Allele-specific expression variation at different ploidy levels in Squalius alburnoides

Isa Matos,Miguel P Machado,Manfred Schartl,Maria Manuela Coelho

doi:10.1038/s41598-019-40210-8

Abstract

Allopolyploid plants are long known to be subject to a homoeolog expression bias of varying degree. The same phenomenon was only much later suspected to occur also in animals based on studies of single selected genes in an allopolyploid vertebrate, the Iberian fish Squalius alburnoides. Consequently, this species became a good model for understanding the evolution of gene expression regulation in polyploid vertebrates. Here, we analyzed for the first time genome-wide allele-specific expression data from diploid and triploid hybrids of S. alburnoides and compared homoeolog expression profiles of adult livers and of juveniles. Co-expression of alleles from both parental genomic types was observed for the majority of genes, but with marked homoeolog expression bias, suggesting homoeolog specific reshaping of expression level patterns in hybrids. Complete silencing of one allele was also observed irrespective of ploidy level, but not transcriptome wide as previously speculated. Instead, it was found only in a restricted number of genes, particularly ones with functions related to mitochondria and ribosomes. This leads us to hypothesize that allelic silencing may be a way to overcome intergenomic gene expression interaction conflicts, and that homoeolog expression bias may be an important mechanism in the achievement of sustainable genomic interactions, mandatory to the success of allopolyploid systems, as in S. alburnoides.

Highlights

By the classical Mendelian rules of inheritance for traits with intermediate phenotypes an equal contribution from the maternally and paternally inherited alleles to the overall expression was the intuitive solution
We first considered single-nucleotide variants (SNV’s) for homoeolog specific expression (HSE) quantification in liver tissue and used 2807 single-nucleotide polymorphisms (SNPs) in liv-PA, distributed over 1121 transcripts, and 2305 SNPs in liv-PAA distributed over 937 transcripts
We found for liv-PA 764 of 1121 transcripts (68%) with balanced homoeolog expression and 357 transcripts (32%) showing strong homoeolog expression bias (Table 1)

Summary

Introduction

By the classical Mendelian rules of inheritance for traits with intermediate phenotypes an equal contribution from the maternally and paternally inherited alleles to the overall expression was the intuitive solution. The same phenomenon was only much later described in a vertebrate organism[16,17], the allopolyploid teleost fish S. alburnoides complex. The allopolyploid cyprinid Squalius alburnoides is a freshwater fish endemic from the Iberian Peninsula It resulted from interspecific hybridization between females of Squalius pyrenaicus (PP genome) and males of an already extinct species belonging to the Anaecypris hispanica lineage (AA genome) (Fig. 1a). Based on the analysis of a set of 7 genes, it was shown that a gene-regulatory mechanism involving allelic silencing (AS), which is the most extreme case of HEB, contributes to the regulation of gene expression in allotriploid S. alburnoides individuals. In addition to the phenomenon of AS, gene expression dosage compensation was described to occur in S. alburnoides, reducing the allotriploid expression levels to the same levels of the hybrid diploid counterparts[16,17,21]. A more detailed knowledge on how expression regulation occurs at the whole genome level in this allopolyploid species was necessary

Methods

Results

Conclusion