دورية أكاديمية

Uniparental silencing of 5S rRNA genes in plant allopolyploids - insights from Cardamine (Brassicaceae).

التفاصيل البيبلوغرافية
العنوان: Uniparental silencing of 5S rRNA genes in plant allopolyploids - insights from Cardamine (Brassicaceae).
المؤلفون: Mandáková T; Central European Institute of Technology (CEITEC), Masaryk University, 625 00, Brno, Czech Republic.; Department of Experimental Biology, Faculty of Science, Masaryk University, 611 37, Brno, Czech Republic., Krumpolcová A; Department of Experimental Biology, Faculty of Science, Masaryk University, 611 37, Brno, Czech Republic.; Department of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, 612 00, Brno, Czech Republic., Matyášek R; Department of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, 612 00, Brno, Czech Republic., Volkov R; Department of Molecular Genetics and Biotechnology, Yuriy Fedkovych Chernivtsi National University, 58012, Chernivtsi, Ukraine., Lysak MA; Central European Institute of Technology (CEITEC), Masaryk University, 625 00, Brno, Czech Republic.; Faculty of Science, National Centre for Biomolecular Research, Masaryk University, 625 00, Brno, Czech Republic., Kovařík A; Department of Molecular Epigenetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, 612 00, Brno, Czech Republic.
المصدر: The Plant journal : for cell and molecular biology [Plant J] 2024 Aug; Vol. 119 (3), pp. 1313-1326. Date of Electronic Publication: 2024 Jun 05.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology Country of Publication: England NLM ID: 9207397 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-313X (Electronic) Linking ISSN: 09607412 NLM ISO Abbreviation: Plant J Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Oxford : Blackwell Scientific Publishers and BIOS Scientific Publishers in association with the Society for Experimental Biology, c1991-
مواضيع طبية MeSH: RNA, Ribosomal, 5S*/genetics , Polyploidy* , Cardamine*/genetics , Gene Silencing* , Phylogeny*, Genome, Plant/genetics ; DNA, Ribosomal/genetics ; In Situ Hybridization, Fluorescence ; Gene Expression Regulation, Plant
مستخلص: While the phenomenon of uniparental silencing of 35S rDNA in interspecific hybrids and allopolyploids is well documented, there is a notable absence of information regarding whether such silencing extends to the 5S RNA component of ribosomes. To address this gap in knowledge, we analyzed the 5S and 35S rDNA expression in Cardamine (Brassicaceae) allopolyploids, namely C. × insueta (2n = 3x = 24, genome composition RRA), C. flexuosa (2n = 4x = 32, AAHH), and C. scutata (2n = 4x = 32, PPAA) which share a common diploid ancestor (AA). We employed high-throughput sequencing of transcriptomes and genomes and phylogenetic analyses of 5S rRNA variants. The genomic organization of rDNA was further scrutinized through clustering and fluorescence in situ hybridization. In the C. × insueta allotriploid, we observed uniparental dominant expression of 5S and 35S rDNA loci. In the C. flexuosa and C. scutata allotetraploids, the expression pattern differed, with the 35S rDNA being expressed from the A subgenome, whereas the 5S rDNA was expressed from the partner subgenome. Both C. flexuosa and C. scutata but not C. × insueta showed copy and locus number changes. We conclude that in stabilized allopolyploids, transcription of ribosomal RNA components occurs from different subgenomes. This phenomenon appears to result in the formation of chimeric ribosomes comprising rRNA molecules derived from distinct parental origins. We speculate that the interplay of epigenetic silencing and rDNA rearrangements introduces an additional layer of variation in multimolecule ribosomal complexes, potentially contributing to the evolutionary success of allopolyploids.
(© 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.)
References: Alexandrov, O.S., Razumova, O.V. & Karlov, G.I. (2021) A comparative study of 5S rDNA non‐transcribed spacers in Elaeagnaceae species. Plants (Basel), 10, 4.
Barciszewska, M.Z., Erdmann, V.A. & Barciszewski, J. (1994) The dynamic conformation of plant cytoplasmic 5S rRNAs. Phytochemistry, 37, 113-117.
