Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions, and accelerated rate of evolution in clpP

The Leguminosae has emerged as a model for studying angiosperm plastome evolution because of its striking diversity of structural rearrangements and sequence variation. However, most of what is known about legume plastomes comes from few genera representing a subset of lineages in subfamily Papilionoideae. We investigate plastome evolution in subfamily Mimosoideae based on two newly sequenced plastomes (Inga and Leucaena) and two recently published plastomes (Acacia and Prosopis), and discuss the results in the context of other legume and rosid plastid genomes. Mimosoid plastomes have a typical angiosperm gene content and general organization as well as a generally slow rate of protein coding gene evolution, but they are the largest known among legumes. The increased length results from tandem repeat expansions and an unusual 13 kb IR-SSC boundary shift in Acacia and Inga. Mimosoid plastomes harbor additional interesting features, including loss of clpP intron1 in Inga, accelerated rates of evolution in clpP for Acacia and Inga, and dN/dS ratios consistent with neutral and positive selection for several genes. These new plastomes and results provide important resources for legume comparative genomics, plant breeding, and plastid genetic engineering, while shedding further light on the complexity of plastome evolution in legumes and angiosperms.

[1]  Frédéric Delsuc,et al.  MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons , 2011, PloS one.

[2]  Daniel R Zerbino,et al.  Using the Velvet de novo Assembler for Short‐Read Sequencing Technologies , 2010, Current protocols in bioinformatics.

[3]  Tracey A Ruhlman,et al.  Plastid genome sequences of legumes reveal parallel inversions and multiple losses of rps16 in papilionoids , 2015 .

[4]  C. Hughes,et al.  The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants. , 2011, American journal of botany.

[5]  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.

[6]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[7]  J. Brewbaker.  Leucaena: a multipurpose tree genus for tropical agroforestry. , 1987 .

[8]  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.

[9]  Tracey A Ruhlman,et al.  Evolutionary and biotechnology implications of plastid genome variation in the inverted-repeat-lacking clade of legumes. , 2014, Plant biotechnology journal.

[10]  D. Soltis,et al.  Complete Plastid Genome Sequencing of Trochodendraceae Reveals a Significant Expansion of the Inverted Repeat and Suggests a Paleogene Divergence between the Two Extant Species , 2013, PloS one.

[11]  J. Palmer,et al.  Conservation of chloroplast genome structure among vascular plants , 1986, Current Genetics.

[12]  T. J. Edwards,et al.  Legumes of the World , 2007 .

[13]  Tracey A Ruhlman,et al.  Plastid Genomes of Seed Plants , 2012 .

[14]  Ian Small,et al.  The Complete Sequence of the Acacia ligulata Chloroplast Genome Reveals a Highly Divergent clpP1 Gene , 2015, PloS one.

[15]  A. Liston,et al.  Building a model: developing genomic resources for common milkweed (Asclepias syriaca) with low coverage genome sequencing , 2011, BMC Genomics.

[16]  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.

[17]  D. Smith.  Mitochondrion-to-plastid DNA transfer: it happens. , 2014, The New phytologist.

[18]  K. A. Cunningham,et al.  The plastid clpP gene may not be essential for plant cell viability. , 2003, Plant & cell physiology.

[19]  C. N. Stewart,et al.  Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes. , 2015, Molecular biology and evolution.

[20]  John Healy,et al.  GapCoder automates the use of indel characters in phylogenetic analysis , 2003, BMC Bioinformatics.

[21]  S. Downie,et al.  A Comparative Analysis of Whole Plastid Genomes from the Apiales: Expansion and Contraction of the Inverted Repeat, Mitochondrial to Plastid Transfer of DNA, and Identification of Highly Divergent Noncoding Regions , 2015 .

[22]  Rupart C. Barneby.  Sensitivae censitae : a description of the genus Mimosa Linnaeus (Mimosaceae) in the new world , 1992 .

[23]  Daniel B. Sloan,et al.  Correlation between sequence divergence and polymorphism reveals similar evolutionary mechanisms acting across multiple timescales in a rapidly evolving plastid genome , 2014, BMC Evolutionary Biology.

[24]  M. Luckow,et al.  A PHYLOGENETIC ANALYSIS OF THE MIMOSOIDEAE (LEGUMINOSAE) BASED ON CHLOROPLAST DNA SEQUENCE DATA , 2003 .

[25]  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.

[26]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[27]  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.

[28]  J. Palmer,et al.  The chloroplast genome arrangement ofLobelia thuliniana (Lobeliaceae): Expansion of the inverted repeat in an ancestor of theCampanulales , 1999, Plant Systematics and Evolution.

[29]  C. Hughes.  Leucaena: A genetic resources handbook. , 1998 .

[30]  R. Hill,et al.  Integration of morphological data sets for phylogenetic analysis of Amniota: the importance of integumentary characters and increased taxonomic sampling. , 2005, Systematic biology.

