The GC-rich mitochondrial and plastid genomes of the green alga Coccomyxa give insight into the evolution of organelle DNA nucleotide landscape

Smith, David Roy; Burki, Fabien; Yamada, Takashi; Grimwood, Jane; Grigoriev, Igor V.; Van Etten, James L.; Keeling, Patrick J.; Kroymann, Juergen

doi:10.1371/journal.pone.0023624

The GC-rich mitochondrial and plastid genomes of the green alga Coccomyxa give insight into the evolution of organelle DNA nucleotide landscape

Journal Article · Fri Aug 26 00:00:00 EDT 2011 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0023624· OSTI ID:1344788

Smith, David Roy ^[1]; Burki, Fabien ^[1]; Yamada, Takashi ^[2]; Grimwood, Jane ^[3]; Grigoriev, Igor V. ^[4]; Van Etten, James L. ^[5]; Keeling, Patrick J. ^[1]; Kroymann, Juergen ^[6]

Univ. of British Columbia, Vancouver, BC (Canada)
Hiroshima Univ., Higashi-Hiroshima (Japan)
HudsonAlpha Genome Sequencing Center, Huntsville, AL (United States)
Joint Genome Institute, Walnut Creek, CA (United States)
Univ. of Nebraska, Lincoln, NE (United States)
Univ. Paris-Sud (France)

Here, most of the available mitochondrial and plastid genome sequences are biased towards adenine and thymine (AT) over guanine and cytosine (GC). Examples of GC-rich organelle DNAs are limited to a small but eclectic list of species, including certain green algae. Here, to gain insight in the evolution of organelle nucleotide landscape, we present the GC-rich mitochondrial and plastid DNAs from the trebouxiophyte green alga Coccomyxa sp. C-169. We compare these sequences with other GC-rich organelle DNAs and argue that the forces biasing them towards G and C are nonadaptive and linked to the metabolic and/or life history features of this species. The Coccomyxa organelle genomes are also used for phylogenetic analyses, which highlight the complexities in trying to resolve the interrelationships among the core chlorophyte green algae, but ultimately favour a sister relationship between the Ulvophyceae and Chlorophyceae, with the Trebouxiophyceae branching at the base of the chlorophyte crown.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Genomics Division; USDOE

OSTI ID:: 1344788

Alternate ID(s):: OSTI ID: 1154041
OSTI ID: 1165994

Report Number(s):: LBNL--156329; ir:156329

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 8 Vol. 6; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (50)

