Section: Genomics
Topic: Genetics/Genomics, Plant biology, Evolution

Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks

10.24072/pcjournal.68 - Peer Community Journal, Volume 2 (2022), article no. e14.

Get full text PDF Peer reviewed and recommended by PCI
article image

Transposable elements (TEs) are mobile, repetitive DNA sequences that make the largest contribution to genome bulk. They thus contribute to the so-called “dark matter of the genome”, the part of the genome in which nothing is immediately recognizable as biologically functional. We developed a new method, based on k-mers, to identify degenerate TE sequences. With this new algorithm, we detect up to 10% of the A. thaliana genome as derived from as yet unidentified TEs, bringing the proportion of the genome known to be derived from TEs up to 50%. A significant proportion of these sequences overlapped conserved non-coding sequences identified in crucifers and rosids, and transcription factor binding sites. They are overrepresented in some gene regulation networks, such as the flowering gene network, suggesting a functional role for these sequences that have been conserved for more than 100 million years, since the spread of flowering plants in the Cretaceous.

Published online:
DOI: 10.24072/pcjournal.68
Type: Research article

Baud, Agnès 1; Wan, Mariène 1; Nouaud, Danielle 2; Francillonne, Nicolas 3; Anxolabéhère, Dominique 2, 4; Quesneville, Hadi 3, 1

1 Université Paris-Saclay, INRAE, URGI, 78026, Versailles, France
2 IJM, Institut Jacques Monod, CNRS UMR 7592, Université Paris-Diderot, Paris, France
3 Université Paris-Saclay, INRAE, BioinfOmics, Plant bioinformatics facility, 78026, Versailles, France
4 Université Paris-Sorbonne, Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Baud, Agn\`es and Wan, Mari\`ene and Nouaud, Danielle and Francillonne, Nicolas and Anxolab\'eh\`ere, Dominique and Quesneville, Hadi},
     title = {Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks},
     journal = {Peer Community Journal},
     eid = {e14},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.68},
     url = {}
AU  - Baud, Agnès
AU  - Wan, Mariène
AU  - Nouaud, Danielle
AU  - Francillonne, Nicolas
AU  - Anxolabéhère, Dominique
AU  - Quesneville, Hadi
TI  - Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.68
ID  - 10_24072_pcjournal_68
ER  - 
%0 Journal Article
%A Baud, Agnès
%A Wan, Mariène
%A Nouaud, Danielle
%A Francillonne, Nicolas
%A Anxolabéhère, Dominique
%A Quesneville, Hadi
%T Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.68
%F 10_24072_pcjournal_68
Baud, Agnès; Wan, Mariène; Nouaud, Danielle; Francillonne, Nicolas; Anxolabéhère, Dominique; Quesneville, Hadi. Traces of transposable elements in genome dark matter co-opted by flowering gene regulation networks. Peer Community Journal, Volume 2 (2022), article  no. e14. doi : 10.24072/pcjournal.68.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.genomics.100004

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Ackerman, H.; Udalova, I.; Hull, J.; Kwiatkowski, D. Evolution of a Polymorphic Regulatory Element in Interferon-γ Through Transposition and Mutation, Molecular Biology and Evolution, Volume 19 (2002) no. 6, pp. 884-890 | DOI

[2] Altschul, S. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Research, Volume 25 (1997) no. 17, pp. 3389-3402 | DOI

[3] Bailey, T. L.; Boden, M.; Buske, F. A.; Frith, M.; Grant, C. E.; Clementi, L.; Ren, J.; Li, W. W.; Noble, W. S. MEME SUITE: tools for motif discovery and searching, Nucleic Acids Research, Volume 37 (2009) no. Web Server | DOI

[4] Bao, W.; Kojima, K. K.; Kohany, O. Repbase Update, a database of repetitive elements in eukaryotic genomes, Mobile DNA, Volume 6 (2015) no. 1 | DOI

[5] Barabási, A.-L.; Oltvai, Z. N. Network biology: understanding the cell's functional organization, Nature Reviews Genetics, Volume 5 (2004) no. 2, pp. 101-113 | DOI

[6] Barah, P.; B N, M. N.; Jayavelu, N. D.; Sowdhamini, R.; Shameer, K.; Bones, A. M. Transcriptional regulatory networks inArabidopsis thalianaduring single and combined stresses, Nucleic Acids Research, Volume 44 (2016) no. 7, pp. 3147-3164 | DOI

