Abstract
Chloroplast function is orchestrated by the organelle's intricate architecture. By combining cryo-focused ion beam milling of vitreous Chlamydomonas cells with cryo-electron tomography, we acquired three-dimensional structures of the chloroplast in its native state within the cell. Chloroplast envelope inner membrane invaginations were frequently found in close association with thylakoid tips, and the tips of multiple thylakoid stacks converged at dynamic sites on the chloroplast envelope, implicating lipid transport in thylakoid biogenesis. Subtomogram averaging and nearest neighbor analysis revealed that RuBisCO complexes were hexagonally packed within the pyrenoid, with ∼15 nm between their centers. Thylakoid stacks and the pyrenoid were connected by cylindrical pyrenoid tubules, physically bridging the sites of light-dependent photosynthesis and light-independent carbon fixation. Multiple parallel minitubules were bundled within each pyrenoid tubule, possibly serving as conduits for the targeted one-dimensional diffusion of small molecules such as ATP and sugars between the chloroplast stroma and the pyrenoid matrix.
Authors
6
- Benjamin D Engel (first)
- Miroslava Schaffer (additional)
- Luis Kuhn Cuellar (additional)
- Elizabeth Villa (additional)
- Jürgen M Plitzko (additional)
- Wolfgang Baumeister (additional)
References
125
Referenced
224
10.1038/sj.emboj.7600366
/ The EMBO Journal / Cryo-electron microscopy of vitreous sections by Al-Amoudi (2004)10.1016/j.jsb.2005.01.003
/ Journal of Structural Biology / Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy by Al-Amoudi (2005)10.1105/tpc.113.113118
/ The Plant Cell / Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature by Armbruster (2013)10.1105/tpc.105.039859
/ The Plant Cell / Plastoglobules are lipoprotein subcompartments of the chloroplast that are permanently coupled to thylakoid membranes and contain biosynthetic enzymes by Austin (2006)10.1104/pp.110.170647
/ Plant Physiology / Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography by Austin (2011)10.1016/0014-5793(79)80875-3
/ FEBS Letters / A mechanism for controlling the stacking and unstacking of chloroplast thylakoid membranes by Barber (1979)10.1016/S0962-8924(98)01423-8
/ Trends in Cell Biology / Electron tomography of molecules and cells by Baumeister (1999)10.1126/science.1055071
/ Science / Biospheric primary production during an ENSO transition by Behrenfeld (2001)10.1145/361002.361007
/ Communications of the ACM / Multidimensional binary search trees used for associative searching by Bentley (1975)10.1016/j.tplants.2014.05.008
/ Trends in Plant Science / The Chlamydomonas genome project: a decade on by Blaby (2014)10.1371/journal.pone.0049063
/ PLOS ONE / Phosphorylation controls the localization and activation of the lumenal carbonic anhydrase in Chlamydomonas reinhardtii by Blanco-Rivero (2012)10.1104/pp.116.4.1585
/ Plant Physiology / The intracellular localization of ribulose-1,5-bisphosphate Carboxylase/Oxygenase in Chlamydomonas reinhardtii by Borkhsenious (1998)10.1016/j.micron.2010.07.003
/ Micron / Cryo-electron tomography on vitrified sections: a critical analysis of benefits and limitations for structural cell biology by Bouchet-Marquis (2011)10.1016/j.molcel.2010.08.003
/ Molecular Cell / The three-dimensional organization of polyribosomes in intact human cells by Brandt (2010)10.1016/j.cell.2008.11.016
/ Cell / The native 3D organization of bacterial polysomes by Brandt (2009)10.1016/j.jsb.2013.03.002
/ Journal of Structural Biology / Fast and accurate reference-free alignment of subtomograms by Chen (2013)10.1039/b507310n
/ Photochemical & Photobiological Sciences / Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue by Chow (2005)10.1038/226421a0
/ Nature / Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs by Crowther (1970)10.1105/tpc.109.071431
/ The Plant Cell / Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea by Daum (2010)10.1016/j.jsb.2013.05.016
