Nucleolar dominance arises in Spartina homoploid hybrids and persists after allopolyploidization

TL;DR

This study shows that nucleolar dominance, an epigenetic phenomenon, is present in hybrid Spartina plants and persists even after becoming a new allopolyploid species.

Contribution

The study demonstrates that nucleolar dominance is already established in homoploid hybrids and is maintained in the allopolyploid Spartina anglica.

Findings

Nucleolar dominance favors rDNA inherited from S. alterniflora in all hybrid and allopolyploid Spartina individuals.

Silenced S. maritima-inherited rDNA shows hypermethylation at M-loci.

Only 2% of S. anglica individuals have completely lost M-loci, indicating rapid rDNA diploidization.

Abstract

Allopolyploid Spartina anglica C.E. Hubbard (2n = 120–124) has become recognized as a model system of recent allopolyploid speciation. It arose by interspecific hybridization between S. alterniflora (2n = 62) introduced from North America and the native European S. maritima (2n = 60) about 150 years ago. In addition, sterile first‐generation homoploid hybrids S. × townsendii and S. × neyrautii (both 2n = 62) are still extant. In this study, we carried out a population‐level study of epigenetic silencing of 35S rDNA loci, also known as nucleolar dominance. Using molecular, genomic, and cytogenetic methods, we analyzed 75 individuals of S. anglica (collected from 11 French populations and 5 UK populations), 34 individuals of S. × townsendii (3 populations, all from the UK), and 2 individuals of S. × neyrautii from the south of France. We observed strong transcriptional dominance of S. alterniflora‐inherited rDNA in all hybrid and allopolyploid individuals. The dominant rDNA units were nearly devoid of methylation at CWG sites, in contrast to those of the silenced S. maritima‐inherited rDNA (M‐loci), which exhibited hypermethylation. At the DNA level, few (2%) S. anglica individuals have completely lost M‐loci, indicating that rDNA diploidization proceeds extremely fast in Spartina, and such a process may be influenced by preceding epigenetic processes. We conclude that nucleolar dominance is already present in extant homoploid hybrid lineages and is largely maintained in S. anglica, with occasional partial relaxation.

Evolution of nucleolar dominance in Spartina anglica since its origin c. 150 years ago. mC, cytosine methylation; NOR, nucleolar organizer regions. rDNA resides within the NORs.

Spartina anglica C.E. Hubbard presents an iconic allopolyploid species that formed only 150 years ago, spreading worldwide since then. The availability of homoploid hybrids and derived allopolyploids enabled the assessment of the immediate impacts of allopolyploidy on the genome. We showed that the homoploid hybrids present at the site of the initial hybridization event exhibit strong uniparental silencing of rDNA. Thus, subsequent diploidization processes seem to preferentially act on epigenetically modified genomic regions.

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