Protein-induced modulation of chloroplast membrane morphology
Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membran...
Saved in:
Published in | Frontiers in plant science Vol. 2; p. 118 |
---|---|
Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Switzerland
Frontiers Research Foundation
01.01.2012
Frontiers Media S.A |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membranes. We therefore analyzed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach with protoplasts. Transient expression of outer envelope proteins or protein domains such as CHUP1-TM-GFP, outer envelope protein of 7 kDa-GFP, or outer envelope protein of 24 kDa-GFP at high levels led to the formation of punctate, circular, and tubular membrane protrusions. Expression of inner membrane proteins such as translocase of inner chloroplast membrane 20, isoform II (Tic20-II)-GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we could show that the frequency, size, and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of CHUP1-TM-Cherry and Tic20-II-GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high expression levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongate mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. Finally, the observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies. |
---|---|
AbstractList | Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect shape and organization of membranes. We analysed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach. Transient expression of outer envelope proteins or protein domains such as TM-CHUP1-GFP, OEP7-GFP or OEP24-GFP at high levels led to the formation of punctate, circular and tubular membrane protrusions. Expression of inner membrane proteins such as Tic20II-GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we show that the frequency, size and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of TM-CHUP1-Cherry and Tic20II-GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongated mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. The observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies. Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa , it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membranes. We therefore analyzed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach with protoplasts. Transient expression of outer envelope proteins or protein domains such as CHUP1-TM–GFP, outer envelope protein of 7 kDa–GFP, or outer envelope protein of 24 kDa–GFP at high levels led to the formation of punctate, circular, and tubular membrane protrusions. Expression of inner membrane proteins such as translocase of inner chloroplast membrane 20, isoform II (Tic20-II)–GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we could show that the frequency, size, and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of CHUP1-TM–Cherry and Tic20-II–GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high expression levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongate mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. Finally, the observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies. Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and vice versa, it has been only recently suggested that elevated membrane protein concentrations may affect the shape and organization of membranes. We therefore analyzed the effects of high chloroplast envelope protein concentrations on membrane structures using an in vivo approach with protoplasts. Transient expression of outer envelope proteins or protein domains such as CHUP1-TM-GFP, outer envelope protein of 7 kDa-GFP, or outer envelope protein of 24 kDa-GFP at high levels led to the formation of punctate, circular, and tubular membrane protrusions. Expression of inner membrane proteins such as translocase of inner chloroplast membrane 20, isoform II (Tic20-II)-GFP led to membrane protrusions including invaginations. Using increasing amounts of DNA for transfection, we could show that the frequency, size, and intensity of these protrusions increased with protein concentration. The membrane deformations were absent after cycloheximide treatment. Co-expression of CHUP1-TM-Cherry and Tic20-II-GFP led to membrane protrusions of various shapes and sizes including some stromule-like structures, for which several functions have been proposed. Interestingly, some structures seemed to contain both proteins, while others seem to contain one protein exclusively, indicating that outer and inner envelope dynamics might be regulated independently. While it was more difficult to investigate the effects of high expression levels of membrane proteins on mitochondrial membrane shapes using confocal imaging, it was striking that the expression of the outer membrane protein Tom20 led to more elongate mitochondria. We discuss that the effect of protein concentrations on membrane structure is possibly caused by an imbalance in the lipid to protein ratio and may be involved in a signaling pathway regulating membrane biogenesis. Finally, the observed phenomenon provides a valuable experimental approach to investigate the relationship between lipid synthesis and membrane protein expression in future studies. |
Author | Sommer, Maik S Schleiff, Enrico Englich, Gisela Königer, Martina Machettira, Anu B Weis, Benjamin L Groß, Lucia E Tillmann, Bodo |
AuthorAffiliation | 2 Department of Biological Sciences, Wellesley College Wellesley, MA, USA 3 Cluster of Excellence “Macromolecular Complexes”, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany 1 Molecular Cell Biology of Plants, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany 4 Department of Biosciences, Center of Membrane Proteomics, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany |
AuthorAffiliation_xml | – name: 1 Molecular Cell Biology of Plants, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany – name: 4 Department of Biosciences, Center of Membrane Proteomics, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany – name: 3 Cluster of Excellence “Macromolecular Complexes”, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany – name: 2 Department of Biological Sciences, Wellesley College Wellesley, MA, USA |
Author_xml | – sequence: 1 givenname: Anu B surname: Machettira fullname: Machettira, Anu B organization: Molecular Cell Biology of Plants, Johann-Wolfgang-Goethe University Frankfurt Frankfurt am Main, Germany – sequence: 2 givenname: Lucia E surname: Groß fullname: Groß, Lucia E – sequence: 3 givenname: Bodo surname: Tillmann fullname: Tillmann, Bodo – sequence: 4 givenname: Benjamin L surname: Weis fullname: Weis, Benjamin L – sequence: 5 givenname: Gisela surname: Englich fullname: Englich, Gisela – sequence: 6 givenname: Maik S surname: Sommer fullname: Sommer, Maik S – sequence: 7 givenname: Martina surname: Königer fullname: Königer, Martina – sequence: 8 givenname: Enrico surname: Schleiff fullname: Schleiff, Enrico |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22639631$$D View this record in MEDLINE/PubMed |
