Transcriptional activity of transposable elements along an elevational gradient in Arabidopsis arenosa

. 2021 Feb 27 ; 12 (1) : 7. [epub] 20210227

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33639991

Grantová podpora
17-20357Y Grantová Agentura České Republiky
262033 Norwegian Research Council

Odkazy

PubMed 33639991
PubMed Central PMC7916287
DOI 10.1186/s13100-021-00236-0
PII: 10.1186/s13100-021-00236-0
Knihovny.cz E-zdroje

BACKGROUND: Plant genomes can respond rapidly to environmental changes and transposable elements (TEs) arise as important drivers contributing to genome dynamics. Although some elements were reported to be induced by various abiotic or biotic factors, there is a lack of general understanding on how environment influences the activity and diversity of TEs. Here, we combined common garden experiment with short-read sequencing to investigate genomic abundance and expression of 2245 consensus TE sequences (containing retrotransposons and DNA transposons) in an alpine environment in Arabidopsis arenosa. To disentangle general trends from local differentiation, we leveraged four foothill-alpine population pairs from different mountain regions. Seeds of each of the eight populations were raised under four treatments that differed in temperature and irradiance, two factors varying with elevation. RNA-seq analysis was performed on leaves of young plants to test for the effect of elevation and subsequently of temperature and irradiance on expression of TE sequences. RESULTS: Genomic abundance of the 2245 consensus TE sequences varied greatly between the mountain regions in line with neutral divergence among the regions, representing distinct genetic lineages of A. arenosa. Accounting for intraspecific variation in abundance, we found consistent transcriptomic response for some TE sequences across the different pairs of foothill-alpine populations suggesting parallelism in TE expression. In particular expression of retrotransposon LTR Copia (e.g. Ivana and Ale clades) and LTR Gypsy (e.g. Athila and CRM clades) but also non-LTR LINE or DNA transposon TIR MuDR consistently varied with elevation of origin. TE sequences responding specifically to temperature and irradiance belonged to the same classes as well as additional TE clades containing potentially stress-responsive elements (e.g. LTR Copia Sire and Tar, LTR Gypsy Reina). CONCLUSIONS: Our study demonstrated that the A. arenosa genome harbours a considerable diversity of TE sequences whose abundance and expression response varies across its native range. Some TE clades may contain transcriptionally active elements responding to a natural environmental gradient. This may further contribute to genetic variation between populations and may ultimately provide new regulatory mechanisms to face environmental challenges.

Zobrazit více v PubMed

McClintock B. The significance of responses of the genome to challenge. Science. 1984;226:792–801. doi: 10.1126/science.15739260. PubMed DOI

Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH. Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. PNAS. 2000;97:6603–6607. doi: 10.1073/pnas.110587497. PubMed DOI PMC

Bui QT, Grandbastien M-A. LTR retrotransposons as controlling elements of genome response to stress? Plant transposable elements. Springer. 2012. pp. 273–296.

Bennetzen JL. Transposable element contributions to plant gene and genome evolution. Plant Mol Biol. 2000;42:251–269. doi: 10.1023/A:1006344508454. PubMed DOI

Kidwell MG, Lisch D. Transposable elements as sources of variation in animals and plants. PNAS. 1997;94:7704–7711. doi: 10.1073/pnas.94.15.7704. PubMed DOI PMC

Feschotte C, Jiang N, Wessler SR. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002;3:329–341. doi: 10.1038/nrg793. PubMed DOI

Blot M. Transposable elements and adaptation of host bacteria. Genetica. 1994;93:5–12. doi: 10.1007/BF01435235. PubMed DOI

Orgel LE, Crick FHC. Selfish DNA: the ultimate parasite. Nature. 1980;284:604–607. doi: 10.1038/284604a0. PubMed DOI

Capy P, Gasperi G, Biémont C, Bazin C. Stress and transposable elements: co-evolution or useful parasites? Heredity. 2000;85:101–106. doi: 10.1046/j.1365-2540.2000.00751.x. PubMed DOI

Grandbastien M-A. Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 1998;3:181–187. doi: 10.1016/S1360-1385(98)01232-1. DOI

Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973–982. doi: 10.1038/nrg2165. PubMed DOI

Picault N, Chaparro C, Piegu B, Stenger W, Formey D, Llauro C, et al. Identification of an active LTR retrotransposon in rice. Plant J. 2009;58:754–765. doi: 10.1111/j.1365-313X.2009.03813.x. PubMed DOI

Vicient CM. Transcriptional activity of transposable elements in maize. BMC Genomics. 2010;11:601. doi: 10.1186/1471-2164-11-601. PubMed DOI PMC

Negi P, Rai AN, Suprasanna P. Moving through the stressed genome: emerging regulatory roles for transposons in plant stress response. Front Plant Sci. 2016;7:1448. PubMed PMC

Grandbastien M-A, Audeon C, Bonnivard E, Casacuberta J, Chalhoub B, Costa A-P, et al. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenetic and genome research. Karger Publishers. 2005;110:229–241. PubMed

Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature. 2011;472:115–119. doi: 10.1038/nature09861. PubMed DOI

Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H, et al. Mobilization of a transposon in the rice genome. Nature. 2003;421:170–172. doi: 10.1038/nature01219. PubMed DOI

Uchiyama T, Saito Y, Kuwabara H, Fujino K, Kishima Y, Martin C, et al. Multiple regulatory mechanisms influence the activity of the transposon, Tam3, of Antirrhinum. New Phytol. 2008;179:343–355. doi: 10.1111/j.1469-8137.2008.02477.x. PubMed DOI

Domb K, Keidar D, Yaakov B, Khasdan V, Kashkush K. Transposable elements generate population-specific insertional patterns and allelic variation in genes of wild emmer wheat (Triticum turgidum ssp. dicoccoides) BMC Plant Biol. 2017;17:175. doi: 10.1186/s12870-017-1134-z. PubMed DOI PMC

Stuart T, Eichten SR, Cahn J, Karpievitch YV, Borevitz JO, Lister R. Population scale mapping of transposable element diversity reveals links to gene regulation and epigenomic variation. elife. 2016;5:e20777. doi: 10.7554/eLife.20777. PubMed DOI PMC

Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. The Arabidopsis thaliana mobilome and its impact at the species level. Zilberman D, editor. eLife. 2016;5:e15716. PubMed PMC

Pietzenuk B, Markus C, Gaubert H, Bagwan N, Merotto A, Bucher E, et al. Recurrent evolution of heat-responsiveness in Brassicaceae COPIA elements. Genome Biol. 2016;17:209. doi: 10.1186/s13059-016-1072-3. PubMed DOI PMC

Marcon HS, Domingues DS, Silva JC, Borges RJ, Matioli FF, de Mattos Fontes MR, et al. Transcriptionally active LTR retrotransposons in Eucalyptus genus are differentially expressed and insertionally polymorphic. BMC Plant Biol. 2015;15:198. doi: 10.1186/s12870-015-0550-1. PubMed DOI PMC

Giordani T, Cossu RM, Mascagni F, Marroni F, Morgante M, Cavallini A, et al. Genome-wide analysis of LTR-retrotransposon expression in leaves of Populus × canadensis water-deprived plants. Tree Genet Genomes. 2016;12:75. doi: 10.1007/s11295-016-1036-5. DOI

Voytas DF, Cummings MP, Koniczny A, Ausubel FM, Rodermel SR. Copia-like retrotransposons are ubiquitous among plants. PNAS. 1992;89:7124–7128. doi: 10.1073/pnas.89.15.7124. PubMed DOI PMC

Suoniemi A, Tanskanen J, Schulman AH. Gypsy-like retrotransposons are widespread in the plant kingdom. Plant J. 1998;13:699–705. doi: 10.1046/j.1365-313X.1998.00071.x. PubMed DOI

Kumar A, Bennetzen JL. Plant retrotransposons. Annu Rev Genet. 1999;33:479–532. doi: 10.1146/annurev.genet.33.1.479. PubMed DOI

Monnahan P, Kolář F, Baduel P, Sailer C, Koch J, Horvath R, et al. Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa. Nat Ecol Evol. 2019;3:457. doi: 10.1038/s41559-019-0807-4. PubMed DOI

