Abstract
Background
Unlike peoples’ belief that transposable elements (TEs) are “junk DNAs” or “genomic parasites”, TEs are essential genomic elements that bring about genetic diversity and enable evolution of a species. In fact, transposons are major constituent of chromosome in crop genomes, particularly in major cereal crops, the primary type of which is long terminal repeat (LTR) retrotransposon. Since TE mobilization can be controlled by specific environmental stimulation and as the result can generate novel genetic variations, it has been suggested that controlled mobilization of TEs can be a plausible method for crop breeding. To achieve this goal, series of sequencing techniques have been recently established to identify TEs that are active in mobility. These methods target and detect extrachromosomal DNAs (ecDNAs), which are final products of integration. The newly identified TEs by these methods exhibit strong transpositional activity which can generate novel genetic diversity and provide useful breeding resources.
Conclusions
In this mini review, we summarize and introduce ALE-seq, mobilome-seq, and VLP DNA-seq techniques employed to detect active TEs in plants.
Similar content being viewed by others
References
Avery DB, Usher CL, McCarroll SA, Digital PCR (2018) Analyzing copy number variation with Droplet Digital PCR. Methods Protoc 9:143–160. https://doi.org/10.1007/978-1-4939-7778-9_9
Brown PO, Bowerman B, Varmus HE, Bishop JM (1987) Correct integration of retroviral DNA in vitro. Cell 49:347–356. https://doi.org/10.1016/0092-8674(87)90287-X
Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255. https://doi.org/10.1105/tpc.111.095232
Cho J (2018) Transposon-derived non-coding RNAs and their function in plants. Front Plant Sci 9:600. https://doi.org/10.3389/fpls.2018.00600
Cho J, Benoit M, Catoni M, Drost HG, Brestovitsky A, Oosterbeek M, Paszkowski J (2019) Sensitive detection of pre-integration intermediates of long terminal repeat retrotransposons in crop plants. Nat Plants 5:26–33. https://doi.org/10.1038/s41477-018-0320-9
Deniz Ö, Frost JM, Branco MR (2019) Regulation of transposable elements by DNA modifications. Nat Rev Genet 20:417–431. https://doi.org/10.1038/s41576-019-0106-6
Fan W, Cho J (2021) Quantitative measurement of transposon copy number using the Droplet Digital PCR. In: Cho J (ed) Plant transposable elements. Springer, New York. https://doi.org/10.1007/978-1-0716-1134-0
Flavel AJ, Brierley C (1986) The termini of extrachromosomal linear copia elements. Nucleic Acids Res 14:3659–3669. https://doi.org/10.1093/nar/14.9.3659
Freeling M, Xu J, Woodhouse M, Lisch D (2015) A solution to the c-value paradox and the function of junk DNA: the genome balance hypothesis. Mol Plant 8(6):899–910. https://doi.org/10.1016/j.molp.2015.02.009
Galindo-González L, Mhiri C, Deyholos MK, Grandbastien MA (2017) LTR-retrotransposons in plants: engines of evolution. Gene 626:14–25. https://doi.org/10.1016/j.gene.2017.04.051
Grandbastien MA (2015) LTR retrotransposons, handy hitchhikers of plant regulation and stress response. Biochim Biophys Acta 1849:403–416. https://doi.org/10.1016/j.bbagrm.2014.07.017
Greenblatt IM, Brink RA (1963) Transpositions of modulator in maize into divided and undivided chromosome segments. Nature 197:412–413. https://doi.org/10.1038/197412a0
Griffiths J, Catoni M, Iwasaki M, Paszkowski J (2018) Sequence-independent identification of active LTR retrotransposons in Arabidopsis. Mol Plant 11:508–511. https://doi.org/10.1016/j.molp.2017.10.012
Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119. https://doi.org/10.1038/nature09861
Kobayashi S, Goto-Yamamoto N, Hirochika H (2004) Retrotransposon-induced mutations in grape skin color. Science 304:982. https://doi.org/10.1126/science.1095011
Lanciano S, Carpentier MC, Llauro C, Jobet E, Robakowska-Hyzorek D, Lasserre E, Ghesquière A, Panaud O, Mirouze M (2017) Sequencing the extrachromosomal circular mobilome reveals retrotransposon activity in plants. PloS Genet 13:e1006630. https://doi.org/10.1371/journal.pgen.1006630
