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Tree Genetics & Genomes

, 13:96 | Cite as

Comparative genome-wide analysis of repetitive DNA in the genus Populus L.

  • Gabriele Usai
  • Flavia Mascagni
  • Lucia Natali
  • Tommaso Giordani
  • Andrea CavalliniEmail author
Original Article
Part of the following topical collections:
  1. Genome Biology

Abstract

Genome skimming was performed, using Illumina sequence reads, in order to obtain a detailed comparative picture of the repetitive component of the genome of Populus species. Read sets of seven Populus and two Salix species (as outgroups) were subjected to clustering using RepeatExplorer (Novák et al. BMC Bioinformatics 11:378 2010). The repetitive portion of the genome ranged from 33.8 in Populus nigra to 46.5% in Populus tremuloides. The large majority of repetitive sequences were long terminal repeat-retrotransposons. Gypsy elements were over-represented compared to Copia ones, with a mean ratio Gypsy to Copia of 6.7:1. Satellite DNAs showed a mean genome proportion of 2.2%. DNA transposons and ribosomal DNA showed genome proportions of 1.8 and 1.9%, respectively. The other repeat types accounted for less of 1% each. Long terminal repeat-retrotransposons were further characterized, identifying the lineage to which they belong and studying the proliferation times of each lineage in the different species. The most abundant lineage was Athila, which showed large differences among species. Concerning Copia lineages, similar transpositional profiles were observed among all the analysed species; by contrast, differences in transpositional peaks of Gypsy lineages were found. The genome proportions of repeats were compared in the seven species, and a phylogenetic tree was built, showing species separation according to the botanical section to which the species belongs, although significant differences could be found within sections, possibly related to the different geographical origin of the species. Overall, the data indicate that the repetitive component of the genome in the poplar genus is still rapidly evolving.

Keywords

Populus LTR-retrotransposons Repetitive DNA Comparative retrotransposon dynamics 

Notes

Acknowledgements

This research work was supported by the Department of Agriculture, Food and Environment, University of Pisa, Italy, project Plantomics.

Supplementary material

11295_2017_1181_MOESM1_ESM.docx (181 kb)
ESM 1 (DOCX 181 kb)

