tRNA functional signatures classify plastids as late-branching cyanobacteria

Lawrence, Travis J.; Amrine, Katherine C. H.; Swingley, Wesley D.; Ardell, David H.

doi:10.1186/s12862-019-1552-7

Title: tRNA functional signatures classify plastids as late-branching cyanobacteria

Abstract

Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylogenetic root of plastids remains controversial. Although a single origin of plastids by endosymbiosis is broadly supported, recent phylogenomic studies are contradictory on whether plastids branch early or late within Cyanobacteria. One underlying cause may be poor fit of evolutionary models to complex phylogenomic data. Using Posterior Predictive Analysis, we show that recently applied evolutionary models poorly fit three phylogenomic datasets curated from cyanobacteria and plastid genomes because of heterogeneities in both substitution processes across sites and of compositions across lineages. To circumvent these sources of bias, we developed CYANO-MLP, a machine learning algorithm that consistently and accurately phylogenetically classifies (“phyloclassifies”) cyanobacterial genomes to their clade of origin based on bioinformatically predicted function-informative features in tRNA gene complements. Classification of cyanobacterial genomes with CYANO-MLP is accurate and robust to deletion of clades, unbalanced sampling, and compositional heterogeneity in input tRNA data. CYANO-MLP consistently classifies plastid genomes into a late-branching cyanobacterial sub-clade containing single-cell, starch-producing, nitrogen-fixing ecotypes, consistent with metabolic and gene transfer data. Phylogenomic data of cyanobacteria and plastids exhibit both site-process heterogeneities and compositionalmore »« less

Authors:

^[1]; Amrine, Katherine C. H. ^[2]; Swingley, Wesley D. ^[3]; Ardell, David H. ^[4]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of California, Merced, CA (United States)
Univ. of California, Merced, CA (United States); Insight Data Science, San Francisco, CA (United States)
Northern Illinois Univ., DeKalb, IL (United States)
Univ. of California, Merced, CA (United States)

Publication Date:: Mon Dec 09 00:00:00 EST 2019

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE; National Science Foundation (NSF); NIH/NIAID

OSTI Identifier:: 1606714

Grant/Contract Number:: AC05-00OR22725; INSPIRE-1344279; 1R21AI127582-0; ACI-1429783

Resource Type:: Accepted Manuscript

Journal Name:: BMC Evolutionary Biology (Online)

Additional Journal Information:: Journal Name: BMC Evolutionary Biology (Online); Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2148

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; plastids; tRNAs; cyanobacteria; primary endosymbiosis; machine learning

Citation Formats


                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., and Ardell, David H. tRNA functional signatures classify plastids as late-branching cyanobacteria.  United States: N. p., 2019. 
Web.  doi:10.1186/s12862-019-1552-7.

Copy to clipboard


                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., & Ardell, David H. tRNA functional signatures classify plastids as late-branching cyanobacteria.  United States.  https://doi.org/10.1186/s12862-019-1552-7

Copy to clipboard


                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., and Ardell, David H. Mon .  
"tRNA functional signatures classify plastids as late-branching cyanobacteria".  United States.  https://doi.org/10.1186/s12862-019-1552-7.  https://www.osti.gov/servlets/purl/1606714.

Copy to clipboard


                    
@article{osti_1606714,

  title        = {tRNA functional signatures classify plastids as late-branching cyanobacteria},

  author       = {Lawrence, Travis J. and Amrine, Katherine C. H. and Swingley, Wesley D. and Ardell, David H.},