Baduel P, Quadrana L, Hunter B, Bomblies K, Colot V. Relaxed purifying selection in autopolyploids drives transposable element over-accumulation which provides variants for local adaptation. Nat Commun. 2019;10:5818. doi: 10.1038/s41467-019-13730-0. PubMed DOI PMC

Knotek A, Konečná V, Wos G, Požárová D, Šrámková G, Bohutínská M, et al. Parallel alpine differentiation in Arabidopsis arenosa. Front Plant Sci. 2020;11:561526. doi: 10.3389/fpls.2020.561526. PubMed DOI PMC

Lanciano S, Cristofari G. Measuring and interpreting transposable element expression. Nat Rev Genet. 2020;21:721–736. doi: 10.1038/s41576-020-0251-y. PubMed DOI

Kumar A. The adventures of the Ty1-Copia group of retrotransposons in plants. Trends Genet. 1996;12:41–43. doi: 10.1016/0168-9525(96)81393-X. PubMed DOI

Legrand S, Caron T, Maumus F, Schvartzman S, Quadrana L, Durand E, et al. Differential retention of transposable element-derived sequences in outcrossing Arabidopsis genomes. Mob DNA. 2019;10:30. doi: 10.1186/s13100-019-0171-6. PubMed DOI PMC

Paz RC, Kozaczek ME, Rosli HG, Andino NP, Sanchez-Puerta MV. Diversity, distribution and dynamics of full-length Copia and Gypsy LTR retroelements in Solanum lycopersicum. Genetica. 2017;145:417–430. doi: 10.1007/s10709-017-9977-7. PubMed DOI

Underwood CJ, Henderson IR, Martienssen RA. Genetic and epigenetic variation of transposable elements in Arabidopsis. Curr Opin Plant Biol. 2017;36:135–141. doi: 10.1016/j.pbi.2017.03.002. PubMed DOI PMC

Presting GG, Malysheva L, Fuchs J, Schubert I. A TY3/GYPSY retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J. 1998;16:721–728. doi: 10.1046/j.1365-313x.1998.00341.x. PubMed DOI

Cavrak VV, Lettner N, Jamge S, Kosarewicz A, Bayer LM, Scheid OM. How a Retrotransposon exploits the Plant’s heat stress response for its activation. PLoS Genet. 2014;10:e1004115. doi: 10.1371/journal.pgen.1004115. PubMed DOI PMC

Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Scheid OM. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell. 2010;22:3118–3129. doi: 10.1105/tpc.110.078493. PubMed DOI PMC

Ivancevic AM, Kortschak RD, Bertozzi T, Adelson DL, LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life. Genome Biol Evol. 2016;8(11):3301–22. PubMed PMC

Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, et al. Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet. 2015;11:e1004915. doi: 10.1371/journal.pgen.1004915. PubMed DOI PMC

Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S-Y, Sarpan N, et al. Loss of karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature. 2015;525:533–537. doi: 10.1038/nature15365. PubMed DOI PMC

Joly-Lopez Z, Bureau TE. Diversity and evolution of transposable elements in Arabidopsis. Chromosom Res. 2014;22:203–216. doi: 10.1007/s10577-014-9418-8. PubMed DOI

Qüesta JI, Walbot V, Casati P. Mutator transposon activation after UV-B involves chromatin remodeling. Epigenetics. 2010;5:352–363. doi: 10.4161/epi.5.4.11751. PubMed DOI PMC

Yang L, Bennetzen JL. Distribution, diversity, evolution, and survival of Helitrons in the maize genome. Proceedings of the National Academy of Sciences. Natl Acad Sci. 2009;106:19922–19927. doi: 10.1073/pnas.0908008106. PubMed DOI PMC

Barbaglia AM, Klusman KM, Higgins J, Shaw JR, Hannah LC, Lal SK. Gene capture by Helitron transposons reshuffles the transcriptome of maize. Genetics. 2012;190:965–975. doi: 10.1534/genetics.111.136176. PubMed DOI PMC