/ Journal of Structural Biology / In-situ integrity control of frozen-hydrated, vitreous lamellas prepared by the cryo-focused ion beam-scanning electron microscope by de Winter (2013)10.1016/S1360-1385(01)02018-0
/ Trends in Plant Science / Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii by Dent (2001)10.1017/S0033583500004297
/ Quarterly Reviews of Biophysics / Cryo-electron microscopy of vitrified specimens by Dubochet (1988)10.1126/science.1093087
/ Science / Architecture of the photosynthetic oxygen-evolving Center by Ferreira (2004)10.1126/science.281.5374.237
/ Science / Primary production of the biosphere: integrating terrestrial and oceanic components by Field (1998)10.1128/MMBR.44.4.572-630.1980
/ Microbiological Reviews / Light Antennas in phototactic algae by Foster (1980)10.1073/pnas.172520299
/ Proceedings of the National Academy of Sciences of USA / Identification of macromolecular complexes in cryoelectron tomograms of phantom cells by Frangakis (2002)10.1016/j.ultramic.2013.11.008
/ Ultramicroscopy / Coordinate transformation based cryo-correlative methods for electron tomography and focused ion beam milling by Fukuda (2014)10.1016/S0003-9365(11)80297-6
/ Archiv für Protistenkunde / Morphodynamical changes of the chloroplast of Chlamydomonas reinhardtii during the 1st round of division by Gaffal (1995)10.1111/j.1365-313X.2010.04225.x
/ The Plant Journal / The chloroplast protein CPSAR1, dually localized in the stroma and the inner envelope membrane, is involved in thylakoid biogenesis by Garcia (2010)10.1074/jbc.M110.124230
/ The Journal of Biological Chemistry / Functional hybrid rubisco enzymes with plant small subunits and algal large subunits: engineered rbcS cDNA for expression in Chlamydomonas by Genkov (2010)10.1016/S0022-5320(62)90038-2
/ Journal of Ultrastructure Research / The ultrastructure of the chloroplasts of algae by Gibbs (1962)10.1083/jcb.48.3.594
/ The Journal of Cell Biology / Structural differentiation of stacked and unstacked chloroplast membranes. Freeze-etch electron microscopy of wild-type and mutant strains of Chlamydomonas by Goodenough (1971)10.1128/ec.05242-11
/ Eukaryot Cell / Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost by Goodson (2011)10.1111/j.1365-313X.2011.04541.x
/ The Plant Journal / Chloroplast genomes of photosynthetic eukaryotes by Green (2011)10.1016/0006-3002(63)91620-2
/ Biochimica Et Biophysica Acta / The osmiophilic globules of chloroplasts: I. Osmiophilic globules as a normal component of chloroplasts and their isolation and composition in Vicia faba L by Greenwood (1963)10.1007/BF02859154
/ The Botanical Review / The pyrenoid by Griffiths (1970)10.1016/S1369-5266(99)00053-9
/ Current Opinion in Plant Biology / Chlamydomonas reinhardtii and photosynthesis: genetics to genomics by Grossman (2000)10.1111/j.1365-2818.2008.01972.x
/ Journal of Microscopy / Compression and crevasses in vitreous sections under different cutting conditions by Han (2008)10.1104/pp.103.023481
/ Plant Physiology / The Chlamydomonas reinhardtii cia3 mutant lacking a thylakoid lumen-localized carbonic anhydrase is limited by CO2 supply to rubisco and not photosystem II function in vivo by Hanson (2003){'key': 'bib40', 'first-page': '2000', 'volume-title': 'The Chlamydomonas Sourcebook', 'author': 'Harris', 'year': '2009'}
/ The Chlamydomonas Sourcebook by Harris (2009)10.1016/j.jsb.2010.07.004
/ Journal of Structural Biology / The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy by Hayles (2010)10.1111/j.1365-2818.2007.01775.x
/ Journal of Microscopy / A technique for improved focused ion beam milling of cryo-prepared life science specimens by Hayles (2007)10.1371/journal.pone.0000749
/ PLOS ONE / 3-D ultrastructure of O. tauri: electron cryotomography of an entire eukaryotic cell by Henderson (2007)10.1007/BF01937960
/ Planta / Structure and Morphogenesis of lamellar systems in grana-containing chloroplasts by Heslop-Harrison (1963)10.1083/jcb.1.6.605
