In Depth Characterization of Repetitive DNA in 23 Plant Genomes Reveals Sources of Genome Size Variation in the Legume Tribe Fabeae

The differential accumulation and elimination of repetitive DNA are key drivers of genome size variation in flowering plants, yet there have been few studies which have analysed how different types of repeats in related species contribute to genome size evolution within a phylogenetic context. This question is addressed here by conducting large-scale comparative analysis of repeats in 23 species from four genera of the monophyletic legume tribe Fabeae, representing a 7.6-fold variation in genome size. Phylogenetic analysis and genome size reconstruction revealed that this diversity arose from genome size expansions and contractions in different lineages during the evolution of Fabeae. Employing a combination of low-pass genome sequencing with novel bioinformatic approaches resulted in identification and quantification of repeats making up 55–83% of the investigated genomes. In turn, this enabled an analysis of how each major repeat type contributed to the genome size variation encountered. Differential accumulation of repetitive DNA was found to account for 85% of the genome size differences between the species, and most (57%) of this variation was found to be driven by a single lineage of Ty3/gypsy LTR-retrotransposons, the Ogre elements. Although the amounts of several other lineages of LTR-retrotransposons and the total amount of satellite DNA were also positively correlated with genome size, their contributions to genome size variation were much smaller (up to 6%). Repeat analysis within a phylogenetic framework also revealed profound differences in the extent of sequence conservation between different repeat types across Fabeae. In addition to these findings, the study has provided a proof of concept for the approach combining recent developments in sequencing and bioinformatics to perform comparative analyses of repetitive DNAs in a large number of non-model species without the need to assemble their genomes.

[1]  M. Morgante,et al.  The Ty1-copia LTR retroelement family PARTC is highly conserved in conifers over 200 MY of evolution. , 2015, Gene.

[2]  Peter D. Day,et al.  Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size , 2015, The New phytologist.

[3]  M. Bakkali,et al.  A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs , 2015, Chromosoma.

[4]  G. García,et al.  Next-generation sequencing detects repetitive elements expansion in giant genomes of annual killifish genus Austrolebias (Cyprinodontiformes, Rivulidae) , 2015, Genetica.

[5]  T. Michael,et al.  Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. , 2014, Annals of botany.

[6]  W. Jin,et al.  Differential genome evolution and speciation of Coix lacryma-jobi L. and Coix aquatica Roxb. hybrid guangxi revealed by repetitive sequence analysis and fine karyotyping , 2014, BMC Genomics.

[7]  S. Wright,et al.  No evidence that sex and transposable elements drive genome size variation in evening primroses , 2014, bioRxiv.

[8]  D. Weigel,et al.  Mating system shifts and transposable element evolution in the plant genus Capsella , 2014, BMC Genomics.

[9]  T. Michael Plant genome size variation: bloating and purging DNA. , 2014, Briefings in functional genomics.

[10]  J. Macas,et al.  Genome-Wide Analysis of Repeat Diversity across the Family Musaceae , 2014, PloS one.

[11]  J. Bennetzen,et al.  The contributions of transposable elements to the structure, function, and evolution of plant genomes. , 2014, Annual review of plant biology.

[12]  M. Fay,et al.  A universe of dwarfs and giants: genome size and chromosome evolution in the monocot family Melanthiaceae. , 2014, The New phytologist.

[13]  Ales Krenek,et al.  Genome assembly and annotation for red clover (Trifolium pratense; Fabaceae). , 2014, American journal of botany.

[14]  Keith R. Oliver,et al.  Transposable Elements: Powerful Contributors to Angiosperm Evolution and Diversity , 2013, Genome biology and evolution.

[15]  Tyler A. Elliott,et al.  Distinguishing ecological from evolutionary approaches to transposable elements , 2013, Biological reviews of the Cambridge Philosophical Society.

[16]  T. Wicker,et al.  High-copy sequences reveal distinct evolution of the rye B chromosome. , 2013, The New phytologist.

[17]  Petr Novák,et al.  RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads , 2013, Bioinform..

[18]  O. Panaud,et al.  Comparative Genomic Paleontology across Plant Kingdom Reveals the Dynamics of TE-Driven Genome Evolution , 2013, Genome biology and evolution.

[19]  Jeremy D. DeBarry,et al.  The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution , 2013, Heredity.

[20]  A. Santos‐Guerra,et al.  Systematics, biogeography, and character evolution of the legume tribe Fabeae with special focus on the middle-Atlantic island lineages , 2012, BMC Evolutionary Biology.

[21]  Jiming Jiang,et al.  Repeatless and Repeat-Based Centromeres in Potato: Implications for Centromere Evolution[C][W] , 2012, Plant Cell.

[22]  M. Fay,et al.  Why size really matters when sequencing plant genomes , 2012 .

[23]  J. Macas,et al.  Stretching the Rules: Monocentric Chromosomes with Multiple Centromere Domains , 2012, PLoS genetics.

[24]  D. Ray,et al.  Survey Sequencing Reveals Elevated DNA Transposon Activity, Novel Elements, and Variation in Repetitive Landscapes among Vesper Bats , 2012, Genome biology and evolution.

[25]  J. Macas,et al.  Correction: Next Generation Sequencing-Based Analysis of Repetitive DNA in the Model Dioceous Plant Silene latifolia , 2011, PLoS ONE.

[26]  J. Macas,et al.  A widespread occurrence of extra open reading frames in plant Ty3/gypsy retrotransposons , 2011, Genetica.

[27]  L. J. Kelly,et al.  Exploring giant plant genomes with next-generation sequencing technology , 2011, Chromosome Research.

[28]  M. Chase,et al.  Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. , 2011, Molecular biology and evolution.