Baum, B.R., Edwards, T. & Johnson, D.A. (2008) Loss of 5S rDNA units in the evolution of Agropyron, Pseudoroegneria, and Douglasdeweya. Genome, 51, 589–598.
Bennett, M.D. & Leitch, I. (2012) Angiosperm DNA C‐values database (release 8.0). Available from: http://data.kew.org/cvalues/ [Accessed 24th November 2023].
Borowska‐Zuchowska, N., Kovarik, A., Robaszkiewicz, E., Tuna, M., Tuna, G.S., Gordon, S. et al. (2020) The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum. The Plant Journal, 103, 1810–1825.
Borowska‐Zuchowska, N., Mykhailyk, S., Robaszkiewicz, E., Matysiak, N., Mielanczyk, L., Wojnicz, R. et al. (2023) Switch them off or not: selective rRNA gene repression in grasses. Trends in Plant Science, 28, 661–672.
Buckler, E.S., Ippolito, A. & Holtsford, T.P. (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics, 145, 821–832.
Cardoni, S., Piredda, R., Denk, T., Grimm, G.W., Papageorgiou, A.C., Schulze, E.D. et al. (2021) 5S‐IGS rDNA in wind‐pollinated trees (Fagus L.) encapsulates 55 million years of reticulate evolution and hybrid origins of modern species. The Plant Journal, 109, 909–926.
Chen, Z.J. & Pikaard, C.S. (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes & Development, 11, 2124–2136.
Ciganda, M. & Williams, N. (2011) Eukaryotic 5S rRNA biogenesis. Wiley Interdisciplinary Reviews: RNA, 2, 523–533.
Cloix, C., Tutois, S., Mathieu, O., Cuvillier, C., Espagnol, M.C., Picard, G. et al. (2000) Analysis of 5S rDNA arrays in Arabidopsis thaliana: physical mapping and chromosome‐specific polymorphisms. Genome Research, 10, 679–690.
Earley, K., Lawrence, R.J., Pontes, O., Reuther, R., Enciso, A.J., Silva, M. et al. (2006) Erasure of histone acetylation by Arabidopsis HDAC6 mediates large‐scale gene silencing in nucleolar dominance. Genes & Development, 20, 1283–1293.
Feliner, G.N., Casacuberta, J. & Wendel, J.F. (2020) Genomics of evolutionary novelty in hybrids and polyploids. Frontiers in Genetics, 11, 792.
Franzke, A. & Mummenhoff, K. (1999) Recent hybrid speciation in Cardamine (Brassicaceae) – conversion of nuclear ribosomal ITS sequences in statu nascendi. Theoretical and Applied Genetics, 98, 831–834.
Fulnecek, J., Matyasek, R., Kovarik, A. & Bezdek, M. (1998) Mapping of 5‐methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Molecular & General Genetics, 259, 133–141.
Galián, J.A., Rosato, M. & Rosselló, J.A. (2014) Partial sequence homogenization in the 5S multigene families may generate sequence chimeras and spurious results in phylogenetic reconstructions. Systematic Biology, 63, 219–230.
Garcia, S., Crhak Khaitova, L. & Kovarik, A. (2012) Expression of 5S rRNA genes linked to 35 S rDNA in plants, their epigenetic modification and regulatory element divergence. BMC Plant Biology, 12, 95.
Garcia, S., Pascual‐Diaz, J.P., Krumpolcova, A. & Kovarik, A. (2023) Analysis of 5S rDNA genomic organization through the RepeatExplorer2 pipeline: a simplified protocol. Methods in Molecular Biology, 2672, 501–512.
Garcia, S., Wendel, J.F., Borowska‐Zuchowska, N., Ainouche, M., Kuderova, A. & Kovarik, A. (2020) The utility of graph clustering of 5S ribosomal DNA homoeologs in plant allopolyploids, homoploid hybrids, and cryptic Introgressants. Frontiers in Plant Science, 11, 41.
Gongadze, G.M. (2011) 5S rRNA and ribosome. Biochemistry (Moscow), 76, 1450–1464.
Guo, X. & Han, F.P. (2014) Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell, 26, 4311–4327.
Gustafson, J.P., Dera, A.R. & Petrovic, S. (1988) Expression of modified rye ribosomal‐RNA genes in wheat. Proceedings of the National Academy of Sciences of the United States of America, 85, 3943–3945.