  abstractNote = {Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylogenetic root of plastids remains controversial. Although a single origin of plastids by endosymbiosis is broadly supported, recent phylogenomic studies are contradictory on whether plastids branch early or late within Cyanobacteria. One underlying cause may be poor fit of evolutionary models to complex phylogenomic data. Using Posterior Predictive Analysis, we show that recently applied evolutionary models poorly fit three phylogenomic datasets curated from cyanobacteria and plastid genomes because of heterogeneities in both substitution processes across sites and of compositions across lineages. To circumvent these sources of bias, we developed CYANO-MLP, a machine learning algorithm that consistently and accurately phylogenetically classifies (“phyloclassifies”) cyanobacterial genomes to their clade of origin based on bioinformatically predicted function-informative features in tRNA gene complements. Classification of cyanobacterial genomes with CYANO-MLP is accurate and robust to deletion of clades, unbalanced sampling, and compositional heterogeneity in input tRNA data. CYANO-MLP consistently classifies plastid genomes into a late-branching cyanobacterial sub-clade containing single-cell, starch-producing, nitrogen-fixing ecotypes, consistent with metabolic and gene transfer data. Phylogenomic data of cyanobacteria and plastids exhibit both site-process heterogeneities and compositional heterogeneities across lineages. These aspects of the data require careful modeling to avoid bias in phylogenomic estimation. Furthermore, we show that amino acid recoding strategies may be insufficient to mitigate bias from compositional heterogeneities. However, the combination of our novel tRNA-specific strategy with machine learning in CYANO-MLP appears robust to these sources of bias with high accuracy in phyloclassification of cyanobacterial genomes. CYANO-MLP consistently classifies plastids as late-branching Cyanobacteria, consistent with independent evidence from signature-based approaches and some previous phylogenetic studies.},

  doi          = {10.1186/s12862-019-1552-7},

  journal      = {BMC Evolutionary Biology (Online)},

  number       = 1,

  volume       = 19,

  place        = {United States},

  year         = {Mon Dec 09 00:00:00 EST 2019},

  month        = {Mon Dec 09 00:00:00 EST 2019}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (DOE)

Publisher's Version of Record

https://doi.org/10.1186/s12862-019-1552-7

Other availability

Search WorldCat to find libraries that may hold this journal

Save / Share:

Export Metadata

Save to My Library

Works referenced in this record:

A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process
journal, June 2004

Lartillot, Nicolas; Philippe, Hervé
Molecular Biology and Evolution, Vol. 21, Issue 6
DOI: 10.1093/molbev/msh112

A Site- and Time-Heterogeneous Model of Amino Acid Replacement
journal, January 2008

Blanquart, Samuel; Lartillot, Nicolas
Molecular Biology and Evolution, Vol. 25, Issue 5
DOI: 10.1093/molbev/msn018

Phylogeny and Self-Splicing Ability of the Plastid tRNA-Leu Group I Intron
journal, December 2003

Simon, Dawn; Fewer, David; Friedl, Thomas
Journal of Molecular Evolution, Vol. 57, Issue 6
DOI: 10.1007/s00239-003-2533-3

An Early-Branching Freshwater Cyanobacterium at the Origin of Plastids
journal, February 2017

Ponce-Toledo, Rafael I.; Deschamps, Philippe; López-García, Purificación
Current Biology, Vol. 27, Issue 3
DOI: 10.1016/j.cub.2016.11.056

The plastid ancestor originated among one of the major cyanobacterial lineages
journal, September 2014

Ochoa de Alda, Jesús A. G.; Esteban, Rocío; Diago, María Luz
Nature Communications, Vol. 5, Issue 1
DOI: 10.1038/ncomms5937

ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences
journal, January 2004

Laslett, Dean; Canback, Bjorn
Nucleic Acids Research, Vol. 32, Issue 1, p. 11-16
DOI: 10.1093/nar/gkh152

Investigating Deep Phylogenetic Relationships among Cyanobacteria and Plastids by Small Subunit rRNA Sequence Analysis
journal, July 1999

Turner, SeÁN; Pryer, Kathleen M.; Miao, Vivian P. W.
The Journal of Eukaryotic Microbiology, Vol. 46, Issue 4
DOI: 10.1111/j.1550-7408.1999.tb04612.x

Compilation of tRNA sequences and sequences of tRNA genes
journal, January 1998

Sprinzl, Mathias; Horn, Carsten; Brown, Melissa
Nucleic Acids Research, Vol. 26, Issue 1, p. 148-153
DOI: 10.1093/nar/26.1.148

Estimating the timing of early eukaryotic diversification with multigene molecular clocks
journal, August 2011

Parfrey, L. W.; Lahr, D. J. G.; Knoll, A. H.
Proceedings of the National Academy of Sciences, Vol. 108, Issue 33
DOI: 10.1073/pnas.1110633108

An Improved General Amino Acid Replacement Matrix
journal, April 2008

Le, S. Q.; Gascuel, O.
Molecular Biology and Evolution, Vol. 25, Issue 7
DOI: 10.1093/molbev/msn067

Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor
journal, February 2008

Deusch, O.; Landan, G.; Roettger, M.
Molecular Biology and Evolution, Vol. 25, Issue 4
DOI: 10.1093/molbev/msn022