[7] Bejerano, G.; Lowe, C. B.; Ahituv, N.; King, B.; Siepel, A.; Salama, S. R.; Rubin, E. M.; James Kent, W.; Haussler, D. A distal enhancer and an ultraconserved exon are derived from a novel retroposon, Nature, Volume 441 (2006) no. 7089, pp. 87-90 | DOI

[8] Buchmann, R. C.; Asad, S.; Wolf, J. N.; Mohannath, G.; Bisaro, D. M. Geminivirus AL2 and L2 Proteins Suppress Transcriptional Gene Silencing and Cause Genome-Wide Reductions in Cytosine Methylation, Journal of Virology, Volume 83 (2009) no. 10, pp. 5005-5013 | DOI

[9] Buisine, N.; Quesneville, H.; Colot, V. Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets, Genomics, Volume 91 (2008) no. 5, pp. 467-475 | DOI

[10] Bundock, P.; Hooykaas, P. An Arabidopsis hAT-like transposase is essential for plant development, Nature, Volume 436 (2005) no. 7048, pp. 282-284 | DOI

[11] Chen, D.; Yan, W.; Fu, L.-Y.; Kaufmann, K. Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana, Nature Communications, Volume 9 (2018) no. 1 | DOI

[12] Cordaux, R.; Udit, S.; Batzer, M. A.; Feschotte, C. Birth of a chimeric primate gene by capture of the transposase gene from a mobile element, Proceedings of the National Academy of Sciences, Volume 103 (2006) no. 21, pp. 8101-8106 | DOI

[13] Davies, T. J.; Barraclough, T. G.; Chase, M. W.; Soltis, P. S.; Soltis, D. E.; Savolainen, V. Darwin's abominable mystery: Insights from a supertree of the angiosperms, Proceedings of the National Academy of Sciences, Volume 101 (2004) no. 7, pp. 1904-1909 | DOI

[14] Eddy, S. R. Accelerated Profile HMM Searches, PLoS Computational Biology, Volume 7 (2011) no. 10 | DOI

[15] Eddy, S. SQUID - library of functions for biological sequence analysis Copyright (C) 1992-2002 Washington University School of Medicine.

[16] El-Gebali, S.; Mistry, J.; Bateman, A.; Eddy, S. R.; Luciani, A.; Potter, S. C.; Qureshi, M.; Richardson, L. J.; Salazar, G. A.; Smart, A.; Sonnhammer, E. L. L.; Hirsh, L.; Paladin, L.; Piovesan, D.; Tosatto, S. C. E.; Finn, R. D. The Pfam protein families database in 2019, Nucleic Acids Research, Volume 47 (2018) no. D1 | DOI

[17] Feschotte, C.; Jiang, N.; Wessler, S. R. Plant transposable elements: where genetics meets genomics, Nature Reviews Genetics, Volume 3 (2002) no. 5, pp. 329-341 | DOI

[18] Flutre, T.; Duprat, E.; Feuillet, C.; Quesneville, H. Considering Transposable Element Diversification in De Novo Annotation Approaches, PLoS ONE, Volume 6 (2011) no. 1 | DOI

[19] Grandbastien, M.-A.; Audeon, C.; Bonnivard, E.; Casacuberta, J.; Chalhoub, B.; Costa, A.-P.; Le, Q.; Melayah, D.; Petit, M.; Poncet, C.; Tam, S.; van Sluys, M.-A.; Mhiri, C. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae, Cytogenetic and Genome Research, Volume 110 (2005) no. 1-4, pp. 229-241 | DOI

[20] Haudry, A.; Platts, A. E.; Vello, E.; Hoen, D. R.; Leclercq, M.; Williamson, R. J.; Forczek, E.; Joly-Lopez, Z.; Steffen, J. G.; Hazzouri, K. M.; Dewar, K.; Stinchcombe, J. R.; Schoen, D. J.; Wang, X.; Schmutz, J.; Town, C. D.; Edger, P. P.; Pires, J. C.; Schumaker, K. S.; Jarvis, D. E.; Mandáková, T.; Lysak, M. A.; van den Bergh, E.; Schranz, M. E.; Harrison, P. M.; Moses, A. M.; Bureau, T. E.; Wright, S. I.; Blanchette, M. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions, Nature Genetics, Volume 45 (2013) no. 8, pp. 891-898 | DOI