BookMark | eNpVkbtLBDEQxoMovms7udJmz7w22RQKcvgCQQsLu5Dn3Up2sya7gv-9OU9FU0yGmW9-CfMdgO0-9g6AEwTnhDTi3A8hzzFEaA5LaLbAPmKMVpThl-0_-R44zvkVllNDKATfBXsYMyIYQfvg4inF0bV91fZ2Ms7OuminoMY29rPoZ2YVYopDUHmcda7TSfWuSNKwiiEuP47Ajlchu-Pv-xA831w_L-6qh8fb-8XVQ2VoLcbKauU9bWqBCGsMURwrpB1GxteaK-S5tlB7hp0RlniinFCIWtMIqikphUNwv8HaqF7lkNpOpQ8ZVSu_CjEtpUpja4KTnHohtOWCIV1SKLCGtPGwwLlAHhXW5YY1TLpz1rh-TCr8g_7v9O1KLuO7JKSuy9YK4OwbkOLb5PIouzYbF0JZTZyyRBBxzgiEuEjPN1KTYs7J-d9nEJRrC-XaQrm2UH5ZWCZO__7uV_9jGPkE7vSbcg |
CitedBy_id | crossref_primary_10_1093_jxb_erac334 crossref_primary_10_3390_ijms23084209 crossref_primary_10_1016_j_bbamcr_2019_01_004 crossref_primary_10_3390_ijms21145018 crossref_primary_10_1083_jcb_201807166 crossref_primary_10_3389_fpls_2018_01496 crossref_primary_10_3389_fpls_2018_00754 crossref_primary_10_1111_pce_12973 crossref_primary_10_1111_tpj_13317 crossref_primary_10_1111_tpj_13028 crossref_primary_10_1002_cpz1_673 crossref_primary_10_3389_fpls_2017_00283 crossref_primary_10_1111_pce_12483 crossref_primary_10_1371_journal_pone_0146489 crossref_primary_10_1016_j_plantsci_2019_110357 crossref_primary_10_1002_2211_5463_12791 crossref_primary_10_1007_s00299_016_2053_4 crossref_primary_10_1016_j_ijbiomac_2023_129125 crossref_primary_10_1093_pcp_pcy234 |
ContentType | Journal Article |
Copyright | Copyright © 2012 Machettira, Groß, Tillmann, Weis, Englich, Sommer, Königer and Schleiff. 2012 |
Copyright_xml | – notice: Copyright © 2012 Machettira, Groß, Tillmann, Weis, Englich, Sommer, Königer and Schleiff. 2012 |
DBID | NPM AAYXX CITATION 7X8 5PM DOA |
DOI | 10.3389/fpls.2011.00118 |
DatabaseName | PubMed CrossRef MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals |
DatabaseTitle | PubMed CrossRef MEDLINE - Academic |
DatabaseTitleList | PubMed |
Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Botany |
EISSN | 1664-462X |
EndPage | 118 |
ExternalDocumentID | oai_doaj_org_article_74f99bd7961b4f9092b048f062e791f1 10_3389_fpls_2011_00118 22639631 |
Genre | Journal Article |
GroupedDBID | 5VS 9T4 AAFWJ AAKDD ACGFO ACGFS ACXDI ADBBV ADRAZ AENEX ALMA_UNASSIGNED_HOLDINGS AOIJS BCNDV EBD ECGQY GROUPED_DOAJ GX1 HYE IAO IEA IGS IPNFZ ISR KQ8 M48 M~E NPM OK1 PGMZT RIG RNS RPM AAYXX AFPKN CITATION 7X8 5PM |
ID | FETCH-LOGICAL-c459t-dbaff48591368c3a72a1be21cf5b7a1f7bd0bf62ec9d3f3ae9a14dc894b433f3 |
IEDL.DBID | RPM |
ISSN | 1664-462X |
IngestDate | Thu Sep 05 15:37:16 EDT 2024 Tue Sep 17 20:46:25 EDT 2024 Fri Aug 16 07:13:11 EDT 2024 Thu Sep 26 15:21:04 EDT 2024 Tue Oct 15 23:39:45 EDT 2024 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Keywords | lipid to protein ratio chloroplast envelopes membrane proteins membrane structure organelle structure |
Language | English |
