Massive losses of taste receptor genes in toothed and baleen whales.

This article has been accepted for publication in [Genome Biology and Evolution Published by Oxford University Press. Taste receptor genes are functionally important in animals, with a surprising exception in the bottlenose dolphin, which shows extensive losses of sweet, umami, and bitter taste rece...

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Published in:Genome Biology and Evolution
Main Authors: Feng, P, Zheng, J, Rossiter, SJ, Wang, D, Zhao, H
Format: Article in Journal/Newspaper
Language:English
Published: 2018
Subjects:
Online Access:http://qmro.qmul.ac.uk/xmlui/handle/123456789/37183
https://doi.org/10.1093/gbe/evu095
id ftqueenmaryuniv:oai:qmro.qmul.ac.uk:123456789/37183
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spelling ftqueenmaryuniv:oai:qmro.qmul.ac.uk:123456789/37183 2023-05-15T15:37:00+02:00 Massive losses of taste receptor genes in toothed and baleen whales. Feng, P Zheng, J Rossiter, SJ Wang, D Zhao, H 2018-03-06T10:08:46.148Z 1254 - 1265 http://qmro.qmul.ac.uk/xmlui/handle/123456789/37183 https://doi.org/10.1093/gbe/evu095 eng en eng Genome Biol Evol doi:10.1093/gbe/evu095 http://qmro.qmul.ac.uk/xmlui/handle/123456789/37183 Creative Commons Attribution License The Author(s) 2014. CC-BY diet evolution pseudogenization taste receptor whales Animals Base Sequence Biological Evolution Molecular Feeding Behavior Molecular Sequence Data Pseudogenes Receptors G-Protein-Coupled Taste Taste Buds Article 2018 ftqueenmaryuniv https://doi.org/10.1093/gbe/evu095 2022-09-25T20:17:12Z This article has been accepted for publication in [Genome Biology and Evolution Published by Oxford University Press. Taste receptor genes are functionally important in animals, with a surprising exception in the bottlenose dolphin, which shows extensive losses of sweet, umami, and bitter taste receptor genes. To examine the generality of taste gene loss, we examined seven toothed whales and five baleen whales and sequenced the complete repertoire of three sweet/umami (T1Rs) and ten bitter (T2Rs) taste receptor genes. We found all amplified T1Rs and T2Rs to be pseudogenes in all 12 whales, with a shared premature stop codon in 10 of the 13 genes, which demonstrated massive losses of taste receptor genes in the common ancestor of whales. Furthermore, we analyzed three genome sequences from two toothed whales and one baleen whale and found that the sour taste marker gene Pkd2l1 is a pseudogene, whereas the candidate salty taste receptor genes are intact and putatively functional. Additionally, we examined three genes that are responsible for taste signal transduction and found the relaxation of functional constraints on taste signaling pathways along the ancestral branch leading to whales. Together, our results strongly suggest extensive losses of sweet, umami, bitter, and sour tastes in whales, and the relaxation of taste function most likely arose in the common ancestor of whales between 36 and 53 Ma. Therefore, whales represent the first animal group to lack four of five primary tastes, probably driven by the marine environment with high concentration of sodium, the feeding behavior of swallowing prey whole, and the dietary switch from plants to meat in the whale ancestor. This work was supported by the National Natural Science Foundation of China (Grant No. 31300313) and a start-up fund from Wuhan University awarded to H.Z Article in Journal/Newspaper baleen whale baleen whales toothed whales Queen Mary University of London: Queen Mary Research Online (QMRO) Genome Biology and Evolution 6 6 1254 1265
institution Open Polar
collection Queen Mary University of London: Queen Mary Research Online (QMRO)
op_collection_id ftqueenmaryuniv
language English
topic diet
evolution
pseudogenization
taste receptor
whales
Animals
Base Sequence
Biological Evolution
Molecular
Feeding Behavior
Molecular Sequence Data
Pseudogenes
Receptors
G-Protein-Coupled
Taste
Taste Buds
spellingShingle diet
evolution
pseudogenization
taste receptor
whales
Animals
Base Sequence
Biological Evolution
Molecular
Feeding Behavior
Molecular Sequence Data
Pseudogenes
Receptors
G-Protein-Coupled
Taste
Taste Buds
Feng, P
Zheng, J
Rossiter, SJ
Wang, D
Zhao, H
Massive losses of taste receptor genes in toothed and baleen whales.
topic_facet diet
evolution
pseudogenization
taste receptor
whales
Animals
Base Sequence
Biological Evolution
Molecular
Feeding Behavior
Molecular Sequence Data
Pseudogenes
Receptors
G-Protein-Coupled
Taste
Taste Buds
description This article has been accepted for publication in [Genome Biology and Evolution Published by Oxford University Press. Taste receptor genes are functionally important in animals, with a surprising exception in the bottlenose dolphin, which shows extensive losses of sweet, umami, and bitter taste receptor genes. To examine the generality of taste gene loss, we examined seven toothed whales and five baleen whales and sequenced the complete repertoire of three sweet/umami (T1Rs) and ten bitter (T2Rs) taste receptor genes. We found all amplified T1Rs and T2Rs to be pseudogenes in all 12 whales, with a shared premature stop codon in 10 of the 13 genes, which demonstrated massive losses of taste receptor genes in the common ancestor of whales. Furthermore, we analyzed three genome sequences from two toothed whales and one baleen whale and found that the sour taste marker gene Pkd2l1 is a pseudogene, whereas the candidate salty taste receptor genes are intact and putatively functional. Additionally, we examined three genes that are responsible for taste signal transduction and found the relaxation of functional constraints on taste signaling pathways along the ancestral branch leading to whales. Together, our results strongly suggest extensive losses of sweet, umami, bitter, and sour tastes in whales, and the relaxation of taste function most likely arose in the common ancestor of whales between 36 and 53 Ma. Therefore, whales represent the first animal group to lack four of five primary tastes, probably driven by the marine environment with high concentration of sodium, the feeding behavior of swallowing prey whole, and the dietary switch from plants to meat in the whale ancestor. This work was supported by the National Natural Science Foundation of China (Grant No. 31300313) and a start-up fund from Wuhan University awarded to H.Z
format Article in Journal/Newspaper
author Feng, P
Zheng, J
Rossiter, SJ
Wang, D
Zhao, H
author_facet Feng, P
Zheng, J
Rossiter, SJ
Wang, D
Zhao, H
author_sort Feng, P
title Massive losses of taste receptor genes in toothed and baleen whales.
title_short Massive losses of taste receptor genes in toothed and baleen whales.
title_full Massive losses of taste receptor genes in toothed and baleen whales.
title_fullStr Massive losses of taste receptor genes in toothed and baleen whales.
title_full_unstemmed Massive losses of taste receptor genes in toothed and baleen whales.
title_sort massive losses of taste receptor genes in toothed and baleen whales.
publishDate 2018
url http://qmro.qmul.ac.uk/xmlui/handle/123456789/37183
https://doi.org/10.1093/gbe/evu095
genre baleen whale
baleen whales
toothed whales
genre_facet baleen whale
baleen whales
toothed whales
op_relation Genome Biol Evol
doi:10.1093/gbe/evu095
http://qmro.qmul.ac.uk/xmlui/handle/123456789/37183
op_rights Creative Commons Attribution License
The Author(s) 2014.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1093/gbe/evu095
container_title Genome Biology and Evolution
container_volume 6
container_issue 6
container_start_page 1254
op_container_end_page 1265
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