The Repetitive Content in Lupin Genomes

Part of the Compendium of Plant Genomes book series (CPG)


In this chapter, we present the first detailed evaluation of the repetitive compartment in Lupinus genomes. Low-depth next-generation sequencing (NGS) genomic resources from four closely related smooth-seeded Mediterranean lupin species (L. albus, L. angustifolius, L. luteus, and L. micranthus), exhibiting remarkable differences in genome size and chromosome number have been investigated. The repetitive compartment is composed of a wide diversity of repeats and represents 23–51% of the genomes. This compartment is essentially comprised of transposable elements (43–85%), mainly represented by copia and gypsy LTR retrotransposon families. Among the latter, some prominent families (Tekay, Athila, Maximus-SIRE) significantly contribute to genome size differences among species and in shaping different species-specific repeat profiles, regardless of their chromosome numbers. Also particular lineages of these elements have been differentially and recently amplified within species, such as in L. luteus, L. albus, and L. angustifolius. Moreover, this study highlighted the diversity of tandem repeats in lupin genomes, with minisatellites and satellites mostly being species-specific, whereas microsatellites (SSRs) are ubiquitously distributed. Strikingly, L. angustifolius exhibited a tremendous amount of tandem repeats in its genome (26%), including a noteworthy accumulation of one particular hexamer SSR (15.24% of the genome), which demonstrate that also tandem repeats may greatly contribute to genome obesity and dynamics in lupins. Therefore, differential lineage-specific amplifications of retrotransposons and tandem repeats occurred among lupins. Accordingly, this strongly suggests that different processes and mechanisms regulating amplification, proliferation, and clearance of repeats have differentially operated within the same genus among closely related Mediterranean species over the last ~10–12 Myr. Further extension of such evaluation to various representatives of the lupins diversity and outgroups will provide a better overview of the repetitive compartment and its evolutionary dynamics in the genus. Additionally, the genomic resources generated by this work represent a valuable basis to start building a repeats database specifically dedicated to best understand the genomic landscape, repeats distribution, and localization in lupins. This will facilitate further investigations on the functional and evolutionary impact of repeats on genes of interest, such as those responsive for important agronomical, adaptive, and defense features.



We are grateful to INEE-CNRS (France) and to the University of Rennes for their support to this work as part of the research program of the International Associated Laboratory “Ecological Genomics of Polyploidy” involving the University of Rennes (France) and the Iowa State University (Ames, USA). We thank Prof. Barbara Naganowska (Institut of Plant Genetics/PAS, Poznan, Poland) for kindly providing L. angustifolius seeds (IPG2 accession).


  1. Ainouche A, Bayer RJ, Misset M-T (2004) Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupines. Plant Syst Evol 246(3–4):211–222Google Scholar
  2. Aïnouche A, Bayer RJ (1999) Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Am J Bot 86(4):590–607PubMedGoogle Scholar
  3. Alix K, Heslop-harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54:895–909PubMedGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  5. Atnaf M, Yao N, Martina K, Dagne K, Wegary D, Tesfaye K (2017) Molecular genetic diversity and population structure of Ethiopian white lupin landraces: implications for breeding and conservation. PLoS ONE 12(11):e0188696PubMedPubMedCentralGoogle Scholar
  6. Ávila Robledillo L, Koblížková A, Novák P, Böttinger K, Vrbová I, Neumann P, Schubert I, Macas J (2018) Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci Rep 8:5838PubMedPubMedCentralGoogle Scholar
