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MBE Advance Access published online on December 12, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn285
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

The Chloroplast Genomes of the Green Algae Pyramimonas, Monomastix and Pycnococcus Shed New light on the Evolutionary History of Prasinophytes and the Origin of the Secondary Chloroplasts of Euglenids

Monique Turmel*, Marie-Christine Gagnon*, Charley J. O'Kelly{dagger}, Christian Otis* and Claude Lemieux*

* Département de biochimie et de microbiologie, Université Laval, Québec (Québec) Canada
{dagger} Botany Department, University of Hawaii, Honolulu

Corresponding Author: Monique Turmel, Département de biochimie et microbiologie, Université Laval, 1030 avenue de la Médecine, Québec (Québec) Canada G1V 0A6. Tel: (418) 656-2131 ext. 7623; FAX: (418) 656-7176; Email: monique.turmel{at}rsvs.ulaval.ca

Received for publication September 25, 2008. Revision received December 5, 2008. Accepted for publication December 8, 2008.

Because they represent the earliest divergences of the Chlorophyta and include the smallest known eukaryotes (e.g. the coccoid Ostreococcus), the morphologically diverse unicellular green algae making up the Prasinophyceae are central to our understanding of the evolutionary patterns that accompanied the radiation of chlorophytes and the reduction of cell size in some lineages. Seven prasinophyte lineages, 4 of which exhibit a coccoid cell organization (no flagella nor scales), were uncovered from analysis of nuclear-encoded 18S rDNA data; however their order of divergence remains unknown. In this study, the chloroplast genome sequences of the scaly quadriflagellate Pyramimonas parkeae (clade I), the coccoid Pycnococcus pravosoli (clade V) and the scaly uniflagellate Monomastix (unknown affiliation) were determined, annotated and compared to those previously reported for green algae/land plants, including 2 prasinophytes (Nephroselmis olivacea, clade III and Ostreococcus tauri, clade II). The chlororachniophyte Bigelowiella natans and the euglenid Euglena gracilis, whose chloroplasts originate presumably from distinct green algal endosymbionts, were also included in our comparisons. The 3 newly sequenced prasinophyte genomes differ considerably from one another and from their homologs in overall structure, gene content and gene order, with the 80,211-bp Pycnococcus and 114,528-bp Monomastix genomes (98 and 94 conserved genes, respectively) resembling the 71,666-bp Ostreococcus genome (88 genes) in featuring a significantly reduced gene content. The 101,605-bp Pyramimonas genome (110 genes) features 2 conserved genes (rpl22 and ycf65) and ancestral gene linkages previously unrecognized in chlorophytes as well as a DNA primase gene putatively acquired from a virus. The Pyramimonas and Euglena cpDNAs revealed uniquely shared derived gene clusters. Besides providing unequivocal evidence that the green algal ancestor of the euglenid chloroplasts belonged to the Pyramimonadales, phylogenetic analyses of concatenated chloroplast genes and proteins elucidated the position of Monomastix and showed that the Mamiellales, a clade comprising Ostreococcus and Monomastix, are sister to the Pyramimonadales + Euglena clade. Our results also revealed that major reduction in gene content and restructuring of the chloroplast genome occurred in conjunction with important changes in cell organization in at least 2 independent prasinophyte lineages, the Mamiellales and the Pycnococcaceae.

Key Words: prasinophyte green algae • euglenids • chloroplast genome evolution • phylogenomics • secondary endosymbiosis • genome reduction • horizontal DNA transfers


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