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

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          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 co-transfected 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.

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          Most cited references33

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          The receptors for mammalian sweet and umami taste.

          Sweet and umami (the taste of monosodium glutamate) are the main attractive taste modalities in humans. T1Rs are candidate mammalian taste receptors that combine to assemble two heteromeric G-protein-coupled receptor complexes: T1R1+3, an umami sensor, and T1R2+3, a sweet receptor. We now report the behavioral and physiological characterization of T1R1, T1R2, and T1R3 knockout mice. We demonstrate that sweet and umami taste are strictly dependent on T1R-receptors, and show that selective elimination of T1R-subunits differentially abolishes detection and perception of these two taste modalities. To examine the basis of sweet tastant recognition and coding, we engineered animals expressing either the human T1R2-receptor (hT1R2), or a modified opioid-receptor (RASSL) in sweet cells. Expression of hT1R2 in mice generates animals with humanized sweet taste preferences, while expression of RASSL drives strong attraction to a synthetic opiate, demonstrating that sweet cells trigger dedicated behavioral outputs, but their tastant selectivity is determined by the nature of the receptors.
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            Estimating divergence times in large molecular phylogenies.

            Molecular dating of species divergences has become an important means to add a temporal dimension to the Tree of Life. Increasingly larger datasets encompassing greater taxonomic diversity are becoming available to generate molecular timetrees by using sophisticated methods that model rate variation among lineages. However, the practical application of these methods is challenging because of the exorbitant calculation times required by current methods for contemporary data sizes, the difficulty in correctly modeling the rate heterogeneity in highly diverse taxonomic groups, and the lack of reliable clock calibrations and their uncertainty distributions for most groups of species. Here, we present a method that estimates relative times of divergences for all branching points (nodes) in very large phylogenetic trees without assuming a specific model for lineage rate variation or specifying any clock calibrations. The method (RelTime) performed better than existing methods when applied to very large computer simulated datasets where evolutionary rates were varied extensively among lineages by following autocorrelated and uncorrelated models. On average, RelTime completed calculations 1,000 times faster than the fastest Bayesian method, with even greater speed difference for larger number of sequences. This speed and accuracy will enable molecular dating analysis of very large datasets. Relative time estimates will be useful for determining the relative ordering and spacing of speciation events, identifying lineages with significantly slower or faster evolutionary rates, diagnosing the effect of selected calibrations on absolute divergence times, and estimating absolute times of divergence when highly reliable calibration points are available.
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              Genome evolution and biodiversity in teleost fish.

              J-N Volff (2005)
              Teleost fish, which roughly make up half of the extant vertebrate species, exhibit an amazing level of biodiversity affecting their morphology, ecology and behaviour as well as many other aspects of their biology. This huge variability makes fish extremely attractive for the study of many biological questions, particularly of those related to evolution. New insights gained from different teleost species and sequencing projects have recently revealed several peculiar features of fish genomes that might have played a role in fish evolution and speciation. There is now substantial evidence that a round of tetraploidization/rediploidization has taken place during the early evolution of the ray-finned fish lineage, and that hundreds of duplicate pairs generated by this event have been maintained over hundreds of millions of years of evolution. Differential loss or subfunction partitioning of such gene duplicates might have been involved in the generation of fish variability. In contrast to mammalian genomes, teleost genomes also contain multiple families of active transposable elements, which might have played a role in speciation by affecting hybrid sterility and viability. Finally, the amazing diversity of sex determination systems and the plasticity of sex chromosomes observed in teleost might have been involved in both pre- and postmating reproductive isolation. Comparison of data generated by current and future genome projects as well as complementary studies in other species will allow one to approach the molecular and evolutionary mechanisms underlying genome diversity in fish, and will certainly significantly contribute to our understanding of gene evolution and function in humans and other vertebrates.
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                Author and article information

                Contributors
                xufang_liang@hotmail.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                11 February 2020
                11 February 2020
                2020
                : 20
                : 25
                Affiliations
                [1 ]ISNI 0000 0004 1790 4137, GRID grid.35155.37, College of Fisheries, Chinese Perch Research Center, , Huazhong Agricultural University, ; No.1, Shizishan Street, Hongshan District, Wuhan, 430070 Hubei Province China
                [2 ]ISNI 0000 0004 0369 6250, GRID grid.418524.e, Innovation Base for Chinese Perch Breeding, Key Lab of Freshwater Animal Breeding, Ministry of Agriculture, ; Wuhan, 430070 China
                [3 ]ISNI 0000 0001 2152 3263, GRID grid.4422.0, The Key Laboratory of Aquaculture Nutrition and Feeds, Ministry of Agriculture, The Key Laboratory of Mariculture, Ministry of Education, , Ocean University of China, ; Qingdao, 266003 Shandong China
                Article
                1590
                10.1186/s12862-020-1590-1
                7014666
                32046636
                e775fdd8-711a-4c55-ad70-2ef489037f06
                © The Author(s). 2020

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 31 July 2019
                : 28 January 2020
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Evolutionary Biology
                taste receptor,gene expansion,adaptive evolution,food habit transition,herbivory

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