The size and form of chromosomes are constant in the nucleus, but highly variable in bacteria, mitochondria and chloroplasts Bendich, Arnold J. BioEssays, Vol. 29, Issue 5 https://doi.org/10.1002/bies.20576	journal	January 2007
The Mitochondrial Genome of Chlorogonium elongatum Inferred from the Complete Sequence Kroymann, Jürgen; Zetsche, Klaus Journal of Molecular Evolution, Vol. 47, Issue 4 https://doi.org/10.1007/pl00006400	journal	October 1998
Maintenance of mitochondrial DNA integrity: repair and degradation Kang, Dongchon; Hamasaki, Naotaka Current Genetics, Vol. 41, Issue 5 https://doi.org/10.1007/s00294-002-0312-0	journal	August 2002
The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses Tsuji, Sumika; Ueda, Kunihiko; Nishiyama, Tomoaki Journal of Plant Research, Vol. 120, Issue 2 https://doi.org/10.1007/s10265-006-0055-y	journal	February 2007
Unparalleled GC content in the plastid DNA of Selaginella Smith, David Roy Plant Molecular Biology, Vol. 71, Issue 6 https://doi.org/10.1007/s11103-009-9545-3	journal	September 2009
Mitochondrial introns: a critical view Lang, B. Franz; Laforest, Marie-Josée; Burger, Gertraud Trends in Genetics, Vol. 23, Issue 3 https://doi.org/10.1016/j.tig.2007.01.006	journal	March 2007
Biased gene conversion: implications for genome and sex evolution Marais, Gabriel Trends in Genetics, Vol. 19, Issue 6 https://doi.org/10.1016/s0168-9525(03)00116-1	journal	June 2003
Human polymorphism around recombination hotspots Spencer, C. C. A. Biochemical Society Transactions, Vol. 34, Issue 4 https://doi.org/10.1042/bst0340535	journal	July 2006
Parallels in Genome Evolution in Mitochondria and Bacterial Symbionts Burger, Gertraud; Lang, B. Franz IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Vol. 55, Issue 4-5 https://doi.org/10.1080/1521654031000137380	journal	January 2003
PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating Lartillot, Nicolas; Lepage, Thomas; Blanquart, Samuel Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp368	journal	June 2009
Correlation between Nuclear Plastid DNA Abundance and Plastid Number Supports the Limited Transfer Window Hypothesis Smith, David Roy; Crosby, Kate; Lee, Robert W. Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr001	journal	January 2011
Extreme RNA Editing in Coding Islands and Abundant Microsatellites in Repeat Sequences of Selaginella moellendorffii Mitochondria: The Root of Frequent Plant mtDNA Recombination in Early Tracheophytes Hecht, Julia; Grewe, Felix; Knoop, Volker Genome Biology and Evolution, Vol. 3 https://doi.org/10.1093/gbe/evr027	journal	January 2011
The Chloroplast Genome Sequence of the Green Alga Pseudendoclonium akinetum (Ulvophyceae) Reveals Unusual Structural Features and New Insights into the Branching Order of Chlorophyte Lineages Pombert, Jean-François; Otis, Christian; Lemieux, Claude Molecular Biology and Evolution, Vol. 22, Issue 9 https://doi.org/10.1093/molbev/msi182	journal	June 2005
The Chloroplast Genomes of the Green Algae Pedinomonas minor, Parachlorella kessleri, and Oocystis solitaria Reveal a Shared Ancestry between the Pedinomonadales and Chlorellales Turmel, M.; Otis, C.; Lemieux, C. Molecular Biology and Evolution, Vol. 26, Issue 10 https://doi.org/10.1093/molbev/msp138	journal	July 2009
Evolution and Cytological Diversification of the Green Seaweeds (Ulvophyceae) Cocquyt, E.; Verbruggen, H.; Leliaert, F. Molecular Biology and Evolution, Vol. 27, Issue 9 https://doi.org/10.1093/molbev/msq091	journal	April 2010
Low Nucleotide Diversity for the Expanded Organelle and Nuclear Genomes of Volvox carteri Supports the Mutational-Hazard Hypothesis Smith, D. R.; Lee, R. W. Molecular Biology and Evolution, Vol. 27, Issue 10 https://doi.org/10.1093/molbev/msq110	journal	April 2010
