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

Jonas Collén; Betina Porcel; Wilfrid Carré; Steven G Ball; Cristian Chaparro; Thierry Tonon; Tristan Barbeyron; Gurvan Michel; Benjamin Noel; Klaus Valentin; Marek Elias; François Artiguenave; Alok Arun; Jean-Marc Aury; José F Barbosa-Neto; John H Bothwell; François-Yves Bouget; Loraine Brillet; Francisco Cabello-Hurtado; Salvador Capella-Gutiérrez; Bénédicte Charrier; Lionel Cladière; J Mark Cock; Susana M Coelho; Christophe Colleoni; Mirjam Czjzek; Corinne Da Silva; Ludovic Delage; France Denoeud; Philippe Deschamps; Simon M Dittami; Toni Gabaldón; Claire M M Gachon; Agnès Groisillier; Cécile Hervé; Kamel Jabbari; Michael Katinka; Bernard Kloareg; Nathalie Kowalczyk; Karine Labadie; Catherine Leblanc; Pascal J Lopez; Deirdre H McLachlan; Laurence Meslet-Cladiere; Ahmed Moustafa; Zofia Nehr; Pi Nyvall Collén; Olivier Panaud; Frédéric Partensky; Julie Poulain; Stefan A Rensing; Sylvie Rousvoal; Gaelle Samson; Aikaterini Symeonidi; Jean Weissenbach; Antonios Zambounis; Patrick Wincker; Catherine Boyen

doi:10.1073/pnas.1221259110

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

Jonas Collén, Betina Porcel, Wilfrid Carré, Steven G Ball, Cristian Chaparro, Thierry Tonon, Tristan Barbeyron, Gurvan Michel, Benjamin Noel, Klaus Valentin, Marek Elias, François Artiguenave, Alok Arun, Jean-Marc Aury, José F Barbosa-Neto, John H Bothwell, François-Yves Bouget, Loraine Brillet, Francisco Cabello-Hurtado, Salvador Capella-GutiérrezBénédicte Charrier, Lionel Cladière, J Mark Cock, Susana M Coelho, Christophe Colleoni, Mirjam Czjzek, Corinne Da Silva, Ludovic Delage, France Denoeud, Philippe Deschamps, Simon M Dittami, Toni Gabaldón, Claire M M Gachon, Agnès Groisillier, Cécile Hervé, Kamel Jabbari, Michael Katinka, Bernard Kloareg, Nathalie Kowalczyk, Karine Labadie, Catherine Leblanc, Pascal J Lopez, Deirdre H McLachlan, Laurence Meslet-Cladiere, Ahmed Moustafa, Zofia Nehr, Pi Nyvall Collén, Olivier Panaud, Frédéric Partensky, Julie Poulain, Stefan A Rensing, Sylvie Rousvoal, Gaelle Samson, Aikaterini Symeonidi, Jean Weissenbach, Antonios Zambounis, Patrick Wincker, Catherine Boyen

CNAP

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Pages (from-to)	5247-52
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	110
Issue number	13
DOIs	https://doi.org/10.1073/pnas.1221259110
Publication status	Published - 26 Mar 2013

Keywords

Base Sequence
Chondrus/genetics
Evolution, Molecular
Genes, Plant
MicroRNAs/genetics
Molecular Sequence Data
Plant Proteins/genetics
RNA, Plant/genetics

Access to Document

10.1073/pnas.1221259110

Cite this

Collén, J., Porcel, B., Carré, W., Ball, S. G., Chaparro, C., Tonon, T., Barbeyron, T., Michel, G., Noel, B., Valentin, K., Elias, M., Artiguenave, F., Arun, A., Aury, J.-M., Barbosa-Neto, J. F., Bothwell, J. H., Bouget, F.-Y., Brillet, L., Cabello-Hurtado, F., ... Boyen, C. (2013). 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, 110(13), 5247-52. https://doi.org/10.1073/pnas.1221259110

@article{3f63903004ee49f391e14032d92479d7,

title = "Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida",

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.",

keywords = "Base Sequence, Chondrus/genetics, Evolution, Molecular, Genes, Plant, MicroRNAs/genetics, Molecular Sequence Data, Plant Proteins/genetics, RNA, Plant/genetics",

author = "Jonas Coll{\'e}n and Betina Porcel and Wilfrid Carr{\'e} and Ball, {Steven G} and Cristian Chaparro and Thierry Tonon and Tristan Barbeyron and Gurvan Michel and Benjamin Noel and Klaus Valentin and Marek Elias and Fran{\c c}ois Artiguenave and Alok Arun and Jean-Marc Aury and Barbosa-Neto, {Jos{\'e} F} and Bothwell, {John H} and Fran{\c c}ois-Yves Bouget and Loraine Brillet and Francisco Cabello-Hurtado and Salvador Capella-Guti{\'e}rrez and B{\'e}n{\'e}dicte Charrier and Lionel Cladi{\`e}re and Cock, {J Mark} and Coelho, {Susana M} and Christophe Colleoni and Mirjam Czjzek and {Da Silva}, Corinne and Ludovic Delage and France Denoeud and Philippe Deschamps and Dittami, {Simon M} and Toni Gabald{\'o}n and Gachon, {Claire M M} and Agn{\`e}s Groisillier and C{\'e}cile Herv{\'e} and Kamel Jabbari and Michael Katinka and Bernard Kloareg and Nathalie Kowalczyk and Karine Labadie and Catherine Leblanc and Lopez, {Pascal J} and McLachlan, {Deirdre H} and Laurence Meslet-Cladiere and Ahmed Moustafa and Zofia Nehr and {Nyvall Coll{\'e}n}, Pi and Olivier Panaud and Fr{\'e}d{\'e}ric Partensky and Julie Poulain and Rensing, {Stefan A} and Sylvie Rousvoal and Gaelle Samson and Aikaterini Symeonidi and Jean Weissenbach and Antonios Zambounis and Patrick Wincker and Catherine Boyen",