[21] Heyndrickx, K. S.; de Velde, J. V.; Wang, C.; Weigel, D.; Vandepoele, K. A Functional and Evolutionary Perspective on Transcription Factor Binding in Arabidopsis thaliana, The Plant Cell, Volume 26 (2014) no. 10, pp. 3894-3910 | DOI

[22] Hoede, C.; Arnoux, S.; Moisset, M.; Chaumier, T.; Inizan, O.; Jamilloux, V.; Quesneville, H. PASTEC: An Automatic Transposable Element Classification Tool, PLoS ONE, Volume 9 (2014) no. 5 | DOI

[23] Hohmann, N.; Wolf, E. M.; Lysak, M. A.; Koch, M. A. A Time-Calibrated Road Map of Brassicaceae Species Radiation and Evolutionary History, The Plant Cell (2015) | DOI

[24] Huang, P.; Studer, A. J.; Schnable, J. C.; Kellogg, E. A.; Brutnell, T. P. Cross species selection scans identify components of C4 photosynthesis in the grasses, Journal of Experimental Botany, Volume 68 (2017) no. 2, pp. 127-135 | DOI

[25] Huang, C.-H.; Sun, R.; Hu, Y.; Zeng, L.; Zhang, N.; Cai, L.; Zhang, Q.; Koch, M. A.; Al-Shehbaz, I.; Edger, P. P.; Pires, J. C.; Tan, D.-Y.; Zhong, Y.; Ma, H. Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution, Molecular Biology and Evolution, Volume 33 (2016) no. 2, pp. 394-412 | DOI

[26] Ito, H.; Gaubert, H.; Bucher, E.; Mirouze, M.; Vaillant, I.; Paszkowski, J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress, Nature, Volume 472 (2011) no. 7341, pp. 115-119 | DOI

[27] Jacob, Y.; Stroud, H.; LeBlanc, C.; Feng, S.; Zhuo, L.; Caro, E.; Hassel, C.; Gutierrez, C.; Michaels, S. D.; Jacobsen, S. E. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases, Nature, Volume 466 (2010) no. 7309, pp. 987-991 | DOI

[28] Jamilloux, V.; Daron, J.; Choulet, F.; Quesneville, H. De Novo Annotation of Transposable Elements: Tackling the Fat Genome Issue, Proceedings of the IEEE, Volume 105 (2017) no. 3, pp. 474-481 | DOI

[29] Jurka, J.; Klonowski, P.; Dagman, V.; Pelton, P. Censor—a program for identification and elimination of repetitive elements from DNA sequences, Computers & Chemistry, Volume 20 (1996) no. 1, pp. 119-121 | DOI

[30] Kidwell, M. G. Genetica, 115 (2002) no. 1, pp. 49-63 | DOI

[31] Kinoshita, Y.; Saze, H.; Kinoshita, T.; Miura, A.; Soppe, W. J.; Koornneef, M.; Kakutani, T. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats, The Plant Journal, Volume 49 (2007) no. 1, pp. 38-45 | DOI

[32] Kohany, O.; Gentles, A. J.; Hankus, L.; Jurka, J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor, BMC Bioinformatics, Volume 7 (2006) no. 1 | DOI

[33] Li, L.; Stoeckert, C. J.; Roos, D. S. OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes, Genome Research, Volume 13 (2003) no. 9, pp. 2178-2189 | DOI

[34] Lisch, D. How important are transposons for plant evolution?, Nature Reviews Genetics, Volume 14 (2013) no. 1, pp. 49-61 | DOI

[35] Lister, R.; O'Malley, R. C.; Tonti-Filippini, J.; Gregory, B. D.; Berry, C. C.; Millar, A. H.; Ecker, J. R. Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis, Cell, Volume 133 (2008) no. 3, pp. 523-536 | DOI

[36] Liu, J.; He, Y.; Amasino, R.; Chen, X. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis, Genes & Development, Volume 18 (2004) no. 23, pp. 2873-2878 | DOI

[37] Lowe, C. B.; Bejerano, G.; Haussler, D. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 19, pp. 8005-8010 | DOI