Mismatch repair activity in mammalian mitochondria Mason, P. A. Nucleic Acids Research, Vol. 31, Issue 3 https://doi.org/10.1093/nar/gkg167	journal	February 2003
MAFFT version 5: improvement in accuracy of multiple sequence alignment Katoh, K. Nucleic Acids Research, Vol. 33, Issue 2 https://doi.org/10.1093/nar/gki198	journal	January 2005
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis Castresana, J. Molecular Biology and Evolution, Vol. 17, Issue 4 https://doi.org/10.1093/oxfordjournals.molbev.a026334	journal	April 2000
Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia De Wever, Aaike; Leliaert, Frederik; Verleyen, Elie Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1673 https://doi.org/10.1098/rspb.2009.0994	journal	July 2009
The mitochondrial genome of the pathogenic yeast Candida subhashii: GC-rich linear DNA with a protein covalently attached to the 5' termini Fricova, D.; Valach, M.; Farkas, Z. Microbiology, Vol. 156, Issue 7 https://doi.org/10.1099/mic.0.038646-0	journal	April 2010
The Complete Mitochondrial DNA Sequences of Nephroselmis olivacea and Pedinomonas minor : Two Radically Different Evolutionary Patterns within Green Algae Turmel, Monique; Lemieux, Claude; Burger, Gertraud The Plant Cell, Vol. 11, Issue 9 https://doi.org/10.1105/tpc.11.9.1717	journal	September 1999
Circular Chloroplast Chromosomes: The Grand Illusion Bendich, Arnold J. The Plant Cell, Vol. 16, Issue 7 https://doi.org/10.1105/tpc.160771	journal	July 2004
Further Studies of Presumedly Primitive Green Algae, Including the Description of Pedinophyceae Class. nov. and Resultor gen. Nov.1 Moestrup, Øjvind Journal of Phycology, Vol. 27, Issue 1 https://doi.org/10.1111/j.0022-3646.1991.00119.x	journal	February 1991
The Bryopsis hypnoides Plastid Genome: Multimeric Forms and Complete Nucleotide Sequence Lü, Fang; Xü, Wei; Tian, Chao PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0014663	journal	February 2011
Green algae and the origin of land plants Lewis, Louise A.; McCourt, Richard M. American Journal of Botany, Vol. 91, Issue 10 https://doi.org/10.3732/ajb.91.10.1535	journal	October 2004
Complete Sequence of the Mitochondrial DNA of the Chlorophyte Alga Prototheca wickerhamii Wolff, Gabriele; Plante, Isabelle; Lang, B. Franz Journal of Molecular Biology, Vol. 237, Issue 1 https://doi.org/10.1006/jmbi.1994.1210	journal	March 1994
The Mitochondrial Genome of Chlorogonium elongatum Inferred from the Complete Sequence Kroymann, Jürgen; Zetsche, Klaus Journal of Molecular Evolution, Vol. 47, Issue 4 https://doi.org/10.1007/PL00006400	journal	October 1998
Compositional Properties of Green-Plant Plastid Genomes Kusumi, Junko; Tachida, Hidenori Journal of Molecular Evolution, Vol. 60, Issue 4 https://doi.org/10.1007/s00239-004-0086-8	journal	April 2005
Diagnosing Mitochondrial DNA Diversity: Applications of a Sentinel Gene Approach Clare, Elizabeth L.; Kerr, Kevin C. R.; von Königslöw, Taika E. Journal of Molecular Evolution, Vol. 66, Issue 4 https://doi.org/10.1007/s00239-008-9088-2	journal	March 2008
The neutral theory of molecular evolution Dover, Gabriel A. Endeavour, Vol. 8, Issue 2 https://doi.org/10.1016/0160-9327(84)90064-4	journal	January 1984
Biased gene conversion: implications for genome and sex evolution Marais, Gabriel Trends in Genetics, Vol. 19, Issue 6 https://doi.org/10.1016/S0168-9525(03)00116-1	journal	June 2003
Recent surprises in protein targeting to mitochondria and plastids Millar, A. Harvey; Whelan, Jim; Small, Ian Current Opinion in Plant Biology, Vol. 9, Issue 6 https://doi.org/10.1016/j.pbi.2006.09.002	journal	December 2006
The Neutral Theory of Molecular Evolution Kimura, Motoo Scientific American, Vol. 241, Issue 5 https://doi.org/10.1038/scientificamerican1179-98	journal	November 1979
Human polymorphism around recombination hotspots Spencer, C. C. A. Biochemical Society Transactions, Vol. 34, Issue 4 https://doi.org/10.1042/BST0340535	journal	July 2006