  7. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedGoogle Scholar
  8. Bao W, Kojima KK, Kohany O (2015) Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6Google Scholar
  9. Barghini E, Natali L, Cossu RM, Giordani T, Pindo M, Cattonaro F, Scalabrin S, Velasco R, Morgante M, Cavallini A (2014) The peculiar landscape of repetitive sequences in the olive (Olea europaea L.) genome. Genome Biol Evol 6:776–791PubMedPubMedCentralGoogle Scholar
  10. Bennett MD (2005) Nuclear DNA amounts in angiosperms: progress, problems and prospects. Ann Bot 95:45–90PubMedPubMedCentralGoogle Scholar
  11. Bennetzen JL (2000) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269PubMedGoogle Scholar
  12. Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36PubMedGoogle Scholar
  13. Bennetzen JL (2005) Transposable elements, gene creation and genome rearrangement in flowering plants. Curr Opin Genet Dev 15:621–627PubMedGoogle Scholar
  14. Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 65:505–530PubMedGoogle Scholar
  15. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580PubMedPubMedCentralGoogle Scholar
  16. Biémont C, Vieira C (2006) Genetics: Junk DNA as an evolutionary force. Nature 443:521–524PubMedGoogle Scholar
  17. Biscotti MA, Olmo E, Heslop-Harrison JS (2015) Repetitive DNA in eukaryotic genomes. Chromosome Res 23(3):415–420PubMedGoogle Scholar
  18. Cabello-Hurtado F, Keller J, Ley J, Sanchez-Lucas R, Jorrín-Novo JV, Aïnouche A (2016) Proteomics for exploiting diversity of lupin seed storage proteins and their use as nutraceuticals for health and welfare. J Proteomics 143:57–68PubMedGoogle Scholar
  19. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421Google Scholar
  20. Castel SE, Martienssen RA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14:100–112PubMedPubMedCentralGoogle Scholar
  21. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedGoogle Scholar
  22. Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A, Segurens B, Carter M, Huteau V, Coriton O et al (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics 180:1071–1086PubMedPubMedCentralGoogle Scholar
  23. Chénais B, Caruso A, Hiard S, Casse N (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509:7–15PubMedGoogle Scholar
  24. Chevreux B, Wetter T, Suhai S (1999) Genome sequence assembly using trace signals and additional sequence information. Comput Sci Biol: Proc German Conf Bioinform 99:45–56Google Scholar
  25. Chu C, Nielsen R, Wu Y, Antoniewski C (2016) REPdenovo: Inferring de novo repeat motifs from short sequence reads. PLOS ONE 11 (3):e0150719Google Scholar
  26. Conterato IF, Schifino-Wittmann MT (2006) New chromosome numbers, meiotic behaviour and pollen fertility in American taxa of Lupinus (Leguminosae): contributions to taxonomic and evolutionary studies. Bot J Linn Soc 150:229–240Google Scholar
  27. Devos KM (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079PubMedPubMedCentralGoogle Scholar
  28. Dolezel J, Bartos J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry 51A:127–128Google Scholar
  29. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603PubMedGoogle Scholar
  30. Eastwood RJ, Drummond CS, Schifino-Wittmann MT, Hughes CE (2008) Diversity and evolutionary history of lupins–insights from new phylogenies. In: Lupins for health and wealth: 12th international lupin conference, vol 10Google Scholar
  31. Estep MC, DeBarry JD, Bennetzen JL (2013) The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution. Heredity 110:194–204PubMedPubMedCentralGoogle Scholar
  32. Ferree PM, Barbash DA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7:e1000234 (MAF Noor, Ed.)Google Scholar
  33. Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A (1992) Ty1–copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res 20:3639–3644PubMedPubMedCentralGoogle Scholar
