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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Plant Sci. | doi: 10.3389/fpls.2019.01066

Unique epigenetic features of ribosomal RNA genes (rDNA) in early diverging plants (bryophytes)

Roman Matyasek1, Alice Krumpolcova1, Jana Lunerova1, Eva Mikulaskova2, Josep Rossello3 and  Ales Kovarik1*
  • 1Institute of Biophysics, Academy of Sciences of the Czech Republic, Czechia
  • 2Masaryk University, Czechia
  • 3University of Valencia, Spain

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 in situ hybridization (FISH) and immunoprecipitation (CHIP) assays.

Results: In contrast to seed plants, bryophytes 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 non-coding 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 to 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 which exist in haploid state for most of their life cycles.

Keywords: rDNA, cytosine methylation, Bryophytes, epigenetics, histone marks, genome evolution

Received: 11 Mar 2019; Accepted: 06 Aug 2019.

Edited by:

Matthew A. Gitzendanner, University of Florida, United States

Reviewed by:

Andrea Pedrosa-Harand, Federal University of Pernambuco, Brazil
Xiaoxian Liu, Lawrence Berkeley National Laboratory, United States  

Copyright: © 2019 Matyasek, Krumpolcova, Lunerova, Mikulaskova, Rossello and Kovarik. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Ales Kovarik, Institute of Biophysics, Academy of Sciences of the Czech Republic, Brno, 612 65, South Moravia, Czechia, kovarik@ibp.cz