Lee SC, Ernst E, Berube B, Borges F, Parent JS, Ledon P, Schorn A, Martienssen RA (2020) Arabidopsis retrotransposon virus-like particles and their regulation by epigenetically activated small RNA. Genome Res 30:576–588. https://doi.org/10.1101/gr.259044.119
Lisch D (2013) How important are transposons for plant evolution? Nat Rev Genet 14:49–61. https://doi.org/10.1038/nrg3374
Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605. https://doi.org/10.1016/0092-8674(93)90078-5
Lynch VJ, Leclerc RD, May G, Wagner GP (2011) Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat Genet 43:1154–1159. https://doi.org/10.1038/ng.917
Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:1135–1138. https://doi.org/10.1038/nature08498
Panda K, Slotkin RK (2020) Long-read cDNA sequencing enables a “gene-like” transcript annotation of transposable elements. Plant Cell 32:2687–2698. https://doi.org/10.1105/TPC.20.00115
Paszkowski J (2015) Controlled activation of retrotransposition for plant breeding. Curr Opin Biotechnol. https://doi.org/10.1016/j.copbio.2015.01.003
Rebollo R, Romanish MT, Mager DL (2012) Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet 46:21–42. https://doi.org/10.1146/annurev-genet-110711-155621
Rey O, Danchin E, Mirouze M, Loot C, Blanchet S (2016) Adaptation to global change: a transposable element-epigenetics perspective. Trends Ecol Evol 31:514–526. https://doi.org/10.1016/j.tree.2016.03.013
Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29:987–994. https://doi.org/10.1016/0092-8674(82)90462-7
Sabot F, Schulman A (2006) Parasitism and the retrotransposon life cycle in plants: a hitchhiker’s guide to the genome. Heredity 97:381–388. https://doi.org/10.1038/sj.hdy.6800903
Shahid S, Slotkin RK (2020) The current revolution in transposable element biology enabled by long reads. Curr Opin Plant Biol 54:49–56. https://doi.org/10.1016/j.pbi.2019.12.012
Thomas J, Pritham E (2015) Helitrons, the eukaryotic rolling-circle transposable elements. In: Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (eds) Mobile DNA III. ASM Press, Washington, DC, pp 893–926. https://doi.org/10.1128/microbiolspec.MDNA3-0049-2014
Thieme M, Lanciano S, Balzergue S, Daccord N, Mirouze M, Bucher E (2017) Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding. Genome Biol 18:134. https://doi.org/10.1186/s13059-017-1265-4
Thieme M, Bucher E (2018) Transposable elements as tool for crop improvement. Adv Bot Res 88:165–202. https://doi.org/10.1016/bs.abr.2018.09.001
Wang B, Tseng E, Regulski M, Clark TA, Hon T, Jiao Y, Lu Z, Olson A, Stein JC, Ware D (2016) Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing. Nat Commun 7:11708. https://doi.org/10.1038/ncomms11708
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. https://doi.org/10.1038/nrg2165
Yao JL, Dong YH, Morris BAM (2001) Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc Natl Acad Sci 98:1306–1311. https://doi.org/10.1073/pnas.98.3.1306
Zhang L, Hu J, Han X, Li J, Gao Y, Richards CM, Zhang C, Tian Y, Liu G, Gul H et al (2019) A high-quality apple genome assembly reveals the association of a retrotransposon and red fruit colour. Nat Commun 10:1494. https://doi.org/10.1038/s41467-019-09518-x
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (31970518) and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27030209).
Funding
This work was supported by grants from the National Natural Science Foundation of China (31970518) and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27030209).
Author information
Authors and Affiliations
Contributions
Conceptualization: JC; Literature search: VS, WF, JC, JC; Writing—figure composition: VS, WF, JC; Writing—original draft: VS, WF; Writing—review and editing: JC; Funding acquisition: JC; Supervision: JC.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Satheesh, V., Fan, W., Chu, J. et al. Recent advancement of NGS technologies to detect active transposable elements in plants. Genes Genom 43, 289–294 (2021). https://doi.org/10.1007/s13258-021-01040-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-021-01040-z