Large-Scale Phylogenomic Analyses Indicate a Deep Origin of Primary Plastids within Cyanobacteria
journal, June 2011

Criscuolo, Alexis; Gribaldo, Simonetta
Molecular Biology and Evolution, Vol. 28, Issue 11
DOI: 10.1093/molbev/msr108

RNA sequence analysis using covariance models
journal, January 1994

Eddy, Sean R.; Durbin, Richard
Nucleic Acids Research, Vol. 22, Issue 11
DOI: 10.1093/nar/22.11.2079

Initiator tRNA genes template the 3′ CCA end at high frequencies in bacteria
journal, December 2016

Ardell, David H.; Hou, Ya-Ming
BMC Genomics, Vol. 17, Issue 1
DOI: 10.1186/s12864-016-3314-x

Evolution: Red Algal Genome Affirms a Common Origin of All Plastids
journal, July 2004

McFadden, Geoffrey I.; van Dooren, Giel G.
Current Biology, Vol. 14, Issue 13
DOI: 10.1016/j.cub.2004.06.041

Annotated English translation of Mereschkowsky's 1905 paper ‘Über Natur und Ursprung der Chromatophoren imPflanzenreiche’
journal, August 1999

Martin, William; Kowallik, Klaus
European Journal of Phycology, Vol. 34, Issue 3
DOI: 10.1080/09670269910001736342

The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis
journal, January 2011

Ball, Steven; Colleoni, Christophe; Cenci, Ugo
Journal of Experimental Botany, Vol. 62, Issue 6
DOI: 10.1093/jxb/erq411

The origin and early evolution of plants on land
journal, September 1997

Kenrick, Paul; Crane, Peter R.
Nature, Vol. 389, Issue 6646
DOI: 10.1038/37918

tRNA Signatures Reveal a Polyphyletic Origin of SAR11 Strains among Alphaproteobacteria
journal, February 2014

Amrine, Katherine C. H.; Swingley, Wesley D.; Ardell, David H.
PLoS Computational Biology, Vol. 10, Issue 2
DOI: 10.1371/journal.pcbi.1003454

tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997

Lowe, Todd M.; Eddy, Sean R.
Nucleic Acids Research, Vol. 25, Issue 5
DOI: 10.1093/nar/25.5.955

Computational analysis of tRNA identity
journal, November 2009

Ardell, David H.
FEBS Letters, Vol. 584, Issue 2
DOI: 10.1016/j.febslet.2009.11.084

Reductive genome evolution at both ends of the bacterial population size spectrum
journal, September 2014

Batut, Bérénice; Knibbe, Carole; Marais, Gabriel
Nature Reviews Microbiology, Vol. 12, Issue 12
DOI: 10.1038/nrmicro3331

Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades
journal, July 2009

Gupta, R. S.
INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 10
DOI: 10.1099/ijs.0.005678-0

The Evolutionary Origin of a Terrestrial Flora
journal, October 2015

Delwiche, Charles Francis; Cooper, Endymion Dante
Current Biology, Vol. 25, Issue 19
DOI: 10.1016/j.cub.2015.08.029

Intraphylum Diversity and Complex Evolution of Cyanobacterial Aminoacyl-tRNA Synthetases
journal, August 2008

Luque, I.; Riera-Alberola, M. L.; Andujar, A.
Molecular Biology and Evolution, Vol. 25, Issue 11
DOI: 10.1093/molbev/msn197

On Reduced Amino Acid Alphabets for Phylogenetic Inference
journal, May 2007

Susko, E.; Roger, A. J.
Molecular Biology and Evolution, Vol. 24, Issue 9
DOI: 10.1093/molbev/msm144

Compositional Biases among Synonymous Substitutions Cause Conflict between Gene and Protein Trees for Plastid Origins
journal, May 2014

Li, Blaise; Lopes, João S.; Foster, Peter G.
Molecular Biology and Evolution, Vol. 31, Issue 7
DOI: 10.1093/molbev/msu105

Evolutionary constraints on the plastid tRNA set decoding methionine and isoleucine
journal, May 2012

Alkatib, Sibah; Fleischmann, Tobias T.; Scharff, Lars B.
Nucleic Acids Research, Vol. 40, Issue 14
DOI: 10.1093/nar/gks350