[29]  T. Fennell,et al.  Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries , 2011, Genome Biology.

[30]  B. Gaut,et al.  Genome Size and Transposable Element Content as Determined by High-Throughput Sequencing in Maize and Zea luxurians , 2011, Genome biology and evolution.

[31]  José M. Sempere,et al.  The Gypsy Database (GyDB) of mobile genetic elements: release 2.0 , 2010, Nucleic Acids Res..

[32]  Ilia J. Leitch,et al.  The largest eukaryotic genome of them all , 2010 .

[33]  J. Macas,et al.  Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data , 2010, BMC Bioinformatics.

[34]  B. Gaut,et al.  The evolution of transposable elements in natural populations of self-fertilizing Arabidopsis thaliana and its outcrossing relative Arabidopsis lyrata , 2010, BMC Evolutionary Biology.

[35]  Ryan A. Rapp,et al.  Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants , 2009, Proceedings of the National Academy of Sciences.

[36]  Keith R. Oliver,et al.  Transposable elements: powerful facilitators of evolution , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  R. Ford,et al.  Evolutionary conserved lineage of Angela-family retrotransposons as a genome-wide microsatellite repeat dispersal agent , 2009, Heredity.

[38]  J. Macas,et al.  Experimental evidence for splicing of intron-containing transcripts of plant LTR retrotransposon Ogre , 2008, Molecular Genetics and Genomics.

[39]  Pavel Neumann,et al.  Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula , 2007, BMC Genomics.

[40]  J. Doležel,et al.  Estimation of nuclear DNA content in plants using flow cytometry , 2007, Nature Protocols.

[41]  Andrea Zuccolo,et al.  Transposable element distribution, abundance and role in genome size variation in the genus Oryza , 2007, BMC Evolutionary Biology.

[42]  A. Kovařík,et al.  Plant highly repeated satellite DNA: Molecular evolution, distribution and use for identification of hybrids , 2007 .

[43]  Beat Keller,et al.  Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. , 2007, Genome research.

[44]  Jirí Macas,et al.  Ogre elements--a distinct group of plant Ty3/gypsy-like retrotransposons. , 2007, Gene.

[45]  Rod A Wing,et al.  Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. , 2006, Genome research.

[46]  S. Jackson,et al.  Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. , 2006, Genome research.

[47]  J. Macas,et al.  Significant Expansion of Vicia pannonica Genome Size Mediated by Amplification of a Single Type of Giant Retroelement , 2006, Genetics.

[48]  M. Lynch,et al.  The Origins of Genome Complexity , 2003, Science.

[49]  J. Macas,et al.  Sequence subfamilies of satellite repeats related to rDNA intergenic spacer are differentially amplified on Vicia sativa chromosomes , 2003, Chromosoma.

[50]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[51]  J. Macas,et al.  Karyotype analysis of four Vicia species using in situ hybridization with repetitive sequences. , 2003, Annals of botany.

[52]  John Quackenbush,et al.  TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets , 2003, Bioinform..

[53]  J. Doležel,et al.  Nuclear DNA content and genome size of trout and human. , 2003, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[54]  James K. M. Brown,et al.  Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. , 2002, Genome research.

[55]  T. Gregory,et al.  Coincidence, coevolution, or causation? DNA content, cellsize, and the C‐value enigma , 2001, Biological reviews of the Cambridge Philosophical Society.

[56]  M. G. Kidwell,et al.  PERSPECTIVE: TRANSPOSABLE ELEMENTS, PARASITIC DNA, AND GENOME EVOLUTION , 2001, Evolution; international journal of organic evolution.

[57]  J. Macas,et al.  Two new families of tandem repeats isolated from genus Vicia using genomic self-priming PCR , 2000, Molecular and General Genetics MGG.

[58]  L Nardi,et al.  Plant Genome Size Estimation by Flow Cytometry: Inter-laboratory Comparison , 1998 .

[59]  J. Doležel,et al.  Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata andM. balbisiana) , 1994, Biologia Plantarum.

[60]  L. C. Hannah,et al.  Origin of the main class of repetitive DNA within selected Pennisetum species , 1993, Molecular and General Genetics MGG.

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

[62]  R. B. Flavell,et al.  Genome size and the proportion of repeated nucleotide sequence DNA in plants , 1974, Biochemical Genetics.

[63]  R. Britten,et al.  Repeated Sequences in DNA , 1968 .

[64]  J. Macas,et al.  Employing next generation sequencing to explore the repeat landscape of the plant genome , 2015 .

[65]  H. Gundlach,et al.  Research article Next-Generation Sequencing Reveals the Impact of Repetitive DNA Across Phylogenetically Closely Related Genomes of Orobanchaceae , 2012 .

[66]  C. Feschotte,et al.  Plant Transposable Elements: Biology and Evolution , 2012 .

[67]  J. Suda,et al.  The distribution of cytotypes of Vicia cracca in Central Europe: the changes that have occurred over the last four decades. , 2010 .

[68]  Jaroslav Dolezel,et al.  The origin, evolution and proposed stabilization of the terms 'genome size' and 'C-value' to describe nuclear DNA contents. , 2005, Annals of botany.

[69]  D. Galbraith,et al.  Microarray-based survey of repetitive genomic sequences in Vicia spp. , 2004, Plant Molecular Biology.

[70]  Jirí Macas,et al.  PlantSat: a specialized database for plant satellite repeats , 2002, Bioinform..

[71]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[72]  J. Doležel,et al.  Estimation of nuclear DNA content in Sesleria (Poaceae) , 1998 .

[73]  F Otto,et al.  DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. , 1990, Methods in cell biology.

[74]  C. A. Thomas The genetic organization of chromosomes. , 1971, Annual review of genetics.