Hemleben, V. & Werts, D. (1988) Sequence organization and putative regulatory elements in the 5S rRNA genes of two higher plants (Vigna radiata and Matthiola incana). Gene, 62, 165–169.
Houchins, K., O'Dell, M., Flavell, R.B. & Gustafson, J.P. (1997) Cytosine methylation and nucleolar dominance in cereal hybrids. Molecular & General Genetics, 255, 294–301.
Huang, S., Aleksashin, N.A., Loveland, A.B., Klepacki, D., Reier, K., Kefi, A. et al. (2020) Ribosome engineering reveals the importance of 5S rRNA autonomy for ribosome assembly. Nature Communications, 11, 2900.
Jang, T.S., McCann, J., Parker, J.S., Takayama, K., Hong, S.P., Schneeweiss, G.M. et al. (2016) rDNA loci evolution in the genus Glechoma (Lamiaceae). PLoS One, 11, e0167177.
Joachimiak, A., Nalaskowska, M., Barciszewska, M., Barciszewski, J. & Mashkova, T. (1990) Higher‐plant 5S ribosomal‐RNAs share common secondary and tertiary structure –a new 3 domains model. International Journal of Biological Macromolecules, 12, 321–327.
Kellogg, E.A. & Appels, R. (1995) Intraspecific and interspecific variation in 5S RNA genes are decoupled in diploid wheat relatives. Genetics, 140, 325–343.
Knies, J.L., Dang, K.K., Vision, T.J., Hoffman, N.G., Swanstrom, R. & Burch, C.L. (2008) Compensatory evolution in RNA secondary structures increases substitution rate variation among sites. Molecular Biology and Evolution, 25, 1778–1787.
Kouvela, E.C., Gerbanas, G.V., Xaplanteri, M.A., Petropoulos, A.D., Dinos, G.P. & Kalpaxis, D.L. (2007) Changes in the conformation of 5S rRNA cause alterations in principal functions of the ribosomal nanomachine. Nucleic Acids Research, 35, 5108–5119.
Layat, E., Cotterell, S., Vaillant, I., Yukawa, Y., Tutois, S. & Tourmente, S. (2012) Transcript levels, alternative splicing and proteolytic cleavage of TFIIIA control 5S rRNA accumulation during Arabidopsis thaliana development. The Plant Journal, 71, 35–44.
Layat, E., Saez‐Vasquez, J. & Tourmente, S. (2012) Regulation of pol I‐transcribed 45S rDNA and pol III‐transcribed 5S rDNA in Arabidopsis. Plant & Cell Physiology, 53, 267–276.
Lihova, J. & Marhold, K. (2006) Phylogenetic and diversity patterns in Cardamine (Brassicaceae) – a genus with conspicuous polyploid and reticulate evolution. In: Sharma, A.K. & Sharma, A. (Eds.) Plant genome: biodiversity and evolution. Enfield, New Hampshire: Science Publishers, Inc, pp. 149–186.
Lihova, J., Marhold, K., Kudoh, H. & Koch, M.A. (2006) Worldwide phylogeny and biogeography of Cardamine flexuosa (Brassicaceae) and its relatives. American Journal of Botany, 93, 1206–1221.
Lorenz, R., Bernhart, S.H., Höner zu Siederdissen, C., Tafer, H., Flamm, C., Stadler, P.F. et al. (2011) ViennaRNA package 2.0. Algorithms for Molecular Biology, 6, 26.
Mahelka, V., Kopecky, D. & Baum, B.R. (2013) Contrasting patterns of evolution of 45S and 5S rDNA families uncover new aspects in the genome constitution of the agronomically important grass Thinopyrum intermedium (Triticeae). Molecular Biology and Evolution, 30, 2065–2086.
Mahelka, V., Kopecký, D., Majka, J. & Krak, K. (2023) Uniparental expression of ribosomal RNA in ×Festulolium grasses: a link between the genome and nucleolar dominance. Frontiers in Plant Science, 14, 1276252.
