Expansion of sweet taste receptor genes in grass carp (Ctenopharyngodon idellus) coincided with vegetarian adaptation

Abstract

Background: Taste is fundamental to diet selection in vertebrates. Genetic basis of sweet taste receptor in the shaping of food habits has been extensively studied in mammals and birds, but scarcely studied in fishes. Grass carp is an excellent model for studying vegetarian adaptation, as it exhibits food habit transition from carnivory to herbivory. Results: We identified six sweet taste receptors (gcT1R2A-F) in grass carp. The four gcT1R2s (gcT1R2C-F) have been suggested to be evolved from and paralogous to the two original gcT1R2s (gcT1R2A and gcT1R2B). All gcT1R2s were expressed in taste organs and mediated glucose-, fructose-or arginine-induced intracellular calcium signaling, revealing they were functional. In addition, grass carp was performed to prefer fructose to glucose under a behavioral experiment. Parallelly, compared with gcT1R2A-F/gcT1R3 co-transfected cells, gcT1R2C-F/gcT1R3 cotransfected cells showed a higher response to plant-specific fructose. Moreover, food habit transition from carnivory to herbivory in grass carp was accompanied by increased gene expression of certain gcT1R2s. Conclusions: We suggested that the gene expansion of T1R2s in grass carp was an adaptive strategy to accommodate the change in food environment. Moreover, the selected gene expression of gcT1R2s might drive the food habit transition from carnivory to herbivory in grass carp. This study provided some evolutional and physiological clues for the formation of herbivory in grass carp.

Exploring the potential for an evolutionarily conserved role of the taste 1 receptor gene family in gut sensing mechanisms of fish

“…Hence, gene expression was quantified by qPCR in different tissues within oropharingeal, GIT and brain regions. Our findings are in accordance with previous studies that reported several taste receptors and taste signaling components in the GIT of different fish species ( Polakof and Soengas, 2013 ; Latorre et al., 2013 ; Ronnestad et al., 2016 ; Yuan et al., 2020 ; Calo et al., 2021 ; Kinnamon, 2012 ; Morais, 2017 ), reinforcing the hypothesis that the T1R-mediated gut sensing mechanisms could be conserved throughout vertebrate evolution. The significantly higher levels of sa T1R3 expression observed in oropharyngeal and GIT tissues suggest that this gene might be locally demanded at higher transcriptional rates due to heterodimerization with sa T1R1 or sa T1R2 subunits, since sa T1R3 / sa T1R3 homodimers do not seem to respond to L-amino acids stimulations in this species ( Angotzi et al., 2020 ).…”

“…Interestingly, there were significantly higher mRNA levels of both sa T1R2b and sa T1R2f than sa T1R2a / T1R2d / T1R2e in gills. These gene expression patterns are in agreement with those recently described for T1R2b / e ortholog counterparts in grass carp ( Ctenopharyn godonidellus ) ( Yuan et al., 2020 ), suggesting that the T1R2-mediated chemosensing functions may have been highly retained in gills throughout teleost radiation. We found also high levels of expression for the paralog subtypes sa T1R2d / e and sa T1R2d / e / f in forebrain and hindbrain, respectively, suggesting that these genes might have a tissue-specific chemosensory role in these brain compartments.…”

The feeding ecology of grass carp: A review

“…These genes were collected either from published studies or by against species genome for functions by generating umami, sweet and bitter tastes (Figure 6). 132–135 In grass carp, expanded T1R2s (gene copy numbers = 6) were found compared to other herbivorous fish. Gene expansion was also observed in another herbivorous Indian major carp compared with others.…”

Latent taste diversity revealed by a vertebrate-wide catalogue of T1R receptors

“…The copyright holder for this preprint (which this version posted April 9, 2023. ; https://doi.org/10.1101/2023.04.08.532961 doi: bioRxiv preprint only T1R2A/T1R3A is responsible for sugar perception in mammals and reptiles 24 , we previously demonstrated that T1R1/T1R3A of birds has gained the ability to detect sugars 25,26 . Also, T1R2B/T1R3B of two teleost fishes, namely carp 27 and gilthead seabream 28 , can detect sugars at high concentrations (100-200 mM). In addition, we found that bichir T1R7/T1R4 could respond to GMP, although a previous study reported that neither T1R1/T1R3B nor T1R2B/T1R3B of medaka fish nor T1R2B/T1R3B of zebrafish could be activated by 5'-ribonucleotides 10 .…”