A new criterion and method for amino acid classification
journal, May 2004

Kosiol, Carolin; Goldman, Nick; H. Buttimore, Nigel
Journal of Theoretical Biology, Vol. 228, Issue 1
DOI: 10.1016/j.jtbi.2003.12.010

Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing
journal, December 2012

Shih, P. M.; Wu, D.; Latifi, A.
Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058
DOI: 10.1073/pnas.1217107110

SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building
journal, October 2009

Gouy, M.; Guindon, S.; Gascuel, O.
Molecular Biology and Evolution, Vol. 27, Issue 2
DOI: 10.1093/molbev/msp259

Plastid establishment did not require a chlamydial partner
journal, March 2015

Domman, Daryl; Horn, Matthias; Embley, T. Martin
Nature Communications, Vol. 6, Issue 1
DOI: 10.1038/ncomms7421

A brief review of molecular information theory
journal, September 2010

Schneider, Thomas D.
Nano Communication Networks, Vol. 1, Issue 3
DOI: 10.1016/j.nancom.2010.09.002

Visualizing bacterial tRNA identity determinants and antideterminants using function logos and inverse function logos
journal, February 2006

Freyhult, E.
Nucleic Acids Research, Vol. 34, Issue 3
DOI: 10.1093/nar/gkj478

PhyloBayes MPI: Phylogenetic Reconstruction with Infinite Mixtures of Profiles in a Parallel Environment
journal, April 2013

Lartillot, Nicolas; Rodrigue, Nicolas; Stubbs, Daniel
Systematic Biology, Vol. 62, Issue 4
DOI: 10.1093/sysbio/syt022

Match fitness landscapes for macromolecular interaction networks: Selection for translational accuracy and rate can displace tRNA-binding interfaces of non-cognate aminoacyl-tRNA synthetases
journal, October 2019

Collins-Hed, Andrea I.; Ardell, David H.
Theoretical Population Biology, Vol. 129
DOI: 10.1016/j.tpb.2019.03.007

Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants
journal, October 1999

Vogel, J.
Nucleic Acids Research, Vol. 27, Issue 19
DOI: 10.1093/nar/27.19.3866

Computing Bayes Factors Using Thermodynamic Integration
journal, April 2006

Lartillot, Nicolas; Philippe, Hervé
Systematic Biology, Vol. 55, Issue 2
DOI: 10.1080/10635150500433722

Opportunities and obstacles for deep learning in biology and medicine
journal, April 2018

Ching, Travers; Himmelstein, Daniel S.; Beaulieu-Jones, Brett K.
Journal of The Royal Society Interface, Vol. 15, Issue 141
DOI: 10.1098/rsif.2017.0387

Modeling Compositional Heterogeneity
journal, June 2004

Foster, Peter G.
Systematic Biology, Vol. 53, Issue 3
DOI: 10.1080/10635150490445779

Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins
journal, June 2013

Shih, P. M.; Matzke, N. J.
Proceedings of the National Academy of Sciences, Vol. 110, Issue 30
DOI: 10.1073/pnas.1305813110

The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants
journal, May 1990

Manhart, J. R.; Palmer, J. D.
Nature, Vol. 345, Issue 6272
DOI: 10.1038/345268a0

The Phylogeny of Plastids: a Review Based on Comparisons of Small-Subunit Ribosomal rna Coding Regions
journal, August 1995

Bhattacharya, Debashish; Medlin, Linda
Journal of Phycology, Vol. 31, Issue 4
DOI: 10.1111/j.1529-8817.1995.tb02542.x

Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes
journal, February 2004

Timmis, Jeremy N.; Ayliffe, Michael A.; Huang, Chun Y.
Nature Reviews Genetics, Vol. 5, Issue 2
DOI: 10.1038/nrg1271

Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model
journal, January 2007

Lartillot, Nicolas; Brinkmann, Henner; Philippe, Hervé
BMC Evolutionary Biology, Vol. 7, Issue Suppl 1
DOI: 10.1186/1471-2148-7-S1-S4

Compilation and comparison of transfer RNA genes from tobacco chloroplasts
journal, January 1989

Sugiura, Masahiro; Wakasugi, Tatsuya; Kung, Shain‐dow
Critical Reviews in Plant Sciences, Vol. 8, Issue 2
DOI: 10.1080/07352688909382271

The Revised Classification of Eukaryotes
journal, September 2012

Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E.
Journal of Eukaryotic Microbiology, Vol. 59, Issue 5
DOI: 10.1111/j.1550-7408.2012.00644.x

