Contrasting distributions and expression characteristics of transcribing repeats in Setaria viridis
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
Grantová podpora
001
Coordination for the Improvement of Higher Education Personnel-Brazil, Finance Code: 001 (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior)
Queen Mary University of London
PubMed
39789756
PubMed Central
PMC11718148
DOI
10.1002/tpg2.20551
Knihovny.cz E-zdroje
- MeSH
- genetická transkripce MeSH
- genom rostlinný MeSH
- koncové repetice * MeSH
- regulace genové exprese u rostlin MeSH
- retroelementy * MeSH
- Setaria (rostlina) * genetika MeSH
- transkriptom MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- retroelementy * MeSH
Repetitive DNA contributes significantly to plant genome size, adaptation, and evolution. However, little is understood about the transcription of repeats. This is addressed here in the plant green foxtail millet (Setaria viridis). First, we used RepeatExplorer2 to calculate the genome proportion (GP) of all repeat types and compared the GP of long terminal repeat (LTR) retroelements against annotated complete and incomplete LTR retroelements (Ty1/copia and Ty3/gypsy) identified by DANTE in a whole genome assembly. We show that DANTE-identified LTR retroelements can comprise ∼0.75% of the inflorescence poly-A transcriptome and ∼0.24% of the stem ribo-depleted transcriptome. In the RNA libraries from inflorescence tissue, both LTR retroelements and DNA transposons identified by RepeatExplorer2 were highly abundant, where they may be taking advantage of the reduced epigenetic silencing in the germ line to amplify. Typically, there was a higher representation of DANTE-identified LTR retroelements in the transcriptome than RepeatExplorer2-identified LTR retroelements, potentially reflecting the transcription of elements that have insufficient genomic copy numbers to be detected by RepeatExplorer2. In contrast, for ribo-depleted libraries of stem tissues, the reverse was observed, with a higher transcriptome representation of RepeatExplorer2-identified LTR retroelements. For RepeatExplorer2-identified repeats, we show that the GP of most Ty1/copia and Ty3/gypsy families were positively correlated with their transcript proportion. In addition, guanine- and cytosine-rich repeats with high sequence similarity were also the most abundant in the transcriptome, and these likely represent young elements that are most capable of amplification due to their ability to evade epigenetic silencing.
Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
Institute of Biological Sciences Federal University of Juiz de Fora Juiz de Fora Minas Gerais Brazil
Royal Botanic Gardens Kew Richmond UK
School of Biological and Behavioural Sciences Queen Mary University of London London E1 4NS UK
Zobrazit více v PubMed
Anderson, S. N. , Stitzer, M. C. , Zhou, P. , Ross‐Ibarra, J. , Hirsch, C. D. , & Springer, N. M. (2019). Dynamic patterns of transcript abundance of transposable element families in maize. G3: Genes, Genomes, Genetics, 9(11), 3673–3682. 10.1534/g3.119.400431 PubMed DOI PMC
Ansaloni, F. , Scarpato, M. , Di Schiavi, E. , Gustincich, S. , & Sanges, R. (2019). Exploratory analysis of transposable elements expression in the C. elegans early embryo. BMC Bioinformatics, 20, Article 484. 10.1186/s12859-019-3088-7 PubMed DOI PMC
