A transcriptomic investigation of appetite‐regulation and digestive processes in giant grouper Epinephelus lanceolatus during early larval development

Abstract

The giant grouper Epinephelus lanceolatus is an ecologically vulnerable species with high market demand. However, efforts to improve larval husbandry are hindered by a lack of knowledge surrounding larval developmental physiology. To address this shortfall, a transcriptomic approach was applied to larvae between 1 and 14 days post hatch (dph) to characterise the molecular ontogenesis of genes that influence appetite and digestion. Appetite regulating factors were detected from 1 dph, including neuropeptide Y, nesfatin-1, cocaine and amphetamine regulated transcript, cholecystokinin and pituitary adenylate cyclase activating peptide and the expression level of several genes changed sharply with the onset of exogenous feeding. The level of expression for proteases, chitinases, lipases and amylases typically followed one of two expression patterns, a general increase as development progressed, or an inverted U-shape with maximal expression at c. 6 dph. Similarly, the tendency among both expression patterns was for the level of expression to increase around the time of mouth-opening. There was also evidence to suggest the presence of putative isoforms for several digestion-related genes. We have provided an insight into appetite-regulation and digestive processes in groupers during early larval development and have developed a transcriptomic database that will aid future efforts to rear this species in an aquaculture setting.

Recent advances in neuropeptide-related omics and gene editing: Spotlight on NPY and somatostatin and their roles in growth and food intake of fish

“…In goldfish and zebrafish, Y1 antagonist BIBP3226 icv inhibits the orexigenic effects of NPY ( 16 , 192 ). ICV injection of Y1 agonist (Leu31, Pro34)-NPY and Y5 agonist (D-32Trp)-NPY promoted the food intake in goldfish, but neither the Y2 agonist NPY ( 2 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) nor the (Pro13, Tyr36)-NPY ( 13 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) has significant effect on feeding behaviors, suggesting that NPY receptors similar to mammalian Y1 and Y5 may be involved in feeding regulation in teleost ( 235 , 236 ). On the other hand, in rainbow trout, ICV injection of both the Y1 agonist (Leu31, Pro34)-NPY and the Y2 agonist NPY ( 3 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) stimulated food intake ( 208 ).…”

“…ICV injection of Y1 agonist (Leu31, Pro34)-NPY and Y5 agonist (D-32Trp)-NPY promoted the food intake in goldfish, but neither the Y2 agonist NPY ( 2 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) nor the (Pro13, Tyr36)-NPY ( 13 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) has significant effect on feeding behaviors, suggesting that NPY receptors similar to mammalian Y1 and Y5 may be involved in feeding regulation in teleost ( 235 , 236 ). On the other hand, in rainbow trout, ICV injection of both the Y1 agonist (Leu31, Pro34)-NPY and the Y2 agonist NPY ( 3 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) stimulated food intake ( 208 ). Recently, it is reported that ICV injection of Y1 agonist (Leu31, Pro34)-NPY and Y2 agonist NPY ( 13 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) both increased the appetite of Siberian sturgeon within 30 min ( 228 ).…”

“…The introduction of transcriptomics has helped the mechanistic exploration of neuropeptides at the RNA level and the network of interactions. NPY, SS, and CCK have been found to influence feeding behavior, and in recent years new evidence has been found in mammalian ( 24 ), avian ( 85 ), and fish species ( 27 , 29 , 53 , 65 ) using transcriptomics. Among them, NPY is involved in promoting feeding, and analysis of the hypothalamus transcriptome of mice subjected to a daily 2-h heat treatment (36°C) for 14 d suggested that up-regulated neuropeptide Y acted to attenuate reduced food intake ( 24 ).…”

“…While the affinity of Y2 with PYYb is about 50 times higher than that of PYYa and the affinity of Y7 with PYYa is about three times lower than that of NPY and PYYb ( 190 , 191 ). In addition, unlike mammalian Y2, the two Y2 family receptors in rainbow trout, Y2 and Y7, are both sensitive to NPY with N-terminal deletion and have minimal binding capacity to NPY ( 13 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ) and NPY ( 18 – 24 , 27 – 29 , 31 , 53 , 65 , 79 , 80 , 83 – 85 ), and neither binds to the mammalian Y2-specific antagonist BIIE0246 ( 207 ).…”

Patterns of gene expression in larvae of the giant grouper

“…In this issue, Anderson et al . () used a transcriptomic approach to explore molecular processes that underpin development of appetite, feeding and digestion in E. lanceolatus larvae. They focussed on the first two weeks of life, a critical period for larval husbandry during which the larvae first open their mouth and start exogenous feeding.…”