Variable presence of the inverted repeat and plastome stability in Erodium.

BACKGROUND AND AIMS Several unrelated lineages such as plastids, viruses and plasmids, have converged on quadripartite genomes of similar size with large and small single copy regions and a large inverted repeat (IR). Except for Erodium (Geraniaceae), saguaro cactus and some legumes, the plastomes of all photosynthetic angiosperms display this structure. The functional significance of the IR is not understood and Erodium provides a system to examine the role of the IR in the long-term stability of these genomes. We compared the degree of genomic rearrangement in plastomes of Erodium that differ in the presence and absence of the IR. METHODS We sequenced 17 new Erodium plastomes. Using 454, Illumina, PacBio and Sanger sequences, 16 genomes were assembled and categorized along with one incomplete and two previously published Erodium plastomes. We conducted phylogenetic analyses among these species using a dataset of 19 protein-coding genes and determined if significantly higher evolutionary rates had caused the long branch seen previously in phylogenetic reconstructions within the genus. Bioinformatic comparisons were also performed to evaluate plastome evolution across the genus. KEY RESULTS Erodium plastomes fell into four types (Type 1-4) that differ in their substitution rates, short dispersed repeat content and degree of genomic rearrangement, gene and intron content and GC content. Type 4 plastomes had significantly higher rates of synonymous substitutions (dS) for all genes and for 14 of the 19 genes non-synonymous substitutions (dN) were significantly accelerated. We evaluated the evidence for a single IR loss in Erodium and in doing so discovered that Type 4 plastomes contain a novel IR. CONCLUSIONS The presence or absence of the IR does not affect plastome stability in Erodium. Rather, the overall repeat content shows a negative correlation with genome stability, a pattern in agreement with other angiosperm groups and recent findings on genome stability in bacterial endosymbionts.

[1]  Douglas E. Soltis,et al.  Molecular Systematics of Plants , 1992, Springer US.

[2]  Daniel B. Sloan,et al.  The Evolution of Genomic Instability in the Obligate Endosymbionts of Whiteflies , 2013, Genome biology and evolution.

[3]  G. Cannon,et al.  DNA Replication in Chloroplasts , 1993 .

[4]  K. H. Wolfe,et al.  Ebb and flow of the chloroplast inverted repeat , 1996, Molecular and General Genetics MGG.

[5]  Thomas Wetter,et al.  Genome Sequence Assembly Using Trace Signals and Additional Sequence Information , 1999, German Conference on Bioinformatics.

[6]  Simon Whelan,et al.  Statistical Methods in Molecular Evolution , 2005 .

[7]  K. H. Wolfe,et al.  Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. , 2002 .

[8]  R. Bock.  Structure, function, and inheritance of plastid genomes , 2007 .

[9]  B. Klitgaard.  Advances in Legume Systematics Part 10. Higher Level Systematics , 2003 .

[10]  N. Brisson,et al.  Short‐range inversions: Rethinking organelle genome stability , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  A. Davison.  Copyright © 1998, American Society for Microbiology The Genome of Salmonid Herpesvirus 1 , 1997 .

[12]  Jeffrey P. Mower,et al.  The complete chloroplast genome sequence of Pelargonium x hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. , 2006, Molecular biology and evolution.

[13]  R. Jansen,et al.  Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. , 2014, Molecular biology and evolution.

[14]  Peter Schattner,et al.  The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs , 2005, Nucleic Acids Res..

[15]  R. Jansen,et al.  Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions. , 2007, Molecular biology and evolution.

[16]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[17]  K. Isono,et al.  Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA , 2001, Zeitschrift für Induktive Abstammungs- und Vererbungslehre.

[18]  M. Kunnimalaiyaan,et al.  Fine mapping of replication origins (ori A and ori B) in Nicotiana tabacum chloroplast DNA. , 1997, Nucleic acids research.

[19]  R. Jansen,et al.  Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions , 2008, Proceedings of the National Academy of Sciences.

[20]  Emily L. Gillespie,et al.  Complete plastid genome sequence of Vaccinium macrocarpon: structure, gene content, and rearrangements revealed by next generation sequencing , 2013, Tree Genetics & Genomes.

[21]  Sergei L. Kosakovsky Pond,et al.  HyPhy: hypothesis testing using phylogenies , 2005, Bioinform..

[22]  L. Casano,et al.  Balanced Gene Losses, Duplications and Intensive Rearrangements Led to an Unusual Regularly Sized Genome in Arbutus unedo Chloroplasts , 2013, PloS one.

[23]  M. Sanderson,et al.  Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): Loss of the ndh gene suite and inverted repeat. , 2015, American journal of botany.

[24]  E. Birney,et al.  Velvet: algorithms for de novo short read assembly using de Bruijn graphs. , 2008, Genome research.

[25]  Jeffrey D. Palmer,et al.  Use of Chloroplast DNA Rearrangements in Reconstructing Plant Phylogeny , 1992 .

[26]  N. Moran,et al.  50 Million Years of Genomic Stasis in Endosymbiotic Bacteria , 2002, Science.

[27]  F. Jenkins,et al.  Herpes simplex virus 1 recombinants with noninverting genomes frozen in different isomeric arrangements are capable of independent replication , 1986, Journal of virology.