/ The Journal of Biophysical and Biochemical Cytology / ULTRASTRUCTURE OF THE LAMELLAE AND GRANA IN THE CHLOROPLASTS OF ZEA MAYS L by Hodge (1955)10.1083/jcb.37.3.831
/ The Journal of Cell Biology / The presence of a crystalline matrix in pyrenoids of the diatom, Achnanthes brevipes by Holdsworth (1968)10.1083/jcb.51.2.499
/ The Journal of Cell Biology / The isolation and partial characterization of the pyrenoid protein of Eremosphaera viridis by Holdsworth (1971)10.1016/j.jsb.2011.12.003
/ Journal of Structural Biology / PyTom: a python-based toolbox for localization of macromolecules in cryo-electron tomograms and subtomogram analysis by Hrabe (2012)10.1016/j.jsb.2013.10.019
/ Journal of Structural Biology / Practical workflow for cryo focused-ion-beam milling of tissues and cells for cryo-TEM tomography by Hsieh (2014)10.1016/S1047-8477(02)00034-5
/ Journal of Structural Biology / Electron tomographic analysis of frozen-hydrated tissue sections by Hsieh (2002)10.1016/0263-7855(96)00018-5
/ Journal of Molecular Graphics / VMD: visual molecular dynamics by Humphrey (1996)10.1016/j.jmb.2007.06.059
/ Journal of Molecular Biology / The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography by Iancu (2007)10.1016/j.jmb.2009.11.019
/ Journal of Molecular Biology / Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells by Iancu (2010)10.1038/ismej.2010.36
/ The ISME Journal / Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean by Jardillier (2010)10.1093/emboj/17.5.1208
/ The EMBO Journal / A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2 by Karlsson (1998)10.1016/j.pbi.2004.03.009
/ Current Opinion in Plant Biology / Green light for galactolipid trafficking by Kelly (2004)10.1371/journal.pone.0059898
/ PLOS ONE / New putative chloroplast vesicle transport components and cargo proteins revealed using a bioinformatics approach: an Arabidopsis model by Khan (2013)10.1073/pnas.1104141109
/ Proceedings of the National Academy of Sciences of the USA / Dynamic control of protein diffusion within the granal thylakoid lumen by Kirchhoff (2011)10.1021/bi900267r
/ Biochemistry / Photosynthetic system in Blastochloris viridis revisited by Konorty (2009)10.1016/j.jsb.2007.09.014
/ Journal of Structural Biology / Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseudomonas viridis cells by Konorty (2008)10.1016/j.jsb.2011.06.003
/ Journal of Structural Biology / Computer controlled cryo-electron microscopy–TOM2 a software package for high-throughput applications by Korinek (2011)10.1016/j.bbabio.2010.11.007
/ Biochimica Et Biophysica Acta / Fine structure of granal thylakoid membrane organization using cryo electron tomography by Kouřil (2011)10.1242/jcs.5.1.251
/ Journal of Cell Science / The crystal lattice of the pyrenoid matrix of Prorocentrum micans by Kowallik (1969)10.1007/s00294-008-0224-8
/ Current Genetics / The green algal eyespot apparatus: a primordial visual system and more? by Kreimer (2009){'key': 'bib65', 'first-page': '101', 'article-title': 'Reflection confocal laser scanning microscopy of eyespots in flagellated green algae', 'volume': '53', 'author': 'Kreimer', 'year': '1990', 'journal-title': 'European Journal of Cell Biology'}
/ European Journal of Cell Biology / Reflection confocal laser scanning microscopy of eyespots in flagellated green algae by Kreimer (1990)10.1073/pnas.061500998
/ Proceedings of the National Academy of Sciences of the USA / VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation by Kroll (2001)10.1007/BF00413518
/ Archives of Microbiology / Thylakoid centers: structures associated with the cyanobacterial photosynthetic membrane system by Kunkel (1982)10.1104/pp.83.3.602
/ Plant Physiology / Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase in the pyrenoid and thylakoid region of the chloroplast of Chlamydomonas reinhardtii by Lacoste-Royal (1987)10.1073/pnas.1200881109
/ Proceedings of the National Academy of Sciences of the USA / Contribution of cryoelectron microscopy of vitreous sections to the understanding of biological membrane structure by Leforestier (2012)10.4161/psb.6.4.14946
