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Open Access Research article

A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum

Marianne A Minge1, Kamran Shalchian-Tabrizi2, Ole K Tørresen1, Kiyotaka Takishita3, Ian Probert4, Yuji Inagaki5, Dag Klaveness2 and Kjetill S Jakobsen12*

Author Affiliations

1 Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, N-0316 Oslo, Norway

2 Microbial Evolutionary Research Group (MERG), Department of Biology, University of Oslo, N-0316 Oslo, Norway

3 Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa, 237-0061, Japan

4 Roscoff Culture Collection (RCC), Station Biologique de Roscoff, Place Georges Teissier, 29682 Roscoff, France

5 Center for Computational Sciences, Institute for Biological Sciences, University of Tsukuba, Tsukuba Ibaraki, 305-8577, Japan

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BMC Evolutionary Biology 2010, 10:191  doi:10.1186/1471-2148-10-191

Published: 21 June 2010

Abstract

Background

Plastid replacements through secondary endosymbioses include massive transfer of genes from the endosymbiont to the host nucleus and require a new targeting system to enable transport of the plastid-targeted proteins across 3-4 plastid membranes. The dinoflagellates are the only eukaryotic lineage that has been shown to have undergone several plastid replacement events, and this group is thus highly relevant for studying the processes involved in plastid evolution. In this study, we analyzed the phylogenetic origin and N-terminal extensions of plastid-targeted proteins from Lepidodinium chlorophorum, a member of the only dinoflagellate genus that harbors a green secondary plastid rather than the red algal-derived, peridinin-containing plastid usually found in photosynthetic dinoflagellates.

Results

We sequenced 4,746 randomly picked clones from a L. chlorophorum cDNA library. 22 of the assembled genes were identified as genes encoding proteins functioning in plastids. Some of these were of green algal origin. This confirms that genes have been transferred from the plastid to the host nucleus of L. chlorophorum and indicates that the plastid is fully integrated as an organelle in the host. Other nuclear-encoded plastid-targeted protein genes, however, are clearly not of green algal origin, but have been derived from a number of different algal groups, including dinoflagellates, streptophytes, heterokonts, and red algae. The characteristics of N-terminal plastid-targeting peptides of all of these genes are substantially different from those found in peridinin-containing dinoflagellates and green algae.

Conclusions

L. chlorophorum expresses plastid-targeted proteins with a range of different origins, which probably arose through endosymbiotic gene transfer (EGT) and horizontal gene transfer (HGT). The N-terminal extension of the genes is different from the extensions found in green alga and other dinoflagellates (peridinin- and haptophyte plastids). These modifications have likely enabled the mosaic proteome of L. chlorophorum.