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Genome-wide analysis of LTR-retrotransposon expression in leaves of Populus × canadensis water-deprived plants

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Abstract

Retrotransposons represent a major component of plant genomes; however, large-scale studies on their expression are rare. Massively parallel sequencing offers new analytical possibilities enabling a comprehensive study of retrotransposon RNA transcription. We evaluated the expression of long terminal repeat-retrotransposons in leaves of two sister hybrids Populus × canadensis (P. deltoides × P. nigra), subjected to moderate or severe water deprivation by mapping Illumina RNA-Seq reads onto a set of 958 unique full-length retrotransposons of P. trichocarpa. Detectable levels of transcription were ascertained for 140 retrotransposons in 1 hybrid and 182 in the other. The two hybrids showed different retrotransposon expression levels, and these differences reduced at increasing drought levels. The number of expressed Gypsy elements in control and water-deprived plants was higher than those of Copia, as were their expression levels. The two hybrids showed different retrotransposon expression patterns following water deprivation. Such variations between hybrids were related to differential expression of a few genes involved in chromatin methylation and remodeling. Overall, our data indicate that even in genetically close individuals, large differences can occur in retrotransposon expression, with possible consequences for genome differentiation.

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Abbreviations

RE:

Retrotransposon

LTR-RE:

Long terminal repeat-retrotransposon

RPKM:

Reads per kilobase per million reads mapped

References

  • Baggerly KA, Deng L, Morris JS, Aldaz CM (2003) Differential expression in SAGE: accounting for normal between-library variation. Bioinformatics 19:1477–1483

    Article  CAS  PubMed  Google Scholar 

  • Barber WT, Zhang W, Win H, Varala KK, Dorweiler JE, Hudson ME, Moose SP (2012) Repeat associated small RNAs vary among parents and following hybridization in maize. Proc Natl Acad Sci U S A 109:10444–10449

    Article  CAS  PubMed  PubMed Central  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 (2015) LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome. DNA Res 22:91–100

    Article  CAS  PubMed  Google Scholar 

  • Bennetzen JL (2000) Transposable elements contributions to plant gene and genome evolution. Plant Mol Biol 42:251–269

    Article  CAS  PubMed  Google Scholar 

  • Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buti M, Giordani T, Vukich M, Gentzbittel L, Pistelli L, Cattonaro F, Morgante M, Cavallini A, Natali L (2009) HACRE1, a recently inserted copia-like retrotransposon of sunflower (Helianthus annuus L.). Genome 52:904–911

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Buti M, Giordani T, Vukich M, Pugliesi C, Natali L, Cavallini A (2013) Retrotransposon-related genetic distance and hybrid performance in sunflower (Helianthus annuus L.). Euphytica 192:289–303

    Article  CAS  Google Scholar 

  • Chang W, Jääskeläinen M, Li S, Schulman AH (2013) BARE retrotransposons are translated and replicated via distinct RNA pools. PLoS One 8:e72270

    Article  CAS  PubMed  PubMed Central  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 

  • Cossu RM, Giordani T, Cavallini A, Natali L (2014) High-throughput analysis of transcriptome variation during water deficit in a poplar hybrid: a general overview. Tree Genet Genomes 10:53–66

    Article  Google Scholar 

  • Dieguez MJ, Vaucheret H, Paszkowski J, Mittelsten Scheid O (1998) Cytosine methylation at CG and CNG sites is not a prerequisite for the initiation of transcriptional gene silencing in plants, but it is required for its maintenance. Mol Gen Genet 259:207–215

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1989) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Feldman M, Levy AA (2012) Genome evolution due to allopolyploidization in wheat. Genetics 192:763–774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–189

    Article  Google Scholar 

  • Grandbastien MA (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta 1849:403–416

    Article  CAS  PubMed  Google Scholar 

  • Hamanishi ET, Campbell MM (2011) Genome-wide responses to drought in forest trees. Forestry 84:273–283