  34. Flutre T, Duprat E, Feuillet C, Quesneville H (2011) Considering transposable element diversification in de novo annotation approaches. PLoS ONE 6 (Y Xu, Ed.)Google Scholar
  35. Fry K, Salser W (1977) Nucleotide sequences of HS-a satellite DNA from Kangaroo Rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12:1069–1084PubMedGoogle Scholar
  36. Garrido-Ramos MA (2015) Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146:153–170PubMedGoogle Scholar
  37. Garrido-Ramos M (2017) Satellite DNA: an evolving topic. Genes 8:230PubMedCentralGoogle Scholar
  38. Gladstones JS, Atkins CA, Hamblin J (eds) (1998) Lupins as crop plants: biology, production, and utilization. CAB International, Wallingford, Oxon, UK ; New York, NY, USAGoogle Scholar
  39. Grandbastien M-A, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa A-PP, Le QH, Melayah D, Petit M, Poncet C et al (2005) Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res 110:229–241PubMedGoogle Scholar
  40. Gregory TR (2005) The C-value Enigma in plants and animals: a review of parallels and an appeal for partnership. Ann Bot 95:133–146PubMedPubMedCentralGoogle Scholar
  41. Greilhuber J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott W (2006) Smallest angiosperm genomes found in lentibulariaceae, with chromosomes of bacterial size. Plant Biol 8:770–777PubMedGoogle Scholar
  42. Hane JK, Ming Y, Kamphuis LG, Nelson MN, Garg G, Atkins CA, Bayer PE, Bravo A, Bringans S, Cannon S et al (2017) A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant-microbe interactions and legume evolution. Plant Biotechnol J 15:318–330PubMedGoogle Scholar
  43. Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16:1252–1261PubMedPubMedCentralGoogle Scholar
  44. Hawkins JS, Proulx SR, Rapp RA, Wendel JF (2009) Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc Natl Acad Sci 106:17811–17816PubMedGoogle Scholar
  45. Heitkam T, Petrasch S, Zakrzewski F, Kögler A, Wenke T, Wanke S, Schmidt T (2015) Next-generation sequencing reveals differentially amplified tandem repeats as a major genome component of Northern Europe’s oldest Camellia japonica. Chromosome Res 23:791–806PubMedGoogle Scholar
  46. Hoang DT, Chernomor O, von Haeseler A, Quang Minh B, Sy VL (2017) Ufboot 2: improving the ultrafast bootstrap approximation. Mol Biol Evol 32:518–522Google Scholar
  47. Hosaka A, Kakutani T (2018) Transposable elements, genome evolution and transgenerational epigenetic variation. Curr Opin Genet Dev 49:43–48PubMedGoogle Scholar
  48. Hřibová E, Neumann P, Matsumoto T, Roux N, Macas J, Doležel J (2010) Repetitive part of the banana (Musa acuminata) genome investigated by low-depth 454 sequencing. BMC Plant Biol 10Google Scholar
  49. Hu TT, Pattyn P, Bakker EG, Cao J, Cheng J-F, Clark RM, Fahlgren N, Fawcett JA, Grimwood J, Gundlach H et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–481PubMedPubMedCentralGoogle Scholar
  50. Hughes C, Eastwood R (2006) Island radiation on a continental scale: Exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci 103 (27):10334–10339.
  51. Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR (2003) An active DNA transposon family in rice. Nature 421:163–167PubMedGoogle Scholar
  52. Jiang N, Feschotte C, Zhang X, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7:115–119PubMedGoogle Scholar
  53. Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci 97:6603–6607PubMedGoogle Scholar
  54. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589PubMedPubMedCentralGoogle Scholar
  55. Kamphuis LG, Hane JK, Nelson MN, Gao L, Atkins CA, Singh KB (2015) Transcriptome sequencing of different narrow-leafed lupin tissue types provides a comprehensive uni-gene assembly and extensive gene-based molecular markers. Plant Biotechnol J 13:14–25PubMedGoogle Scholar
  56. Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106PubMedGoogle Scholar
  57. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780PubMedPubMedCentralGoogle Scholar