REPuter: fast computation of maximal repeats in complete genomes Kurtz, S.; Schleiermacher, C. Bioinformatics, Vol. 15, Issue 5 https://doi.org/10.1093/bioinformatics/15.5.426	journal	May 1999
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models Stamatakis, Alexandros Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl446	journal	August 2006
The Complete Mitochondrial DNA Sequence of the Green Alga Pseudendoclonium akinetum (Ulvophyceae) Highlights Distinctive Evolutionary Trends in the Chlorophyta and Suggests a Sister-Group Relationship Between the Ulvophyceae and Chlorophyceae Pombert, J. -F. Molecular Biology and Evolution, Vol. 21, Issue 5 https://doi.org/10.1093/molbev/msh099	journal	January 2004
Mitochondrial Genome of the Colorless Green Alga Polytomella capuana: A Linear Molecule with an Unprecedented GC Content Smith, D. R.; Lee, R. W. Molecular Biology and Evolution, Vol. 25, Issue 3 https://doi.org/10.1093/molbev/msm245	journal	January 2008
Improvement of molecular phylogenetic inference and the phylogeny of Bilateria Lartillot, Nicolas; Philippe, Hervé Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1496 https://doi.org/10.1098/rstb.2007.2236	journal	January 2008
Elimination of deleterious mutations in plastid genomes by gene conversion Khakhlova, Olga; Bock, Ralph The Plant Journal, Vol. 46, Issue 1 https://doi.org/10.1111/j.1365-313X.2006.02673.x	journal	April 2006
Ultrastructure and phylogenetic relationships of the unicellular green algae Ignatius tetrasporus and Pseudocharacium americanum (Chlorophyta) Watanabe, Shin; Nakayama, Takeshi Phycological Research, Vol. 55, Issue 1 https://doi.org/10.1111/j.1440-1835.2006.00439.x	journal	March 2007
Mycosporine-Like Amino Acids and Phylogenies in Green Algae: Prasiola and its Relatives from the Trebouxiophyceae (Chlorophyta)1: maas and Phylogeny in Trebouxiophyceae Karsten, Ulf; Friedl, Thomas; Schumann, Rhena Journal of Phycology, Vol. 41, Issue 3 https://doi.org/10.1111/j.1529-8817.2005.00081.x	journal	May 2005
MITOCHONDRIAL DNA IN THE OOGAMOCHLAMYS CLADE (CHLOROPHYCEAE): HIGH GC CONTENT AND UNIQUE GENOME ARCHITECTURE FOR GREEN ALGAE1: mtDNA IN THE OOGAMOCHLAMYS CLADE Borza, Tudor; Redmond, Erin K.; Laflamme, Mark Journal of Phycology, Vol. 45, Issue 6 https://doi.org/10.1111/j.1529-8817.2009.00753.x	journal	November 2009
Protein transport in organelles: Dual targeting of proteins to mitochondria and chloroplasts: Dual targeting of proteins Carrie, Chris; Giraud, Estelle; Whelan, James FEBS Journal, Vol. 276, Issue 5 https://doi.org/10.1111/j.1742-4658.2009.06876.x	journal	January 2009
Biased Gene Conversion and the Evolution of Mammalian Genomic Landscapes Duret, Laurent; Galtier, Nicolas Annual Review of Genomics and Human Genetics, Vol. 10, Issue 1 https://doi.org/10.1146/annurev-genom-082908-150001	journal	September 2009
The chloroplast genome sequence of the green alga Leptosira terrestris: multiple losses of the inverted repeat and extensive genome rearrangements within the Trebouxiophyceae de Cambiaire, Jean-Charles; Otis, Christian; Turmel, Monique BMC Genomics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2164-8-213	journal	January 2007
The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured de Koning, Audrey P.; Keeling, Patrick J. BMC Biology, Vol. 4, Issue 1 https://doi.org/10.1186/1741-7007-4-12	journal	April 2006
The Mitochondrial Genome of the Entomoparasitic Green Alga Helicosporidium Pombert, Jean-François; Keeling, Patrick J. PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008954	journal	January 2010
Isolation and Culture of Terrestrial and Fresh-water Algae of Antarctica Holm-Hansen, Osmund Phycologia, Vol. 4, Issue 1 https://doi.org/10.2216/i0031-8884-4-1-43.1	journal	August 1964