License | This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited. |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c459t-dbaff48591368c3a72a1be21cf5b7a1f7bd0bf62ec9d3f3ae9a14dc894b433f3 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 This article was submitted to Frontiers in Technical Advances in Plant Science, a specialty of Frontiers in Plant Science. Anu B. Machettira and Lucia E. Groß have contributed equally to this work. Edited by: Anja Geitmann, Université de Montréal, Canada Reviewed by: Maureen Hanson, Cornell University, USA; Richard S. Smith, University of Bern, Switzerland; Carole Dabney-Smith, Miami University, USA |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355639/ |
PMID | 22639631 |
PQID | 1017763002 |
PQPubID | 23479 |
PageCount | 1 |
ParticipantIDs | doaj_primary_oai_doaj_org_article_74f99bd7961b4f9092b048f062e791f1 pubmedcentral_primary_oai_pubmedcentral_nih_gov_3355639 proquest_miscellaneous_1017763002 crossref_primary_10_3389_fpls_2011_00118 pubmed_primary_22639631 |
PublicationCentury | 2000 |
PublicationDate | 2012-01-01 |
PublicationDateYYYYMMDD | 2012-01-01 |
PublicationDate_xml | – month: 01 year: 2012 text: 2012-01-01 day: 01 |
PublicationDecade | 2010 |
PublicationPlace | Switzerland |
PublicationPlace_xml | – name: Switzerland |
PublicationTitle | Frontiers in plant science |
PublicationTitleAlternate | Front Plant Sci |
PublicationYear | 2012 |
Publisher | Frontiers Research Foundation Frontiers Media S.A |
Publisher_xml | – name: Frontiers Research Foundation – name: Frontiers Media S.A |
References | 18559960 - Plant Cell. 2008 Jun;20(6):1555-66 12080093 - Genes Dev. 2002 Jun 15;16(12):1555-67 21825140 - Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13841-6 11024463 - FEBS Lett. 2000 Oct 6;482(3):215-9 16461275 - Curr Biol. 2006 Feb 7;16(3):221-9 21120657 - Plant Cell Rep. 2011 Feb;30(2):177-93 15102061 - J Microsc. 2004 May;214(Pt 2):124-37 10948212 - J Exp Bot. 2000 May;51(346):865-71 11739803 - Mol Biol Cell. 2001 Dec;12(12):4090-102 11257114 - J Cell Biol. 2001 Mar 19;152(6):1123-34 15519309 - Biochim Biophys Acta. 2004 Nov 3;1666(1-2):62-87 19561168 - Plant Cell. 2009 Jun;21(6):1625-31 21448009 - Plant Signal Behav. 2011 May;6(5):715-8 14523248 - Plant Cell. 2003 Oct;15(10):2357-69 11402190 - Plant Physiol. 2001 Jun;126(2):601-12 15018639 - BMC Plant Biol. 2004 Feb 10;4:2 20424177 - Plant Cell. 2010 Apr;22(4):1333-43 16997872 - Biophys J. 2006 Dec 15;91(12):4427-39 21274561 - Planta. 2011 May;233(5):961-70 18294954 - Biochim Biophys Acta. 2008 Jul-Aug;1778(7-8):1545-75 9197266 - Science. 1997 Jun 27;276(5321):2039-42 8700911 - Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):2219-23 16384899 - Plant Physiol. 2006 Feb;140(2):466-83 18216768 - Nat Rev Mol Cell Biol. 2008 Feb;9(2):112-24 17240988 - Biochemistry. 2007 Jan 30;46(4):1042-54 19572810 - Annu Rev Cell Dev Biol. 2009;25:71-91 7159561 - Biochemistry. 1982 Dec 21;21(26):6790-8 18543065 - Plant Mol Biol. 2008 Sep;68(1-2):159-71 18643969 - Plant J. 2008 Nov;56(3):364-75 12880861 - J Chromatogr B Analyt Technol Biomed Life Sci. 2003 Aug 5;793(1):141-50 15699062 - J Exp Bot. 2005 Mar;56(413):787-97 19036033 - Plant J. 2009 Mar;57(6):1128-39 10737809 - Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 21330493 - Plant Physiol. 2011 Apr;155(4):1486-92 19175770 - Plant J. 2009 May;58(4):694-705 16545471 - Biochim Biophys Acta. 2006 May-Jun;1763(5-6):430-41 21874592 - Plant Mol Biol. 2011 Nov;77(4-5):381-90 3292536 - J Cell Biol. 1988 Jul;107(1):101-14 19060109 - Plant Cell. 2008 Dec;20(12):3405-17 18643950 - Plant Cell Environ. 