[31]  G. Reighard,et al.  Construction of a BAC library and its application to the identification of simple sequence repeats in peach [Prunus persica (L.) Batsch] , 2002, Theoretical and Applied Genetics.

[32]  J. Palmer,et al.  CHAPTER 2 – Plastid Chromosomes: Structure and Evolution , 1991 .

[33]  D. Naquin,et al.  The first complete chloroplast genome of the Genistoid legume Lupinus luteus: evidence for a novel major lineage-specific rearrangement and new insights regarding plastome evolution in the legume family. , 2014, Annals of botany.

[34]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[35]  Daniel J. Murphy,et al.  Legume phylogeny and classification in the 21st century: Progress, prospects and lessons for other species-rich clades , 2013 .

[36]  Y. Yamazaki,et al.  Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. , 2002, Molecular biology and evolution.

[37]  J. Palmer,et al.  Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. , 1991, The EMBO journal.

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

[39]  Wei Zhu,et al.  The complete chloroplast genome sequence of Mahonia bealei (Berberidaceae) reveals a significant expansion of the inverted repeat and phylogenetic relationship with other angiosperms. , 2013, Gene.

[40]  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.

[41]  J. Palmer,et al.  Multiple Independent Losses of Two Genes and One Intron from Legume Chloroplast Genomes , 1995 .

[42]  Aaron R. Quinlan,et al.  Bioinformatics Applications Note Genome Analysis Bedtools: a Flexible Suite of Utilities for Comparing Genomic Features , 2022 .

[43]  Q. Cronk,et al.  Evolutionary origin of highly repetitive plastid genomes within the clover genus (Trifolium) , 2014, BMC Evolutionary Biology.

[44]  Daniel B. Sloan,et al.  A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). , 2014, Molecular phylogenetics and evolution.

[45]  James Leebens-Mack,et al.  Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns , 2007, Proceedings of the National Academy of Sciences.

[46]  F. Sisay-Joof,et al.  Inactive alleles of cytochrome P450 2C19 may be positively selected in human evolution , 2014, BMC Evolutionary Biology.

[47]  G. Stacey,et al.  Advances in Legume Biology , 2003, Plant Physiology.

[48]  Huanming Yang,et al.  De novo assembly of human genomes with massively parallel short read sequencing. , 2010, Genome research.

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

[50]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[51]  Andrew J. Alverson,et al.  Recent Acceleration of Plastid Sequence and Structural Evolution Coincides with Extreme Mitochondrial Divergence in the Angiosperm Genus Silene , 2012, Genome biology and evolution.

[52]  J. Palmer,et al.  Localized hypermutation and associated gene losses in legume chloroplast genomes. , 2010, Genome research.

[53]  R. Jansen,et al.  Extensive Reorganization of the Plastid Genome of Trifolium subterraneum (Fabaceae) Is Associated with Numerous Repeated Sequences and Novel DNA Insertions , 2008, Journal of Molecular Evolution.

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

[55]  Jasper J. Koehorst,et al.  Capturing the Biofuel Wellhead and Powerhouse: The Chloroplast and Mitochondrial Genomes of the Leguminous Feedstock Tree Pongamia pinnata , 2012, PloS one.

[56]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

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

[58]  J. Palmer,et al.  The distribution and phylogenetic significance of a 50-kb chloroplast DNA inversion in the flowering plant family Leguminosae. , 1996, Molecular phylogenetics and evolution.

[59]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[60]  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.

[61]  R. Jansen,et al.  Complete plastid genome sequence of the chickpea (Cicer arietinum) and the phylogenetic distribution of rps12 and clpP intron losses among legumes (Leguminosae). , 2008, Molecular phylogenetics and evolution.

[62]  D. Murphy,et al.  Molecular phylogeny of Acacia Mill. (Mimosoideae: Leguminosae): Evidence for major clades and informal classification , 2010 .

[63]  Casey W. Dunn,et al.  Phyutility: a phyloinformatics tool for trees, alignments and molecular data , 2008, Bioinform..

[64]  D. Richardson,et al.  Trees and shrubs as invasive alien species – a global review , 2011 .

[65]  Jungeun Kim,et al.  Complete sequencing and comparative analyses of the pepper (Capsicum annuum L.) plastome revealed high frequency of tandem repeats and large insertion/deletions on pepper plastome , 2011, Plant Cell Reports.

[66]  M. Luckow,et al.  The Rest of the Iceberg. Legume Diversity and Evolution in a Phylogenetic Context1 , 2003, Plant Physiology.

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

[68]  Herrmann,et al.  Gene transfer from organelles to the nucleus: how much, what happens, and Why? , 1998, Plant Physiology.

[69]  M. Wojciechowski,et al.  Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. , 2005, Systematic biology.

[70]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

[71]  Wenpan Dong,et al.  Complete Chloroplast Genome of Sedum sarmentosum and Chloroplast Genome Evolution in Saxifragales , 2013, PloS one.

[72]  Steven J. M. Jones,et al.  Abyss: a Parallel Assembler for Short Read Sequence Data Material Supplemental Open Access , 2022 .