/ Plant Signaling & Behavior / Insights into the complex 3-D architecture of thylakoid membranes in unicellular cyanobacterium Cyanothece sp. ATCC 51142 by Liberton (2011a)10.1104/pp.110.165332
/ Plant Physiology / Unique thylakoid membrane architecture of a unicellular N2-fixing cyanobacterium revealed by electron tomography by Liberton (2011b)10.1074/jbc.M703896200
/ The Journal of Biological Chemistry / Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA by Long (2007)10.1104/pp.110.154948
/ Plant Physiology / Functional cyanobacterial beta-carboxysomes have an absolute requirement for both long and short forms of the CcmM protein by Long (2010)10.1104/pp.111.173922
/ Plant Physiology / Identification of a novel gene, CIA6, required for normal pyrenoid formation in Chlamydomonas reinhardtii by Ma (2011)10.1038/nmeth1014
/ Nature Methods / Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy by Marko (2007)10.1006/jsbi.1997.3919
/ Journal of Structural Biology / Dual-axis tomography: an approach with alignment methods that preserve resolution by Mastronarde (1997)10.1016/j.jsb.2005.07.007
/ Journal of Structural Biology / Automated electron microscope tomography using robust prediction of specimen movements by Mastronarde (2005)10.1139/b91-134
/ Canadian Journal of Botany / Composition and function of pyrenoids: cytochemical and immunocytochemical approaches by McKay (1991)10.1093/jxb/ers390
/ Journal of Experimental Botany / Origins and diversity of eukaryotic CO2-concentrating mechanisms: lessons for the future by Meyer (2013)10.1073/pnas.1210993109
/ Proceedings of the National Academy of Sciences of the USA / Rubisco small-subunit alpha-helices control pyrenoid formation in Chlamydomonas by Meyer (2012)10.1093/nar/gkp889
/ Nucleic Acids Research / BioNumbers–the database of key numbers in molecular and cell biology by Milo (2010)10.1104/pp.114.246918
/ Plant Physiology / Dynamics of carbon-concentrating mechanism induction and protein Relocalization during the dark-to-light transition in Synchronized Chlamydomonas reinhardtii by Mitchell (2014)10.1007/s00227-006-0321-5
/ Marine Biology / Differences in chloroplast ultrastructure of Phaeocystis antarctica in low and high light by Moisan (2006)10.1007/s11120-011-9635-3
/ Photosynthesis Research / The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles by Moroney (2011)10.1016/S1360-1385(03)00015-3
/ Trends in Plant Science / Granum revisited. A three-dimensional model – where things fall into place by Mustárdy (2003)10.1038/sj.emboj.7601594
/ The EMBO Journal / Thylakoid membrane perforations and connectivity enable intracellular traffic in cyanobacteria by Nevo (2007)10.1016/j.jsb.2004.10.006
/ Journal of Structural Biology / TOM software toolbox: acquisition and analysis for electron tomography by Nickell (2005)10.1105/tpc.111.092692
/ The Plant Cell / Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas by Nordhues (2012)10.1083/jcb.35.3.521
/ The Journal of Cell Biology / Biogenesis of chloroplast membranes. I. Plastid dedifferentiation in a dark-grown algal mutant (Chlamydomonas reinhardii) by Ohad (1967a)10.1083/jcb.35.3.553
/ The Journal of Cell Biology / Biogenesis of chloroplast membranes. II. Plastid differentiation during greening of a dark-grown algal mutant (Chlamydomonas reinhardii) by Ohad (1967b)10.1242/jcs.5.1.299
/ Journal of Cell Science / Ultrastructural observations on deep-etched thylakoids by Park (1969)10.1073/pnas.0910866107
/ Proceedings of the National Academy of Sciences of the USA / Structural basis of the oxidative activation of the carboxysomal gamma-carbonic anhydrase, CcmM by Peña (2010)10.1002/jcc.20084
/ Journal of Computational Chemistry / UCSF Chimera–a visualization system for exploratory research and analysis by Pettersen (2004)10.1016/j.str.2012.06.010
/ Structure / Structure and 3D arrangement of endoplasmic reticulum membrane-associated ribosomes by Pfeffer (2012)10.1093/jxb/eru090