Cited By (19)

Auxenochlorella protothecoides and Prototheca wickerhamii plastid genome sequences give insight into the origins of non-photosynthetic algae Yan, Dong; Wang, Yun; Murakami, Tatsuya Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep14465	journal	September 2015
Plastid Genome-Based Phylogeny Pinpointed the Origin of the Green-Colored Plastid in the Dinoflagellate Lepidodinium chlorophorum Kamikawa, Ryoma; Tanifuji, Goro; Kawachi, Masanobu Genome Biology and Evolution, Vol. 7, Issue 4 https://doi.org/10.1093/gbe/evv060	journal	April 2015
Dynamic Evolution of the Chloroplast Genome in the Green Algal Classes Pedinophyceae and Trebouxiophyceae Turmel, Monique; Otis, Christian; Lemieux, Claude Genome Biology and Evolution, Vol. 7, Issue 7 https://doi.org/10.1093/gbe/evv130	journal	July 2015
Plastid and mitochondrion genomic sequences from Arctic Chlorella sp. ArM0029B Jeong, Haeyoung; Lim, Jong-Min; Park, Jihye BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-286	journal	January 2014
Chloroplast phylogenomic analysis resolves deep-level relationships within the green algal class Trebouxiophyceae Lemieux, Claude; Otis, Christian; Turmel, Monique BMC Evolutionary Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12862-014-0211-2	journal	October 2014
Evolution of organellar genes of chlorophyte algae: Relevance to phylogenetic inference Mekvipad, Nuttapong; Satjarak, Anchittha PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0216608	journal	May 2019
Updating Our View of Organelle Genome Nucleotide Landscape Smith, David Roy Frontiers in Genetics, Vol. 3 https://doi.org/10.3389/fgene.2012.00175	journal	January 2012
A siphonous macroalgal genome suggests convergent functions of homeobox genes in algae and land plants Arimoto, Asuka; Nishitsuji, Koki; Higa, Yoshimi DNA Research, Vol. 26, Issue 2 https://doi.org/10.1093/dnares/dsz002	journal	March 2019
Unexpectedly Streamlined Mitochondrial Genome of the Euglenozoan Euglena gracilis Dobáková, Eva; Flegontov, Pavel; Skalický, Tomáš Genome Biology and Evolution, Vol. 7, Issue 12 https://doi.org/10.1093/gbe/evv229	journal	November 2015
Strategies for complete plastid genome sequencing Twyford, Alex D.; Ness, Rob W. Molecular Ecology Resources, Vol. 17, Issue 5 https://doi.org/10.1111/1755-0998.12626	journal	November 2016
The mitochondrial genome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals two unsuspected trans -splicing events of group I introns Pelin, Adrian; Pombert, Jean-François; Salvioli, Alessandra New Phytologist, Vol. 194, Issue 3 https://doi.org/10.1111/j.1469-8137.2012.04072.x	journal	February 2012
Mitochondrial genomes of the green macroalga Ulva pertusa (Ulvophyceae, Chlorophyta): novel insights into the evolution of mitogenomes in the Ulvophyceae Liu, Feng; Melton, James T.; Bi, Yuping Journal of Phycology, Vol. 53, Issue 5 https://doi.org/10.1111/jpy.12561	journal	July 2017
Evolution of the Chlorophyta: Insights from chloroplast phylogenomic analyses: Chloroplast phylogenomics of the Chlorophyta Fang, Ling; Leliaert, Frederik; Zhang, Zhen-Hua Journal of Systematics and Evolution, Vol. 55, Issue 4 https://doi.org/10.1111/jse.12248	journal	May 2017
Horizontal Transfer of Entire Genomes via Mitochondrial Fusion in the Angiosperm Amborella Rice, D. W.; Alverson, A. J.; Richardson, A. O. Science, Vol. 342, Issue 6165 https://doi.org/10.1126/science.1246275	journal	December 2013
Complete Mitochondrial and Plastid Genomes of the Green Microalga Trebouxiophyceae sp. Strain MX-AZ01 Isolated from a Highly Acidic Geothermal Lake Servín-Garcidueñas, Luis E.; Martínez-Romero, Esperanza Eukaryotic Cell, Vol. 11, Issue 11 https://doi.org/10.1128/ec.00244-12	journal	October 2012
The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation Blanc, Guillaume; Agarkova, Irina; Grimwood, Jane Genome Biology, Vol. 13, Issue 5 https://doi.org/10.1186/gb-2012-13-5-r39	journal	January 2012
Proposal of a new nomenclature for introns in protein-coding genes in fungal mitogenomes Zhang, Shu; Zhang, Yong-Jie IMA Fungus, Vol. 10, Issue 1 https://doi.org/10.1186/s43008-019-0015-5	journal	October 2019
The Complete Chloroplast and Mitochondrial Genomes of the Green Macroalga Ulva sp. UNA00071828 (Ulvophyceae, Chlorophyta) Melton, James T.; Leliaert, Frederik; Tronholm, Ana PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0121020	journal	April 2015
The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns Repetti, Sonja I.; Jackson, Christopher J.; Judd, Louise M. PeerJ, Vol. 8 https://doi.org/10.7717/peerj.8273	journal	January 2020

Similar Records

The GC-Rich Mitochondrial and Plastid Genomes of the Green Alga Coccomyxa Give Insight into the Evolution of Organelle DNA Nucleotide Landscape

Journal Article · Fri May 13 00:00:00 EDT 2011 · PLoS ONE · OSTI ID:1165994

The Dunaliella salina organelle genomes: large sequences, inflated with intronic and intergenic DNA

Journal Article · Fri May 07 00:00:00 EDT 2010 · BMC Plant Biology, 10:Article Number: 83 · OSTI ID:982954

Crystal Structures of DNA-Whirly Complexes and Their Role in Arabidopsis Organelle Genome Repair

Journal Article · Tue Sep 07 00:00:00 EDT 2010 · Plant Cell · OSTI ID:1002678

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
algae
cellular structures and organelles
introns
mitochondria
mitochondrial DNA
phylogenetic analysis
plastids
repeated sequences

The GC-rich mitochondrial and plastid genomes of the green alga Coccomyxa give insight into the evolution of organelle DNA nucleotide landscape

Citation Formats

References (50)

Cited By (19)

Similar Records

Related Subjects