Homoeolog expression bias in allopolyploid oleaginous marine diatom Fistulifera solaris

Abstract

BackgroundAllopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adaptability and increased crop productivity. We previously reported the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to be a promising host for biofuel production and that its genome is allopolyploid, which had never previously been reported in eukaryotic microalgae. However, the study of allopolyploidy in F. solaris was hindered by the difficulty in classifying the homoeologous genes based on their progenitor origins, owing to the shortage of diatom genomic references.ResultsIn this study, the allopolyploid genome of F. solaris was tentatively classified into two pseudo-parental subgenomes using sequence analysis based on GC content and codon frequency in each homoeologous gene pair. This approach clearly separated the genome into two distinct fractions, subgenome Fso_h and Fso_l, which also showed the potency of codon usage analysis to differentiate the allopolyploid subgenome. Subsequent homoeolog expression bias analysis revealed that, although both subgenomes appear to contribute to global transcription, there were subgenomic preferences in approximately 61% of homoeologous gene pairs, and the majority of these genes showed continuous bias towards a specific subgenome during lipid accumulation. Additional promoter analysis indicated the possibility of promoter motifs involved in biased transcription of homoeologous genes. Among these subgenomic preferences, genes involved in lipid metabolic pathways showed interesting patterns in that biosynthetic and degradative pathways showed opposite subgenomic preferences, suggesting the possibility that the oleaginous characteristics of F. solaris derived from one of its progenitors.ConclusionsWe report the detailed genomic structure and expression patterns in the allopolyploid eukaryotic microalga F. solaris. The allele-specific patterns reported may contribute to the oleaginous characteristics of F. solaris and also suggest the robust oleaginous characteristics of one of its progenitors. Our data reveal novel aspects of allopolyploidy in a diatom that is not only important for evolutionary studies but may also be advantageous for biofuel production in microalgae.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4691-0) contains supplementary material, which is available to authorized users.

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

“…The possibility that aASE could be involved in adaptation still faces the question of the clonal heterogeneity of this cellular response (being epigenetic or genetic by nature). This was not ruled out by the studies reported in either F. cylindrus 27 or F. solaris 28 . We thus strongly suggest that any experiments evaluating the impact of aASE upon changing environments in diatoms should be interpreted with care in several sub-populations of clonally isolated cells for genes with AEB > 60%.…”

“…Around 66% of these genes showed allelic imbalance in at least one experiment, strongly suggesting that allelic imbalance results from species adaptation to new environments. In diatoms, homoeologous gene expression bias (HEB) was furthermore described in the allodiploid and highly oleaginous diatom Fistulifera solaris 28 . In this naturally occurring hybrid species, HEB is widespread with 61% of homoeologous genes showing differential expression (expressed allele ratios > 2).…”

Integrative Omics Analysis Reveals a Limited Transcriptional Shock After Yeast Interspecies Hybridization

“…The study of the allelic imbalance of a synthetic hexaploid wheat showed that 24.1% of the identified homeologous genes were imbalanced in the hybrid, and this difference in expression could not be attributed to preexisting expression divergence between the parentals (Li et al, 2014). Finally, a recent study on the diatom microalgae Fistulifera solaris showed that ∼61% of homeologous genes displayed allelic imbalance (Nomaguchi et al, 2018).…”

Genome-wide analysis of the HSP101/CLPB gene family for heat tolerance in hexaploid wheat

“…Homoeolog expression bias is unequal expression among the homoeologs at different tissues or developmental stages; or as anomaly of their expression level relative to their diploid progenitors 47,49 . Subgenomic preferences have been reported in octoploid strawberry with a single subgenome exhibited significant dominance in gene expression and control of certain metabolomic and disease resistance traits 50 . Contribution of homoeolog expression dominance in facilitating selection of glucosinolate and lipid metabolism genes was also reported in the vegetable-use and oil-use sub-varieties of Brassica juncea 51 .…”