References

  1. Ammiraju JS, Zuccolo A, Yu Y, Song X, Piegu P, Chevalier F, Walling JG, Ma J, Talag J, Brar DS, San Miguel PJ, Jiang N, Jackson SA, Panaud O, Wing RA (2007) Evolutionary dynamics of an ancient retrotransposon family provides insights into evolution of genome size in the genus Oryza. Plant J 52:342–351CrossRefPubMedGoogle Scholar
  2. Azuma T, Kajita T, Yokoyama J, Ohashi H (2000) Phylogenetic relationships of Salix based on rbcL sequence data. Am J Bot 87:67–75CrossRefPubMedGoogle Scholar
  3. 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 6:776–791CrossRefPubMedPubMedCentralGoogle Scholar
  4. Barghini E, Natali L, Giordani T, Cossu RM, Scalabrin S, Cattonaro F, Šimková H, Vrána J, Doležel J, Morgante M, Cavallini A (2015a) LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome. DNA Res 22:91–100CrossRefPubMedGoogle Scholar
  5. Barghini E, Mascagni F, Natali L, Giordani T, Cavallini A (2015b) Analysis of the repetitive component and retrotransposon population in the genome of a marine angiosperm, Posidonia oceanica (L.) Delile. Mar Genomics 24:397–404CrossRefPubMedGoogle Scholar
  6. Barghini E, Mascagni F, Natali L, Giordani T, Cavallini A (2017) Identification and characterisation of short interspersed nuclear elements in the olive tree (Olea europaea L.) genome. Mol Gen Genomics 292:53–61CrossRefGoogle Scholar
  7. Bedbrook JR, Jones J, O’Dell M, Thompson RD, Flavell RB (1980) A molecular description of telomeric heterochromatin in Secale species. Cell 19:545–560CrossRefPubMedGoogle Scholar
  8. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefPubMedPubMedCentralGoogle Scholar
  9. Braatne JH, Hinckly TM, Stettler RF (1992) Influence of soil water supply on the physiological and morphological components of plant water balance in Populus trichocarpa, Populus deltoides and their F1 hybrids. Tree Physiol 11:325–340CrossRefPubMedGoogle Scholar
  10. Brayshaw TC (1965) Native poplars of southern Alberta and their hybrids. Can Forest Serv Publication 1109, Ottawa, Ontario, Canada, pp 1-40Google Scholar
  11. Buti M, Giordani T, Cattonaro F, Cossu RM, Pistelli L, Vukich M, Morgante M, Cavallini A, Natali L (2011) Temporal dynamics in the evolution of the sunflower genome as revealed by sequencing and annotation of three large genomic regions. Theor Appl Genet 123:779–791CrossRefPubMedGoogle Scholar
  12. Cavallini A, Natali L, Zuccolo A, Giordani T, Jurman I, Ferrillo V, Vitacolonna N, Sarri V, Cattonaro F, Ceccarelli M, Cionini PG, Morgante M (2010) Analysis of transposons and repeat composition of the sunflower (Helianthus annuus L.) genome. Theor Appl Genet 120:491–508CrossRefPubMedGoogle Scholar
  13. Cossu RM, Buti M, Giordani T, Natali L, Cavallini A (2012) A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Genet Genomes 8:61–75CrossRefGoogle Scholar
  14. Dodsworth S, Chase MW, Kelly LJ, Leitch IJ, Macas J, Novák P, Piednoël M, Weiss-Schneeweiss H, Leitch AR (2015) Genomic repeat abundances contain phylogenetic signal. Syst Biol 64:112–126CrossRefPubMedGoogle Scholar
  15. Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, Shoemaker RC, Ma J (2010) Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J 63:584–598CrossRefPubMedGoogle Scholar
  16. Dvořáčková M, Fojtová M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J 83:18–37CrossRefPubMedGoogle Scholar
  17. Eckenwalder JE (1982) Populus xinopia hybr. nov. (Salicaceae), a natural hybrid between the native North American P. fremontii S. Watts and the introduced Eurasian P. nigra L. Madrono 29:67–78Google Scholar
  18. Eckenwalder JE (1996) Systematics and evolution of Populus. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation, NRC Research Press, National Research Council of Canada, Ottawa, Ontario, Canada, pp 7–32Google Scholar
  19. Giordani T, Cossu RM, Mascagni F, Marroni F, Morgante M, Cavallini A, Natali L (2016) Genome-wide analysis of LTR-retrotransposon expression in leaves of Populus × canadensis water-deprived plants. Tree Genet Genomes 12:75CrossRefGoogle Scholar
  20. Gorinsek B, Gubensek F, Kordis D (2004) Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol 21:781–798CrossRefPubMedGoogle Scholar
  21. Guyot R, Darré T, Dupeyron M, de Kochko A, Hamon S, Couturon E, Crouzillat D, Rigoreau M, Rakotomalala JJ, Raharimalala NE, Doffou Akaffou S, Hamon P (2016) Partial sequencing reveals the transposable element composition of Coffea genomes and provides evidence for distinct evolutionary stories. Mol Gen Genomics 291:1979–1990CrossRefGoogle Scholar
  22. Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast trnt-trnf region and nuclear rDNA. Am J Bot 91:1398–1408CrossRefPubMedGoogle Scholar
  23. 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 16:1252–1261CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kazazian HH (2000) L1 retrotransposons shape the mammalian genome. Science 289:1152–1153CrossRefPubMedGoogle Scholar
  25. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  26. Kubis S, Schmidt T, Heslop-Harrison JS (1998) Repetitive DNA elements as a major component of plant genomes. Ann Bot 82:45–55CrossRefGoogle Scholar
  27. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532CrossRefPubMedGoogle Scholar
  28. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  29. Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol 194:629–646CrossRefPubMedGoogle Scholar
  30. Lermontova I, Sandmann M, Mascher M, Schmit AC, Chabouté ME (2015) Centromeric chromatin and its dynamics in plants. Plant J 83:4–17CrossRefPubMedGoogle Scholar
  31. Leskinen E, Alstrom-Rapaport C (1999) Molecular phylogeny of Salicaceae and closely related Flacourtiaceae: evidence from 5.8S, ITS1 and ITS2 of the rDNA. Plant Syst Evol 215:209–227CrossRefGoogle Scholar
