Gene expression regulation and lineage evolution: the North and South tale of the hybrid polyploidSqualius alburnoidescomplex

Abstract

The evolution of hybrid polyploid vertebrates, their viability and their perpetuation over evolutionary time have always been questions of great interest. However, little is known about the impact of hybridization and polyploidization on the regulatory networks that guarantee the appropriate quantitative and qualitative gene expression programme. The Squalius alburnoides complex of hybrid fish is an attractive system to address these questions, as it includes a wide variety of diploid and polyploid forms, and intricate systems of genetic exchange. Through the study of genome-specific allele expression of seven housekeeping and tissue-specific genes, we found that a gene copy silencing mechanism of dosage compensation exists throughout the distribution range of the complex. Here we show that the allele-specific patterns of silencing vary within the complex, according to the geographical origin and the type of genome involved in the hybridization process. In southern populations, triploids of S. alburnoides show an overall tendency for silencing the allele from the minority genome, while northern population polyploids exhibit preferential biallelic gene expression patterns, irrespective of genomic composition. The present findings further suggest that gene copy silencing and variable expression of specific allele combinations may be important processes in vertebrate polyploid evolution.

Polyploidy in Animals: Effects of Gene Expression on Sex Determination, Evolution and Ecology

“…In contrast, northern triploid hybrid fish containing a C allele showed bi-allelic expression of C and A alleles. This demonstrates environmental effects on hybrid gene expression, but may also reflect differential interaction of hybridizing genomes [Pala et al, 2010].…”

“…Pala et al [2008Pala et al [ , 2010 demonstrated that for southern triploid PAA hybrid fish predominantly the A allele was expressed. In contrast, northern triploid hybrid fish containing a C allele showed bi-allelic expression of C and A alleles.…”

Gene copy silencing and DNA methylation in natural and artificially produced allopolyploid fish

“…It has been previously shown (Pala et al, 2010) that the patterns of gene expression in triploid S. alburnoides depend on the genomic contexts brought about by different parental contributions. For instance, the presence of c or p genomes in allopolyploid S. alburnoides biotypes results in substantial difference in genome-specific allele usage in either paa or caa genomic contexts (Pala et al, 2010).…”

“…It has been previously shown (Pala et al, 2010) that the patterns of gene expression in triploid S. alburnoides depend on the genomic contexts brought about by different parental contributions. For instance, the presence of c or p genomes in allopolyploid S. alburnoides biotypes results in substantial difference in genome-specific allele usage in either paa or caa genomic contexts (Pala et al, 2010). Because the effect of the q genome to the overall gene expression in natural occurring S. alburnoides of qaa and qqa genomotypes has never been assessed, the absence of AS in the TGH fish with one q haplome is difficult to assess, and the effects of the presence of the q genome are difficult to infer.…”

“…However, it remained unclear whether the silencing mechanism reported for triploid S. alburnoides, which is very frequent among both natural and synthesized allopolyploid plants (Adams et al, 2003), was also a common mechanism in allopolyploid vertebrates. A further restriction for generalization is that the allotriploid S. alburnoides analyzed so far were all carriers of a duplicated genomic set from one parental species and an unpaired genomic set from another parental species: paa and ppa in southern populations, and cca and caa in northern populations, where S. pyrenaicus is absent and is replaced by Squalius carolitertii (contributing the c genome) (Pala et al, 2008(Pala et al, , 2010. This situation did not allow the exclusion of monoallelic expression in those cases where the minority genome was not expressed.…”