[38] Luo, C.; Sidote, D. J.; Zhang, Y.; Kerstetter, R. A.; Michael, T. P.; Lam, E. Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production, The Plant Journal, Volume 73 (2013) no. 1, pp. 77-90 | DOI

[39] Machanick, P.; Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets, Bioinformatics, Volume 27 (2011) no. 12, pp. 1696-1697 | DOI

[40] Magallón, S.; Castillo, A. Angiosperm diversification through time, American Journal of Botany, Volume 96 (2009) no. 1, pp. 349-365 | DOI

[41] Maumus, F.; Quesneville, H. Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana, Nature Communications, Volume 5 (2014) no. 1 | DOI

[42] Mhiri, C.; Morel, J.-B.; Vernhettes, S.; Casacuberta, J. M.; Lucas, H.; Grandbastien, M.-A. Plant Molecular Biology, 33 (1997) no. 2, pp. 257-266 | DOI

[43] Morgulis, A.; Coulouris, G.; Raytselis, Y.; Madden, T. L.; Agarwala, R.; Schäffer, A. A. Database indexing for production MegaBLAST searches, Bioinformatics, Volume 24 (2008) no. 16, pp. 1757-1764 | DOI

[44] Naito, K.; Zhang, F.; Tsukiyama, T.; Saito, H.; Hancock, C. N.; Richardson, A. O.; Okumoto, Y.; Tanisaka, T.; Wessler, S. R. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression, Nature, Volume 461 (2009) no. 7267, pp. 1130-1134 | DOI

[45] Oh, S.; Park, S.; van Nocker, S. Genic and Global Functions for Paf1C in Chromatin Modification and Gene Expression in Arabidopsis, PLoS Genetics, Volume 4 (2008) no. 8 | DOI

[46] Quesneville, H.; Bergman, C. M.; Andrieu, O.; Autard, D.; Nouaud, D.; Ashburner, M.; Anxolabéhère, D. Combined Evidence Annotation of Transposable Elements in Genome Sequences, PLoS Computational Biology, Volume 1 (2005) no. 2, pp. 166-175 | DOI

[47] Quesneville, H.; Nouaud, D.; Anxolabéhère, D. Detection of New Transposable Element Families in Drosophila melanogaster and Anopheles gambiae Genomes, Journal of Molecular Evolution, Volume 57 (2003) | DOI

[48] Rice, P.; Longden, I.; Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite, Trends in Genetics, Volume 16 (2000) no. 6, pp. 276-277 | DOI

[49] Schnable, P. S.; Ware, D.; Fulton, R. S.; Stein, J. C.; Wei, F.; Pasternak, S.; Liang, C.; Zhang, J.; Fulton, L.; Graves, T. A.; Minx, P.; Reily, A. D.; Courtney, L.; Kruchowski, S. S.; Tomlinson, C.; Strong, C.; Delehaunty, K.; Fronick, C.; Courtney, B.; Rock, S. M.; Belter, E.; Du, F.; Kim, K.; Abbott, R. M.; Cotton, M.; Levy, A.; Marchetto, P.; Ochoa, K.; Jackson, S. M.; 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.; Kohlberg, S.; Sgro, J.; Delgado, B.; Mead, K.; Chinwalla, A.; Leonard, S.; Crouse, K.; Collura, K.; Kudrna, D.; Currie, J.; He, R.; Angelova, A.; Rajasekar, S.; Mueller, T.; Lomeli, R.; Scara, G.; Ko, A.; Delaney, K.; Wissotski, M.; Lopez, G.; Campos, D.; Braidotti, M.; Ashley, E.; Golser, W.; Kim, H.; Lee, S.; Lin, J.; Dujmic, Z.; Kim, W.; Talag, J.; Zuccolo, A.; Fan, C.; Sebastian, A.; Kramer, M.; Spiegel, L.; Nascimento, L.; Zutavern, T.; Miller, B.; Ambroise, C.; Muller, S.; Spooner, W.; Narechania, A.; Ren, L.; Wei, S.; Kumari, S.; Faga, B.; Levy, M. J.; McMahan, L.; Van Buren, P.; Vaughn, M. W.; Ying, K.; Yeh, C.-T.; Emrich, S. J.; Jia, Y.; Kalyanaraman, A.; Hsia, A.-P.; Barbazuk, W. B.; Baucom, R. S.; Brutnell, T. P.; Carpita, N. C.; Chaparro, C.; Chia, J.-M.; Deragon, J.-M.; Estill, J. C.; Fu, Y.; Jeddeloh, J. A.; Han, Y.; Lee, H.; Li, P.; Lisch, D. R.; Liu, S.; Liu, Z.; Nagel, D. H.; McCann, M. C.; SanMiguel, P.; Myers, A. M.; Nettleton, D.; Nguyen, J.; Penning, B. W.; Ponnala, L.; Schneider, K. L.; Schwartz, D. C.; Sharma, A.; Soderlund, C.; Springer, N. M.; Sun, Q.; Wang, H.; Waterman, M.; Westerman, R.; Wolfgruber, T. K.; Yang, L.; Yu, Y.; Zhang, L.; Zhou, S.; Zhu, Q.; Bennetzen, J. L.; Dawe, R. K.; Jiang, J.; Jiang, N.; Presting, G. G.; Wessler, S. R.; Aluru, S.; Martienssen, R. A.; Clifton, S. W.; McCombie, W. R.; Wing, R. A.; Wilson, R. K. The B73 Maize Genome: Complexity, Diversity, and Dynamics, Science, Volume 326 (2009) no. 5956, pp. 1112-1115 | DOI

