Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis

Deg proteases are involved in protein quality control in prokaryotes. Of the three Arabidopsis (Arabidopsis thaliana) homologs, Deg1, Deg5, and Deg8, located in the thylakoid lumen, Deg1 forms a homohexamer, whereas Deg5 and Deg8 form a hetero-complex. Both Deg1 and Deg5-Deg8 were shown separately t...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Plant physiology (Bethesda) 2018-11, Vol.178 (3), p.1065-1080
Hauptverfasser: Butenko, Yana, Lin, Albina, Naveh, Leah, Kupervaser, Meital, Levin, Yishai, Reich, Ziv, Adam, Zach
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1080
container_issue 3
container_start_page 1065
container_title Plant physiology (Bethesda)
container_volume 178
creator Butenko, Yana
Lin, Albina
Naveh, Leah
Kupervaser, Meital
Levin, Yishai
Reich, Ziv
Adam, Zach
description Deg proteases are involved in protein quality control in prokaryotes. Of the three Arabidopsis (Arabidopsis thaliana) homologs, Deg1, Deg5, and Deg8, located in the thylakoid lumen, Deg1 forms a homohexamer, whereas Deg5 and Deg8 form a hetero-complex. Both Deg1 and Deg5-Deg8 were shown separately to degrade photosynthetic proteins during photoinhibition. To investigate whether Deg1 and Deg5-Deg8 are redundant, a full set of Arabidopsis Deg knockout mutants were generated and their phenotypes were compared. Under all conditions tested, deg1 mutants were affected more than the wild type and deg5 and deg8 mutants. Moreover, overexpression of Deg5-Deg8 could only partially compensate for the loss of Deg1. Comparative proteomics of deg1 mutants revealed moderate up-regulation of thylakoid proteins involved in photoprotection, assembly, repair, and housekeeping and down-regulation of those that form photosynthetic complexes. Quantification of protein levels in the wild type revealed that Deg1 was 2-fold more abundant than Deg5-Deg8. Moreover, recombinant Deg1 displayed higher in vitro proteolytic activity. Affinity enrichment assays revealed that Deg1 was precipitated with very few interacting proteins, whereas Deg5-Deg8 was associated with a number of thylakoid proteins, including D1, OECs, LHCBs, Cyt b₆f, and NDH subunits, thus implying that Deg5-Deg8 is capable of binding substrates but is unable to degrade them efficiently. This work suggests that differences in protein abundance and proteolytic activity underlie the differential importance of Deg1 and Deg5-Deg8 protease complexes observed in vivo.
doi_str_mv 10.1104/pp.18.00912
format Article
fullrecord <record><control><sourceid>jstor_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_2111145789</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26568626</jstor_id><sourcerecordid>26568626</sourcerecordid><originalsourceid>FETCH-LOGICAL-c348t-177a6b6def51f21318585b9ef5abf7a688af07d151a7b44ed722d49cf399daf73</originalsourceid><addsrcrecordid>eNo9kN1LwzAUxYMobk6ffFbyKEhnPtomfZRNnTBQZD5KSNtkq6ZLTdKH_fdGO3df7r2cH4fDAeASoynGKL3ruinmU4QKTI7AGGeUJCRL-TEYIxRvxHkxAmfefyKEMMXpKRhRRCgjiI3Bx7zRWjm1DY008M0a5aHVMGwUXG12Rn7ZpobLvlXbKM_VGr46G5T0Ci5sa41de9hs4WxjrLOdkT4MgPVB-safgxMtjVcX-z0B748Pq9kiWb48Pc_ul0lFUx4SzJjMy7xWOsOaxIw841lZxFeWOkqcS41YjTMsWZmmqmaE1GlRaVoUtdSMTsDN4Ns5-90rH0Tb-EoZI7fK9l4QHCfNGC8iejuglbPeO6VF55pWup3ASPz2KbpOYC7--oz09d64L1tVH9j_AiNwNQCfPlh30Eme5TwnOf0BpEt6yA</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2111145789</pqid></control><display><type>article</type><title>Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis</title><source>MEDLINE</source><source>JSTOR Archive Collection A-Z Listing</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Butenko, Yana ; Lin, Albina ; Naveh, Leah ; Kupervaser, Meital ; Levin, Yishai ; Reich, Ziv ; Adam, Zach</creator><creatorcontrib>Butenko, Yana ; Lin, Albina ; Naveh, Leah ; Kupervaser, Meital ; Levin, Yishai ; Reich, Ziv ; Adam, Zach</creatorcontrib><description>Deg proteases are involved in protein quality