Multigenic Delineation of Lower Jaw Deformity in Triploid Atlantic Salmon (Salmo salar L.)

Abstract

Lower jaw deformity (LJD) is a skeletal anomaly affecting farmed triploid Atlantic salmon (Salmo salar L.) which leads to considerable economic losses for industry and has animal welfare implications. The present study employed transcriptome analysis in parallel with real-time qPCR techniques to characterise for the first time the LJD condition in triploid Atlantic salmon juveniles using two independent sample sets: experimentally-sourced salmon (60 g) and commercially produced salmon (100 g). A total of eleven genes, some detected/identified through the transcriptome analysis (fbn2, gal and gphb5) and others previously determined to be related to skeletal physiology (alp, bmp4, col1a1, col2a1, fgf23, igf1, mmp13, ocn), were tested in the two independent sample sets. Gphb5, a recently discovered hormone, was significantly (P < 0.05) down-regulated in LJD affected fish in both sample sets, suggesting a possible hormonal involvement. In-situ hybridization detected gphb5 expression in oral epithelium, teeth and skin of the lower jaw. Col2a1 showed the same consistent significant (P < 0.05) down-regulation in LJD suggesting a possible cartilaginous impairment as a distinctive feature of the condition. Significant (P < 0.05) differential expression of other genes found in either one or the other sample set highlighted the possible effect of stage of development or condition progression on transcription and showed that anomalous bone development, likely driven by cartilage impairment, is more evident at larger fish sizes. The present study improved our understanding of LJD suggesting that a cartilage impairment likely underlies the condition and col2a1 may be a marker. In addition, the involvement of gphb5 urges further investigation of a hormonal role in LJD and skeletal physiology in general.

A temperature shift during embryogenesis impacts prevalence of deformity in diploid and triploid Atlantic salmon (Salmo salarL.)

“…This would support the findings of Amoroso, et al. (2016) who linked temperature induced LJD with cartilage impairment rather than disruption of ECM mineralization directly. Amoroso, et al.…”

“…Lower temperatures may reduce skeletal abnormalities in salmon. Recent studies have shown a correlation between higher temperatures, low survival and increased prevalence of jaw (Amoroso, et al., 2016; Amoroso, et al., 2016; Fraser et al., 2015) and vertebral (Vågsholm & Djupvik, 1998; Wargelius et al., 2005; Ytteborg et al., 2010) deformities. There is little known about the underlying mechanisms of skeletal abnormalities as a result of elevated temperatures; however, it has been suggested that increased muscle mass is poorly supported by under‐mineralized bone found in faster growing salmon (Fjelldal et al., 2006).…”

“…However, no studies to date have investigated how temperature changes during embryogenesis may affect survival and growth performance of triploid salmon. Further, bone regulatory mechanism discussions, specific to triploid salmon, are limited to later life stages (Amoroso, et al., 2016; Fjelldal et al., 2015; Smedley et al., 2018; Vera et al., 2019) and results during embryogenesis have not yet been reported. Ytteborg, et al.…”

Impact of dietary phosphorous in diploid and triploid Atlantic salmon (Salmo salar L.) with reference to early skeletal development in freshwater

“…Conversely, in our study, no differences in fgf23 expression were observed between ploidy or dietary P at smolt, however, levels of expression were significantly higher than at parr stages. Similarly, Amoroso et al (2016b) also found no change in fgf23 between normal jaw and LJD affected triploid smolts. Collectively, this may suggest that early life stages (i.e.…”

“…In this respect, dietary P deficiency during freshwater grow-out may further exacerbate already pre-existing jaw malformation in triploids. Furthermore, Amoroso et al (2016b) also demonstrated cartilage impairment and associated gene ( col2a1 ) downregulation in LJD affected triploids, and that prevalence of LJD was greater in triploids experiencing higher water temperatures during ongrowing ( Amoroso et al, 2016a ). Thus, given bone that mineral content of the jaw was not different between diets in this study, this supports the hypothesis that dietary minerals may be sufficient for jaw formation, but that cartilage impairment of the lower jaw formation, particularly in response to rearing temperature, is the primary cause of jaw malformation through incorrect architectural arrangement.…”