Mandáková, T., Gloss, A.D., Whiteman, N.K. & Lysak, M.A. (2016) How diploidization turned a tetraploid into a pseudotriploid. American Journal of Botany, 103, 1187–1196.
Mandáková, T., Kovarik, A., Zozomova‐Lihova, J., Shimizu‐Inatsugi, R., Shimizu, K.K., Mummenhoff, K. et al. (2013) The more the merrier: recent hybridization and polyploidy in cardamine. Plant Cell, 25, 3280–3295.
Mandáková, T. & Lysak, M.A. (2018) Post‐polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology, 42, 55–65.
Mandáková, T., Marhold, K. & Lysak, M.A. (2014) The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure. The New Phytologist, 201, 982–992.
Mandáková, T., Zozomová‐Lihová, J., Kudoh, H., Zhao, Y., Lysak, M.A. & Marhold, K. (2019) The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives. Annals of Botany, 124, 209–220.
Mandáková, T.M. & Lysak, M.A. (2023) Chromosome painting using chromosome‐specific BAC clones. Methods in Molecular Biology, 2672, 303–313.
Nei, M. (1987) Molecular evolutionary genetics. New York: Columbia Univ. Press.
Neves, N., Heslopharrison, J.S. & Viegas, W. (1995) Ribosomal RNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat × rye hybrids. Theoretical and Applied Genetics, 91, 529–533.
Novak, 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.
Pikaard, C.S., Chandrasekhara, C., McKinlay, A., Enganti, R. & Fultz, D. (2023) Reaching for the off switch in nucleolar dominance. The Plant Journal, 115, 1185–1192.
Pontes, O., Neves, N., Silva, M., Lewis, M.S., Madlung, A., Comai, L. et al. (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proceedings of the National Academy of Sciences of the United States of America, 101, 18240–18245.
Pontvianne, F., Abou‐Ellail, M., Douet, J., Comella, P., Matia, I., Chandrasekhara, C. et al. (2010) Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS Genetics, 6, e1001225.
Röser, M., Winterfeld, G., Grebenstein, B. & Hemleben, V. (2001) Molecular diversity and physical mapping of 5S rDNA in wild, and cultivated oat grasses (Poaceae: Aveneae). Molecular Phylogenetics and Evolution, 21, 198–217.
Rozas, J., Sanchez‐DelBarrio, J.C., Messeguer, X. & Rozas, R. (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497.
Sáez‐Vásquez, J. & Delseny, M. (2019) Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell, 31, 1945–1967.
Schilbert, H., Holzenkamp, K., Viehoever, P., Holtgräwe, D. & Möllers, C. (2023) Homoeologous non‐reciprocal translocation explains a major QTL for seed lignin content in oilseed rape (Brassica napus L.). Theoretical and Applied Genetics, 136, 172.
Schubert, I. & Kunzel, G. (1990) Position‐dependent nor activity in barley. Chromosoma, 99, 352–359.
Sergeeva, E.M., Shcherban, A.B., Adonina, I.G., Nesterov, M.A., Beletsky, A.V., Rakitin, A.L. et al. (2017) Fine organization of genomic regions tagged to the 5S rDNA locus of the bread wheat 5B chromosome. BMC Plant Biology, 17, 183.
Simon, L., Rabanal, F.A., Dubos, T., Oliver, C., Lauber, D., Poulet, A. et al. (2018) Genetic and epigenetic variation in 5S ribosomal RNA genes reveals genome dynamics in Arabidopsis thaliana. Nucleic Acids Research, 46, 3019–3033.
Sims, J., Sestini, G., Elgert, C., von Haeseler, A. & Schlogelhofer, P. (2021) Sequencing of the Arabidopsis NOR2 reveals its distinct organization and tissue‐specific rRNA ribosomal variants. Nature Communications, 12, 387.
Soga, E., Sugisaka, J., Watanabe, M. & Kudoh, H. (2021) Population differentiation in the leaf shape and growth form of Cardamine scutata Thunb. in tidal and non‐tidal habitats. Plant Species Biology, 36, 399–411.
Sun, F.J. & Caetano‐Anolles, G. (2009) The evolutionary history of the structure of 5S ribosomal RNA. Journal of Molecular Evolution, 69, 430–443.