  58. Keller J, Imperial J, Ruiz-Argüeso T, Privet K, Lima O, Michon-Coudouel S, Biget M, Salmon A, Aïnouche A, Cabello-Hurtado F (2018) RNA sequencing and analysis of three Lupinus nodulomes provide new insights into specific host-symbiont relationships with compatible and incompatible Bradyrhizobium strains. Plant Sci 266:102–116PubMedGoogle Scholar
  59. Kroc M, Koczyk G, Święcicki W, Kilian A, Nelson MN (2014) New evidence of ancestral polyploidy in the Genistoid legume Lupinus angustifolius L. (narrow-leafed lupin). Theor Appl Genet 127:1237–1249PubMedGoogle Scholar
  60. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645PubMedPubMedCentralGoogle Scholar
  61. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532PubMedGoogle Scholar
  62. Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483PubMedGoogle Scholar
  63. Lerat E (2010) Identifying repeats and transposable elements in sequenced genomes: how to find your way through the dense forest of programs. Heredity 104:520–533PubMedGoogle Scholar
  64. Levinson G, Gutman G (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4:203–221PubMedGoogle Scholar
  65. Li Y-C (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007PubMedGoogle Scholar
  66. Lim KG, Kwoh CK, Hsu LY, Wirawan A (2013) Review of tandem repeat search tools: a systematic approach to evaluating algorithmic performance. Brief Bioinform 14:67–81PubMedGoogle Scholar
  67. Lippman Z, Gendrel A-V, Black M, Vaughn MW, Dedhia N, Richard McCombie W, Lavine K, Mittal V, May B, Kasschau KD et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476PubMedGoogle Scholar
  68. Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66PubMedGoogle Scholar
  69. Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61PubMedGoogle Scholar
  70. Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43:874–880PubMedGoogle Scholar
  71. Lönnig W-E, Saedler H (1997) Plant transposons: contributors to evolution? Gene 205:245–253PubMedGoogle Scholar
  72. Lower SS, McGurk MP, Clark AG, Barbash DA (2018) Satellite DNA evolution: old ideas, new approaches. Curr Opin Genet Dev 49:70–78PubMedPubMedCentralGoogle Scholar
  73. Lynch VJ, Nnamani MC, Kapusta A, Brayer K, Plaza SL, Mazur EC, Emera D, Sheikh SZ, Grützner F, Bauersachs S et al (2015) Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy. Cell Rep 10:551–561PubMedPubMedCentralGoogle Scholar
  74. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci 101:12404–12410PubMedGoogle Scholar
  75. Macas J, Neumann P, Navrátilová A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8Google Scholar
  76. Mahé F (2009) Phylogénie, éléments transposables et évolution de la taille des génomes chez les lupinsGoogle Scholar
  77. Mahé F, Pascual H, Coriton O, Huteau V, Navarro Perris A, Misset M-T, Aïnouche A (2011) New data and phylogenetic placement of the enigmatic Old World lupin: Lupinus mariae-josephi H Pascual. Genet Resour Crop Evol 58:101–114Google Scholar
  78. Mayer KFX, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263PubMedPubMedCentralGoogle Scholar
  79. McClintock B (1948) Mutable loci in maize. Carnegie Institution of Washington Year Book, 47, 155–169Google Scholar
  80. Metzgar D, Bytof J, Wills C (2000) Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res 9Google Scholar
  81. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002PubMedGoogle Scholar
  82. Naganowska B (2003) Nuclear DNA content variation and species relationships in the genus Lupinus (Fabaceae). Ann Bot 92:349–355PubMedPubMedCentralGoogle Scholar
  83. Naganowska B, Wolko B, Śliwińska E, Kaczmarek Z, Schifino-Wittmann MT (2005) 2C DNA variation and relationships among New World species of the genus Lupinus (Fabaceae). Plant Syst Evol 256:147–157Google Scholar
  84. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274PubMedPubMedCentralGoogle Scholar
  85. Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11Google Scholar