Bao, W. , Kojima, K. K. , & Kohany, O. (2015). Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA, 6(1), 4–9. 10.1186/s13100-015-0041-9 PubMed DOI PMC
Bennett, M. D. , Leitch, I. J. , & Hanson, L. (1998). DNA amounts in two samples of angiosperm weeds. Annals of Botany, 82, 121–134. 10.1006/anbo.1998.0785 DOI
Bennetzen, J. L. , Schmutz, J. , Wang, H. , Percifield, R. , Hawkins, J. , Pontaroli, A. C. , Estep, M. , Feng, L. , Vaughn, J. N. , Grimwood, J. , Jenkins, J. , Barry, K. , Lindquist, E. , Hellsten, U. , Deshpande, S. , Wang, X. , Wu, X. , Mitros, T. , Triplett, J. , … Devos, K. M. (2012). Reference genome sequence of the model plant Setaria . Nature Biotechnology, 30(6), 555–561. 10.1038/nbt.2196 PubMed DOI
Bernal‐Gallardo, J. J. , & de Folter, S. (2024). Plant genome information facilitates plant functional genomics. Planta, 259(5), 117. 10.1007/s00425-024-04397-z PubMed DOI PMC
Bolger, A. M. , Lohse, M. , & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC
Criscione, S. W. , Zhang, Y. , Thompson, W. , Sedivy, J. M. , & Neretti, N. (2014). Transcriptional landscape of repetitive elements in normal and cancer human cells. BMC Genomics, 15(1), Article 583. 10.1186/1471-2164-15-583 PubMed DOI PMC
Devos, K. M. (2010). Grass genome organization and evolution. Current Opinion in Plant Biology, 13(2), 139–145. 10.1016/j.pbi.2009.12.005 PubMed DOI
Dobin, A. , Davis, C. A. , Schlesinger, F. , Drenkow, J. , Zaleski, C. , Jha, S. , Batut, P. , Chaisson, M. , & Gingeras, T. R. (2013). STAR: Ultrafast universal RNA‐seq aligner. Bioinformatics, 29(1), 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC
Dodsworth, S. , Chase, M. W. , Kelly, L. J. , Leitch, I. J. , Macas, J. , Novák, P. , Piednoel, M. , Weiss‐Schneeweiss, H. , & Leitch, A. R. (2015). Genomic repeat abundances contain phylogenetic signal. Systematic Biology, 64(1), 112–126. 10.1093/sysbio/syu080 PubMed DOI PMC
Du, H. , Yu, Y. , Ma, Y. , Gao, Q. , Cao, Y. , Chen, Z. , Ma, B. , Qi, M. , Li, Y. , Zhao, X. , Wang, J. , Liu, K. , Qin, P. , Yang, X. , Zhu, L. , Li, S. , & Liang, C. (2017). Sequencing and de novo assembly of a near complete indica rice genome. Nature Communications, 8(1), Article 15324. 10.1038/ncomms15324 PubMed DOI PMC
Fernández, P. , Amice, R. , Bruy, D. , Christenhusz, M. J. M. , Leitch, I. J. , Leitch, A. L. , Pokorny, L. , Hidalgo, O. , & Pellicer, J. (2024). A 160 Gbp fork fern genome shatters size record for eukaryotes. iScience, 27, 109889. 10.1016/j.isci.2024.109889 PubMed DOI PMC
Galindo‐González, L. , Mhiri, C. , Deyholos, M. K. , & Grandbastien, M. A. (2017). LTR‐retrotransposons in plants: Engines of evolution. Gene, 626, 14–25. 10.1016/j.gene.2017.04.051 PubMed DOI
Garrido‐Ramos, M. A. (2017). Satellite DNA: An evolving topic. Genes, 8(9), 230. 10.3390/genes8090230 PubMed DOI PMC
Giraud, D. , Lima, O. , Huteau, V. , Coriton, O. , Boutte, J. , Kovarik, A. , Leitch, A. R. , Leitch, I. J. , Aïnouche, M. , & Salmon, A. (2021). Plant science evolutionary dynamics of transposable elements and satellite DNAs in polyploid Spartina species. Plant Science, 302, 110671. 10.1016/j.plantsci.2020.110671 PubMed DOI