Szymanski, M., Barciszewska, M.Z., Barciszewski, J. & Erdmann, V.A. (1999) 5S ribosomal RNA data bank. Nucleic Acids Research, 27, 158–160.
Szymanski, M., Barciszewska, M.Z., Erdmann, V.A. & Barciszewski, J. (2003) 5S rRNA: structure and interactions. The Biochemical Journal, 371, 641–651.
Tynkevich, Y.O., Shelyfist, A.Y., Kozub, L.V., Hemleben, V., Panchuk, I.I. & Volkov, R.A. (2022) 5S ribosomal DNA of genus Solanum: molecular organization, evolution, and taxonomy. Frontiers in Plant Science, 13, 852406.
Tynkevich, Y.O., Valin, M.O., Moysiyenko, I.I., Panchuk, I.I. & Volkov, R.A. (2023) 5S ribosomal DNA in the family Plumbaginaceae. Cytology and Genetics, 57, 524–537.
Vaillant, I., Tutois, S., Cuvillier, C., Schubert, I. & Tourmente, S. (2007) Regulation of Arabidopsis thaliana 5S rRNA genes. Plant & Cell Physiology, 48, 745–752.
Veitia, R.A., Bottani, S. & Birchler, J.A. (2013) Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends in Genetics, 29, 385–393.
Vizoso, M., Vierna, J., Gonzalez‐Tizon, A.M. & Martinez‐Lage, A. (2011) The 5S rDNA gene family in mollusks: characterization of transcriptional regulatory regions, prediction of secondary structures, and long‐term evolution, with special attention to Mytilidae mussels. The Journal of Heredity, 102, 433–447.
Volkov, R.A., Panchuk, I.I., Borisjuk, N.V., Hosiawa‐Baranska, M., Maluszynska, J. & Hemleben, V. (2017) Evolutional dynamics of 45S and 5S ribosomal DNA in ancient allohexaploid Atropa belladonna. BMC Plant Biology, 17, 21.
Volkov, R.A., Zanke, C., Panchuk, I.I. & Hemleben, V. (2001) Molecular evolution of 5S rDNA of Solanum species (sect. Petota): application for molecular phylogeny and breeding. Theoretical and Applied Genetics, 103, 1273–1282.
Wang, W., Wan, T., Becher, H., Kuderova, A., Leitch, I.J., Garcia, S., Leitch, A.R. & Kova?ík, A. (2018) Remarkable variation of ribosomal DNA organization and copy number in gnetophytes, a distinct lineage of gymnosperms. Annals of Botany, 123, 767-781.
Weiss‐Schneeweiss, H., Emadzade, K., Jang, T.‐S. & Schneeweiss, G. (2013) Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenetic and Genome Research, 140, 1727.
Zozomová‐Lihová, J., Krak, K., Mandáková, T., Shimizu, K.K., Spaniel, S., Vít, P. et al. (2014) Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy. Annals of Botany, 113, 817–830.
Zozomova‐Lihova, J., Mandáková, T., Kovarikova, A., Muhlhausen, A., Mummenhoff, K., Lysak, M.A. et al. (2014) When fathers are instant losers: homogenization of rDNA loci in recently formed Cardamine × schulzii trigenomic allopolyploid. The New Phytologist, 203, 1096–1108.
معلومات مُعتمدة: 20-28029S Grantová Agentura České Republiky; 22-16826S Grantová Agentura České Republiky; LM2018131 Czech Ministry of Education; MUNI/R/1268/2022 Masaryk University Grant Agency; CZ.02.01.01/00/22_008/0004581 ERDF Programme Johannes Amos Comenius
فهرسة مساهمة: Keywords: Cardamine; 35S rDNA; 5S rDNA; chromosome evolution; gene silencing; polyploidy; rRNA genes
المشرفين على المادة: 0 (RNA, Ribosomal, 5S)
0 (DNA, Ribosomal)
تواريخ الأحداث: Date Created: 20240605 Date Completed: 20240731 Latest Revision: 20240731
رمز التحديث: 20240731
DOI: 10.1111/tpj.16850
PMID: 38838061
قاعدة البيانات: MEDLINE
الوصف
تدمد:1365-313X
DOI:10.1111/tpj.16850