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Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida.

Jonas Collén 1, 2, * Betina Porcel 3, 4 Wilfrid Carré 5 Steven G Ball 6 Cristian Chaparro 7 Thierry Tonon 1, 2 Tristan Barbeyron 1, 2 Gurvan Michel 1, 2 Benjamin Noel 4 Klaus Valentin 8 Marek Elias 9 François Artiguenave 4 Alok Arun 1, 2 Jean-Marc Aury 4 José F Barbosa-Neto 7 John H Bothwell 10 François-Yves Bouget 11 Loraine Brillet 5 Francisco Cabello-Hurtado 12 Salvador Capella-Gutiérrez 13, 14 Bénédicte Charrier 1, 2 Lionel Cladière 1, 2 J Mark Cock 1, 2 Susana M Coelho 1, 2 Christophe Colleoni 6 Mirjam Czjzek 1, 2 Corinne da Silva 4, 15 Ludovic Delage 1, 2 France Denoeud 4 Philippe Deschamps 6 Simon M Dittami 16, 1 Toni Gabaldón 17, 13 Claire M M Gachon 18 Agnès Groisillier 1, 2 Cécile Hervé 1, 2 Kamel Jabbari 4, 19 Michael Katinka 4 Bernard Kloareg 1, 2 Nathalie Kowalczyk 1, 2 Karine Labadie 4 Catherine Leblanc 1, 2 Pascal J Lopez 20 Deirdre H Mclachlan 10 Laurence Meslet-Cladiere 1, 21, 2 Ahmed Moustafa 22 Zofia Nehr 1, 2 Pi Nyvall Collén 1, 2 Olivier Panaud 7 Frédéric Partensky 2 Julie Poulain 15 Stefan A Rensing 23 Sylvie Rousvoal 16 Gaelle Samson 15 Aikaterini Symeonidi 24 Jean Weissenbach 15 Antonios Zambounis 25 Patrick Wincker 26 Catherine Boyen 1, 2
Abstract : Red seaweeds are key components of coastal ecosystems and are economically important as food and as a source of gelling agents, but their genes and genomes have received little attention. Here we report the sequencing of the 105-Mbp genome of the florideophyte Chondrus crispus (Irish moss) and the annotation of the 9,606 genes. The genome features an unusual structure characterized by gene-dense regions surrounded by repeat-rich regions dominated by transposable elements. Despite its fairly large size, this genome shows features typical of compact genomes, e.g., on average only 0.3 introns per gene, short introns, low median distance between genes, small gene families, and no indication of large-scale genome duplication. The genome also gives insights into the metabolism of marine red algae and adaptations to the marine environment, including genes related to halogen metabolism, oxylipins, and multicellularity (microRNA processing and transcription factors). Particularly interesting are features related to carbohydrate metabolism, which include a minimalistic gene set for starch biosynthesis, the presence of cellulose synthases acquired before the primary endosymbiosis showing the polyphyly of cellulose synthesis in Archaeplastida, and cellulases absent in terrestrial plants as well as the occurrence of a mannosylglycerate synthase potentially originating from a marine bacterium. To explain the observations on genome structure and gene content, we propose an evolutionary scenario involving an ancestral red alga that was driven by early ecological forces to lose genes, introns, and intergenetic DNA; this loss was followed by an expansion of genome size as a consequence of activity of transposable elements.
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Jonas Collén, Betina Porcel, Wilfrid Carré, Steven G Ball, Cristian Chaparro, et al.. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida.. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2013, 110 (13), pp.5247-52. ⟨10.1073/pnas.1221259110⟩. ⟨hal-01073830⟩



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