year = "2013",

month = mar,

day = "26",

doi = "10.1073/pnas.1221259110",

language = "English",

volume = "110",

pages = "5247--52",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "13",

}

Collén, J, Porcel, B, Carré, W, Ball, SG, Chaparro, C, Tonon, T, Barbeyron, T, Michel, G, Noel, B, Valentin, K, Elias, M, Artiguenave, F, Arun, A, Aury, J-M, Barbosa-Neto, JF, Bothwell, JH, Bouget, F-Y, Brillet, L, Cabello-Hurtado, F, Capella-Gutiérrez, S, Charrier, B, Cladière, L, Cock, JM, Coelho, SM, Colleoni, C, Czjzek, M, Da Silva, C, Delage, L, Denoeud, F, Deschamps, P, Dittami, SM, Gabaldón, T, Gachon, CMM, Groisillier, A, Hervé, C, Jabbari, K, Katinka, M, Kloareg, B, Kowalczyk, N, Labadie, K, Leblanc, C, Lopez, PJ, McLachlan, DH, Meslet-Cladiere, L, Moustafa, A, Nehr, Z, Nyvall Collén, P, Panaud, O, Partensky, F, Poulain, J, Rensing, SA, Rousvoal, S, Samson, G, Symeonidi, A, Weissenbach, J, Zambounis, A, Wincker, P & Boyen, C 2013, '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, vol. 110, no. 13, pp. 5247-52. https://doi.org/10.1073/pnas.1221259110

Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. / Collén, Jonas; Porcel, Betina; Carré, Wilfrid et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 13, 26.03.2013, p. 5247-52.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida

AU - Collén, Jonas

AU - Porcel, Betina

AU - Carré, Wilfrid

AU - Ball, Steven G

AU - Chaparro, Cristian

AU - Tonon, Thierry

AU - Barbeyron, Tristan

AU - Michel, Gurvan

AU - Noel, Benjamin

AU - Valentin, Klaus

AU - Elias, Marek

AU - Artiguenave, François

AU - Arun, Alok

AU - Aury, Jean-Marc

AU - Barbosa-Neto, José F

AU - Bothwell, John H

AU - Bouget, François-Yves

AU - Brillet, Loraine

AU - Cabello-Hurtado, Francisco

AU - Capella-Gutiérrez, Salvador

AU - Charrier, Bénédicte

AU - Cladière, Lionel

AU - Cock, J Mark

AU - Coelho, Susana M

AU - Colleoni, Christophe

AU - Czjzek, Mirjam

AU - Da Silva, Corinne

AU - Delage, Ludovic

AU - Denoeud, France

AU - Deschamps, Philippe

AU - Dittami, Simon M

AU - Gabaldón, Toni

AU - Gachon, Claire M M

AU - Groisillier, Agnès

AU - Hervé, Cécile

AU - Jabbari, Kamel

AU - Katinka, Michael

AU - Kloareg, Bernard

AU - Kowalczyk, Nathalie

AU - Labadie, Karine

AU - Leblanc, Catherine

AU - Lopez, Pascal J

AU - McLachlan, Deirdre H

AU - Meslet-Cladiere, Laurence

AU - Moustafa, Ahmed

AU - Nehr, Zofia

AU - Nyvall Collén, Pi

AU - Panaud, Olivier

AU - Partensky, Frédéric

AU - Poulain, Julie

AU - Rensing, Stefan A

AU - Rousvoal, Sylvie

AU - Samson, Gaelle

AU - Symeonidi, Aikaterini

AU - Weissenbach, Jean

AU - Zambounis, Antonios

AU - Wincker, Patrick

AU - Boyen, Catherine

PY - 2013/3/26

Y1 - 2013/3/26

N2 - 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.

AB - 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.

KW - Base Sequence

KW - Chondrus/genetics

KW - Evolution, Molecular

KW - Genes, Plant

KW - MicroRNAs/genetics

KW - Molecular Sequence Data

KW - Plant Proteins/genetics

KW - RNA, Plant/genetics

U2 - 10.1073/pnas.1221259110

DO - 10.1073/pnas.1221259110

M3 - Article

C2 - 23503846

SN - 0027-8424

VL - 110

SP - 5247

EP - 5252

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 13

ER -