Gozashti, L. , Roy, S. W. , Thornlow, B. , Kramer, A. , Ares, M. , & Corbett‐Detig, R. (2022). Transposable elements drive intron gain in diverse eukaryotes. Proceedings of the National Academy of Sciences, 119(48), e2209766119. 10.1073/pnas.2209766119 PubMed DOI PMC
Gremme, G. , Steinbiss, S. , & Kurtz, S. (2013). GenomeTools: A comprehensive software library for efficient processing of structured genome annotations. IEEE/ACM Transactions on Computational Biology and Bioinformatics, 10(3), 645–656. 10.1109/TCBB.2013.68 PubMed DOI
Gruber, K. (2017). Agrobiodiversity: The living library. Nature, 544(7651), S8–S10. 10.1038/544S8a PubMed DOI
Gualandi, N. , Iperi, C. , Esposito, M. , Ansaloni, F. , Gustincich, S. , & Sanges, R. (2022). Meta‐analysis suggests that intron retention can affect quantification of transposable elements from RNA‐Seq data. Biology, 11(6), 826. 10.3390/biology11060826 PubMed DOI PMC
Hodkinson, T. R. (2018). Evolution and taxonomy of the grasses (Poaceae): A model family for the study of species‐rich groups. In Roberts J. (Ed.), Annual plant reviews online (Vol. 1, pp. 1–39). Jonh Wiley & Sons, Ltd. 10.1002/9781119312994.apr0622 DOI
Husband, B. C. , Baldwin, S. J. , & Suda, J. (2013). The incidence of polyploidy in natural plant populations: Major patterns and evolutionary processes. In Leitch I. J., Greilhuber J., Doležel J., & Wendel J. F. (Eds.), Plant genome diversity volume 2: Physical structure, behaviour and evolution of plant genomes (pp. 255–276). Springer‐Verlag.
Initiative, T. I. B. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon . Nature, 463(7282), 763–768. 10.1038/nature08747 PubMed DOI
Jeong, H. H. , Yalamanchili, H. K. , Guo, C. , Shulman, J. M. , & Liu, Z. (2018). An ultra‐fast and scalable quantification pipeline for transposable elements from next generation sequencing data. Biocomputing, 2018, 168–179. 10.1142/9789813235533_0016 PubMed DOI
Jiang, S. , & Ramachandran, S. (2013). Genome‐wide survey and comparative analysis of LTR retrotransposons and their captured genes in rice and sorghum. PLoS One, 8(7), e71118. 10.1371/journal.pone.0071118 PubMed DOI PMC
Jin, Y. , Tam, O. H. , Paniagua, E. , & Hammell, M. (2015). TEtranscripts: A package for including transposable elements in differential expression analysis of RNA‐seq datasets. Bioinformatics, 31(22), 3593–3599. 10.1093/bioinformatics/btv422 PubMed DOI PMC
Kellogg, E. A. (2001). Update on evolution evolutionary history of the grasses. Plant Physiology, 125, 1198–1205. 10.1104/pp.125.3.1198 PubMed DOI PMC
Kellogg, E. A. (2017). Evolution of Setaria . In Doust A. & Diao X. (Eds.), Genetics and genomics of Setaria (pp. 3–27). Springer International Publishing. 10.1007/978-3-319-45105-3_1 DOI
Kelly, L. J. , Renny‐Byfield, S. , Pellicer, J. , Macas, J. , Novák, P. , Neumann, P. , Lysak, M. A. , Day, P. D. , Berger, M. , Fay, M. F. , Nichols, R. A. , Leitch, A. R. , & Leitch, I. J. (2015). Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytologist, 208(2), 596–607. 10.1111/nph.13471 PubMed DOI PMC
Kenchanmane Raju, S. K. , Ritter, E. J. , & Niederhuth, C. E. (2019). Establishment, maintenance, and biological roles of non‐CG methylation in plants. Essays in Biochemistry, 63(6), 743–755. 10.1042/EBC20190032 PubMed DOI PMC
Kirov, I. , Omarov, M. , Merkulov, P. , Dudnikov, M. , Gvaramiya, S. , Kolganova, E. , Komakhin, R. , Karlov, G. , & Soloviev, A. (2020). Genomic and transcriptomic survey provides new insight into the organization and transposition activity of highly expressed LTR retrotransposons of sunflower (Helianthus annuus L.). International Journal of Molecular Sciences, 21, 9331. PubMed PMC
Kong, Y. , Rose, C. M. , Cass, A. A. , Williams, A. G. , Darwish, M. , Lianoglou, S. , Haverty, P. M. , Tong, A. J. , Blanchette, C. , Albert, M. L. , Mellman, I. , Bourgon, R. , Greally, J. , Jhunjhunwala, S. , & Chen‐Harris, H. (2019). Transposable element expression in tumors is associated with immune infiltration and increased antigenicity. Nature Communications, 10(1), Article 5228. 10.1038/s41467-019-13035-2 PubMed DOI PMC
Kovařík, A. , Matyášek, R. , Leitch, A. , Gazdová, B. , Fulneček, J. , & Bezděk, M. (1997). Variability in CpNpG methylation in higher plant genomes. Gene, 204(1–2), 25–33. 10.1016/S0378-1119(97)00503-9 PubMed DOI
Kuo, Y. T. , Ishii, T. , Fuchs, J. , Hsieh, W. H. , Houben, A. , & Lin, Y. R. (2021). The evolutionary dynamics of repetitive DNA and its impact on the genome diversification in the genus Sorghum . Frontiers in Plant Science, 12, Article 729734. 10.3389/fpls.2021.729734 PubMed DOI PMC
Lanciano, S. , & Cristofari, G. (2020). Measuring and interpreting transposable element expression. Nature Reviews Genetics, 21(12), 721–736. 10.1038/s41576-020-0251-y PubMed DOI
Langmead, B. , & Salzberg, S. L. (2012). Fast gapped‐read alignment with Bowtie 2. Nature Methods, 9(4), 357–359. 10.1038/nmeth.1923 PubMed DOI PMC
Lerat, E. , Fablet, M. , Modolo, L. , Lopez‐Maestre, H. , & Vieira, C. (2017). TEtools facilitates big data expression analysis of transposable elements and reveals an antagonism between their activity and that of piRNA genes. Nucleic Acids Research, 45(4), e17. 10.1093/nar/gkw953 PubMed DOI PMC
Li, H. , Handsaker, B. , Wysoker, A. , Fennell, T. , Ruan, J. , Homer, N. , Marth, G. , Abecasis, G. , & Durbin, R. (2009). & Subgroup, 1000 genome project data processing. The sequence slignment/map format and SAMtools. Bioinformatics, 25(16), 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC
Lin, G. , He, C. , Zheng, J. , Koo, D.‐H. , Le, H. , Zheng, H. , Tamang, T. M. , Lin, J. , Liu, Y. , Zhao, M. , Hao, Y. , McFraland, F. , Wang, B. , Qin, Y. , Tang, H. , McCarty, D. R. , Wei, H. , Cho, M.‐J. , Park, S. , … Liu, S. (2021). Chromosome‐level genome assembly of a regenerable maize inbred line A188. Genome Biology, 22(1), Article 175. 10.1186/s13059-021-02396-x PubMed DOI PMC
Lisch, D. (2013). How important are transposons for plant evolution ? Nature Reviews Genetics, 14, 13–15. 10.1038/nrg3374 PubMed DOI
Macas, J. , Novák, P. , Pellicer, J. , Cizkova, J. , Koblizkova, A. , Neumann, P. , Fukova, I. , Dolezel, J. , Kelly, L. J. , & Leitch, I. J. (2015). In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae . PLoS One, 10(11), e0143424. 10.1371/journal.pone.0143424 PubMed DOI PMC
Mamidi, S. , Healey, A. , Huang, P. , Grimwood, J. , Jenkins, J. , Barry, K. , Sreedasyam, A. , Shu, S. , Lovell, J. T. , Feldman, M. , Wu, J. , Yu, Y. , Chen, C. , Johnson, J. , Sakakibara, H. , Kiba, T. , Sakurai, T. , Tavares, R. , Nusinow, D. A. , … Kellogg, E. A. (2020). A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci. Nature Biotechnology, 38(10), 1203–1210. 10.1038/s41587-020-0681-2 PubMed DOI PMC
