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Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140 year old naturally established neo-allopolyploid monkeyflower

ABSTRACT: The importance and applications of polyploidy have long been recognized, from shaping the evolutionary success of flowering plants to improving agricultural productivity. Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant - having both retained more genes and being more highly expressed - a phenomenon termed subgenome dominance. How quickly one subgenome dominates within a newly formed polyploid, if immediate or after millions of years, and the genomic features that determine which genome dominates remain poorly understood. To investigate the rate of subgenome dominance emergence, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural less than 140 year old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and diploid progenitors (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of two divergent genomes and that subgenome expression dominance significantly increases over generations. Additionally, CHH methylation levels are significantly reduced in regions near genes and within transposons in the first generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and submissive subgenomes in the natural allopolyploid. Our analyses reveal that the subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following the hybridization. These findings not only provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events, but may also contribute to uncovering the mechanistic basis of heterosis and subgenomic dominance.

ORGANISM(S): Erythranthe lutea x Erythranthe guttata Erythranthe lutea Mimulus peregrinus Erythranthe guttata

PROVIDER: GSE95799 | GEO | 2018/05/23

REPOSITORIES: GEO

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Project description:Background: Polyploidy has long been recognized as an important mechanism in eukaryotes evolution. Recent studies have documented dynamic changes in plant polyploid gene expression, which reflects genomic and functional plasticity of duplicate genes and genomes in plants. Genomewide approaches in a variety of allopolyploids, mostly synthetics, reveal a trend of non-additive gene expression. The aim of the study was to document expression divergence between a relatively recently formed natural allopolyploid (Coffea arabica) and its ancestral parents (Coffea canephora and Coffea eugenioides) and to verify if the divergence was ‘environment-dependent’.Results: Employing a microarray platform designed against 15,522 unigenes, we assayed gene expression levels in allopolyploid and its two parental diploids. For each gene, we determined expression variation levels between the three species grown under two sets of temperature conditions (26-22°C/30-26°C). More than 35% of genes were differentially expressed in each comparison at both temperatures, except for ‘allopolyploid versus Canephora’ at the ‘hottest’ temperature where an unexpected low gene expression divergence (<9%) were observed. Genes were binned in categories: ‘no change’, ‘additivity’, ‘transgressive’ and ‘dominance’ (‘Canephora-like’ and ‘Eugenioides-like’). The totally new phenomenon revealed by our study was a drastic modification of proportions between the allopolyploid and its parents when environmental conditions were modified. At the ‘hottest’ temperature, we found a virtual disappearance of gene categories classed as ‘transgressive’, ‘Eugenioides-like dominance’ or ‘additivity’ and a major increase in genes classed in the ‘Canephora-like dominance’ category. At this set of growing conditions, we therefore found very high bias that suggested a phenomenon of ‘dominance’ of C. canephora transcription profile. The Canephora genome parental expression state seems exhibited in strong preference to the Eugenioides genome parental state. Conclusion: Our data constitute evidence for a transcription profile divergence between allopolyploid and its parental species, massively affected by environmental conditions. The parental origin of the transcription profiles was not consistently biased towards one parental species, but appeared to be affected by environmental conditions. This phenomenon indicates the plasticity of allopolyploids and might ultimately explain better adaptation to environmental conditions.

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Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140 year old naturally established neo-allopolyploid monkeyflower

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