Genome-wide analysis of allele-specific expression of genes in the model diatom Phaeodactylum tricornutum

Antoine Hoguin,Leila Tirichine,Chris Bowler,Achal Rastogi

doi:10.1038/s41598-021-82529-1

Abstract

Recent advances in next generation sequencing technologies have allowed the discovery of widespread autosomal allele-specific expression (aASE) in mammals and plants with potential phenotypic effects. Extensive numbers of genes with allele-specific expression have been described in the diatom Fragilariopsis cylindrus in association with adaptation to external cues, as well as in Fistulifera solaris in the context of natural hybridization. However, the role of aASE and its extent in diatoms remain elusive. In this study, we investigate allele-specific expression in the model diatom Phaeodactylum tricornutum by the re-analysis of previously published whole genome RNA sequencing data and polymorphism calling. We found that 22% of P. tricornutum genes show moderate bias in allelic expression while 1% show nearly complete monoallelic expression. Biallelic expression associates with genes encoding components of protein metabolism while moderately biased genes associate with functions in catabolism and protein transport. We validated candidate genes by pyrosequencing and found that moderate biases in allelic expression were less stable than monoallelically expressed genes that showed consistent bias upon experimental validations at the population level and in subcloning experiments. Our approach provides the basis for the analysis of aASE in P. tricornutum and could be routinely implemented to test for variations in allele expression under different environmental conditions.

Highlights

Allele-specific expression (ASE) of genes refers to transcriptional imbalance between alleles in non-haploid organisms
It has been hypothesized to provide an advantage over haploid algal genomes for fine tuning gene expression in response to environmental triggers. autosomal allele-specific expression (aASE) was first reported in the polar diatom Fragilariopsis cylindrus[27]
In a recent study that compared whole genome sequences (WGS) of different ecotypes of the model pennate diatom Phaeodactylum tricornutum, we revealed an extensive map of polymorphic sites clustering ecotypes in different haplotypes[29]

Summary

Introduction

Allele-specific expression (ASE) of genes refers to transcriptional imbalance between alleles in non-haploid organisms. Female cells epigenetically inactivate the paternal or maternal X-chromosome in a stochastic manner resulting in a paternal or maternal monoallelic expression of most X-linked g enes[2,3]. This process equilibrates X-chromosome gene dosage between hemizygote males and females. We found that strong allelic expression bias was scarce (1% of genes) but stable in P. tricornutum while 22% of genes displayed more pervasive and less stringent allelespecific expression patterns in standard culture conditions These results provide a methodology for interpreting the consequences of aASE in this ecologically important group of organisms. Our work can be extended as well to other species of the Stramenopile group of eukaryotes to which diatoms belong, which includes numerous other lineages of phytoplankton as well as important plant pathogens

Results

Discussion

Conclusion