  32. Llorens C, Futami R, Covelli L, Domínguez-Escribá L, Viu JM, Tamarit D, Aguilar-Rodríguez J, Vicente-Ripolles M, Fuster G, Bernet GP, Maumus F, Munoz-Pomer A, Sempere JM, Latorre A, Moya A (2011) The Gypsy database (GyDB) of mobile genetic elements: release 2.0. Nucl Acids Res 39:D70–D74CrossRefPubMedGoogle Scholar
  33. Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410CrossRefPubMedPubMedCentralGoogle Scholar
  34. Macas J, Neumann P, Navratilova A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterisation using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 8:427CrossRefPubMedPubMedCentralGoogle Scholar
  35. Mascagni F, Barghini E, Giordani T, Rieseberg LH, Cavallini A, Natali L (2015) Repetitive DNA and plant domestication: variation in copy number and proximity to genes of LTR-retrotransposons among wild and cultivated sunflower (Helianthus annuus) genotypes. Genome Biol Evol 7:3368–3382CrossRefPubMedPubMedCentralGoogle Scholar
  36. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucl Acids Res 41:W597–W600CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 37:997–1002CrossRefPubMedGoogle Scholar
  38. Natali L, Cossu RM, Barghini E, Giordani T, Buti M, Mascagni F, Morgante M, Gill N, Kane NC, Rieseberg L, Cavallini A (2013) The repetitive component of the sunflower genome as revealed by different procedures for assembling next generation sequencing reads. BMC Genomics 14:686CrossRefPubMedPubMedCentralGoogle Scholar
  39. Natali L, Cossu RM, Mascagni F, Giordani T, Cavallini A (2015) A survey of Gypsy and Copia LTR-retrotransposon superfamilies and lineages and their distinct dynamics in the Populus trichocarpa (L.) genome. Tree Genet Genomes 11:107CrossRefGoogle Scholar
  40. Neumann P, Požárková D, Macas J (2003) Highly abundant pea LTR-retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol 53:399–410CrossRefPubMedGoogle Scholar
  41. Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378CrossRefPubMedPubMedCentralGoogle Scholar
  42. Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) Repeat Explorer: a galaxy based web server for genome-wide characterization of eukaryotic repetitive elements from next generation sequence reads. Bioinformatics 29:792–793CrossRefPubMedGoogle Scholar
  43. Novák P, Hřibová E, Neumann P, Koblížková A, Doležel J, Macas J (2014) Genome-wide analysis of repeat diversity across the family Musaceae. PLoS One 9:e98918CrossRefPubMedPubMedCentralGoogle Scholar
  44. Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269CrossRefPubMedPubMedCentralGoogle Scholar
  45. Pinosio S, Giacomello S, Faivre-Rampant P, Taylor G, Jorge V, Le Paslier MC, Zaina G, Bastien C, Cattonaro F, Marroni F, Morgante M (2016) Characterization of the poplar pan-genome by genome-wide identification of structural variation. Mol Biol Evol 33:2706–2719CrossRefPubMedPubMedCentralGoogle Scholar
  46. Renny-Byfield S, Kovarik A, Kelly LJ, Macas J, Novak P, Chase MW, Nichols RA, Pancholi MR, Grandbastien MA, Leitch AR (2013) Diploidization and genome size change in allopolyploids is associated with differential dynamics of low- and high copy sequences. Plant J 74:829–839CrossRefPubMedGoogle Scholar
  47. San Miguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768CrossRefGoogle Scholar
  48. Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large scale organization of plant chromosomes. Trends Plant Sci 3:195–199CrossRefGoogle Scholar
  49. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nature Rev Genet 8:272–285CrossRefPubMedGoogle Scholar
  50. Smith RL, Sytsma KJ (1990) Evolution of Populus nigra (sect. Aigeiros): introgressive hybridization and the chloroplast contribution of Populus alba (sect. Populus). Am J Bot 77:1176–1187CrossRefGoogle Scholar
  51. Staton SE, Bakken BE, Blackman BK, Chapman MA, Kane NC, Tang S, Ungerer MC, Knapp SJ, Rieseberg LH, Burke JM (2012) The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements. Plant J 72:142–153CrossRefPubMedGoogle Scholar
  52. Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM (1996) Biology of Populus and its implications for management and conservation, NRC Research Press, National Research Council of Canada, Ottawa, Ontario, Canada, pp 1-539Google Scholar
  53. Straub SCK, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next generation sequencing for plant systematics. Am J Bot 99:349–364CrossRefPubMedGoogle Scholar
  54. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542CrossRefPubMedGoogle Scholar
  55. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604CrossRefPubMedGoogle Scholar
  56. Vitte C, Fustier MA, Alix K, Tenaillon MI (2014) The bright side of transposons in crop evolution. Brief Funct Genom 13:276–295CrossRefGoogle Scholar
  57. Von-Sternberg R, Shapiro JA (2005) How repeated retroelements format genome function. Cytogenet Genome Res 110:108–116CrossRefPubMedGoogle Scholar
  58. Wang ZX, Kurata N, Saji S, Katayose Y, Minobe Y (1995) A chromosome 5-specific repetitive DNA-sequence in rice (Oryza sativa L.) Theor Appl Genet 90:907–913CrossRefPubMedGoogle Scholar
  59. Wicker T, Keller B (2007) Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res 17:1072–1081CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, San Miguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nature Rev Genet 8:973–982CrossRefPubMedGoogle Scholar
  61. Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Gabriele Usai
    • 1
  • Flavia Mascagni
    • 1
  • Lucia Natali
    • 1
  • Tommaso Giordani
    • 1
  • Andrea Cavallini
    • 1
    Email author
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly

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