Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations

Breuers FKH, Bräutigam A, Geimer S, Welzel UY, Stefano G, Renna L, Brandizzi F, Weber APM (2012)
Frontiers in Plant Science 3: 7.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Breuers, Frederique K. H.; Bräutigam, AndreaUniBi ; Geimer, Stefan; Welzel, Ulla Y.; Stefano, Giovanni; Renna, Luciana; Brandizzi, Federica; Weber, Andreas P. M.
Abstract / Bemerkung
Two envelope membranes delimit plastids, the defining organelles of plant cells. The inner and outer envelope membranes are unique in their protein and lipid composition. Several studies have attempted to establish the proteome of these two membranes; however, differentiating between them is difficult due to their close proximity. Here, we describe a novel approach to distinguish the localization of proteins between the two membranes using a straightforward approach based on live cell imaging coupled with transient expression. We base our approach on analyses of the distribution of GFP-fusions, which were aimed to verify outer envelope membrane proteomics data. To distinguish between outer envelope and inner envelope protein localization, we used AtTOC64-GFP and AtTIC40-GFP, as respective controls. During our analyses, we observed membrane proliferations and loss of chloroplast shape in conditions of protein over-expression. The morphology of the proliferations varied in correlation with the suborganellar distribution of the over-expressed proteins. In particular, while layers of membranes built up in the inner envelope membrane, the outer envelope formed long extensions into the cytosol. Using electron microscopy, we showed that these extensions were stromules, a dynamic feature of plastids. Since the behavior of the membranes is different and is related to the protein localization, we propose that in vivo studies based on the analysis of morphological differences of the membranes can be used to distinguish between inner and outer envelope localizations of proteins. To demonstrate the applicability of this approach, we demonstrated the localization of AtLACS9 to the outer envelope membrane. We also discuss protein impact on membrane behavior and regulation of protein insertion into membranes, and provide new hypotheses on the formation of stromules.
Stichworte
chloroplast envelope; membrane proliferation; membrane protein; outer; envelope membrane; inner envelope membrane; LACS9; stromule
Erscheinungsjahr
2012
Zeitschriftentitel
Frontiers in Plant Science
Band
3
Art.-Nr.
7
ISSN
1664-462X
Page URI
https://pub.uni-bielefeld.de/record/2915154

Zitieren

Breuers FKH, Bräutigam A, Geimer S, et al. Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations. Frontiers in Plant Science. 2012;3: 7.
Breuers, F. K. H., Bräutigam, A., Geimer, S., Welzel, U. Y., Stefano, G., Renna, L., Brandizzi, F., et al. (2012). Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations. Frontiers in Plant Science, 3, 7. doi:10.3389/fpls.2012.00007
Breuers, Frederique K. H., Bräutigam, Andrea, Geimer, Stefan, Welzel, Ulla Y., Stefano, Giovanni, Renna, Luciana, Brandizzi, Federica, and Weber, Andreas P. M. 2012. “Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations”. Frontiers in Plant Science 3: 7.
Breuers, F. K. H., Bräutigam, A., Geimer, S., Welzel, U. Y., Stefano, G., Renna, L., Brandizzi, F., and Weber, A. P. M. (2012). Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations. Frontiers in Plant Science 3:7.
Breuers, F.K.H., et al., 2012. Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations. Frontiers in Plant Science, 3: 7.
F.K.H. Breuers, et al., “Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations”, Frontiers in Plant Science, vol. 3, 2012, : 7.
Breuers, F.K.H., Bräutigam, A., Geimer, S., Welzel, U.Y., Stefano, G., Renna, L., Brandizzi, F., Weber, A.P.M.: Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations. Frontiers in Plant Science. 3, : 7 (2012).
Breuers, Frederique K. H., Bräutigam, Andrea, Geimer, Stefan, Welzel, Ulla Y., Stefano, Giovanni, Renna, Luciana, Brandizzi, Federica, and Weber, Andreas P. M. “Dynamic remodeling of the plastid envelope membranes - a tool for chloroplast envelope in vivo localizations”. Frontiers in Plant Science 3 (2012): 7.