  86. Novák P, Ávila Robledillo L, Koblížková A, Vrbová I, Neumann P, Macas J (2017) TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res 45Google Scholar
  87. Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793PubMedGoogle Scholar
  88. O’Rourke JA, Yang SS, Miller SS, Bucciarelli B, Liu J, Rydeen A, Bozsoki Z, Uhde-Stone C, Tu ZJ, Allan D et al (2013) An RNA-Seq transcriptome analysis of orthophosphate-deficient white lupin reveals novel insights into phosphorus acclimation in plants. Plant Physiol 161:705–724Google Scholar
  89. Oliveira EJ, Pádua JG, Zucchi MI, Vencovsky R, Vieira MLC (2006) Origin, evolution and genome distribution of microsatellites. Genet Mol Biol 29:294–307Google Scholar
  90. Oliver KR, McComb JA, Greene WK (2013) Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol Evol 5:1886–1901PubMedPubMedCentralGoogle Scholar
  91. Orgel LE, Crick FH, Sapienza C (1980) Selfish DNA. Nature 288:645–646PubMedGoogle Scholar
  92. Parra-González LB, Aravena-Abarzúa GA, Navarro-Navarro CS, Udall J, Maughan J, Peterson LM, Salvo-Garrido HE, Maureira-Butler IJ (2012) Yellow lupin (Lupinus luteus L.) transcriptome sequencing: molecular marker development and comparative studies. BMC Genomics 13:425Google Scholar
  93. Pellicer J, Hidalgo O, Dodsworth S, Leitch I (2018) Genome size diversity and its impact on the evolution of land plants. Genes 9:88PubMedCentralGoogle Scholar
  94. Petes TD (1980) Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell 19:765–774PubMedGoogle Scholar
  95. Piednoël M, Carrete-Vega G, Renner SS (2013) Characterization of the LTR retrotransposon repertoire of a plant clade of six diploid and one tetraploid species. Plant J 75:699–709PubMedGoogle Scholar
  96. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA et al (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269PubMedPubMedCentralGoogle Scholar
  97. Plohl M, Mestrovic N, Mravinac B (2012) Satellite DNA evolution. In: Garrido-Ramos MA (ed) Genome dynamics. S. KARGER AG, Basel, pp 126–152Google Scholar
  98. Priyam A, Woodcroft BJ, Rai V, Munagala A, Moghul I, Ter F, Gibbins MA, Moon H, Leonard G, Rumpf W, Wurm Y (2015) Sequenceserver: a modern graphical user interface for custom BLAST databases. biorxiv.
  99. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, Ashburner M, Anxolabehere D (2005) Combined evidence annotation of transposable elements in genome sequences. PLoS Comput Biol 1:166–175PubMedGoogle Scholar
  100. Raman R, Cowley RB, Raman HD, Luckett DJ (2014) Analyses using SSR and DArT molecular markers reveal that Ethiopian accessions of white lupin (Lupinus albus L.) represent a unique gene pool. Open J Genet 4:87–98Google Scholar
  101. Renny-Byfield S, Wendel JF (2014) Doubling down on genomes: polyploidy and crop plants. Am J Bot 101:1711–1725PubMedGoogle Scholar
  102. Renny-Byfield S, Chester M, Kovarik A, Le Comber SC, Grandbastien M-A, Deloger M, Nichols RA, Macas J, Novak P, Chase MW et al (2011) Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol 28:2843–2854PubMedGoogle Scholar
  103. Renny-Byfield S, Gallagher JP, Grover CE, Szadkowski E, Page JT, Udall JA, Wang X, Paterson AH, Wendel JF (2014) Ancient gene duplicates in Gossypium (Cotton) exhibit near-complete expression divergence. Genome Biol Evol 6:559–571PubMedPubMedCentralGoogle Scholar
  104. Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6Google Scholar
  105. Satović E, Vojvoda Zeljko T, Plohl M (2018) Characteristics and evolution of satellite DNA sequences in bivalve mollusks. Eur Zool J 85:94–103Google Scholar
  106. Schmuths H (2004) Genome size variation among accessions of Arabidopsis thaliana. Ann Bot 93:317–321PubMedPubMedCentralGoogle Scholar
  107. Sequencing Project IRG (2005) The map-based sequence of the rice genome. Nature 436:793–800Google Scholar
