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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.

Project description:How allopolyploids are able not only to cope but profit from their condition is a question that remain elusive, but of great importance within the wide context of successful hybrid polyploid evolution. One outstanding example of successful allopolyploidy is the endemic Iberian S. alburnoides fish complex. Previously, based on the evaluation of 7 genes, it was reported that the transcription levels between diploid and triploid hybrid S. alburnoides were similar. If this phenomenon would occur on a full genomic scale, a wide functional diploidization could be related to the success of polyploids. We generated RNA-seq data from whole juvenile fish and from an adult tissue, to perform the first comparative quantitative transcriptomic analysis between ploidy levels of a vertebrate allopolyploid. We found 64% in juvenilesM-b full body samples and 44% in liver samples of similar expression between diploid and triploid hybrids, and those genes are mostly involved in processes of basal biological maintenance of the cells. Yet, respectively only 29% and 15% of transcripts presented accurate dosage compensation. Therefore, an exact functional diploidization of the triploid genome does not occur, but globally a significant down regulation of gene expression in triploids was observed. We find that for those genes which show similar expression levels in diploids and triploids, expression in triploids is not globally strictly proportional to gene dosage nor is it set to a perfect diploid level. This quantitative flexibility of expression may be a strong contributor to overcome the 'genomic shock', and be an immediate evolutionary advantage of allopolyploids. Genotypes: Squalius alburnoides is an allopolyploid cyprinid, resulting from interspecific hybridization between females of Squalius pyrenaicus (P genome) and males of a now extinct species related to Anaecypris hispanica (A genome). S. alburnoides natural populations arecomposed of animals of different ploidy levels and genomic constitutions (different genotypes). The predominant S. alburnoides complex intervenients in the Iberian Peninsula southern rivers are the hybrid triploid PAA, diploid PA, the parental-like diploid AA and the parental species S. pyrenaicus PP.

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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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