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26 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Unraveling Hidden Components of the Chloroplast Envelope Proteome: Opportunities and Limits of Better MS Sensitivity.
Bouchnak I, Brugière S, Moyet L, Le Gall S, Salvi D, Kuntz M, Tardif M, Rolland N., Mol Cell Proteomics 18(7), 2019
PMID: 30962257
Three-Dimensional Analysis of Chloroplast Structures Associated with Virus Infection.
Jin X, Jiang Z, Zhang K, Wang P, Cao X, Yue N, Wang X, Zhang X, Li Y, Li D, Kang BH, Zhang Y., Plant Physiol 176(1), 2018
PMID: 28821590
Stromules: Probing Formation and Function.
Hanson MR, Hines KM., Plant Physiol 176(1), 2018
PMID: 29097392
The major leaf ferredoxin Fd2 regulates plant innate immunity in Arabidopsis.
Wang M, Rui L, Yan H, Shi H, Zhao W, Lin JE, Zhang K, Blakeslee JJ, Mackey D, Tang D, Wei Z, Wang GL., Mol Plant Pathol 19(6), 2018
PMID: 28976113
Plastid Envelope-Localized Proteins Exhibit a Stochastic Spatiotemporal Relationship to Stromules.
Delfosse K, Wozny MR, Barton KA, Mathur N, Griffiths N, Mathur J., Front Plant Sci 9(), 2018
PMID: 29915611
Genome-wide identification and analysis of the ALTERNATIVE OXIDASE gene family in diploid and hexaploid wheat.
Brew-Appiah RAT, York ZB, Krishnan V, Roalson EH, Sanguinet KA., PLoS One 13(8), 2018
PMID: 30074999
New Insights Into Sunflower (Helianthus annuus L.) FatA and FatB Thioesterases, Their Regulation, Structure and Distribution.
Aznar-Moreno JA, Sánchez R, Gidda SK, Martínez-Force E, Moreno-Pérez AJ, Venegas Calerón M, Garcés R, Mullen RT, Salas JJ., Front Plant Sci 9(), 2018
PMID: 30459777
Engineering carbon fixation with artificial protein organelles.
Giessen TW, Silver PA., Curr Opin Biotechnol 46(), 2017
PMID: 28126670
Progress and challenges of engineering a biophysical CO2-concentrating mechanism into higher plants.
Rae BD, Long BM, Förster B, Nguyen ND, Velanis CN, Atkinson N, Hee WY, Mukherjee B, Price GD, McCormick AJ., J Exp Bot 68(14), 2017
PMID: 28444330
The DnaJ-Like Zinc-Finger Protein HCF222 Is Required for Thylakoid Membrane Biogenesis in Plants.
Hartings S, Paradies S, Karnuth B, Eisfeld S, Mehsing J, Wolff C, Levey T, Westhoff P, Meierhoff K., Plant Physiol 174(3), 2017
PMID: 28572458
Fatty Acid and Lipid Transport in Plant Cells.
Li N, Xu C, Li-Beisson Y, Philippar K., Trends Plant Sci 21(2), 2016
PMID: 26616197
Plant-Specific Preprotein and Amino Acid Transporter Proteins Are Required for tRNA Import into Mitochondria.
Murcha MW, Kubiszewski-Jakubiak S, Teixeira PF, Gügel IL, Kmiec B, Narsai R, Ivanova A, Megel C, Schock A, Kraus S, Berkowitz O, Glaser E, Philippar K, Maréchal-Drouard L, Soll J, Whelan J., Plant Physiol 172(4), 2016
PMID: 27789739
Fluorescent Protein Aided Insights on Plastids and their Extensions: A Critical Appraisal.
Delfosse K, Wozny MR, Jaipargas EA, Barton KA, Anderson C, Mathur J., Front Plant Sci 6(), 2015
PMID: 26834765
FAX1, a novel membrane protein mediating plastid fatty acid export.
