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

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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.

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References

  • 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 52:342–351

    Article  CAS  PubMed  Google Scholar 

  • Azuma T, Kajita T, Yokoyama J, Ohashi H (2000) Phylogenetic relationships of Salix based on rbcL sequence data. Am J Bot 87:67–75

    Article  CAS  PubMed  Google Scholar 

  • 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 6:776–791

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 22:91–100

    Article  CAS  PubMed  Google Scholar 

  • 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 24:397–404

    Article  PubMed  Google Scholar 

  • 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 292:53–61

    Article  CAS  Google Scholar 

  • Bedbrook JR, Jones J, O’Dell M, Thompson RD, Flavell RB (1980) A molecular description of telomeric heterochromatin in Secale species. Cell 19:545–560

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:325–340

    Article  CAS  PubMed  Google Scholar 

  • Brayshaw TC (1965) Native poplars of southern Alberta and their hybrids. Can Forest Serv Publication 1109, Ottawa, Ontario, Canada, pp 1-40

  • 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 123:779–791

    Article  CAS  PubMed  Google Scholar 

  • 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 120:491–508

    Article  CAS  PubMed  Google Scholar 

  • 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 8:61–75

    Article  Google Scholar 

  • 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 64:112–126

    Article  PubMed  Google Scholar 

  • 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 63:584–598

    Article  CAS  PubMed  Google Scholar 

  • Dvořáčková M, Fojtová M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J 83:18–37

    Article  PubMed  Google Scholar 

  • 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 29:67–78

    Google Scholar 

  • 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 7–32

  • 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 12:75

    Article  Google Scholar 

  • Gorinsek B, Gubensek F, Kordis D (2004) Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol 21:781–798

    Article  CAS  PubMed  Google Scholar 

  • 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 291:1979–1990

    Article  CAS  Google Scholar 

  • Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast trnt-trnf region and nuclear rDNA. Am J Bot 91:1398–1408

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1252–1261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazazian HH (2000) L1 retrotransposons shape the mammalian genome. Science 289:1152–1153

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kubis S, Schmidt T, Heslop-Harrison JS (1998) Repetitive DNA elements as a major component of plant genomes. Ann Bot 82:45–55

    Article  CAS  Google Scholar 

  • Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33:479–532

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Leitch AR, Leitch IJ (2012) Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol 194:629–646

    Article  CAS  PubMed  Google Scholar 

  • Lermontova I, Sandmann M, Mascher M, Schmit AC, Chabouté ME (2015) Centromeric chromatin and its dynamics in plants. Plant J 83:4–17

    Article  CAS  PubMed  Google Scholar 

  • 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 215:209–227

    Article  Google Scholar 

  • 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–D74

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci U S A 101:12404–12410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:427

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:3368–3382

    Article  PubMed  PubMed Central  Google Scholar 

  • 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–W600

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 37:997–1002

    Article  CAS  PubMed  Google Scholar 

  • 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 14:686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:107

    Article  Google Scholar 

  • Neumann P, Požárková D, Macas J (2003) Highly abundant pea LTR-retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol 53:399–410

    Article  CAS  PubMed  Google Scholar 

  • Novák P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 29:792–793

    Article  PubMed  Google Scholar 

  • 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:e98918

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 16:1262–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:2706–2719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 74:829–839

    Article  CAS  PubMed  Google Scholar 

  • 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 274:765–768

    Article  CAS  Google Scholar 

  • Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large scale organization of plant chromosomes. Trends Plant Sci 3:195–199

    Article  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nature Rev Genet 8:272–285

    Article  CAS  PubMed  Google Scholar 

  • 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 77:1176–1187

    Article  Google Scholar 

  • 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 72:142–153

    Article  CAS  PubMed  Google Scholar 

  • 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 1-539

  • 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 99:349–364

    Article  CAS  PubMed  Google Scholar 

  • Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540–1542

    Article  CAS  PubMed  Google Scholar 

  • 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 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Vitte C, Fustier MA, Alix K, Tenaillon MI (2014) The bright side of transposons in crop evolution. Brief Funct Genom 13:276–295

    Article  Google Scholar 

  • Von-Sternberg R, Shapiro JA (2005) How repeated retroelements format genome function. Cytogenet Genome Res 110:108–116

    Article  CAS  PubMed  Google Scholar 

  • 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 90:907–913

    Article  CAS  PubMed  Google Scholar 

  • 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 17:1072–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Wright DA, Voytas DF (2002) Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12:122–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

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

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  1. Gabriele Usai and Flavia Mascagni contributed equally to this work.

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, I-56124, Pisa, Italy

    Gabriele Usai, Flavia Mascagni, Lucia Natali, Tommaso Giordani & Andrea Cavallini

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  1. Gabriele Usai
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  2. Flavia Mascagni
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  3. Lucia Natali
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  4. Tommaso Giordani
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Correspondence to Andrea Cavallini.

Additional information

Communicated by P. Ingvarsson

Data archiving statement

All genomic DNA raw Illumina sequences used in this work are available at the NCBI Sequence Read Archive under the accession numbers SRS1328499 (Populus deltoides), SRS1218640 (P. nigra), SRS1124263 (P. tremula), SRS1124888 (P. tremuloides), SRS1115969 (P. balsamifera), SRS829341 (P. simonii), SRS844395 (P. trichocarpa), SRS161420 (Salix purpurea), and SRS1276361 (S. suchowensis).

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Usai, G., Mascagni, F., Natali, L. et al. Comparative genome-wide analysis of repetitive DNA in the genus Populus L.. Tree Genetics & Genomes 13, 96 (2017). https://doi.org/10.1007/s11295-017-1181-5

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