/ Journal of Experimental Botany / Structure and dynamics of thylakoids in land plants by Pribil (2014)10.1159/000351342
/ Journal of Molecular Microbiology and Biotechnology / Cyanobacterial carboxysomes: microcompartments that facilitate CO2 fixation by Rae (2013)10.1046/j.1365-3040.1997.d01-67.x
/ Plant Cell & Environment / CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? by Raven (1997)10.1007/BF00206252
/ Planta / Chlamydomonas reinhardtii mutants without ribulose-1,5-bisphosphate carboxylase-oxygenase lack a detectable pyrenoid by Rawat (1996)10.1016/j.jsb.2010.02.011
/ Journal of Structural Biology / Micromachining tools and correlative approaches for cellular cryo-electron tomography by Rigort (2010)10.1073/pnas.1201333109
/ Proceedings of the National Academy of Sciences of the USA / Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography by Rigort (2012a)10.1016/b978-0-12-416026-2.00014-5
/ Methods in Cell Biology / Integrative approaches for cellular cryo-electron tomography: correlative imaging and focused ion beam micromachining by Rigort (2012b)10.1083/jcb.3.3.463
/ The Journal of Biophysical and Biochemical Cytology / Structure and development of the chloroplast in Chlamydomonas. I. The normal green cell by Sager (1957)10.21769/BioProtoc.1575
/ Bio-protocol / Cryo-focused ion beam sample preparation for imaging vitreous cells by cryo-electron tomography by Schaffer (2015)10.1016/j.jmb.2006.09.024
/ Journal of Molecular Biology / Structure of Halothiobacillus neapolitanus carboxysomes by cryo-electron tomography by Schmid (2006)10.1073/pnas.1209860109
/ Proceedings of the National Academy of Sciences of the USA / Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii by Schottkowski (2012)10.1105/tpc.105.035030
/ The Plant Cell / Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography by Shimoni (2005)10.1016/j.bbabio.2012.02.014
/ Biochimica Et Biophysica Acta / Identification and functional role of the carbonic anhydrase Cah3 in thylakoid membranes of pyrenoid of Chlamydomonas reinhardtii by Sinetova (2012)10.1023/a:1024994525586
/ Photosynthesis Research / Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes by Staehelin (2003)10.1007/BF00393507
/ Planta / Composition and function of plastoglobuli: I. Isolation and purification from chloroplasts and chromoplasts by Steinmüller (1985)10.1105/tpc.111.093914
/ The Plant Cell / Initial steps of photosystem II de novo assembly and preloading with manganese take place in biogenesis centers in Synechocystis by Stengel (2012)10.1104/pp.85.1.152
/ Plant Physiology / Rubisco activase mediates ATP-dependent activation of ribulose bisphosphate carboxylase by Streusand (1987)10.1111/j.1365-2818.2012.03635.x
/ Journal of Microscopy / Thinning of large mammalian cells for cryo-TEM characterization by cryo-FIB milling by Strunk (2012)10.1104/pp.107.4.1387
/ Plant Physiology / In Situ association of Calvin cycle enzymes, ribulose-1,5-bisphosphate Carboxylase/Oxygenase activase, Ferredoxin-NADP+ Reductase, and Nitrite Reductase with thylakoid and pyrenoid membranes of Chlamydomonas reinhardtii chloroplasts as revealed by Immunoelectron microscopy by Suss (1995)10.1074/jbc.M107765200
/ The Journal of Biological Chemistry / First crystal structure of Rubisco from a green alga, Chlamydomonas reinhardtii by Taylor (2001)10.1007/s00425-002-0961-8
/ Planta / Isolation and characterisation of Chlamydomonas reinhardtii mutants with an impaired CO2-concentrating mechanism by Thyssen (2003)10.1128/jb.01948-06
/ Journal of Bacteriology / Cryo-electron tomography reveals the comparative three-dimensional architecture of Prochlorococcus, a globally important marine cyanobacterium by Ting (2007)10.1105/tpc.107.054882
/ The Plant Cell / Photosystem II assembly and repair are differentially localized in Chlamydomonas by Uniacke (2007)10.1073/pnas.0811268106
/ Proceedings of the National Academy of Sciences of the USA / Chloroplast protein targeting involves localized translation in Chlamydomonas by Uniacke (2009)10.1007/s00203-005-0027-y