Li N, Gügel IL, Giavalisco P, Zeisler V, Schreiber L, Soll J, Philippar K., PLoS Biol 13(2), 2015
PMID: 25646734
Remobilization of Phytol from Chlorophyll Degradation Is Essential for Tocopherol Synthesis and Growth of Arabidopsis.
Vom Dorp K, Hölzl G, Plohmann C, Eisenhut M, Abraham M, Weber AP, Hanson AD, Dörmann P., Plant Cell 27(10), 2015
PMID: 26452599
Division and dynamic morphology of plastids.
Osteryoung KW, Pyke KA., Annu Rev Plant Biol 65(), 2014
PMID: 24471836
The Arabidopsis Tellurite resistance C protein together with ALB3 is involved in photosystem II protein synthesis.
Schneider A, Steinberger I, Strissel H, Kunz HH, Manavski N, Meurer J, Burkhard G, Jarzombski S, Schünemann D, Geimer S, Flügge UI, Leister D., Plant J 78(2), 2014
PMID: 24612058
Transplastomic integration of a cyanobacterial bicarbonate transporter into tobacco chloroplasts.
Pengelly JJ, Förster B, von Caemmerer S, Badger MR, Price GD, Whitney SM., J Exp Bot 65(12), 2014
PMID: 24965541
Unknown components of the plastidial permeome.
Pick TR, Weber AP., Front Plant Sci 5(), 2014
PMID: 25191333
Proteomic analysis of the Cyanophora paradoxa muroplast provides clues on early events in plastid endosymbiosis.
Facchinelli F, Pribil M, Oster U, Ebert NJ, Bhattacharya D, Leister D, Weber AP., Planta 237(2), 2013
PMID: 23212214
PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters.
Pick TR, Bräutigam A, Schulz MA, Obata T, Fernie AR, Weber AP., Proc Natl Acad Sci U S A 110(8), 2013
PMID: 23382251
Protein-induced modulation of chloroplast membrane morphology.
Machettira AB, Groß LE, Tillmann B, Weis BL, Englich G, Sommer MS, Königer M, Schleiff E., Front Plant Sci 2(), 2011
PMID: 22639631

67 References

Daten bereitgestellt von Europe PubMed Central.

Toc64--a preprotein-receptor at the outer membrane with bipartide function.
Qbadou S, Becker T, Bionda T, Reger K, Ruprecht M, Soll J, Schleiff E., J. Mol. Biol. 367(5), 2007
PMID: 17306301
AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis.
Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I., Nat. Cell Biol. 10(2), 2008
PMID: 18193034
Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement.
Oikawa K, Yamasato A, Kong SG, Kasahara M, Nakai M, Takahashi F, Ogura Y, Kagawa T, Wada M., Plant Physiol. 148(2), 2008
PMID: 18715957
Stromules: a characteristic cell-specific feature of plastid morphology.
Natesan SK, Sullivan JA, Gray JC., J. Exp. Bot. 56(413), 2005
PMID: 15699062
Dynamic morphology of plastids and stromules in angiosperm plants.
Hanson MR, Sattarzadeh A., Plant Cell Environ. 31(5), 2007
PMID: 18088332
The chloroplast outer membrane protein CHUP1 interacts with actin and profilin.
Schmidt von Braun S, Schleiff E., Planta 227(5), 2008
PMID: 18193273
PPDB, the Plant Proteomics Database at Cornell.
Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ., Nucleic Acids Res. 37(Database issue), 2008
PMID: 18832363
Challenges to our current view on chloroplasts.
Reski R., Biol. Chem. 390(8), 2009
PMID: 19453278
Mechanisms of lipid transport involved in organelle biogenesis in plant cells.
Benning C., Annu. Rev. Cell Dev. Biol. 25(), 2009
PMID: 19572810
AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins.
Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N., Mol. Cell Proteomics 9(6), 2010
PMID: 20061580
Chloroplast import signals: the length requirement for translocation in vitro and in vivo.
Bionda T, Tillmann B, Simm S, Beilstein K, Ruprecht M, Schleiff E., J. Mol. Biol. 402(3), 2010
PMID: 20688079
Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane.
Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R., Plant Physiol. 152(1), 2009
PMID: 19933383
Myosin XI is required for actin-associated movement of plastid stromules.