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirochika H (1993) Activation of tobacco retrotransposons during tissue culture. EMBO J 12:2521–2528

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A 93:7783–7788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishiguro S, Ogasawara K, Fujino K, Sato Y, Kishima Y (2014) Low temperature-responsive changes in the anther transcriptome’s repeat sequences are indicative of stress sensitivity and pollen sterility in rice strains. Plant Physiol 164:671–682

    Article  CAS  PubMed  Google Scholar 

  • Ito H (2013) Small RNAs and regulation of transposons in plants. Genes Genet Syst 88:3–7

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki M (2014) Identification of genes preventing transgenerational transmission of stress induced epigenetic states. Proc Natl Acad Sci U S A 111:8547–8552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang S, Cai D, Sun Y, Teng Y (2016) Isolation and characterization of putative functional long terminal repeat retrotransposons in the Pyrus genome. Mob DNA 7:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalendar R, Vicient CM, Peleg O, Anamthawat-Jonsson K, Bolshoy A, Schulman AH (2004) LARD retroelements: conserved, non-autonomous components of barley and related genomes. Genetics 166:1437–1450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawakami T, Morgan TJ, Nippert JB, Ochltree TW, Keith R, Dhakal P, Ungerer MC (2011) Natural selection drives clinal life history patterns in the perennial sunflower species, Helianthus maximiliani. Mol Ecol 20:2318–2328

    Article  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisch D (2009) Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol 60:43–66

    Article  CAS  PubMed  Google Scholar 

  • Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20

    Article  CAS  PubMed  Google Scholar 

  • Lu X, Chen D, Shu D, Zhang Z, Wang W, Klukas C, Chen LL, Fan Y, Chen M, Zhang C (2013) The differential transcription network between embryo and endosperm in the early developing maize seed. Plant Physiol 162:440–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Marcon HS, Domingues DS, Costa Silva J, Junqueira Borges R, Filippi Matioli F, de Mattos Fontes MR, Marino CL (2015) Transcriptionally active LTR retrotransposons in Eucalyptus genus are differentially expressed and insertionally polymorphic. BMC Plant Biol 15:198

    Article  PubMed  PubMed Central  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  CAS  PubMed  Google Scholar 

  • Meignin C, Bailly JL, Arnaud F, Dastugue B, Vaury C (2003) The 5′ untranslated region and gag product of Idefix, a long terminal repeat retrotransposon from Drosophila melanogaster, act together to initiate a switch between translated and untranslated states of the genomic mRNA. Mol Cell Biol 23:8246–8254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers BC, Tingey SV, Morgante M (2001) Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res 11:1660–1676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mirouze M, Paszkowski J (2011) ) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274

    Article  CAS  PubMed  Google Scholar 

  • Morgante M, De Paoli E, Radovic S (2007) Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 10:149–155

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5:621–628

    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 shown 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 

  • Parchman TL, Geist KS, Grahnen JA, Benkman CW, Buerkle CA (2010) Transcriptome sequencing in an ecologically important tree species: assembly, annotation, and marker discovery. BMC Genomics 11:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Pecinka A, Mittelsten Scheid O (2012) Stress-induced chromatin changes: a critical view on their heritability. Plant Cell Physiol 53:801–808

    Article  CAS  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 

  • Rai HD, Mock KE, Richardson BA, Cronn RC, Hayden KJ, Wright JW, Knaus BJ, Wolf PG (2013) Transcriptome characterization and detection of gene expression differences in aspen (Populus tremuloides). Tree Genet Genomes 9:1031–1041

    Article  Google Scholar 

  • Ramallo E, Kalendar R, Schulman AH, Martínez-Izquierdo JA (2008) Reme1, a Copia retrotransposon in melon, is transcriptionally induced by UV light. Plant Mol Biol 66:137–150

    Article  CAS  PubMed  Google Scholar 

  • Rico-Cabanas L, Martinez-Izquierdo JA (2007) CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol Gen Genomics 277:365–377