[28]  J. Palmer,et al.  Chloroplast DNA rearrangements are more frequent when a large inverted repeat sequence is lost , 1982, Cell.

[29]  I. Lehman,et al.  Replication of Herpes Simplex Virus DNA* , 1999, The Journal of Biological Chemistry.

[30]  B. Rao,et al.  A comparative approach to elucidate chloroplast genome replication , 2009, BMC Genomics.

[31]  L. Sagan.  On the origin of mitosing cells , 1967, Journal of theoretical biology.

[32]  J. Palmer,et al.  Chloroplast DNA evolution among legumes: Loss of a large inverted repeat occurred prior to other sequence rearrangements , 2004, Current Genetics.

[33]  Tracey A Ruhlman,et al.  Coevolution between Nuclear-Encoded DNA Replication, Recombination, and Repair Genes and Plastid Genome Complexity , 2016, Genome biology and evolution.

[34]  T. Kondo,et al.  Complete nucleotide sequence of the Cryptomeria japonica D. Don. chloroplast genome and comparative chloroplast genomics: diversified genomic structure of coniferous species , 2008, BMC Plant Biology.

[35]  Robert K. Jansen,et al.  Automatic annotation of organellar genomes with DOGMA , 2004, Bioinform..

[36]  N. Perna,et al.  progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement , 2010, PloS one.

[37]  P. Vargas,et al.  Phylogenetic Relationships and Evolution in Erodium (Geraniaceae) based on trnL-trnF Sequences , 2006 .

[38]  R. Bock.  Cell and molecular biology of plastids , 2007 .

[39]  Tracey A Ruhlman,et al.  The plastid genomes of flowering plants. , 2014, Methods in molecular biology.

[40]  S. Massey,et al.  The distribution of recombination repair genes is linked to information content in bacteria. , 2013, Gene.

[41]  K. H. Wolfe,et al.  Nucleotide Substitution Rates in Legume Chloroplast DNA Depend on the Presence of the Inverted Repeat , 2002, Journal of Molecular Evolution.

[42]  B. Lang,et al.  Whirly proteins maintain plastid genome stability in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[43]  R. Jansen,et al.  Extensive Rearrangements in the Chloroplast Genome of Trachelium caeruleum Are Associated with Repeats and tRNA Genes , 2008, Journal of Molecular Evolution.

[44]  Tracey A Ruhlman,et al.  Phylogeny, rate variation, and genome size evolution of Pelargonium (Geraniaceae). , 2012, Molecular phylogenetics and evolution.

[45]  Kazutaka Katoh,et al.  Multiple alignment of DNA sequences with MAFFT. , 2009, Methods in molecular biology.

[46]  J. García,et al.  Phylogeny and Historical Biogeography of Geraniaceae in Relation to Climate Changes and Pollination Ecology , 2008 .

[47]  Marc Lohse,et al.  OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets , 2013, Nucleic Acids Res..

[48]  Jeffrey D. Palmer,et al.  Chloroplast DNA exists in two orientations , 1983, Nature.

[49]  James Leebens-Mack,et al.  Methods for obtaining and analyzing whole chloroplast genome sequences. , 2005, Methods in enzymology.

[50]  E. Knox.  The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms , 2014, Proceedings of the National Academy of Sciences.

[51]  B. Trus,et al.  A novel class of herpesvirus with bivalve hosts. , 2005, The Journal of general virology.

[52]  Ching-Ping Lin,et al.  Loss of Different Inverted Repeat Copies from the Chloroplast Genomes of Pinaceae and Cupressophytes and Influence of Heterotachy on the Evaluation of Gymnosperm Phylogeny , 2011, Genome biology and evolution.

[53]  Jeffrey P. Mower,et al.  Evolutionary dynamics of the plastid inverted repeat: the effects of expansion, contraction, and loss on substitution rates. , 2016, The New phytologist.

[54]  D. Posada.  Bioinformatics for DNA Sequence Analysis , 2009, Methods in Molecular Biology.

[55]  W. Wong,et al.  Improving PacBio Long Read Accuracy by Short Read Alignment , 2012, PloS one.

[56]  N. Brisson,et al.  Recombination and the maintenance of plant organelle genome stability. , 2010, The New phytologist.

[57]  J. Doyle,et al.  A rapid DNA isolation procedure for small amounts of fresh leaf tissue , 1987 .

[58]  Takashi Yamada.  Repetitive sequence-mediated rearragements in Chlorella ellipsoidea chloroplast DNA: completion of nucleotide sequence of the large inverted repeat , 1991, Current Genetics.

[59]  P. Madesis,et al.  DNA replication, recombination, and repair in plastids , 2007 .

[60]  R. Jansen,et al.  Extreme reconfiguration of plastid genomes in the angiosperm family Geraniaceae: rearrangements, repeats, and codon usage. , 2011, Molecular biology and evolution.

[61]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[62]  H. Okamoto,et al.  Double rolling circle replication (DRCR) is recombinogenic , 2011, Genes to cells : devoted to molecular & cellular mechanisms.

[63]  R. Jansen,et al.  Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae) , 2011, Plant Molecular Biology.

[64]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .

[65]  M. Sanderson,et al.  A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. , 2004, American journal of botany.