A whole genome analysis of long-terminal-repeat retrotransposon transcription in leaves of Populus trichocarpa L. subjected to different stresses
DOI:
https://doi.org/10.13128/cayologia-232Keywords:
LTR-retrotransposons, retrotransposon expression, retrotransposon abundance, Illumina cDNA libraries, Populus trichocarpaAbstract
Long terminal repeat retrotransposons have a main role in shaping the structure of plant genomes. We used available genomic resources to study as several factors affect the expression of long terminal repeat retrotransposons in Populus trichocarpa. Such factors included redundancy of a retrotransposon in the genome, chromosomal localization, “genotype” of the retrotransposon, and changes in the environment. Overall, we identified and annotated 828 full-length retrotransposons, and analyzed their abundance in the genome. Then, we measured their expression in leaves of plants subjected to several stresses (drought, cold, heat, and salt) as well as in control plants. Our analyses showed that the expression of retrotransposons was generally low, especially that of abundant elements. The transcription of an element was found to be only slightly dependent on its chromosomal localization, rather it depended on the superfamily and the lineage to which the retrotransposon belonged. Finally, some retrotransposons were specifically activated by different environmental stresses.
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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.
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.
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Lu X, Chen D, Shu D, Zhang Z, Wang W, Klukas C, Chen L, 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.
Ma Y, Sun HY, Zhao GL, Dai HY, Gao XY, Li H, Zhang ZH. 2008. Isolation and characterization of genomic retrotransposon sequences from octoploid strawberry (Fragaria × ananassa Duch.). Plant Cell Rep. 27:499–507.
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Mascagni F, Vangelisti A, Giordani T, Cavallini A, Natali L. 2018a. Specific LTR-retrotransposons show copy number variations between wild and cultivated sunflowers. Genes. 9:433.
Mascagni F, Usai G, Natali L, Cavallini A, Giordani T. 2018b. A comparison of methods for LTR-retrotransposon insertion time profiling in the Populus trichocarpa genome. Caryologia. 71:85-92.
Mascagni F, Vangelisti A, Usai G, Giordani T, Cavallini A, Natali L. 2019. A computational genome-wide analysis of long terminal repeats retrotransposon expression in sunflower roots (Helianthus annuus L.). Submitted.
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.
Meyers BC, Tingey SV, Morgante M. 2001. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11:1660–1676.
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nature Meth. 5:621–628.
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.
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Neumann P, Novák P, Hoštáková N, Macas J. 2019. Systematic survey of plant LTR retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob DNA. 10:1.
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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.
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. 13:96.
Vangelisti A, Mascagni F, Giordani T, Sbrana C, Turrini A, Cavallini A, Giovannetti M, Natali L. 2019. Arbuscular mycorrhizal fungi induce the expression of specific retrotransposons in roots of sunflower (Helianthus annuus L.). PLoS ONE. 14:e0212371.
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Vitte C, Fustier MA, Alix K, Tenaillon MI. 2014. The bright side of transposons in crop evolution. Briefings Funct Genom. 13:276-295.
Voronova A, Belevich V, Rungis D, Jansons A. 2014. Stress-induced transcriptional activation of retrotransposon-like sequences in the Scots pine (Pinus sylvestris L.) genome. Tree Genet Genomes. 10:937–951.
Vukich M, Giordani T, Natali L, Cavallini A. 2009. Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). BMC Plant Biol. 9:150.
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Barghini E, Natali L, Giordani T, Cossu RM, Scalabrin S, Cattonaro F, Šimková H, Vrána J, Doležel J, Morgante M, Cavallini A. 2015b. LTR retrotransposon dynamics in the evolution of the olive (Olea europaea) genome. DNA Res. 22:91-100.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statistic Soc. 57:289-300.
Bennetzen JL. 2000. Transposable elements contributions to plant gene and genome evolution. Plant Mol Biol. 42:251–269.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30:2114-2120.
Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P. 2012. Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell. 24:1242-1255.
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.
Buti M, Moretto M, Barghini E, Mascagni F, Natali L, Brilli M, Lomsadze A, Sonego P, et al. 2018. The genome sequence and transcriptome of Potentilla micrantha and their comparison to Fragaria vesca (the woodland strawberry). GigaScience. 7:1-14.
Chang W, Jääskeläinen M, Li S, Schulman AH. 2013. BARE retrotransposons are translated and replicated via distinct RNA pools. PLoS ONE. 8:e72270.
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.
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.
Ellinghaus D, Kurtz S, Willhoeft U. 2008. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. 9:18.
Falchi R, Vendramin E, Zanon L, Scalabrin S, Cipriani G, Verde I, et al. 2013. Three distinct mutational mechanisms acting on a single gene underpin the origin of yellow flesh in peach. Plant J. 76:175-187.
Fan FH, Cui BW, Zhang T, Ding GJ, Wen XP. 2014. LTR-retrotransposon activation, IRAP marker development and its potential in genetic diversity assessment of masson pine (Pinus massoniana). Tree Genet Genomes. 10:213–222.
Filichkin SA, Hamilton M, Dharmawardhana PD, Singh SK, Sullivan C, Ben-Hur A, Reddy ASN, Jaiswal P. 2018. Abiotic stresses modulate landscape of poplar transcriptome via alternative splicing, differential intron retention, and isoform ratio switching. Front Plant Sci. 9:5.