    Article  CAS  Google Scholar 

  • SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45

    Article  CAS  PubMed  Google Scholar 

  • Scherrer B, Isidore E, Klein P, Kim JS, Bellec A, Chalhoub B, Keller B, Feuillet C (2005) Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17:361–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senerchia N, Felber F, Parisod C (2015) Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation. Proc R Soc B Biol Sci 282. doi:10.1098/rspb.2014.2874

  • Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, et al. (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173:2199–2210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suoniemi A, Tanskanen J, Schulman AH (1998) Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J 13:699–705

    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, et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Ungerer MC, Strakosh SC, Stimpson KM (2009) Proliferation of Ty3/gypsy-like retrotransposons in hybrid sunflower taxa inferred from phylogenetic data. BMC Biol 7:40

    Article  PubMed  PubMed Central  Google Scholar 

  • Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313:320–324

    Article  CAS  PubMed  Google Scholar 

  • Vicient CM, Schulman AH (2002) Copia-like retrotransposons in the rice genome: few and assorted. Genome Lett 1:35–47

    Article  CAS  Google Scholar 

  • Vicient CM, Suoniemi A, Anamthawat-Jonsson 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 11:1769–1784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH (2001) Active retrotransposons are a common feature of grass genomes. Plant Physiol 125:1283–1292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992) Copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci U S A 89:7124–7128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vukich M, Giordani T, Natali L, Cavallini A (2009) Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). BMC Plant Biol 9:150

    Article  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, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982

    Article  CAS  PubMed  Google Scholar 

  • Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM (2009) Genotype and time of day shape the Populus drought response. Plant J 60:703–715

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 98:13778–13783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM, Kasschaul KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:642–652

    Article  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • 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 Gen Genomics 265:336–344

    Article  CAS  Google Scholar 

  • Zabala G, Campos E, Varala KK, Bloomfield S, Jones SI, Win H, Tuteja JH, Calla B, Clough SJ, Hudson M, Vodkin LO (2012) Divergent patterns of endogenous small RNA populations from seed and vegetative tissues of Glycine max. BMC Plant Biol 12:177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research work was 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” and, in part, by European Community’s Seventh Framework Program (FP7/2007-2013), under grant agreement number 211917 (ENERGYPOPLAR).

Thanks are due to Dr. Catherine Bastien (INRA-UAGPF, Orleans, France) for providing the hybrid plants, to Pierfrancesco Miscali (DiSAAA-a, Pisa, Italy) for technical collaboration on data handling and treatment, and to Dr. John A. Walsh (Warwick University, UK) for critical reading of the manuscript.

Data archiving statement

All LTR-RE sequences are available in the Department of Agriculture, Food, and Environment of the University of Pisa repository website (http://www.agr.unipi.it/ricerca/plant-genetics-and-genomics-lab/sequencerepository.html).

All genomic DNA and cDNA raw Illumina sequences used in this work are available at the NCBI Sequence Read Archive under the accession numbers SRP078030 (submission: Hybrid Populus deltoides × Populus nigra Raw sequence reads) and SRP024267 (submission: Populus × canadensis RNAseq).

The global analysis of LTR-RE and gene expression is available in an excel file in the Department of Agriculture, Food, and Environment of University of Pisa repository website (http://www.agr.unipi.it/Sequence-Repository.358.0.html), in which each LTR-RE and each gene were represented by its absolute expression level in control, moderately dehydrated and severely dehydrated leaves.

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Correspondence to Lucia Natali.

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Communicated by A. Brunner

Tommaso Giordani and Rosa Maria Cossu contributed equally to this work.

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Giordani, T., Cossu, R.M., Mascagni, F. et al. Genome-wide analysis of LTR-retrotransposon expression in leaves of Populus × canadensis water-deprived plants. Tree Genetics & Genomes 12, 75 (2016). https://doi.org/10.1007/s11295-016-1036-5

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