Natesan SK, Sullivan JA, Gray JC., Mol Plant 2(6), 2009
PMID: 19995729
The chloroplast protein import machinery: a review.
Strittmatter P, Soll J, Bolter B., Methods Mol. Biol. 619(), 2010
PMID: 20419418
A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus.
Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L., Nat Commun 2(), 2011
PMID: 21934661
The Plastid Outer Envelope - A Highly Dynamic Interface between Plastid and Cytoplasm.
Breuers FK, Brautigam A, Weber AP., Front Plant Sci 2(), 2011
PMID: 22629266
Protein-induced modulation of chloroplast membrane morphology.
Machettira AB, Groß LE, Tillmann B, Weis BL, Englich G, Sommer MS, Koniger M, Schleiff E., Front Plant Sci 2(), 2011
PMID: 22639631
The metabolite transporters of the plastid envelope: an update.
Facchinelli F, Weber AP., Front Plant Sci 2(), 2011
PMID: 22645538
Membrane proteins.
Guidotti G., Annu. Rev. Biochem. 41(), 1972
PMID: 4263713
Plastid tubules of higher plants are tissue-specific and developmentally regulated.
Kohler RH, Hanson MR., J. Cell. Sci. 113 ( Pt 1)(), 2000
PMID: 10591627
Chloroplast tubules visualized in transplastomic plants expressing green fluorescent protein.
Shiina T, Hayashi K, Ishii N, Morikawa K, Toyoshima Y., Plant Cell Physiol. 41(3), 2000
PMID: 10805601
ULTRASTRUCTURE OF THE LAMELLAE AND GRANA IN THE CHLOROPLASTS OF ZEA MAYS L.
Hodge AJ, McLean JD, Mercer FV., J Biophys Biochem Cytol 1(6), 1955
PMID: 19866553
Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism.
Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N., Prog. Lipid Res. 49(2), 2009
PMID: 19879895
Exchange of protein molecules through connections between higher plant plastids.
Kohler RH, Cao J, Zipfel WR, Webb WW, Hanson MR., Science 276(5321), 1997
PMID: 9197266
Characterization of the activity of a plastid-targeted green fluorescent protein in Arabidopsis.
Tirlapur UK, Dahse I, Reiss B, Meurer J, Oelmuller R., Eur. J. Cell Biol. 78(4), 1999
PMID: 10350211
Toc64, a new component of the protein translocon of chloroplasts.
Sohrt K, Soll J., J. Cell Biol. 148(6), 2000
PMID: 10725334
Plastid and stromule morphogenesis in tomato.
Pyke KA, Howells CA., Ann. Bot. 90(5), 2002
PMID: 12466096
Chloroplast unusual positioning1 is essential for proper chloroplast positioning.
Oikawa K, Kasahara M, Kiyosue T, Kagawa T, Suetsugu N, Takahashi F, Kanegae T, Niwa Y, Kadota A, Wada M., Plant Cell 15(12), 2003
PMID: 14615600
Intracellular metabolite transporters in plants.
Linka N, Weber AP., Mol Plant 3(1), 2009
PMID: 20038549
Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana.
Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N., Mol. Cell Proteomics 2(5), 2003
PMID: 12766230
Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant.
Motohashi R, Ito T, Kobayashi M, Taji T, Nagata N, Asami T, Yoshida S, Yamaguchi-Shinozaki K, Shinozaki K., Plant J. 34(5), 2003
PMID: 12787252
Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon.
Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, Li HM., EMBO J. 22(12), 2003
PMID: 12805212
An electron microscope study of the mitochondrial structure.
PALADE GE., J. Histochem. Cytochem. 1(4), 1953
PMID: 13069686
A gateway cloning vector set for high-throughput functional analysis of genes in planta.
Curtis MD, Grossniklaus U., Plant Physiol. 133(2), 2003
PMID: 14555774
On the export of fatty acids from the chloroplast.
Koo AJ, Ohlrogge JB, Pollard M., J. Biol. Chem. 279(16), 2004
PMID: 14764601
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