Mascagni, F. , Vangelisti, A. , Usai, G. , Giordani, T. , Cavallini, A. , & Natali, L. (2020). A computational genome‐wide analysis of long terminal repeats retrotransposon expression in sunflower roots (Helianthus annuus L.). Genetica, 148(1), 13–23. 10.1007/s10709-020-00085-4 PubMed DOI
Matzke, M. A. , Kanno, T. , & Matzke, A. J. M. (2015). RNA‐directed DNA methylation : The evolution of a complex epigenetic pathway in flowering plants. Annual Review of Plant Biology, 66, 243–267. 10.1146/annurev-arplant-043014-114633 PubMed DOI
Maumus, F. , & Quesneville, H. (2014). Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS One, 9(4), e94101. 10.1371/journal.pone.0094101 PubMed DOI PMC
Meneghin, J. (2009). https://github.com/jmeneghin/perl‐for‐reysenbach‐lab/blob/master/get_gc_content.pl
Meyers, B. C. , Tingey, S. V. , & Morgante, M. (2001). Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Research, 11(10), 1660–1676. 10.1101/gr.188201 PubMed DOI PMC
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. Mobile DNA, 10(1), 1. 10.1186/s13100-018-0144-1 PubMed DOI PMC
Novák, P. , Guignard, M. S. , Neumann, P. , Kelly, L. J. , Mlinarec, J. , Koblížková, A. , Dodsworth, S. , Kovařík, A. , Pellicer, J. , Wang, W. , Macas, J. , Leitch, I. J. , & Leitch, A. R. (2020). Repeat‐sequence turnover shifts fundamentally in species with large genomes. Nature Plants, 6, 1325–1329. 10.1038/s41477-020-00785-x PubMed DOI
Novák, P. , Neumann, P. , & Macas, J. (2010). Graph‐based clustering and characterization of repetitive sequences in next‐generation sequencing data. BMC Bioinformatics, 11, Article 378. 10.1186/1471-2105-11-378 PubMed DOI PMC
Novák, P. , Neumann, P. , & Macas, J. (2020). Global analysis of repetitive DNA from unassembled sequence reads using. Nature Protocols, 15, 3745–3776. 10.1038/s41596-020-0400-y PubMed DOI
Pant, S. R. , Irigoyen, S. , Doust, A. N. , & Scholthof, K. G. (2016). Setaria : A food crop and translational research model for C4 grasses. Frontiers in Plant Science, 7(December), Article 1885. 10.3389/fpls.2016.01885 PubMed DOI PMC
Pellicer, J. , Hidalgo, O. , Dodsworth, S. , & Leitch, I. J. (2018). Genome size diversity and its impact on the evolution of land plants. Genes, 9(2), 88. 10.3390/genes9020088 PubMed DOI PMC
Pellicer, J. , & Leitch, I. J. (2020). The Plant DNA C‐values database (release 7.1): An updated online repository of plant genome size data for comparative studies. New Phytologist, 226(2), 301–305. 10.1111/nph.16261 PubMed DOI
Pezer, Ž. , Brajković, J. , Feliciello, I. , & Ugarković, Đ. (2012). Satellite DNA‐mediated effects on genome regulation. Repetitive DNA, 7, 153–169. PubMed
Plohl, M. , Luchetti, A. , Meštrović, N. , & Mantovani, B. (2008). Satellite DNAs between selfishness and functionality: Structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene, 409(1–2), 72–82. 10.1016/j.gene.2007.11.013 PubMed DOI
Plohl, M. , Meštrović, N. , & Mravinac, B. (2012). Satellite DNA evolution. Genome Dynamics, 7, 126–152. 10.1159/000337122 PubMed DOI