TFAM detects co-evolution of tRNA identity rules with lateral transfer of histidyl-tRNA synthetase
journal, February 2006

Ardell, D. H.
Nucleic Acids Research, Vol. 34, Issue 3
DOI: 10.1093/nar/gkj449

Displaying the in formation contents of structural RNA alignments: the structure logos
journal, January 1997

Gorodkin, J.; Heyer, L. J.; Brunak, S.
Bioinformatics, Vol. 13, Issue 6
DOI: 10.1093/bioinformatics/13.6.583

Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome
journal, August 2003

Dufresne, A.; Salanoubat, M.; Partensky, F.
Proceedings of the National Academy of Sciences, Vol. 100, Issue 17
DOI: 10.1073/pnas.1733211100

Origin and early evolution of photosynthetic eukaryotes in freshwater environments: reinterpreting proterozoic paleobiology and biogeochemical processes in light of trait evolution
journal, September 2013

Blank, Carrine E.
Journal of Phycology, Vol. 49, Issue 6
DOI: 10.1111/jpy.12111

Early photosynthetic eukaryotes inhabited low-salinity habitats
journal, August 2017

Sánchez-Baracaldo, Patricia; Raven, John A.; Pisani, Davide
Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
DOI: 10.1073/pnas.1620089114

Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation
journal, August 2003

Rocap, Gabrielle; Larimer, Frank W.; Lamerdin, Jane
Nature, Vol. 424, Issue 6952
DOI: 10.1038/nature01947

FAST: FAST Analysis of Sequences Toolbox
journal, May 2015

Lawrence, Travis J.; Kauffman, Kyle T.; Amrine, Katherine C. H.
Frontiers in Genetics, Vol. 6
DOI: 10.3389/fgene.2015.00172

Genomes of Stigonematalean Cyanobacteria (Subsection V) and the Evolution of Oxygenic Photosynthesis from Prokaryotes to Plastids
journal, December 2012

Dagan, Tal; Roettger, Mayo; Stucken, Karina
Genome Biology and Evolution, Vol. 5, Issue 1
DOI: 10.1093/gbe/evs117

Difficult phylogenetic questions: more data, maybe; better methods, certainly
journal, December 2011

Philippe, Hervé; Roure, Béatrice
BMC Biology, Vol. 9, Issue 1
DOI: 10.1186/1741-7007-9-91

Dating the cyanobacterial ancestor of the chloroplast
journal, March 2010

Falcón, Luisa I.; Magallón, Susana; Castillo, Amanda
The ISME Journal, Vol. 4, Issue 6
DOI: 10.1038/ismej.2010.2

Metabolic Symbiosis and the Birth of the Plant Kingdom
journal, January 2008

Deschamps, P.; Colleoni, C.; Nakamura, Y.
Molecular Biology and Evolution, Vol. 25, Issue 3
DOI: 10.1093/molbev/msm280

Annotated English translation of Mereschkowsky's 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’
journal, August 1999

Martin, William; Kowallik, Klaus V.
European Journal of Phycology, Vol. 34, Issue 3
DOI: 10.1017/s0967026299002231

tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997

Lowe, Todd M.; Eddy, Sean R.
Nucleic Acids Research, Vol. 25, Issue 5
DOI: 10.1093/nar/25.5.0955

Dating the cyanobacterial ancestor of the chloroplast
journal, August 2009

Falcon, Luisa; Magallon, Susana; Castillo, Amanda
Nature Precedings
DOI: 10.1038/npre.2009.3696.1

Metabolic Symbiosis and the Birth of the Plant Kingdom
journal, February 2008

Deschamps, P.; Colleoni, C.; Nakamura, Y.
Molecular Biology and Evolution, Vol. 25, Issue 4
DOI: 10.1093/molbev/msn053

Compilation of tRNA sequences and sequences of tRNA genes
journal, December 2004

Sprinzl, M.
Nucleic Acids Research, Vol. 33, Issue Database issue
DOI: 10.1093/nar/gki012

Compilation of tRNA sequences and sequences of tRNA genes
journal, January 1989

Sprinzl, M.; Hartmann, T.; Weber, J.
Nucleic Acids Research, Vol. 17, Issue suppl
DOI: 10.1093/nar/17.suppl.r1