Jameson N, Georgelis N, Fouladbash E, Martens S, Hannah LC, Lal S. Helitron mediated amplification of cytochrome P450 monooxygenase gene in maize. Plant Mol Biol. 2008;67:295–304. doi: 10.1007/s11103-008-9318-4. PubMed DOI

Zhang J, Gao F, Jia H, Hu J, Feng Z. Molecular response of poplar to single and combined ozone and drought. Sci Total Environ. 2019;655:1364–1375. doi: 10.1016/j.scitotenv.2018.11.195. PubMed DOI

Kolář F, Lučanová M, Záveská E, Fuxová G, Mandáková T, Španiel S, et al. Ecological segregation does not drive the intricate parapatric distribution of diploid and tetraploid cytotypes of the Arabidopsis arenosa group (Brassicaceae) Biol J Linn Soc. 2016;119:673–688. doi: 10.1111/bij.12479. DOI

Wos G, Mořkovská J, Bohutínská M, Šrámková G, Knotek A, Lučanová M, et al. Role of ploidy in colonization of alpine habitats in natural populations of Arabidopsis arenosa. Ann Bot. 2019;124:255–268. doi: 10.1093/aob/mcz070. PubMed DOI PMC

Quesneville H. Transposable element annotation of Arabidopsis lyrata subsp. lyrata [Internet]. Portail Data INRAE. 2018; [cited 2020 Oct 19]. Available from: https://data.inrae.fr/dataset.xhtml?persistentId=doi:10.15454/INYUVZ. DOI

Yant L, Hollister JD, Wright KM, Arnold BJ, Higgins JD, Franklin FCH, et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr Biol. 2013;23:2151–2156. doi: 10.1016/j.cub.2013.08.059. PubMed DOI PMC

Amselem J, Cornut G, Choisne N, Alaux M, Alfama-Depauw F, Jamilloux V, et al. RepetDB: a unified resource for transposable element references. Mob DNA. 2019;10:6. doi: 10.1186/s13100-019-0150-y. PubMed DOI PMC

Novak P, Neumann P, Pech J, Steinhaisl J, Macas J. RepeatExplorer: a galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics. 2013;29:792–793. doi: 10.1093/bioinformatics/btt054. PubMed DOI

Neumann P, Novák P, Hoštáková N, Macas J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob DNA. 2019;10:1. doi: 10.1186/s13100-018-0144-1. PubMed DOI PMC

Du J, Tian Z, Hans CS, Laten HM, Cannon SB, Jackson SA, et al. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. Plant J. 2010;63:584–598. doi: 10.1111/j.1365-313X.2010.04263.x. PubMed DOI

Choudhury RR, Neuhaus J, Parisod C. Resolving fine-grained dynamics of retrotransposons: comparative analysis of inferential methods and genomic resources. Plant J. 2017;90:979–993. doi: 10.1111/tpj.13524. PubMed DOI

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907–915. doi: 10.1038/s41587-019-0201-4. PubMed DOI PMC

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013;30:923–930. doi: 10.1093/bioinformatics/btt656. PubMed DOI

Bertel C, Buchner O, Schönswetter P, Frajman B, Neuner G. Environmentally induced and (epi-)genetically based physiological trait differentiation between Heliosperma pusillum and its polytopically evolved ecologically divergent descendent, H. veselskyi (Caryophyllaceae: Sileneae) Bot J Linn Soc. 2016;182:658–669. doi: 10.1111/boj.12467. DOI

Wos G, Bohutínská M, Nosková J, Mandáková T, Kolář F. Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa. Plant J. 2021. 10.1111/tpj.15105. PubMed

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI

Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC

RStudio Team. In: RStudio, Inc., editor. RStudio: Integrated Development for R. Boston, MA URL http://www.rstudio.com/; 2015.

Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics Oxford University Press. 2011;27:1017–1018. PubMed PMC

Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res Oxford University Press. 2016:gkw982. PubMed PMC

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara R, et al. Vegan: Community Ecology Package. R Package Version. 2.0–10. CRAN. 2013.

Wang M, Zhao Y, Zhang B. Efficient test and visualization of multi-set intersections. Sci Rep. 2015;5:16923. doi: 10.1038/srep16923. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace