DOI: 10.1073/pnas.1209860109. Biogenic membranes of the chloroplast in <i>Chlamydomonas reinhardtii</i>

Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii

10.1073/pnas.1209860109

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

The polypeptide subunits of the photosynthetic electron transport complexes in plants and algae are encoded by two genomes. Nuclear genome-encoded subunits are synthesized in the cytoplasm by 80S ribosomes, imported across the chloroplast envelope, and assembled with the subunits that are encoded by the plastid genome. Plastid genome-encoded subunits are synthesized by 70S chloroplast ribosomes directly into membranes that are widely believed to belong to the photosynthetic thylakoid vesicles. However, in situ evidence suggested that subunits of photosystem II are synthesized in specific regions within the chloroplast and cytoplasm of Chlamydomonas . Our results provide biochemical and in situ evidence of biogenic membranes that are localized to these translation zones. A “chloroplast translation membrane” is bound by the translation machinery and appears to be privileged for the synthesis of polypeptides encoded by the plastid genome. Membrane domains of the chloroplast envelope are located adjacent to the cytoplasmic translation zone and enriched in the translocons of the outer and inner chloroplast envelope membranes protein import complexes, suggesting a coordination of protein synthesis and import. Our findings contribute to a current realization that biogenic processes are compartmentalized within organelles and bacteria.

Bibliography

Schottkowski, M., Peters, M., Zhan, Y., Rifai, O., Zhang, Y., & Zerges, W. (2012). Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, 109(47), 19286â19291.

Authors 6

Marco Schottkowski (first)
Matthew Peters (additional)
Yu Zhan (additional)
Oussama Rifai (additional)
Ying Zhang (additional)
William Zerges (additional)

References 44 Referenced 43

10.1016/j.bbamcr.2011.06.011
10.1155/2012/287852
BL Weis, E Schleiff, W Zerges, Protein targeting to subcellular organelles via mRNA localization. Biochim Biophys Acta, 2012). / Biochim Biophys Acta / Protein targeting to subcellular organelles via mRNA localization by Weis BL (2012)
10.1016/j.tig.2012.03.008
10.1016/S0300-9084(00)00603-9
10.1105/tpc.107.054882
10.1073/pnas.0811268106
10.1105/tpc.107.051722
10.1021/bi035909j
10.1074/jbc.273.33.20935
10.1261/rna.5610403
10.1146/annurev.pp.30.060179.002233
10.1007/978-1-59745-028-7_2
10.1073/pnas.70.5.1554
10.1016/S0021-9258(19)63798-1
10.1016/j.pbi.2012.01.017
10.1074/jbc.M801917200
10.1016/0003-2697(91)90094-A
10.1002/pmic.200700205
10.1093/jxb/eri041
10.1074/jbc.M109.098954
10.1093/emboj/16.20.6095
10.1083/jcb.200805125
10.1046/j.1432-1327.2001.02111.x
10.1083/jcb.140.1.101
10.1023/A:1020246007858
10.1083/jcb.35.3.521
10.1007/s11103-011-9818-5
10.1111/j.1574-6968.2010.02096.x
10.1104/pp.125.4.2154
10.1111/j.1432-1033.1988.tb14366.x
10.1046/j.1432-1327.1999.00337.x
10.1073/pnas.46.1.83
10.1242/jcs.8.3.649
10.1016/0003-2697(85)90442-7
10.1023/A:1020470224740
J Sambrook, DW Russell Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY, Vol 3, pp A8.52–A8.55. (2001). / Molecular Cloning: A Laboratory Manual by Sambrook J (2001)
10.1007/BF02106183
10.1007/BF00333578
10.1074/jbc.274.15.10466
M Schroda, O Vallon, JP Whitelegge, CF Beck, F-A Wollman, The chloroplastic GrpE homolog of Chlamydomonas: Two isoforms generated by differential splicing. Plant Cell 13, 2823–2839 (2001). / Plant Cell / The chloroplastic GrpE homolog of Chlamydomonas: Two isoforms generated by differential splicing by Schroda M (2001)
10.1105/tpc.107.051722
10.1007/978-1-61779-005-8_2
10.1074/jbc.M806116200

Dates

Type	When
Created	12 years, 9 months ago (Nov. 6, 2012, 12:57 a.m.)
Deposited	3 years, 4 months ago (April 12, 2022, 8:58 p.m.)
Indexed	1 month, 3 weeks ago (June 27, 2025, 10:25 a.m.)
Issued	12 years, 9 months ago (Nov. 5, 2012)
Published	12 years, 9 months ago (Nov. 5, 2012)
Published Online	12 years, 9 months ago (Nov. 5, 2012)
Published Print	12 years, 9 months ago (Nov. 20, 2012)

Funders 0

None

BibTeX

@article{Schottkowski_2012, title={Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii}, volume={109}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1209860109}, DOI={10.1073/pnas.1209860109}, number={47}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Schottkowski, Marco and Peters, Matthew and Zhan, Yu and Rifai, Oussama and Zhang, Ying and Zerges, William}, year={2012}, month=nov, pages={19286–19291} }

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