[50] Smit A; Hubley R; Green P Green P RepeatMasker Open-4.0. 2013-2015.

[51] Strange, A.; Li, P.; Lister, C.; Anderson, J.; Warthmann, N.; Shindo, C.; Irwin, J.; Nordborg, M.; Dean, C. Major-Effect Alleles at Relatively Few Loci Underlie Distinct Vernalization and Flowering Variation in Arabidopsis Accessions, PLoS ONE, Volume 6 (2011) no. 5 | DOI

[52] Thieme, M.; Lanciano, S.; Balzergue, S.; Daccord, N.; Mirouze, M.; Bucher, E. Inhibition of RNA polymerase II allows controlled mobilisation of retrotransposons for plant breeding, Genome Biology, Volume 18 (2017) no. 1 | DOI

[53] Turck, F.; Roudier, F.; Farrona, S.; Martin-Magniette, M.-L.; Guillaume, E.; Buisine, N.; Gagnot, S.; Martienssen, R. A.; Coupland, G.; Colot, V. Arabidopsis TFL2/LHP1 Specifically Associates with Genes Marked by Trimethylation of Histone H3 Lysine 27, PLoS Genetics, Volume 3 (2007) no. 6 | DOI

[54] de Velde, J. V.; Heyndrickx, K. S.; Vandepoele, K. Inference of Transcriptional Networks in Arabidopsis through Conserved Noncoding Sequence Analysis, The Plant Cell, Volume 26 (2014) no. 7, pp. 2729-2745 | DOI

[55] Wang, J.; Keightley, P. D.; Halligan, D. L. Effect of Divergence Time and Recombination Rate on Molecular Evolution of Drosophila INE-1 Transposable Elements and Other Candidates for Neutrally Evolving Sites, Journal of Molecular Evolution, Volume 65 (2007) no. 6, pp. 627-639 | DOI

[56] Weiner, A.; Hsieh, T.-H. S.; Appleboim, A.; Chen, H. V.; Rahat, A.; Amit, I.; Rando, O. J.; Friedman, N. High-Resolution Chromatin Dynamics during a Yeast Stress Response, Molecular Cell, Volume 58 (2015) no. 2, pp. 371-386 | DOI

[57] Wicker, T.; Gundlach, H.; Spannagl, M.; Uauy, C.; Borrill, P.; Ramírez-González, R. H.; De Oliveira, R.; Mayer, K. F. X.; Paux, E.; Choulet, F. Impact of transposable elements on genome structure and evolution in bread wheat, Genome Biology, Volume 19 (2018) no. 1 | DOI

[58] Zhang, X.; Clarenz, O.; Cokus, S.; Bernatavichute, Y. V.; Pellegrini, M.; Goodrich, J.; Jacobsen, S. E. Whole-Genome Analysis of Histone H3 Lysine 27 Trimethylation in Arabidopsis, PLoS Biology, Volume 5 (2007) no. 5 | DOI

[59] Zytnicki, M.; Quesneville, H. S-MART, A Software Toolbox to Aid RNA-seq Data Analysis, PLoS ONE, Volume 6 (2011) no. 10 | DOI

Cited by Sources: