Effect of triploidy on liver gene expression in coho salmon (Oncorhynchus kisutch) under different metabolic states

Abstract

Background Triploid coho salmon are excellent models for studying gene dosage and the effects of increased cell volume on gene expression. Triploids have an additional haploid genome in each cell and have fewer but larger cells than diploid coho salmon to accommodate the increased genome size. Studying gene expression in triploid coho salmon provides insight into how gene expression may have been affected after the salmonid-specific genome duplication which occurred some 90 MYA. Triploid coho salmon are sterile and consequently can live longer and grow larger than diploid congeners in many semelparous species (spawning only once) because they never reach maturity and post-spawning mortality is averted. Triploid fishes are also of interest to the commercial sector (larger fish are more valuable) and to fisheries management since sterile fish can potentially minimize negative impacts of escaped fish in the wild. Results The vast majority of genes in liver tissue had similar expression levels between diploid and triploid coho salmon, indicating that the same amount of mRNA transcripts were being produced per gene copy (positive gene dosage effects) within a larger volume cell. Several genes related to nutrition and compensatory growth were differentially expressed between diploid and triploid salmon, indicating that some loci are sensitive to cell size and/or DNA content per cell. To examine how robust expression between ploidies is under different conditions, a genetic/metabolic modifier in the form of different doses of a growth hormone transgene was used to assess gene expression under conditions that the genome has not naturally experienced or adapted to. While many (up to 1400) genes were differentially expressed between non-transgenic and transgenic fish, relatively few genes were differentially expressed between diploids and triploids with similar doses of the transgene. These observations indicate that the small effect of ploidy on gene expression is robust to large changes in physiological state. Conclusions These findings are of interest from a gene regulatory perspective, but also valuable for understanding phenotypic effects in triploids, transgenics, and triploid transgenics that could affect their utility in culture conditions and their fitness and potential consequences of release into nature. Electronic supplementary material The online version of this article (10.1186/s12864-019-5655-8) contains supplementary material, which is available to authorized users.

Transcriptome sequencing and histology reveal dosage compensation in the liver of triploid pre-smolt Atlantic salmon

“…Overall, these quantitative histological findings validate the use of liver as central organ regulating energy metabolism and several other functions to assess the possibility of dosage compensation in our study. This is in line with the work of Christensen et al 50 where liver tissue was chosen to measure gene expression levels in coho salmon under different metabolic states.…”

Telomerase Activity in Somatic Tissues and Ovaries of Diploid and Triploid Rainbow Trout (Oncorhynchus mykiss) Females

“…Despite the large cellular architecture and physiological differences between triploids and diploids, the effect of triploidy on gene expression is surprisingly smaller than expected, as triploid and diploid fish have usually comparable levels of expression in their somatic tissues (a dosage compensation phenomenon) [ 60 , 61 , 62 , 63 , 64 , 65 ]. Only a small number of genes may be subjected to both positive and negative dosage compensation in triploid fish [ 66 ].…”

Early, nonlethal ploidy and genome size quantification using confocal microscopy in zebrafish embryos

“…Nuclei with more tightly packed DNA (i.e., more heterochromatin) would likely appear smaller using this technique than would a nucleus with an equal amount of DNA but with more euchromatin. Gene expression studies have found differences between diploids and triploids under demanding conditions (Ching et al, 2010; Christensen et al, 2019; Van de Pol et al, 2020), but we are unaware of studies comparing the general amount and rate of transcription between ploidies. If there are differences in the ratio of heterochromatin to euchromatin in some myofiber nuclei, this could explain the broader range of nuclear volumes observed in triploids.…”

“…Investigations into the evolution of genome size have revealed a pattern: the amount of DNA in the nucleus correlates with the volume of the nucleus and the cell itself (Gregory, 2001; Levy & Heald, 2010), a pattern that holds true across tissues and taxa for eukaryotic cells (Cavalier‐Smith, 1978; Gillooly et al, 2015; Gregory, 2002). Understanding the mechanism(s) linking nucleus volume and cell volume to the amount of nuclear DNA is a long‐standing goal in fields of biology as diverse as cell biology (Ginzberg et al, 2015; Neurohr et al, 2019; Turner et al, 2012), development (Levy & Heald, 2010; Miller et al, 2020; Roth & Walkowiak, 2015), physiology (Benfey, 1999; Christensen et al, 2019; Saranyan et al, 2017), and evolutionary biology (Elliott & Gregory, 2015; Mueller, 2015; Otto, 2007; Smith & Gregory, 2009).…”