Abstract
Retrotransposons are an ubiquitous component of plant genomes, especially abundant in species with large genomes. Populus trichocarpa has a relatively small genome, which was entirely sequenced; however, studies focused on poplar retrotransposons dynamics are rare. With the aim to study the retrotransposon component of the poplar genome, we have scanned the complete genome sequence searching full-length long-terminal repeat (LTR) retrotransposons, i.e., characterised by two long terminal repeats at the 5′ and 3′ ends. A computational approach based on detection of conserved structural features, on building multiple alignments, and on similarity searches was used to identify 1,479 putative full-length LTR retrotransposons. Ty1-copia elements were more numerous than Ty3-gypsy. However, many LTR retroelements were not assigned to any superfamily because lacking of diagnostic features and non-autonomous. LTR retrotransposon remnants were by far more numerous than full-length elements, indicating that during the evolution of poplar, large amplification of these elements was followed by DNA loss. Within superfamilies, Ty3-gypsy families are made of more members than Ty1-copia ones. Retrotransposition occurred with increasing frequency following the separation of Populus sections, with different waves of retrotransposition activity between Ty3-gypsy and Ty1-copia elements. Recently inserted elements appear more frequently expressed than older ones. Finally, different levels of activity of retrotransposons were observed according to their position and their density in the linkage groups. On the whole, the results support the view of retrotransposons as a community of different organisms in the genome, whose activity (both retrotransposition and DNA loss) has heavily impacted and probably continues to impact poplar genome structure and size.
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Abbreviations
- RE:
-
Retrotransposon
- LTR RE:
-
LTR retrotransposon
- LTR:
-
Long terminal repeat
- MY:
-
Million of years
- MYA:
-
Million years ago
References
Ammiraju JS, Zuccolo A, Yu Y, Song X, Piegu P, Chevalier F, Walling JG, Ma J, Talag J, Brar DS, SanMiguel 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
Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, Westerman RP, SanMiguel PJ, Bennetzen JL (2009a) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732. doi:10.1371/journal.pgen.1000732
Baucom RS, Estill JC, Leebens-Mack J, Bennetzen JL (2009b) Natural selection on gene function drives the evolution of LTR retrotransposon families in the rice genome. Genome Res 19:243–254
Beguiristain T, Grandbastien MA, Puigdomenech P, Casacuberta JM (2001) Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. Plant Physiol 127:212–221
Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132
Benson G (1999) Tandem Repeat Finder: a program to analyze DNA sequences. Nucl Acids Res 27:573–580
Boeke JD, Corces VG (1989) Transcription and reverse transcription of retrotransposons. Ann Rev Microbiol 43:403–434
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
Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A, Segurens B, Carter M, Huteau V, Coriton O, Appels R, Samain S, Chalhoub B (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics 180:1071–1086
Devos KM, Brown JKM, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079
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, pp 7–32
Gaut BS (1998) Molecular clocks and nucleotide substitution rates in higher plants. In: Hecht MK, Macintyre RJ, Clegg MT (eds) Evolutionary Biology, vol 30. Plenum, New York, pp 93–120
Grover C, Hawkins J, Wendel J (2008) Phylogenetic insights into the paceand pattern of plant genome size evolution. In: Volff JN (ed) Plant genomes. Genome dynamics, vol 4. Karger, Basel, pp 57–68
Hawkins JS, Kim HR, 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
Hawkins JS, Hu G, Rapp RA, Grafenberg JL, Wendel JF (2008) Phylogenetic determination of the pace of transposable element proliferation in plants: Copia and LINE-like elements in Gossypium. Genome 51:11–18
Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877
Islam-Faridi MN, Nelson CD, DiFazio SP, Gunter LE, Tuskan GA (2009) Cytogenetic analysis of Populus trichocarpa—ribosomal DNA, telomere repeat sequence, and marker-selected BACs. Cytogenet Genome Res 125:74–80
Jiang N, Jordan IK, Wessler SR (2002) Dasheng and RIRE2. A nonautonomous long terminal repeat element and its putative autonomous partner in the rice genome. Plant Physiol 130:1697–1705
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467
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 USA 97:6603–6607
Kalendar R, Vicient CM, Peleg O, Anamthawat-Jonsson K, Bolshoyb A, Schulman AH (2004) Large retrotransposon derivatives: abundant, conserved but nonautonomous retroelements of barley and related genomes. Genetics 166:1437–1450
Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106
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
Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10:620
Kumar A, Bennetzen J (1999) Plant retrotransposons. Annu Rev Genet 33:479–532
Le Rouzic A, Dupas S, Capy P (2007) Genome ecosystem and transposable elements species. Gene 390:214–220
Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66
Ma J, Bennetzen JL (2004) Rapid recent growth and divergence of rice nuclear genomes. Proc Natl Acad Sci USA 101:12404–12410
Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869
Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, Natali L (2009) Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol 166:1544–1556
Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676
Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Albert H, Suzuki JY, Tripathi S, Moore PH, Gonsalves D (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452:991–997