Gao X, Zhou J, Li J, Zou X, Zhao J, Li Q, et al. 2015. Efficient generation of marker-free transgenic rice plants using an improved transposon-mediated transgene reintegration strategy. Plant Physiol. 167:11-24.
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.
Grandbastien MA. 1998. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3:181–189.
Grandbastien MA. 2015. LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta. 1849:403–416.
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.
He P, Ma Y, Zhao G, Dai H, Li H, Chang L, Zhang ZH. 2010. FaRE1: a transcriptionally active Ty1-copia retrotransposon in strawberry. J Plant Res. 123:707–714.
He P, Ma Y, Dai HY, Li LG, Liu YX, Li H, Zhao GL, Zhang ZH. 2012. Characterization of the hormone and stress-induced expression of FaRE1 retrotransposon promoter in strawberry. J Plant Biol. 55:1–7.
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.
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.
Ito H. 2013. Small RNAs and regulation of transposons in plants. Genes Genet Syst. 88:3–7.
Ito H, Yoshida T, Tsukahara S, Kawabe A. 2013. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene. 518:256–261.
Kashkush K, Feldman M, Levy AA. 2003. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet. 33:102–106.
Lisch D. 2009. Epigenetic regulation of transposable elements in plants. Annu Rev Plant Biol. 60:43–66.
Lisch D. 2013. How important are transposons for plant evolution? Nat Rev Genet. 14:49-61.
Liu Z, Han PF, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak G, Hao S, Liu B. 2004. Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. Theor Appl Genet. 109:200–209.
Lu X, Chen D, Shu D, Zhang Z, Wang W, Klukas C, Chen L, 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.
Ma Y, Sun HY, Zhao GL, Dai HY, Gao XY, Li H, Zhang ZH. 2008. Isolation and characterization of genomic retrotransposon sequences from octoploid strawberry (Fragaria × ananassa Duch.). Plant Cell Rep. 27:499–507.
Mascagni F, Cavallini A, Giordani T, Natali L. 2017. Different histories of two highly variable LTR retrotransposons in sunflower species. Gene. 634:5-14.
Mascagni F, Vangelisti A, Giordani T, Cavallini A, Natali L. 2018a. Specific LTR-retrotransposons show copy number variations between wild and cultivated sunflowers. Genes. 9:433.
Mascagni F, Usai G, Natali L, Cavallini A, Giordani T. 2018b. A comparison of methods for LTR-retrotransposon insertion time profiling in the Populus trichocarpa genome. Caryologia. 71:85-92.
Mascagni F, Vangelisti A, Usai G, Giordani T, Cavallini A, Natali L. 2019. A computational genome-wide analysis of long terminal repeats retrotransposon expression in sunflower roots (Helianthus annuus L.). Submitted.
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.
Meyers BC, Tingey SV, Morgante M. 2001. Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 11:1660–1676.
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nature Meth. 5:621–628.
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.
Neumann P, Navrátilová A, Koblížková A, Kejnovský E, H?ibová E, Hobza R, Widmer A, Doležel J, Macas J. 2011. Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA. 2:4.
Neumann P, Novák P, Hoštáková N, Macas J. 2019. Systematic survey of plant LTR retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob DNA. 10:1.
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. 29:792–793.
Rico-Cabanas L, Martínez-Izquierdo JA. 2007. CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Mol Genet Genom. 277:365.
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. 1998. The paleontology of intergene retrotransposons of maize. Nat Genet. 20:43–45.
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.
Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 8:272–285.
Sonnhammer EL, Durbin R. 1995. A dot-matriprogram with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene. 167:GC1–GC10.
Springer NM, Ying K, Fu Y, Ji T, Yeh CT, Jia Y, et al. 2009. Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 5:e1000734.
Takeda S, Sugimoto K, Otsuki H, Hirochika H. 1999. A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J. 18:383–393.
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.
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. 13:96.
Vangelisti A, Mascagni F, Giordani T, Sbrana C, Turrini A, Cavallini A, Giovannetti M, Natali L. 2019. Arbuscular mycorrhizal fungi induce the expression of specific retrotransposons in roots of sunflower (Helianthus annuus L.). PLoS ONE. 14:e0212371.
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.
Vicient CM, Jaaskelainen MJ, Kalendar R, Schulman AH. 2001. Active retrotransposons are a common feature of grass genomes. Plant Physiol. 125:1283–1292.
Vitte C, Fustier MA, Alix K, Tenaillon MI. 2014. The bright side of transposons in crop evolution. Briefings Funct Genom. 13:276-295.
Voronova A, Belevich V, Rungis D, Jansons A. 2014. Stress-induced transcriptional activation of retrotransposon-like sequences in the Scots pine (Pinus sylvestris L.) genome. Tree Genet Genomes. 10:937–951.
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2020-02-21
How to Cite
Vangelisti, A., Usai, G., Mascagni, F., Natali, L., Giordani, T., & Cavallini, A. (2020). A whole genome analysis of long-terminal-repeat retrotransposon transcription in leaves of Populus trichocarpa L. subjected to different stresses. Caryologia, 72(2), 69–79. https://doi.org/10.13128/cayologia-232
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