control in prokaryotes. Of the three Arabidopsis (Arabidopsis thaliana) homologs, Deg1, Deg5, and Deg8, located in the thylakoid lumen, Deg1 forms a homohexamer, whereas Deg5 and Deg8 form a hetero-complex. Both Deg1 and Deg5-Deg8 were shown separately to degrade photosynthetic proteins during photoinhibition. To investigate whether Deg1 and Deg5-Deg8 are redundant, a full set of Arabidopsis Deg knockout mutants were generated and their phenotypes were compared. Under all conditions tested, deg1 mutants were affected more than the wild type and deg5 and deg8 mutants. Moreover, overexpression of Deg5-Deg8 could only partially compensate for the loss of Deg1. Comparative proteomics of deg1 mutants revealed moderate up-regulation of thylakoid proteins involved in photoprotection, assembly, repair, and housekeeping and down-regulation of those that form photosynthetic complexes. Quantification of protein levels in the wild type revealed that Deg1 was 2-fold more abundant than Deg5-Deg8. Moreover, recombinant Deg1 displayed higher in vitro proteolytic activity. Affinity enrichment assays revealed that Deg1 was precipitated with very few interacting proteins, whereas Deg5-Deg8 was associated with a number of thylakoid proteins, including D1, OECs, LHCBs, Cyt b₆f, and NDH subunits, thus implying that Deg5-Deg8 is capable of binding substrates but is unable to degrade them efficiently. This work suggests that differences in protein abundance and proteolytic activity underlie the differential importance of Deg1 and Deg5-Deg8 protease complexes observed in vivo.</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.18.00912</identifier><identifier>PMID: 30237207</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - physiology ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; BIOCHEMISTRY AND METABOLISM ; Gene Expression Regulation, Plant ; Gene Knockout Techniques ; Mutation ; Phenotype ; Photosynthesis ; Plant Leaves - enzymology ; Plant Leaves - genetics ; Plant Leaves - physiology ; Proteomics ; Proteostasis ; Seedlings - enzymology ; Seedlings - genetics ; Seedlings - physiology ; Serine Endopeptidases - genetics ; Serine Endopeptidases - metabolism ; Thylakoids - enzymology ; Thylakoids - physiology</subject><ispartof>Plant physiology (Bethesda), 2018-11, Vol.178 (3), p.1065-1080</ispartof><rights>2018 American Society of Plant Biologists</rights><rights>2018 American Society of Plant Biologists. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c348t-177a6b6def51f21318585b9ef5abf7a688af07d151a7b44ed722d49cf399daf73</citedby><orcidid>0000-0002-7279-0246 ; 0000-0001-6202-5826</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26568626$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26568626$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,803,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30237207$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Butenko, Yana</creatorcontrib><creatorcontrib>Lin, Albina</creatorcontrib><creatorcontrib>Naveh, Leah</creatorcontrib><creatorcontrib>Kupervaser, Meital</creatorcontrib><creatorcontrib>Levin, Yishai</creatorcontrib><creatorcontrib>Reich, Ziv</creatorcontrib><creatorcontrib>Adam, Zach</creatorcontrib><title>Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>Deg proteases are involved in protein quality control in prokaryotes. Of the three Arabidopsis (Arabidopsis thaliana) homologs, Deg1, Deg5, and Deg8, located in the thylakoid lumen, Deg1 forms a homohexamer, whereas Deg5 and Deg8 form a hetero-complex. Both Deg1 and Deg5-Deg8 were shown separately to degrade photosynthetic proteins during photoinhibition. To investigate whether Deg1 and Deg5-Deg8 are redundant, a full set of Arabidopsis Deg knockout mutants were generated and their phenotypes were compared. Under all conditions tested, deg1 mutants were affected more than the wild type and deg5 and deg8 mutants. Moreover, overexpression of