Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes)
Introduction: In plants, the multicopy genes encoding ribosomal RNA (rDNA) typically exhibit heterochromatic features and high level of DNA methylation. Here, we explored rDNA methylation in early diverging land plants from Bryophyta (15 species, 14 families) and Marchantiophyta (4 species, 4 famili...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-09-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2019.01066/full |
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| author | Roman Matyášek Alice Krumpolcová Jana Lunerová Eva Mikulášková Josep A. Rosselló Aleš Kovařík |
| author_facet | Roman Matyášek Alice Krumpolcová Jana Lunerová Eva Mikulášková Josep A. Rosselló Aleš Kovařík |
| author_sort | Roman Matyášek |
| collection | DOAJ |
| description | Introduction: In plants, the multicopy genes encoding ribosomal RNA (rDNA) typically exhibit heterochromatic features and high level of DNA methylation. Here, we explored rDNA methylation in early diverging land plants from Bryophyta (15 species, 14 families) and Marchantiophyta (4 species, 4 families). DNA methylation was investigated by methylation-sensitive Southern blot hybridization in all species. We also carried out whole genomic bisulfite sequencing in Polytrichum formosum (Polytrichaceae) and Dicranum scoparium (Dicranaceae) and used available model plant methyloms (Physcomitrella patents and Marchantia polymorpha) to determine rDNA unit-wide methylation patterns. Chromatin structure was analyzed using fluorescence in situ hybridization (FISH) and immunoprecipitation (CHIP) assays.Results: In contrast to seed plants, bryophyte rDNAs were efficiently digested with methylation-sensitive enzymes indicating no or low levels of CG and CHG methylation in these loci. The rDNA methylom analyses revealed variation between species ranging from negligible (<3%, P. formosum, P. patens) to moderate (7 and 17% in M. polymorpha and D. scoparium, respectively) methylation levels. There were no differences between coding and noncoding parts of rDNA units and between gametophyte and sporophyte tissues. However, major satellite repeat and transposable elements were heavily methylated in P. formosum and D. scoparium. In P. formosum rDNA, the euchromatic H3K4m3 and heterochromatic H3K9m2 histone marks were nearly balanced contrasting the angiosperms data where H3K9m2 typically dominates rDNA chromatin. In moss interphase nuclei, rDNA was localized at the nucleolar periphery and its condensation level was high.Conclusions: Unlike seed plants, the rRNA genes seem to escape global methylation machinery in bryophytes. Distinct epigenetic features may be related to rDNA expression and the physiology of these early diverging plants that exist in haploid state for most of their life cycles. |
| first_indexed | 2024-12-23T05:59:56Z |
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| id | doaj.art-cdf2b61ffd224d90ae43b1b73921e677 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-23T05:59:56Z |
| publishDate | 2019-09-01 |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-cdf2b61ffd224d90ae43b1b73921e6772022-12-21T17:57:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-09-011010.3389/fpls.2019.01066459414Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes)Roman Matyášek0Alice Krumpolcová1Jana Lunerová2Eva Mikulášková3Josep A. Rosselló4Aleš Kovařík5Department of Molecular Epigenetics, Institute of Biophysics of the Czech Academy of Sciences, Institute of Biophysics of the Czech Academy of Sciences, Brno, CzechiaDepartment of Molecular Epigenetics, Institute of Biophysics of the Czech Academy of Sciences, Institute of Biophysics of the Czech Academy of Sciences, Brno, CzechiaDepartment of Molecular Epigenetics, Institute of Biophysics of the Czech Academy of Sciences, Institute of Biophysics of the Czech Academy of Sciences, Brno, CzechiaDepartment of Botany and Zoology, Masaryk University, Brno, CzechiaJardín Botánico, ICBiBE-Unidad Asociada CSIC, Universidad de Valencia, Valencia, SpainDepartment of Molecular Epigenetics, Institute of Biophysics of the Czech Academy of Sciences, Institute of Biophysics of the Czech Academy of Sciences, Brno, CzechiaIntroduction: In plants, the multicopy genes encoding ribosomal RNA (rDNA) typically exhibit heterochromatic features and high level of DNA methylation. Here, we explored rDNA methylation in early diverging land plants from Bryophyta (15 species, 14 families) and Marchantiophyta (4 species, 4 families). DNA methylation was investigated by methylation-sensitive Southern blot hybridization in all species. We also carried out whole genomic bisulfite sequencing in Polytrichum formosum (Polytrichaceae) and Dicranum scoparium (Dicranaceae) and used available model plant methyloms (Physcomitrella patents and Marchantia polymorpha) to determine rDNA unit-wide methylation patterns. Chromatin structure was analyzed using fluorescence in situ hybridization (FISH) and immunoprecipitation (CHIP) assays.Results: In contrast to seed plants, bryophyte rDNAs were efficiently digested with methylation-sensitive enzymes indicating no or low levels of CG and CHG methylation in these loci. The rDNA methylom analyses revealed variation between species ranging from negligible (<3%, P. formosum, P. patens) to moderate (7 and 17% in M. polymorpha and D. scoparium, respectively) methylation levels. There were no differences between coding and noncoding parts of rDNA units and between gametophyte and sporophyte tissues. However, major satellite repeat and transposable elements were heavily methylated in P. formosum and D. scoparium. In P. formosum rDNA, the euchromatic H3K4m3 and heterochromatic H3K9m2 histone marks were nearly balanced contrasting the angiosperms data where H3K9m2 typically dominates rDNA chromatin. In moss interphase nuclei, rDNA was localized at the nucleolar periphery and its condensation level was high.Conclusions: Unlike seed plants, the rRNA genes seem to escape global methylation machinery in bryophytes. Distinct epigenetic features may be related to rDNA expression and the physiology of these early diverging plants that exist in haploid state for most of their life cycles.https://www.frontiersin.org/article/10.3389/fpls.2019.01066/fullrDNAcytosine methylationbryophytesepigeneticshistone marksgenome evolution |
| spellingShingle | Roman Matyášek Alice Krumpolcová Jana Lunerová Eva Mikulášková Josep A. Rosselló Aleš Kovařík Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) Frontiers in Plant Science rDNA cytosine methylation bryophytes epigenetics histone marks genome evolution |
| title | Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) |
| title_full | Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) |
| title_fullStr | Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) |
| title_full_unstemmed | Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) |
| title_short | Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes) |
| title_sort | unique epigenetic features of ribosomal rna genes rdna in early diverging plants bryophytes |
| topic | rDNA cytosine methylation bryophytes epigenetics histone marks genome evolution |
| url | https://www.frontiersin.org/article/10.3389/fpls.2019.01066/full |
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