2008 Oct;31(10):1470-83 17603748 - Protoplasma. 2007;231(3-4):183-92 17951454 - Plant Physiol. 2007 Dec;145(4):1637-46 21683788 - Cell Signal. 2011 Oct;23(10):1534-45 10406127 - Plant J. 1999 May;18(4):455-63 14684843 - Plant Physiol. 2004 Jan;134(1):255-64 22645566 - Front Plant Sci. 2012;3:7 14611963 - Curr Opin Plant Biol. 2003 Dec;6(6):622-8 20505352 - Plant Signal Behav. 2010 Jul;5(7):856-9 9668138 - Plant Cell. 1998 Jul;10(7):1207-16 12172018 - Plant Cell. 2002 Aug;14(8):1723-35 21395885 - Plant J. 2011 Jun;66(5):877-89 15868211 - Protoplasma. 2005 Apr;225(1-2):33-42 18193273 - Planta. 2008 Apr;227(5):1151-9 17351732 - Protoplasma. 2007;230(1-2):23-30 18466306 - Plant J. 2008 Sep;55(5):734-45 18088332 - Plant Cell Environ. 2008 May;31(5):646-57 20688079 - J Mol Biol. 2010 Sep 24;402(3):510-23 16510519 - J Exp Bot. 2006;57(6):1275-80 14754918 - J Exp Bot. 2004 Mar;55(397):595-604 12729927 - Biochim Biophys Acta. 2003 May 2;1612(1):1-40 21309866 - Plant J. 2011 May;66(4):656-68 19380350 - Plant Cell Physiol. 2009 Jun;50(6):1032-40 9810221 - Trends Biochem Sci. 1998 Oct;23(10):369-74 12228580 - Plant Physiol. 1995 Sep;109(1):15-30 15262942 - J Bacteriol. 2004 Aug;186(15):5052-61 |
References_xml | |
SSID | ssj0000500997 |
Score | 2.1638262 |
Snippet | Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is well established that lipids affect protein functioning and... Organelles are surrounded by membranes with a distinct lipid and protein composition. While it is established that lipids affect protein functioning and vice... |
SourceID | doaj pubmedcentral proquest crossref pubmed |
SourceType | Open Website Open Access Repository Aggregation Database Index Database |
StartPage | 118 |
SubjectTerms | alpha-helical and beta barrel proteins chloroplast envelopes lipid to protein ratio Membrane Proteins membrane structure Mitochondria Plant Science |
SummonAdditionalLinks | – databaseName: DOAJ Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1LS8NAEF6kePAivq0vInjwEprdbLKZoxVLEfRUobeQfVHBJsWmB_-9s9m0NCJ48RY2G3b4Zsh-s5l8Q8gdiwoMFQmhNUaGXBgaSrA8VKnFhIgDi5ruDS-v6fiNP0-T6VarL1cT5uWBPXADwS2A1AJSKvEyAiYx6GyUMiOAWp_40GQrmfKq3o76CK_lg4vCwC4-lq1ip_vZsrMNNWr9v1HMn5WSW1vP6IDst5wxePC2HpIdUx6R3WGFvO7rmDjBe9eyMsDsGv2kg3ml255cQWUDNcOMvFogSa6DuZljclwanILwNgfqJ2Qyepo8jsO2KUKoeAJ1qGVhLXeqc3GaqbgQrKDSMKpsIkVBrZA6khbRUaBjGxcGCsq1yoBLHuPAKemVVWnOSUANGG250pIprhjLjKaRBFpAagVTrE_u1xDlCy99kWPK4NDMHZq5Q7Opicv6ZOgg3ExzmtXNAHoybz2Z_-XJPrldOyDHGHcfLhCRarV0ZWhCOG0wtOnMO2SzFNLHGF8i-LTouKpjS_dO-T5rdLTj2KmjwcV_GH9J9hAO5g9nrkiv_lyZa6QrtbxpIvMb0Nbpng priority: 102 providerName: Directory of Open Access Journals – databaseName: Scholars Portal Open Access Journals dbid: M48 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV07T8MwELagMLAg3pSXgsTAEogfjesBIYqoKqQyUalbFL8oEk1KWyT677lLUqCoA1vk2Irz3dn-znG-I-SCRSm4ilahd06HQjoaauVFaGIPAZFQLCqyN3Sf4k5PPPYb_Z90QBWAk6WhHeaT6o3frj7fZ7cw4G8w4oT19tqP3iaVGCf-R7lK1pjgAt29W3H9Uugb2ZAs5X2WtVtYmQoB_2Ws8-_hyV-rUXuLbFY0Mrgr7b5NVly2Q9ZbOVC92S5BDXzMYhlCwA2ms8Ewt1WariD3gRlAkJ6PgDdPg6EbQrycOagCiBd77Hvkuf3wfN8JqzwJoRENNQ2tTr0XKETH46bhqWQp1Y5R4xtaptRLbSPtY-aMstzz1KmUCmuaSmjBoWCf1LI8c4ckoE4564WxmhlhGGs6SyOtaKpiL5lhdXI5hygZlWoYCUQRiGaCaCaIZnFMrlknLYTwuxrKWBcF-fglqUZFIoVXSlupYqrhMlJMw4ziI-irVNTTOjmfGyABt8dvGYBI_jHBk2lSolwY9OmgNMj3o4BRcphXoLVcMNVCXxbvZK-DQlqbcxRMU0f_eO4x2YC3ZeV2zAmpTccf7hQIylSfFY73BbXW5z4 priority: 102 providerName: Scholars Portal |