Deg5-Deg8 could only partially compensate for the loss of Deg1. Comparative proteomics of deg1 mutants revealed moderate up-regulation of thylakoid proteins involved in photoprotection, assembly, repair, and housekeeping and down-regulation of those that form photosynthetic complexes. Quantification of protein levels in the wild type revealed that Deg1 was 2-fold more abundant than Deg5-Deg8. Moreover, recombinant Deg1 displayed higher in vitro proteolytic activity. Affinity enrichment assays revealed that Deg1 was precipitated with very few interacting proteins, whereas Deg5-Deg8 was associated with a number of thylakoid proteins, including D1, OECs, LHCBs, Cyt b₆f, and NDH subunits, thus implying that Deg5-Deg8 is capable of binding substrates but is unable to degrade them efficiently. This work suggests that differences in protein abundance and proteolytic activity underlie the differential importance of Deg1 and Deg5-Deg8 protease complexes observed in vivo.</description><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BIOCHEMISTRY AND METABOLISM</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene Knockout Techniques</subject><subject>Mutation</subject><subject>Phenotype</subject><subject>Photosynthesis</subject><subject>Plant Leaves - enzymology</subject><subject>Plant Leaves - genetics</subject><subject>Plant Leaves - physiology</subject><subject>Proteomics</subject><subject>Proteostasis</subject><subject>Seedlings - enzymology</subject><subject>Seedlings - genetics</subject><subject>Seedlings - physiology</subject><subject>Serine Endopeptidases - genetics</subject><subject>Serine Endopeptidases - metabolism</subject><subject>Thylakoids - enzymology</subject><subject>Thylakoids - physiology</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kN1LwzAUxYMobk6ffFbyKEhnPtomfZRNnTBQZD5KSNtkq6ZLTdKH_fdGO3df7r2cH4fDAeASoynGKL3ruinmU4QKTI7AGGeUJCRL-TEYIxRvxHkxAmfefyKEMMXpKRhRRCgjiI3Bx7zRWjm1DY008M0a5aHVMGwUXG12Rn7ZpobLvlXbKM_VGr46G5T0Ci5sa41de9hs4WxjrLOdkT4MgPVB-safgxMtjVcX-z0B748Pq9kiWb48Pc_ul0lFUx4SzJjMy7xWOsOaxIw841lZxFeWOkqcS41YjTMsWZmmqmaE1GlRaVoUtdSMTsDN4Ns5-90rH0Tb-EoZI7fK9l4QHCfNGC8iejuglbPeO6VF55pWup3ASPz2KbpOYC7--oz09d64L1tVH9j_AiNwNQCfPlh30Eme5TwnOf0BpEt6yA</recordid><startdate>20181101</startdate><enddate>20181101</enddate><creator>Butenko, Yana</creator><creator>Lin, Albina</creator><creator>Naveh, Leah</creator><creator>Kupervaser, Meital</creator><creator>Levin, Yishai</creator><creator>Reich, Ziv</creator><creator>Adam, Zach</creator><general>American Society of Plant Biologists</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7279-0246</orcidid><orcidid>https://orcid.org/0000-0001-6202-5826</orcidid></search><sort><creationdate>20181101</creationdate><title>Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis</title><author>Butenko, Yana ; Lin, Albina ; Naveh, Leah ; Kupervaser, Meital ; Levin, Yishai ; Reich, Ziv ; Adam, Zach</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c348t-177a6b6def51f21318585b9ef5abf7a688af07d151a7b44ed722d49cf399daf73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BIOCHEMISTRY AND METABOLISM</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene Knockout Techniques</topic><topic>Mutation</topic><topic>Phenotype</topic><topic>Photosynthesis</topic><topic>Plant Leaves - enzymology</topic><topic>Plant Leaves - genetics</topic><topic>Plant Leaves - physiology</topic><topic>Proteomics</topic><topic>Proteostasis</topic><topic>Seedlings - enzymology</topic><topic>Seedlings - genetics</topic><topic>Seedlings - physiology</topic><topic>Serine Endopeptidases - genetics</topic><topic>Serine Endopeptidases - metabolism</topic><topic>Thylakoids - enzymology</topic><topic>Thylakoids - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Butenko, Yana</creatorcontrib><creatorcontrib>Lin, Albina</creatorcontrib><creatorcontrib>Naveh, Leah</creatorcontrib><creatorcontrib>Kupervaser, Meital</creatorcontrib><creatorcontrib>Levin, Yishai</creatorcontrib><creatorcontrib>Reich, Ziv</creatorcontrib><creatorcontrib>Adam, Zach</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Butenko, Yana</au><au>Lin, Albina</au><au>Naveh, Leah</au><au>Kupervaser, Meital</au><au>Levin, Yishai</au><au>Reich, Ziv</au><au>Adam, Zach</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2018-11-01</date><risdate>2018</risdate><volume>178</volume><issue>3</issue><spage>1065</spage><epage>1080</epage><pages>1065-1080</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>Deg proteases are involved in protein quality control in prokaryotes. Of the three Arabidopsis (Arabidopsis thaliana) homologs, Deg1, Deg5, and Deg8, located in the thylakoid lumen, Deg1 forms a homohexamer, whereas Deg5 and Deg8 form a hetero-complex. Both Deg1 and Deg5-Deg8 were shown separately to degrade photosynthetic proteins during photoinhibition. To investigate whether Deg1 and Deg5-Deg8 are redundant, a full set of Arabidopsis Deg knockout mutants were generated and their phenotypes were compared. Under all conditions tested, deg1 mutants were affected more than the wild type and deg5 and deg8 mutants. Moreover, overexpression of Deg5-Deg8 could only partially compensate for the loss of Deg1. Comparative proteomics of deg1 mutants revealed moderate up-regulation of thylakoid proteins involved in photoprotection, assembly, repair, and housekeeping and down-regulation of those that form photosynthetic complexes. Quantification of protein levels in the wild type revealed that Deg1 was 2-fold more abundant than Deg5-Deg8. Moreover, recombinant Deg1 displayed higher in vitro proteolytic activity. Affinity enrichment assays revealed that Deg1 was precipitated with very few interacting proteins, whereas Deg5-Deg8 was associated with a number of thylakoid proteins, including D1, OECs, LHCBs, Cyt b₆f, and NDH subunits, thus implying that Deg5-Deg8 is capable of binding substrates but is unable to degrade them efficiently. This work suggests that differences in protein abundance and proteolytic activity underlie the differential importance of Deg1 and Deg5-Deg8 protease complexes observed in vivo.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>30237207</pmid><doi>10.1104/pp.18.00912</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-7279-0246</orcidid><orcidid>https://orcid.org/0000-0001-6202-5826</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0032-0889
ispartof Plant physiology (Bethesda), 2018-11, Vol.178 (3), p.1065-1080
issn 0032-0889
1532-2548
language eng
recordid cdi_proquest_miscellaneous_2111145789
source MEDLINE; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals
subjects Arabidopsis - enzymology
Arabidopsis - genetics
Arabidopsis - physiology
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
BIOCHEMISTRY AND METABOLISM
Gene Expression Regulation, Plant
Gene Knockout Techniques
Mutation
Phenotype
Photosynthesis
Plant Leaves - enzymology
Plant Leaves - genetics
Plant Leaves - physiology
Proteomics
Proteostasis
Seedlings - enzymology
Seedlings - genetics
Seedlings - physiology
Serine Endopeptidases - genetics
Serine Endopeptidases - metabolism
Thylakoids - enzymology
Thylakoids - physiology
title Differential Roles of the Thylakoid Lumenal Deg Protease Homologs in Chloroplast Proteostasis
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T14%3A31%3A39IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20Roles%20of%20the%20Thylakoid%20Lumenal%20Deg%20Protease%20Homologs%20in%20Chloroplast%20Proteostasis&rft.jtitle=Plant%20physiology%20(Bethesda)&rft.au=Butenko,%20Yana&rft.date=2018-11-01&rft.volume=178&rft.issue=3&rft.spage=1065&rft.epage=1080&rft.pages=1065-1080&rft.issn=0032-0889&rft.eissn=1532-2548&rft_id=info:doi/10.1104/pp.18.00912&rft_dat=%3Cjstor_proqu%3E26568626%3C/jstor_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2111145789&rft_id=info:pmid/30237207&rft_jstor_id=26568626&rfr_iscdi=true