Evolution: Red Algal Genome Affirms a Common Origin of All Plastids
journal, July 2004

McFadden, Geoffrey I.; van Dooren, Giel G.
Current Biology, Vol. 14, Issue 13
DOI: 10.1016/j.cub.2004.06.041

The Evolutionary Origin of a Terrestrial Flora
journal, October 2015

Delwiche, Charles Francis; Cooper, Endymion Dante
Current Biology, Vol. 25, Issue 19
DOI: 10.1016/j.cub.2015.08.029

Computational analysis of tRNA identity
journal, November 2009

Ardell, David H.
FEBS Letters, Vol. 584, Issue 2
DOI: 10.1016/j.febslet.2009.11.084

A new criterion and method for amino acid classification
journal, May 2004

Kosiol, Carolin; Goldman, Nick; H. Buttimore, Nigel
Journal of Theoretical Biology, Vol. 228, Issue 1
DOI: 10.1016/j.jtbi.2003.12.010

The gain of two chloroplast tRNA introns marks the green algal ancestors of land plants
journal, May 1990

Manhart, J. R.; Palmer, J. D.
Nature, Vol. 345, Issue 6272
DOI: 10.1038/345268a0

The origin and early evolution of plants on land
journal, September 1997

Kenrick, Paul; Crane, Peter R.
Nature, Vol. 389, Issue 6646
DOI: 10.1038/37918

Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes
journal, February 2004

Timmis, Jeremy N.; Ayliffe, Michael A.; Huang, Chun Y.
Nature Reviews Genetics, Vol. 5, Issue 2
DOI: 10.1038/nrg1271

Reductive genome evolution at both ends of the bacterial population size spectrum
journal, September 2014

Batut, Bérénice; Knibbe, Carole; Marais, Gabriel
Nature Reviews Microbiology, Vol. 12, Issue 12
DOI: 10.1038/nrmicro3331

Estimating the timing of early eukaryotic diversification with multigene molecular clocks
journal, August 2011

Parfrey, L. W.; Lahr, D. J. G.; Knoll, A. H.
Proceedings of the National Academy of Sciences, Vol. 108, Issue 33
DOI: 10.1073/pnas.1110633108

Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing
journal, December 2012

Shih, P. M.; Wu, D.; Latifi, A.
Proceedings of the National Academy of Sciences, Vol. 110, Issue 3, p. 1053-1058
DOI: 10.1073/pnas.1217107110

Early photosynthetic eukaryotes inhabited low-salinity habitats
journal, August 2017

Sánchez-Baracaldo, Patricia; Raven, John A.; Pisani, Davide
Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
DOI: 10.1073/pnas.1620089114

Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome
journal, August 2003

Dufresne, A.; Salanoubat, M.; Partensky, F.
Proceedings of the National Academy of Sciences, Vol. 100, Issue 17
DOI: 10.1073/pnas.1733211100

Modeling Compositional Heterogeneity
journal, June 2004

Foster, Peter G.
Systematic Biology, Vol. 53, Issue 3
DOI: 10.1080/10635150490445779

Computing Bayes Factors Using Thermodynamic Integration
journal, April 2006

Lartillot, Nicolas; Philippe, Hervé
Systematic Biology, Vol. 55, Issue 2
DOI: 10.1080/10635150500433722

Displaying the in formation contents of structural RNA alignments: the structure logos
journal, January 1997

Gorodkin, J.; Heyer, L. J.; Brunak, S.
Bioinformatics, Vol. 13, Issue 6
DOI: 10.1093/bioinformatics/13.6.583

Genomes of Stigonematalean Cyanobacteria (Subsection V) and the Evolution of Oxygenic Photosynthesis from Prokaryotes to Plastids
journal, December 2012

Dagan, Tal; Roettger, Mayo; Stucken, Karina
Genome Biology and Evolution, Vol. 5, Issue 1
DOI: 10.1093/gbe/evs117

The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis
journal, January 2011

Ball, Steven; Colleoni, Christophe; Cenci, Ugo
Journal of Experimental Botany, Vol. 62, Issue 6
DOI: 10.1093/jxb/erq411

A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process
journal, June 2004

Lartillot, Nicolas; Philippe, Hervé
Molecular Biology and Evolution, Vol. 21, Issue 6
DOI: 10.1093/molbev/msh112

Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor
journal, February 2008

Deusch, O.; Landan, G.; Roettger, M.
Molecular Biology and Evolution, Vol. 25, Issue 4
DOI: 10.1093/molbev/msn022

Metabolic Symbiosis and the Birth of the Plant Kingdom
journal, February 2008

Deschamps, P.; Colleoni, C.; Nakamura, Y.
Molecular Biology and Evolution, Vol. 25, Issue 4
DOI: 10.1093/molbev/msn053

Compositional Biases among Synonymous Substitutions Cause Conflict between Gene and Protein Trees for Plastid Origins
journal, May 2014

Li, Blaise; Lopes, João S.; Foster, Peter G.
Molecular Biology and Evolution, Vol. 31, Issue 7
DOI: 10.1093/molbev/msu105

RNA sequence analysis using covariance models
journal, January 1994

Eddy, Sean R.; Durbin, Richard
Nucleic Acids Research, Vol. 22, Issue 11
DOI: 10.1093/nar/22.11.2079

Compilation of tRNA sequences and sequences of tRNA genes
journal, January 1996

Sprinzl, M.
Nucleic Acids Research, Vol. 24, Issue 1
DOI: 10.1093/nar/24.1.68

tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997

Lowe, Todd M.; Eddy, Sean R.
Nucleic Acids Research, Vol. 25, Issue 5
DOI: 10.1093/nar/25.5.955

Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants
journal, October 1999

Vogel, J.
Nucleic Acids Research, Vol. 27, Issue 19
DOI: 10.1093/nar/27.19.3866

ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences
journal, January 2004

Laslett, Dean; Canback, Bjorn
Nucleic Acids Research, Vol. 32, Issue 1, p. 11-16
DOI: 10.1093/nar/gkh152

PhyloBayes MPI: Phylogenetic Reconstruction with Infinite Mixtures of Profiles in a Parallel Environment
journal, April 2013

Lartillot, Nicolas; Rodrigue, Nicolas; Stubbs, Daniel
Systematic Biology, Vol. 62, Issue 4
DOI: 10.1093/sysbio/syt022

Opportunities and obstacles for deep learning in biology and medicine
journal, April 2018

Ching, Travers; Himmelstein, Daniel S.; Beaulieu-Jones, Brett K.
Journal of The Royal Society Interface, Vol. 15, Issue 141
DOI: 10.1098/rsif.2017.0387

Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades
journal, July 2009

Gupta, R. S.
INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 10
DOI: 10.1099/ijs.0.005678-0

The Phylogeny of Plastids: a Review Based on Comparisons of Small-Subunit Ribosomal rna Coding Regions
journal, August 1995

Bhattacharya, Debashish; Medlin, Linda
Journal of Phycology, Vol. 31, Issue 4
DOI: 10.1111/j.1529-8817.1995.tb02542.x

The Revised Classification of Eukaryotes
journal, September 2012

Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E.
Journal of Eukaryotic Microbiology, Vol. 59, Issue 5
DOI: 10.1111/j.1550-7408.2012.00644.x

tRNA Signatures Reveal a Polyphyletic Origin of SAR11 Strains among Alphaproteobacteria
journal, February 2014

Amrine, Katherine C. H.; Swingley, Wesley D.; Ardell, David H.
PLoS Computational Biology, Vol. 10, Issue 2
DOI: 10.1371/journal.pcbi.1003454

Similar Records in DOE PAGES and OSTI.GOV collections:

Updating algal evolutionary relationships through plastid genome sequencing: did alveolate plastids emerge through endosymbiosis of an ochrophyte?

Journal Article Ševčíková, Tereza ; Horák, Aleš ; Klimeš, Vladimír ; ... - Scientific Reports

Algae with secondary plastids of a red algal origin, such as ochrophytes (photosynthetic stramenopiles), are diverse and ecologically important, yet their evolutionary history remains controversial. We sequenced plastid genomes of two ochrophytes, Ochromonas sp. CCMP1393 (Chrysophyceae) and Trachydiscus minutus (Eustigmatophyceae). A shared split of the clpC gene as well as phylogenomic analyses of concatenated protein sequences demonstrated that chrysophytes and eustigmatophytes form a clade, the Limnista, exhibiting an unexpectedly elevated rate of plastid gene evolution. Our analyses also indicate that the root of the ochrophyte phylogeny falls between the recently redefined Khakista and Phaeista assemblages. Taking advantage of the expandedmore »« less
Cited by 70
https://doi.org/10.1038/srep10134

