Short- and long-term effects on growth and expression patterns in response to incubation temperatures in Senegalese sole

Abstract

In this study, the short-and long-term effects of embryo incubation temperatures (16, 18 and 20ºC) on development and growth of the flatfish Senegalese sole (Solea senegalensis) was determined by investigating the expression patterns of the epigenetic regulators DNA methyltransferases (dnmt) and histone 3 (H3) and genes belonging to the retinoic acid (RA), insulin-like growth factors (IGFs) and hypothalamic-pituitary-thyroid (HPT) axes. Results indicated that egg incubation temperature affected embryo development, but not survival, and incubation at 16ºC significantly delayed development. Coincident with these effects, levels of muscle-specific dnmt3aa transcripts and histone H3 protein levels were significantly different between the 16 and 20ºC groups at hatch. The larvae from eggs incubated at 20ºC relative to the 16ºC group had significantly higher transcript levels of four genes belonging to the HPT axis (trhr1a, tshr, thrb and dio2), four genes of the RA axis (aldh1a2, cyp26a1, rara2, rarg), igfbp1 and the glycolytic enzyme gapdh2. Taken together the data suggest that higher egg incubation temperatures enhance energy production, which accelerates cell proliferation and larval development and that hatching is a key moment for the regulation of epigenetic mechanisms.Long-term effects of egg and larval incubation temperatures were revealed by a higher mRNA abundance of the thyroid-related genes tgb and tpo and the RA degrading enzyme cyp26a1 in preand metamorphic larvae when they were incubated at 20ºC as embryos and may be related to the earlier initiation of metamorphosis in the pelagic larval stages. Evaluation of growth in pelagic larvae and juveniles after weaning (one trial from 42 to 119 and another from 164 to 247 days post-hatch using a longitudinal approach) revealed that juveniles from embryos incubated at 20ºC had a higher growth rate. All these data demonstrate that the thermal regime during embryogenesis modulated mechanisms that regulate larval plasticity and caused imprinting evident in juvenile sole as persistent changes in key endocrinological pathways and growth performance.

Genomic and phylogenetic analysis of choriolysins, and biological activity of hatching liquid in the flatfish Senegalese sole

“…Embryos at the onset of the trials were in gastrula stage (50% epiboly) and they were incubated at 20°C and at an initial density of 2,000 embryo L -1 . Developmental stages were monitored on the microscope before samplings following the classification previously reported [16]. In the first trial, a total of 100 embryos were sampled in pharyngula at 6 h and 1 h before hatching, just at hatch and at 6 h and 26 h post-hatch.…”

“…1 μg of total RNA was reverse-transcribed using an iScript™ cDNA Synthesis kit (Bio-Rad) according to the manufacturer's protocol. In the case of embryo and larvae incubated at different temperatures, total RNA (2 μg) from each sample was reverse-transcribed using the High Capacity cDNA Reverse Transcription Kit (Life Technologies) as previously described for openarray analysis [16, 26].…”

“…The Senegalese sole is a valuable flatfish mainly produced in Southern Europe but with markets worldwide [13, 14]. This species spawns mainly in spring releasing high amounts of small eggs (<1 mm) that hatch in 24 hours if incubated at 20°C [15, 16]. The manipulation thermal regimes during embryonic stages to epigenetically reprogram growth performance is a new practice in hatchery procedures [16–18] but a better knowledge of mechanisms controlling hatching are required to refine and improve larval survival.…”

“…This species spawns mainly in spring releasing high amounts of small eggs (<1 mm) that hatch in 24 hours if incubated at 20°C [15, 16]. The manipulation thermal regimes during embryonic stages to epigenetically reprogram growth performance is a new practice in hatchery procedures [16–18] but a better knowledge of mechanisms controlling hatching are required to refine and improve larval survival. Moreover, proteases, are being used in cosmetics as skin cleansing agents for moisturization and improvements in skin surface characteristics and appearance and for the reduction of cutaneous inflammation.…”

Thermal conditions during embryogenesis influence metabolic rates of juvenile brown trout Salmo trutta

“…Variation in routine metabolism of the fish differed with acclimation temperature, which may indicate a phenotypic response in metabolic rate to temperatures experienced earlier in life. Furthermore, temperature during the embryo stage affects body growth of juveniles, as found for Atlantic salmon Salmo salar Jonsson 2012, Burgerhout et al 2017) and Senegal sole Solea senegalensis (Carballo et al 2018). Thus, there is reason to believe that temperature during early development affects metabolic rates and the scope for activity of fish later in life.…”