Qiu, F. , & Ungerer, M. C. (2018). Genomic abundance and transcriptional activity of diverse gypsy and copia long terminal repeat retrotransposons in three wild sunflower species. BMC Plant Biology, 18(1), 6. 10.1186/s12870-017-1223-z PubMed DOI PMC
Quinlan, A. R. , & Hall, I. M. (2010). BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics, 26(6), 841–842. 10.1093/bioinformatics/btq033 PubMed DOI PMC
R Core Team . (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Saze, H. (2018). Epigenetic regulation of intragenic transposable elements: A two‐edged sword. The Journal of Biochemistry, 164(5), 323–328. 10.1093/jb/mvy060 PubMed DOI
Sebastian, J. , Yee, M. , Goudinho, W. , Rellán‐álvarez, R. , Feldman, M. , Priest, H. , Trontin, C. , Lee, T. , Jiang, H. , Baxter, I. , Mockler, T. , Hochholdinger, F. , Brutnell, T. P. , & Dinneny, J. (2016). Grasses suppress shoot‐borne roots to conserve water during drought. Proceedings of the National Academy of Sciences, 113(14), 8861–8866. 10.1073/pnas.1604021113 PubMed DOI PMC
Stritt, C. , Wyler, M. , Gimmi, E. L. , Pippel, M. , & Roulin, A. C. (2019). Diversity, dynamics and effects of long terminal repeat retrotransposons in the model grass Brachypodium distachyon . New Phytologist, 227(6), 1736–1748. 10.1111/nph.16308 PubMed DOI PMC
Thielen, P. M. , Pendleton, A. L. , Player, R. A. , Bowden, K. V. , Lawton, T. J. , & Wisecaver, J. H. (2020). Reference genome for the highly transformable Setaria viridis ME034V. G3: Genes, Genomes, Genetics, 10, 3467–3478. 10.1534/g3.120.401345 PubMed DOI PMC
Vincent, H. , Amri, A. , Castañeda‐Álvarez, N. P. , Dempewolf, H. , Dulloo, E. , Guarino, L. , Hole, D. , Mba, C. , Toledo, A. , & Maxted, N. (2019). Modeling of crop wild relative species identifies areas globally for in situ conservation. Communications Biology, 2(1), Article 136. 10.1038/s42003-019-0372-z PubMed DOI PMC
Wang, W. , Wan, T. , Becher, H. , Kuderova, A. , Leitch, I. J. , Garcia, S. , Leitch, A. R. , & Kovařík, A. (2019). Remarkable variation of ribosomal DNA organization and copy number in gnetophytes, a distinct lineage of gymnosperms. Annals of Botany, 123(5), 767–781. 10.1093/aob/mcy172 PubMed DOI PMC
Wang, X. , Morton, J. , Pellicer, J. , Leitch, I. J. , & Leitch, A. R. (2021). Genome downsizing after polyploidy: Mechanisms, rates and selection pressures. The Plant Journal, 107(4), 1003–1015. 10.1111/tpj.15363 PubMed DOI
Yadav, C. B. , Bonthala, V. S. , Muthamilarasan, M. , Pandey, G. , Khan, Y. , & Prasad, M. (2015). Genome‐wide development of transposable elements‐based markers in foxtail millet and construction of an integrated database. DNA Research, 22(November 2014), 79–90. 10.1093/dnares/dsu039 PubMed DOI PMC
Yang, J. , Thames, S. , Best, N. B. , Jiang, H. , Huang, P. , Dilkes, B. P. , & Eveland, A. L. (2018). Brassinosteroids modulate meristem fate and differentiation of unique inflorescence morphology in Setaria viridis . Plant Cell, 30(1), 48–66. 10.1105/tpc.17.00816 PubMed DOI PMC
Zhang, G. , Liu, X. , Quan, Z. , Cheng, S. , Xu, X. , Pan, S. , Xie, M. , Zeng, P. , Yue, Z. , Wang, W. , Tao, Y. , Bian, C. , Han, C. , Xia, Q. , Peng, X. , Cao, R. , Yang, X. , Zhan, D. , Hu, J. , … Wang, J. (2012). Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nature Biotechnology, 30(6), 549–554. 10.1038/nbt.2195 PubMed DOI