Evolution of the primate glutamate taste sensor from a nucleotide sensor

Toda, Yasuka; Hayakawa, T.; Itoigawa, Akihiro; Kurihara, Yosuke; Nakagita, Tomoya; Hayashi, Masahiro; Ashino, Ryuichi; Melin, Amanda D.; Ishimaru, Yoshiro; Kawamura, Shoji; Imai, Hiroo; Misaka, Takumi

doi:10.1016/j.cub.2021.08.002

Cited by 36 publications

(37 citation statements)

References 51 publications

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“…Neofunctionalisation and pseudogenisation of taste receptor genes has also been linked to highly specialised diets. In large primates which eat a high proportion of leaves, including humans, the umami taste receptor gene has undergone neofunctionalisation to recognise L-glutamate contained within leaves, which may promote leaf consumption [ 45 ] . In addition, bitter taste receptor genes which recognise leaf-derived toxins have also duplicated in some eutherian lineages [ 46 ] .…”

Section: Resultsmentioning

confidence: 99%

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

et al. 2022

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The numbat (Myrmecobius fasciatus) is an endangered Australian marsupial, and the last surviving member of the Myrmecobiidae family. The numbat regularly undergoes torpor and is unique amongst marsupials as it is the only diurnal and termitivorous species. Here we sequenced the first draft genome of the numbat using 10× Genomics Chromium linked-read technology, resulting in a 3.42 Gbp genome with a scaffold N50 of 223 kbp. A global transcriptome from liver, lung and tongue was also generated to aid genome annotation, identifying 21,465 protein-coding genes. To investigate adaptation to the numbat’s termitivorous diet and arid/semi-arid range, we interrogated the most highly expressed transcripts within the tongue and manually annotated taste, vomeronasal and aquaporin gene families. Antimicrobial proteins and proteins involved in digestion were highly expressed in the tongue, alongside umami taste receptors. However, sweet taste receptors were not expressed in this tissue, which combined with the putative contraction of the bitter taste receptor gene repertoire in the numbat genome, may indicate a potential evolutionary adaptation to their specialised termitivorous diet. Vomeronasal and aquaporin gene repertoires were similar to other marsupials. The draft numbat genome is a valuable tool for conservation and can be applied to population genetics/genomics studies and to investigate the unique biology of this interesting species.

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Section: Resultsmentioning

confidence: 99%

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

et al. 2022

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“…They identify substantial interspecific variation in sensitivity to the different compounds, which they suggest is due to co‐evolution with different fruit‐bearing plants. In another example, Toda et al 189 examined amino acid variation and perception of “umami” taste across primates, linking shift to major diet transitions. Data have now been collected for many species, taste receptors, and compounds.…”

Section: Overview Of Current Knowledgementioning

confidence: 99%

“…Folivory has also recently been discovered to lead to relaxed selection on sweet perception 203 . A recent study has also identified adaptive evolution of the umami (or glutamate) taste receptor in primates 189 . The authors found that insectivorous species have a glutamate receptor sensitive to nucleotides that are common in insect prey, while several larger‐bodied folivorous species have convergently evolved a receptor sensitive to the glutamate present in leaves to overcome bitter/aversive tastes.…”

Section: Overview Of Current Knowledgementioning

confidence: 99%

The sensory ecology of primate food perception, revisited

Veilleux

Dominy

Melin

2022

Evolutionary Anthropology

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Twenty years ago, Dominy and colleagues published “The sensory ecology of primate food perception,” an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades.

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“…Neofunctionalization and pseudogenization of taste receptor genes has also been linked to highly specialized diets. In large primates which eat a high proportion of leaves, including humans, the umami taste receptor gene has undergone neofunctionalization to recognize L-glutamate contained within leaves, which may promote leaf consumption [46]. In addition, bitter taste receptor genes which recognize leaf-derived toxins have also duplicated in some eutherian lineages [47].…”

Section: Resultsmentioning

confidence: 99%

“…All TAS1R genes are likely functional in the numbat, owing to the lack of premature stop codons, insertions or deletions within the gene sequence, and identification of transcripts within the global transcriptome, pseudogenization has not occurred in response to their specialized diet as observed in the giant panda [48]. However, the expression of TAS1R1 and TAS1R3 in the numbat tongue transcriptome (TAS1R1 0.073573 TPM and TAS1R3 0.057388 TPM) may reflect their dietary preference for termites, as the TAS1R1/TAS1R3 heterodimer which forms the umami taste receptor recognizes free nucleotides that are abundant in insects [46]. TAS1R2 which forms the sweet taste receptor was not expressed in the tongue transcriptome, which may relate to the low level of free sugars in termites.…”

Section: Resultsmentioning

confidence: 99%

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

Peel

Silver

Brandies

et al. 2022

Preprint

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The numbat (Myrmecobius fasciatus) is a critically endangered Australian marsupial, and the last surviving member of the Myrmecobiidae family. The numbat regularly undergoes torpor and is unique amongst marsupials as it is the only diurnal and termitivorous species. Here we sequenced the first draft genome of the numbat using 10x Genomics chromium linked-read technology, resulting in a 3.42 Gbp genome with a scaffold N50 of 223 Kbp. A global transcriptome from liver, lung and tongue was also generated to aid genome annotation with Fgenesh++, identifying 21,465 protein-coding genes and 78.7% complete mammalian BUSCOs. To investigate adaptation to the numbat′s termitivorous diet and arid/semi-arid range, we interrogated the most highly expressed transcripts within the tongue and manually annotated taste, vomeronasal and aquaporin gene families. Antimicrobial proteins and proteins involved in digestion were highly expressed in the tongue, as expected. Similarly, umami taste receptors were also expressed in the tongue, however sweet taste receptors were not expressed in this tissue. This pattern of taste receptor expression, combined with the putative contraction of the bitter taste receptor gene repertoire in the numbat genome, may indicate a potential evolutionary adaptation to their specialized termitivorous diet. Vomeronasal and aquaporin gene repertoires were similar to other marsupials and have not undergone expansion or contraction. The draft numbat genome is a valuable tool for conservation and can be applied to population genetics/genomics studies and to investigate the unique biology of this interesting species.

show abstract

Evolution of the primate glutamate taste sensor from a nucleotide sensor

Cited by 36 publications

References 51 publications

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

The sensory ecology of primate food perception, revisited

Genome assembly of the numbat (Myrmecobius fasciatus), the only termitivorous marsupial

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