ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane
Abstract
The plastids of cryptophytes, haptophytes, and heterokontophytes (stramenopiles) (together once known as chromists) are surrounded by four membranes, reflecting the origin of these plastids through secondary endosymbiosis. They share this trait with apicomplexans, which are alveolates, the plastids of which have been suggested to stem from the same secondary symbiotic event and therefore form a phylogenetic clade, the chromalveolates. The chromists are quantitatively the most important eukaryotic contributors to primary production in marine ecosystems. The mechanisms of protein import across their four plastid membranes are still poorly understood. Components of an endoplasmic reticulum-associated degradation (ERAD) machinery in cryptophytes, partially encoded by the reduced genome of the secondary symbiont (the nucleomorph), are implicated in protein transport across the second outermost plastid membrane. Here, we show that the haptophyte Emiliania huxleyi, like cryptophytes, stramenopiles, and apicomplexans, possesses a nuclear-encoded symbiont-specific ERAD machinery (SELMA, symbiont-specific ERAD-like machinery) in addition to the host ERAD system, with targeting signals that are able to direct green fluorescent protein or yellow fluorescent protein to the predicted cellular localization in transformed cells of the stramenopile Phaeodactylum tricornutum. Phylogenies of the duplicated ERAD factors reveal that all SELMA components trace back to a red algal origin. In contrast, themore »
- Authors:
-
- Philipps Univ. of Marburg (Germany). Dept. of Cell Biology
- Univ. of Düsseldorf (Germany). Inst. of Botany III
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; German Research Foundation (DFG); European Research Council (ERC)
- OSTI Identifier:
- 1625325
- Grant/Contract Number:
- AC02-05CH11231; SFB593; 1216; SFB TR1
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology and Evolution
- Additional Journal Information:
- Journal Volume: 3; Journal ID: ISSN 1759-6653
- Publisher:
- Society for Molecular Biology and Evolution
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Evolutionary Biology; Genetics & Heredity; Emiliania huxleyi; secondary endosymbiosis; chromalveolate hypothesis; complex plastid; plastid protein import; algal evolution
Citation Formats
Felsner, Gregor, Sommer, Maik S., Gruenheit, Nicole, Hempel, Franziska, Moog, Daniel, Zauner, Stefan, Martin, William, and Maier, Uwe G. ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane. United States: N. p., 2010.
Web. doi:10.1093/gbe/evq074.
Felsner, Gregor, Sommer, Maik S., Gruenheit, Nicole, Hempel, Franziska, Moog, Daniel, Zauner, Stefan, Martin, William, & Maier, Uwe G. ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane. United States. https://doi.org/10.1093/gbe/evq074
Felsner, Gregor, Sommer, Maik S., Gruenheit, Nicole, Hempel, Franziska, Moog, Daniel, Zauner, Stefan, Martin, William, and Maier, Uwe G. Mon .
"ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane". United States. https://doi.org/10.1093/gbe/evq074. https://www.osti.gov/servlets/purl/1625325.
@article{osti_1625325,
title = {ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane},
author = {Felsner, Gregor and Sommer, Maik S. and Gruenheit, Nicole and Hempel, Franziska and Moog, Daniel and Zauner, Stefan and Martin, William and Maier, Uwe G.},
abstractNote = {The plastids of cryptophytes, haptophytes, and heterokontophytes (stramenopiles) (together once known as chromists) are surrounded by four membranes, reflecting the origin of these plastids through secondary endosymbiosis. They share this trait with apicomplexans, which are alveolates, the plastids of which have been suggested to stem from the same secondary symbiotic event and therefore form a phylogenetic clade, the chromalveolates. The chromists are quantitatively the most important eukaryotic contributors to primary production in marine ecosystems. The mechanisms of protein import across their four plastid membranes are still poorly understood. Components of an endoplasmic reticulum-associated degradation (ERAD) machinery in cryptophytes, partially encoded by the reduced genome of the secondary symbiont (the nucleomorph), are implicated in protein transport across the second outermost plastid membrane. Here, we show that the haptophyte Emiliania huxleyi, like cryptophytes, stramenopiles, and apicomplexans, possesses a nuclear-encoded symbiont-specific ERAD machinery (SELMA, symbiont-specific ERAD-like machinery) in addition to the host ERAD system, with targeting signals that are able to direct green fluorescent protein or yellow fluorescent protein to the predicted cellular localization in transformed cells of the stramenopile Phaeodactylum tricornutum. Phylogenies of the duplicated ERAD factors reveal that all SELMA components trace back to a red algal origin. In contrast, the host copies of cryptophytes and haptophytes associate with the green lineage to the exclusion of stramenopiles and alveolates. Although all chromalveolates with four membrane-bound plastids possess the SELMA system, this has apparently not arisen in a single endosymbiotic event. Thus, our data do not support the chromalveolate hypothesis.},
doi = {10.1093/gbe/evq074},
journal = {Genome Biology and Evolution},
number = ,
volume = 3,
place = {United States},
year = {Mon Nov 15 00:00:00 EST 2010},
month = {Mon Nov 15 00:00:00 EST 2010}
}
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