/ Archives of Microbiology / The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803 by van de Meene (2006)10.1016/j.sbi.2013.08.006
/ Current Opinion in Structural Biology / Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography by Villa (2013)10.1111/j.1399-3054.1996.tb06687.x
/ Physiologia Plantarum / The induction of the CO2 concentrating mechanism in a starch-less mutant of Chlamydomonas reinhardtii by Villarejo (1996)10.1016/j.jsb.2012.07.003
/ Journal of Structural Biology / 3D structure determination of native mammalian cells using cryo-FIB and cryo-electron tomography by Wang (2012)10.1007/s12154-009-0033-7
/ Journal of Chemical Biology / Towards native-state imaging in biological context in the electron microscope by Weston (2009)10.1126/science.1214120
/ Science / Bubblegrams reveal the inner body of bacteriophage ϕKZ by Wu (2012)10.1104/pp.105.076083
/ Plant Physiology / Protein profiling of plastoglobules in chloroplasts and Chromoplasts. A Surprising site for differential accumulation of metabolic enzymes by Ytterberg (2006)
Dates
Type | When |
---|---|
Created | 10 years, 7 months ago (Jan. 13, 2015, 8:24 a.m.) |
Deposited | 1 year, 10 months ago (Oct. 11, 2023, 8:45 p.m.) |
Indexed | 3 weeks ago (July 30, 2025, 1:08 p.m.) |
Issued | 10 years, 7 months ago (Jan. 13, 2015) |
Published | 10 years, 7 months ago (Jan. 13, 2015) |
Published Online | 10 years, 7 months ago (Jan. 13, 2015) |
Funders
6
European Commission
10.13039/501100000780
Region: Europe
gov (National government)
Labels
26
- European Union
- Comisión Europea
- Europäische Kommission
- EU-Kommissionen
- Euroopa Komisjoni
- Ευρωπαϊκής Επιτροπής
- Европейската комисия
- Evropské komise
- Commission européenne
- Choimisiúin Eorpaigh
- Europskoj komisiji
- Commissione europea
- La Commissione europea
- Eiropas Komisiju
- Europos Komisijos
- Európai Bizottságról
- Europese Commissie
- Komisja Europejska
- Comissão Europeia
- Comisia Europeană
- Európskej komisii
- Evropski komisiji
- Euroopan komission
- Europeiska kommissionen
- EC
- EU
Awards
1
- 7th Framework Programme Grant HEALTH-F4-2008-201648/PROSPECTS
Alexander von Humboldt-Stiftung (Humboldt Foundation)
10.13039/100005156
Alexander von Humboldt-StiftungRegion: Europe
pri (Trusts, charities, foundations (both public and private))
Labels
5
- Humboldt-Stiftung
- Humboldt Foundation
- Alexander von Humboldt Foundation
- Humboldt Stiftung
- AvH
Awards
1
- Postdoctoral Research Fellowship
German Academic Exchange Service
10.13039/501100001655
Deutscher Akademischer AustauschdienstRegion: Europe
pri (Universities (academic only))
Labels
2
- German Academic Exchange Service
- DAAD
Awards
1
- CONACyT-DAAD Graduate Scholarship
Deutsche Forschungsgemeinschaft
10.13039/501100001659
Region: Europe
gov (National government)
Labels
3
- German Research Association
- German Research Foundation
- DFG
Awards
1
- Excellence Clusters CIPSM and SFB 1035
Bundesministerium für Bildung und Forschung (Federal Ministry of Education and Research)
10.13039/501100002347
Bundesministerium für Bildung und ForschungRegion: Europe
gov (National government)
Labels
2
- Federal Ministry of Education and Research
- BMBF
Max-Planck-Gesellschaft (Max Planck Society)
10.13039/501100004189
Max-Planck-GesellschaftRegion: Europe
gov (Research institutes and centers)
Labels
4
- Max Planck Society for the Advancement of Science
- Max-Planck-Gesellschaft zur Förderung der Wissenschaften
- Max Planck Society
- MPG
Awards
1
- Inter-Institutional Research Initiative
@article{Engel_2015, title={Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography}, volume={4}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/elife.04889}, DOI={10.7554/elife.04889}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Engel, Benjamin D and Schaffer, Miroslava and Kuhn Cuellar, Luis and Villa, Elizabeth and Plitzko, Jürgen M and Baumeister, Wolfgang}, year={2015}, month=jan }