Moisy C, Garrison KE, Meredith CP, Pelsy F (2008) Characterization of ten novel Ty1/Copia-like retrotransposon families of the grapevine genome. BMC Genomics 9:469
Morse AM, Peterson DG, Islam-Faridi MN, Smith KE, Magbanua Z, Garcia SA, Kubisiak TL, Amerson HV, Carlson JE, Nelson CD, Davis JM (2009) Evolution of genome size and complexity in Pinus. PLoS One 4:e4332
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Neumann P, Koblizkova A, Navratilova A, Macas J (2006) Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics 173:1047–1056
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev I, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Rahman M, Ware D, Westhoff P, Mayer KFX, Messing M, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556
Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C (2006) Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48:463–474
Rajagopal J, Das S, Khurana DK, Srivastava PS, Lakshmikumaran M (1999) Molecular characterization and distribution of a 145-bp tandem repeat family in the genus Populus. Genome 42:909–918
Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D, Ritland CE, Benoit F, Rigby T, Nantel A, Butterfield YSN, Kirkpatrick R, Chun E, Liu J, Palmquist D, Wynhoven B, Stott J, Yang G, Barber S, Holt RA, Siddiqui A, Jones SJM, Marra MA, Ellis BE, Douglas CJ, Ritland K, Bohlmann J (2006) Genomics of hybrid poplar (Populus trichocarpa × deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15:1275–1297
Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175
Sabot F, Schulman AH (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity 97:381–388
SanMiguel P, Tikhonov A, Springer PS, Edwards KJ, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nature Genet 20:43–45
Santini S, Cavallini A, Natali L, Minelli S, Maggini F, Cionini PG (2002) Ty1/Copia- and Ty3/Gypsy-like DNA sequences in Helianthus species. Chromosoma 111:192–200
Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, Chen W, Yan L, Higginbotham J, Cardenas M, Waligorski J, Applebaum E, Phelps L, Falcone J, Kanchi K, Thane T, Scimone A, Thane N, Henke J, Wang T, Ruppert J, Shah N, Rotter K, Hodges J, Ingenthron E, Cordes M et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115. doi:1126/science.1178534
Seberg O, Petersen G (2009) A unified classification system for eukaryotic transposable elements should reflect their phylogeny. Nature Rev Genet 10:276
Sterck L, Rombauts S, Jansson S, Sterky F, Rouzé P, Van de Peer Y (2005) EST data suggest that poplar is an ancient polyploid. New Phytol 167:165–170
Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlen M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951–13956
Sugimoto K, Takeda S, Hirochika H (2000) MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon tto1 and defense-related genes. Plant Cell 12:2511–2528
The French-Italian Public Consortium for Grape Genome Characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467
The International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Thompson JD, Desmond G, Gibson H, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Tian Z, Rizzon C, Du JC, Zhu L, Bennetzen JL, Jackson SA, Gaut BS, Ma J (2009) Do genetic recombination and gene density shape the pattern of DNA elimination in rice long terminal repeat retrotransposons? Genome Res 19:2221–2230
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
Venner S, Feschotte C, Biemont C (2009) Dynamics of transposable elements: towards a community ecology of the genome. Trends Genet 25:317–323
Vicient CM, Kalendar R, Schulman AH (2005) Variability, recombination, and mosaic evolution of the barley BARE-1 retrotransposon. J Mol Evol 61:275–291
Vitte C, Bennetzen JL (2006) Analysis of retrotransposon structural diversity uncovers properties and propensities in angiosperm genome evolution. Proc Natl Acad Sci USA 103:17638–17643
Wawrzynski A, Ashfield T, Chen NWG, Mammadov J, Nguyen A, Podicheti R, Cannon SB, Thareau V, Ameline-Torregrosa C, Cannon E, Chacko B, Couloux A, Dalwani A, Denny R, Deshpande S, Egan AN, Glover N, Howell S, Ilut D, Lai H, Martin del Campo S, Metcalf M, O’Bleness M, Pfeil BE, Ratnaparkhe MB, Samain S, Sanders I, Ségurens B, Sévignac M, Sherman-Broyles S, Tucker DM, Yi J, Doyle JJ, Geffroy V, Roe BA, Saghai Maroof MA, Young NA, Innes RW (2008) Replication of nonautonomous retroelements in soybean appears to be both recent and common. Plant Physiol 148:1760–1771
Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nature Rev Genet 8:973–982
Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13778–13783
Xu Z, Wang H (2007) LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucl Acids Res 35:W265–W268
Yamazaki M, Tsugawa H, Miyao A, Yano M, Wu J, Yamamoto S, Matsumoto T, Sasaki T, Hirochika H (2001) The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol Genet Genomics 265:336–344
Zhou F, Xu Y (2009) RepPop: a database for repetitive elements in Populus trichocarpa. BMC Genomics 10:14
Zuccolo A, Sebastian A, Yu Y, Jackson S, Rounsley S, Billheimer D, Wing RA (2010) Assessing the extent of substitution rate variation of retrotransposon long terminal repeat sequences in Oryza sativa and Oryza glaberrima. Rice 3:242–250
Acknowledgments
This research work supported by PRIN-MIUR, Italy, Project “Verso la delucidazione delle basi molecolari dell’eterosi nelle piante coltivate: variazione cis-regolatoria ed espressione genica in ibridi di pioppo.” Thanks are due to Dr. Andrea Zuccolo (Arizona Genomics Institute, USA) and Dr. John A. Walsh (Warwick University, UK) for their critical reading of the manuscript.
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Cossu, R.M., Buti, M., Giordani, T. et al. A computational study of the dynamics of LTR retrotransposons in the Populus trichocarpa genome. Tree Genetics & Genomes 8, 61–75 (2012). https://doi.org/10.1007/s11295-011-0421-3
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DOI: https://doi.org/10.1007/s11295-011-0421-3