  108. Shi J, Huang S, Fu D, Yu J, Wang X, Hua W, Liu S, Liu G, Wang H (2013) Evolutionary dynamics of microsatellite distribution in plants: insight from the comparison of sequenced Brassica, Arabidopsis and other angiosperm species. PLoS ONE 8:e59988 (BA Vinatzer, Ed.)Google Scholar
  109. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J et al (2014) Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 7:539–539Google Scholar
  110. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285PubMedGoogle Scholar
  111. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, dePamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. Am J Bot 96:336–348PubMedGoogle Scholar
  112. Staton SE, Burke JM (2015) Transposome: Annotation of transposable element families from unassembled sequence reads. Bioinform,
  113. Streelman JT, Kocher TD (2002) Microsatellite variation associated with prolactin expression and growth of salt-challenged tilapia. Physiol Genomics 9:1–4PubMedGoogle Scholar
  114. Thomas CA (1971) The genetic organization of chromosomes. Annu Rev Genet 5:237–256Google Scholar
  115. Toth G (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967–981PubMedPubMedCentralGoogle Scholar
  116. Treangen TJ, Salzberg SL (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46PubMedPubMedCentralGoogle Scholar
  117. Usai G, Mascagni F, Natali L, Giordani T, Cavallini A (2017) Comparative genome-wide analysis of repetitive DNA in the genus Populus L. Tree Genet Genomes 13:96Google Scholar
  118. Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:17Google Scholar
  119. Vu GTH, Schmutzer T, Bull F, Cao HX, Fuchs J, Tran TD, Jovtchev G, Pistrick K, Stein N, Pecinka A et al (2015) Comparative genome analysis reveals divergent genome size evolution in a carnivorous plant genus. Plant Genome 8(3):1–14Google Scholar
  120. Wajid B, Serpedin E (2012) Review of general algorithmic features for genome assemblers for next generation sequencers. Genomics Proteomics Bioinform 10:58–73Google Scholar
  121. Wendel JF, Jackson SA, Meyers BC, Wing RA (2016) Evolution of plant genome architecture. Genome Biol 17:37PubMedPubMedCentralGoogle Scholar
  122. Wessler SR (2006) Transposable elements and the evolution of eukaryotic genomes. Proc Natl Acad Sci 103:17600–17601PubMedGoogle Scholar
  123. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O et al (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982PubMedGoogle Scholar
  124. Wicker T, Gundlach H, Spannagl M, Uauy C, Borrill P, Ramírez-González RH, De Oliveira R, Mayer KFX, Paux E, Choulet F (2018) Impact of transposable elements on genome structure and evolution in bread wheat. Genome Biol 19(1):103PubMedPubMedCentralGoogle Scholar
  125. Wolko B, Weeden NF (1989) Estimation of Lupinus genome polyploidy on the basis of isozymic loci number. Genet Pol 30:165–171Google Scholar
  126. Wu DD, Ruban A, Fuchs J, Macas J, Novak P, Vaio M, Zhou YH, Houben A (2019) Nondisjunction and unequal spindle organization accompany the drive of Aegilops speltoides B chromosomes. New Phytol 223:1340–1352PubMedGoogle Scholar
  127. Yaakov B, Kashkush K (2012) Mobilization of Stowaway-like MITEs in newly formed allohexaploid wheat species. Plant Mol Biol 80:419–427PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.UMR CNRS 6553 ECOBIO, Université de Rennes 1Rennes CedexFrance
  2. 2.Laboratoire de Recherche en Sciences VégétalesUniversité de Toulouse, CNRS, UPSAuzeville, Castanet-TolosanFrance
  3. 3.CIRAD (Centre de coopération Internationale en Recherche Agronomique pour le Développement)Montpellier Cedex 5France
  4. 4.Laboratory of Molecular CytogeneticsBiology Centre of the Czech Academy of Sciences, Institute of Plant Molecular BiologyCeske BudejoviceCzech Republic
  5. 5.CIRAD (Centre de coopération Internationale en Recherche Agronomique pour le Développement), UMR AGAPMontpellierFrance
  6. 6.AGAP, Univ MontpellierCIRAD, INRA, Montpellier SupAgroMontpellierFrance

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