</title><author>Zhuang, Xiaohong ; Chung, Kin Pan ; Cui, Yong ; Lin, Weili ; Gao, Caiji ; Kang, Byung-Ho ; Jiang, Liwen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-7d30192a092879ff3e2ce17c08cc35f5217cde21a6066fea0827276efca3902e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Autophagy</topic><topic>Biological Sciences</topic><topic>Endoplasmic reticulum</topic><topic>Flowers & plants</topic><topic>Genetics</topic><topic>Membranes</topic><topic>PNAS Plus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhuang, Xiaohong</creatorcontrib><creatorcontrib>Chung, Kin Pan</creatorcontrib><creatorcontrib>Cui, Yong</creatorcontrib><creatorcontrib>Lin, Weili</creatorcontrib><creatorcontrib>Gao, Caiji</creatorcontrib><creatorcontrib>Kang, Byung-Ho</creatorcontrib><creatorcontrib>Jiang, Liwen</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhuang, Xiaohong</au><au>Chung, Kin Pan</au><au>Cui, Yong</au><au>Lin, Weili</au><au>Gao, Caiji</au><au>Kang, Byung-Ho</au><au>Jiang, Liwen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2017-01-17</date><risdate>2017</risdate><volume>114</volume><issue>3</issue><spage>E426</spage><epage>E435</epage><pages>E426-E435</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Autophagy is a conserved pathway for bulk degradationof cytoplasmic material by a double-membrane structure named the autophagosome. The initiation of autophagosome formation requires the recruitment of autophagy-related protein 9 (ATG9) vesicles to the preautophagosomal structure. However, the functional relationship between ATG9 vesicles and the phagophore is controversial in different systems, and the molecular function of ATG9 remains unknown in plants. Here, we demonstrate that ATG9 is essential for endoplasmic reticulum (ER)-derived autophagosome formation in plants. Through a combination of genetic, in vivo imaging and electron tomography approaches, we show that Arabidopsis ATG9 deficiency leads to a drastic accumulation of autophagosome-related tubular structures in direct membrane continuity with the ER upon autophagic induction. Dynamic analyses demonstrate a transient membrane association between ATG9 vesicles and the autophagosomal membrane during autophagy. Furthermore, trafficking of ATG18a is compromised in atg9 mutants during autophagy by forming extended tubules in a phosphatidylinositol 3-phosphate–dependent manner. Taken together, this study provides evidence for a pivotal role of ATG9 in regulating autophagosome progression from the ER membrane in Arabidopsis.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>28053229</pmid><doi>10.1073/pnas.1616299114</doi><orcidid>https://orcid.org/0000-0003-2786-3095</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0027-8424 |
| ispartof | Proceedings of the National Academy of Sciences - PNAS, 2017-01, Vol.114 (3), p.E426-E435 |
| issn | 0027-8424 1091-6490 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5255614 |
| source | Jstor Complete Legacy; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Autophagy Biological Sciences Endoplasmic reticulum Flowers & plants Genetics Membranes PNAS Plus |
| title | ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-15T07%3A01%3A47IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=ATG9%20regulates%20autophagosome%20progression%20from%20the%20endoplasmic%20reticulum%20in%20Arabidopsis&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Zhuang,%20Xiaohong&rft.date=2017-01-17&rft.volume=114&rft.issue=3&rft.spage=E426&rft.epage=E435&rft.pages=E426-E435&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1616299114&rft_dat=%3Cjstor_pubme%3E26479019%3C/jstor_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1861336087&rft_id=info:pmid/28053229&rft_jstor_id=26479019&rfr_iscdi=true |