Title | Protein-induced modulation of chloroplast membrane morphology |
URI | https://www.ncbi.nlm.nih.gov/pubmed/22639631 https://search.proquest.com/docview/1017763002 https://pubmed.ncbi.nlm.nih.gov/PMC3355639 https://doaj.org/article/74f99bd7961b4f9092b048f062e791f1 |
Volume | 2 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LT9wwEB4B4sClAgp0oUWp1AOXsPFj48yxrKCoUlAPIO0til-AxCYrWA78e8ZOgljEqRcrcmx59M0onnHG3wD84llNpqIx9c7pVCrHUo1epib3FBBJ5Fms3lBe5Zc38u9sMluDyXAXJibtG31_2jzMT5v7u5hbuZib8ZAnNv5XToUItFY4Xod1JcS7EL0j9A5ej-pofGg9HPvFw1NP1hnuWQb-X07Tc8FWNqPI2f-Zo_kxX_LdBnSxDV96zzH53Um4A2uu2YXNs5a8u5evEGjvQ-HKNNTiMM4mZWv7ylxJ65PpHcXl7YJc5WVSujmFyI2jIQRyPFbfg-uL8-vpZdqXRkiNnOAytbr2XgbuOZEXRtSK10w7zoyfaFUzr7TNtM-5M2iFF7XDmklrCpRaCurYh42mbdw3SJhDZ700VnMjDeeFsyzTyGrMveKGj-BkgKhadAQYFQUOAdgqAFsFYGNmXDGCswDh27DAXB072sfbqtdfpaRH1FZhzjQ9Zsg1fUR8RrIqZJ6N4OeggIosPfy-IETa56eQjKZUYAgjmQ46hbwtNSh0BGpFVSuyrL4h44ps2r0xHf73zCPYIgx4dy7zHTaWj8_uB3kqS30cI3xq_8wYtaUsjqOtvgJC1e0g |
link.rule.ids | 230,315,733,786,790,870,891,2115,24346,27955,27956,53825,53827 |
linkProvider | National Library of Medicine |
linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB6VgkQvlGe7lEeQOHDJbuw48c6RrqgWaCoOC-otil-0ajdZtdkD_HrGTlJ1Ky5wi2wnnsxnxzPO-BuA9zypaKgojJ21KhbSslihE7HOHTlEAnkSsjcUJ_n8u_hymp1uQTachQlB-1qdj-vL5bg-PwuxlaulngxxYpNvxSxNPa0VTu7BfZqvPLvlpHeU3t7ukR2RD_WIE7e6vO7pOv1JS88AzOkBeco2lqPA2v83U_NuxOStJehoF34MwneRJxfjdavG-vcdXsd_frvH8Kg3SqOPXfUT2LL1U3hw2JDh-OsZeEZ9nxMz9mk-tDVR0Zg-6VfUuGh2Ri5_syIrvI0KuyTvu7bUhPALO_bPYXH0aTGbx33WhViLDNvYqMo54Wnt0nyq00ryiinLmXaZkhVzUplEuZxbjSZ1aWWxYsLoKQolUip4Adt1U9t9iJhFa5zQRnEtNOdTa1iikFWYO8k1H8GHQfflquPWKMkn8YiVHrHSIxaC7qYjOPTY3DTzpNihoLn6WfbKK6VwiMpIzJmiywS5ou-TS0hWicyxEbwbkC1pEvk_I6SRZn3t49yk9ORjJNNeh_RNV8NIGYHcGAMbsmzWELKBqLtH8uV_3_kWHs4XxXF5_Pnk6wHskD54t_3zCrbbq7V9TQZRq96E4f8HsqcMZw |
linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB5BQagXyrNdyiNIHLhkEzveeH2kC6vy2KqHIlVcoowftGo3idrsAX49YyepditOvUWOE9vz2cmM8-UbgA88LWmqoIqdtRgLaVmMyolY544CIqF4GrI3LI7yw5_i2-nkdC3VVyDtazwfV5fLcXV-FriVzVInA08sOV7MsszLWqmkMS65Dw9ozXK5Fqh3st7e95GdmA-1qhLXXF73kp3-b0uvAszpJnnGNl5JQbn_f-7mbdbk2mtovgO_hgF07JOL8arFsf57S9vxTiN8Ao975zT61FV5Cvds9QweHtTkQP55Dl5Z3-fGjH26D21NtKhNn_wrql00O6PQv27IG2-jhV1SFF5ZqkI4hp37F3Ay_3IyO4z77AuxFhPVxgZL54SXt8vyqc5KyUuGljPtJihL5iSaFF3OrVYmc1lpVcmE0VMlUGRU8BK2qrqyexAxq6xxQhvkWmjOp9awFBUrVe4k13wEHwf7F02nsVFQbOJRKzxqhUctkO-mIzjw-NxU8-LYoaC--l30BiykcEqhkSpnSIep4kjPKZdSX6Vijo3g_YBuQYvJfyEhi9Sra893k9KLkFGfdju0b5oaZssI5MY82OjL5hlCNwh292i-uvOV7-DR8ed58ePr0fd92CZz8G4X6DVstVcr-4b8ohbfhhXwDxHvDuc |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Protein-induced+modulation+of+chloroplast+membrane+morphology&rft.jtitle=Frontiers+in+plant+science&rft.au=Machettira%2C+Anu+B&rft.au=Gro%C3%9F%2C+Lucia+E&rft.au=Tillmann%2C+Bodo&rft.au=Weis%2C+Benjamin+L&rft.date=2012-01-01&rft.eissn=1664-462X&rft.volume=2&rft.spage=118&rft.epage=118&rft_id=info:doi/10.3389%2Ffpls.2011.00118&rft.externalDBID=NO_FULL_TEXT |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-462X&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-462X&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-462X&client=summon |