Full Text Available
Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates

Journal Article Burki, Fabien ; Inagaki, Yuji ; Bråte, Jon ; ... - Genome Biology and Evolution

Understanding the early evolution and diversification of eukaryotes relies on a fully resolved phylogenetic tree. In recent years, most eukaryotic diversity has been assigned to six putative supergroups, but the evolutionary origin of a few major ‘‘orphan’’ lineages remains elusive. Two ecologically important orphan groups are the heterotrophic Telonemia and Centroheliozoa. Telonemids have been proposed to be related to the photosynthetic cryptomonads or stramenopiles and centrohelids to haptophytes, but molecular phylogenies have failed to provide strong support for any phylogenetic hypothesis. Here, we investigate the origins of Telonema subtilis (a telonemid) and Raphidiophrys contractilis (a centrohelid) by large-scale 454 pyrosequencingmore »« less
https://doi.org/10.1093/gbe/evp022

Full Text Available
Metagenomic Analysis of the Indian Ocean Picocyanobacterial Community: Structure, Potential Function and Evolution

Journal Article Díez, Beatriz ; Nylander, Johan A. A. ; Ininbergs, Karolina ; ... - PLoS ONE

Unicellular cyanobacteria are ubiquitous photoautotrophic microbes that contribute substantially to global primary production. Picocyanobacteria such as Synechococcus and Prochlorococcus depend on chlorophyll a-binding protein complexes to capture light energy. In addition, Synechococcus has accessory pigments organized into phycobilisomes, and Prochlorococcus contains chlorophyll b. Across a surface water transect spanning the sparsely studied tropical Indian Ocean, we examined Synechococcus and Prochlorococcus occurrence, taxonomy and habitat preference in an evolutionary context. Shotgun sequencing of size fractionated microbial communities from 0.1 μm to 20 μm and subsequent phylogenetic analysis indicated that cyanobacteria account for up to 15% of annotated reads, with the generamore »« less
Cited by 22
https://doi.org/10.1371/journal.pone.0155757
ERAD Components in Organisms with Complex Red Plastids Suggest Recruitment of a Preexisting Protein Transport Pathway for the Periplastid Membrane

Journal Article Felsner, Gregor ; Sommer, Maik S. ; Gruenheit, Nicole ; ... - Genome Biology and Evolution

The plastids of cryptophytes, haptophytes, and heterokontophytes (stramenopiles) (together once known as chromists) are surrounded by four membranes, reflecting the origin of these plastids through secondary endosymbiosis. They share this trait with apicomplexans, which are alveolates, the plastids of which have been suggested to stem from the same secondary symbiotic event and therefore form a phylogenetic clade, the chromalveolates. The chromists are quantitatively the most important eukaryotic contributors to primary production in marine ecosystems. The mechanisms of protein import across their four plastid membranes are still poorly understood. Components of an endoplasmic reticulum-associated degradation (ERAD) machinery in cryptophytes, partially encodedmore »« less
https://doi.org/10.1093/gbe/evq074

Full Text Available
Reconstructing the backbone of the Saccharomycotina yeast phylogeny using genome-scale data

Journal Article Shen, Xing -Xing ; Zhou, Xiaofan ; Kominek, Jacek ; ... - G3

Understanding the phylogenetic relationships among the yeasts of the subphylum Saccharomycotina is a prerequisite for understanding the evolution of their metabolisms and ecological lifestyles. In the last two decades, the use of rDNA and multilocus data sets has greatly advanced our understanding of the yeast phylogeny, but many deep relationships remain unsupported. In contrast, phylogenomic analyses have involved relatively few taxa and lineages that were often selected with limited considerations for covering the breadth of yeast biodiversity. Here we used genome sequence data from 86 publicly available yeast genomes representing nine of the 11 known major lineages and 10 nonyeastmore »« less
Cited by 135
https://doi.org/10.1534/g3.116.034744

Full Text Available

Other research related to this record:

MOESM1 of tRNA functional signatures classify plastids as late-branching cyanobacteria
text, January 2019

Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D.
figshare
DOI: 10.6084/m9.figshare.11345768
This text is a supplement to the current record

MOESM2 of tRNA functional signatures classify plastids as late-branching cyanobacteria
text, January 2019

Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D.
figshare
DOI: 10.6084/m9.figshare.11345774
This text is a supplement to the current record