We propose that rDNA epigenetic expression patterns established even in F(1) hybrids have a material influence on the likely patterns of divergence of rDNA. It is the active rDNA units that are vulnerable to homogenization, which probably acts to reduce mutational load across the active array. Those rDNA units that are epigenetically silenced may be less vulnerable to sequence homogenization. Selection cannot act on these silenced genes, and they are likely to accumulate mutations and eventually be eliminated from the genome. It is likely that whole silenced arrays will be deleted in polyploids of 1 million years of age and older.
Summary• This paper establishes relationships between two aspects of ribosomal DNA (rDNA) biology: epigenetic silencing of rDNA loci; and homogenization leading to concerted evolution.• Here, we examined rDNA inheritance and expression patterns in three natural Nicotiana allopolyploids (closest living descendants of diploid parents are given), N. rustica (N. paniculata × N. undulata), N. tabacum (N. sylvestris × N. tomentosiformis) and N. arentsii (N. undulata × N. wigandioides), and synthetic F 1 hybrids and allopolyploids.• The extent of interlocus rDNA homogenization decreased in the direction N. arentsii > N. tabacum > N. rustica. The persistence of parental rDNA units in one of the subgenomes was associated with their transcription inactivity and likely heterochromatization. Of synthetic hybrids and polyploids only N. paniculata × N. undulata showed strong uniparental transcriptional silencing of rDNA triggered already in F 1 .• Epigenetic patterns of expression established early in allopolyploid nucleus formation may render units susceptible or resistant to homogenization over longer time-frames. We propose that nucleolus-associated transcription leaves rDNA units vulnerable to homogenization, while epigenetically inactivated units, wellseparated from the nucleolus, remain unconverted.
SUMMARY
Histone chaperones mediate the assembly and disassembly of nucleosomes and participate in essentially all DNA‐dependent cellular processes. In Arabidopsis thaliana, loss‐of‐function of FAS1 or FAS2 subunits of the H3‐H4 histone chaperone complex CHROMATIN ASSEMBLY FACTOR 1 (CAF‐1) has a dramatic effect on plant morphology, growth and overall fitness. CAF‐1 dysfunction can lead to altered chromatin compaction, systematic loss of repetitive elements or increased DNA damage, clearly demonstrating its severity. How chromatin composition is maintained without functional CAF‐1 remains elusive. Here we show that disruption of the H2A‐H2B histone chaperone NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1) suppresses the FAS1 loss‐of‐function phenotype. The quadruple mutant fas1 nap1;1 nap1;2 nap1;3 shows wild‐type growth, decreased sensitivity to genotoxic stress and suppression of telomere and 45S rDNA loss. Chromatin of fas1 nap1;1 nap1;2 nap1;3 plants is less accessible to micrococcal nuclease and the nuclear H3.1 and H3.3 histone pools change compared to fas1. Consistently, association between NAP1 and H3 occurs in the cytoplasm and nucleus in vivo in protoplasts. Altogether we show that NAP1 proteins play an essential role in DNA repair in fas1, which is coupled to nucleosome assembly through modulation of H3 levels in the nucleus.
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