Molecular mechanism of the tree shrew's insensitivity to spiciness

Yalan Han; Bowen Li; Ting-Ting Yin; Cheng Xu; Rose Ombati; Lei Luo; Yujie Xia; Lizhen Xu; Jie Zheng; Yaping Zhang; Fan Yang; Guo-Dong Wang; Shilong Yang; Ren Lai

doi:10.1371/journal.pbio.2004921

Molecular mechanism of the tree shrew's insensitivity to spiciness

PLoS Biol. 2018 Jul 12;16(7):e2004921. doi: 10.1371/journal.pbio.2004921. eCollection 2018 Jul.

Authors

Yalan Han^{1

2}, Bowen Li^{1

2}, Ting-Ting Yin^{2

3}, Cheng Xu^{1

2}, Rose Ombati^{1

2}, Lei Luo^{1

2}, Yujie Xia⁴, Lizhen Xu⁵, Jie Zheng⁶, Yaping Zhang², Fan Yang⁵, Guo-Dong Wang^{3

7}, Shilong Yang¹, Ren Lai¹

Affiliations

¹ Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences/Key Laboratory of bioactive peptides of Yunnan Province, Kunming Institute of Zoology, Kunming, Yunnan, China.
² University of Chinese Academy of Sciences, Beijing, China.
³ State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
⁴ Kunming Primate Research Center, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China.
⁵ Department of Biophysics and Kidney Disease Center, First Affiliated Hospital, Institute of Neuroscience, National Health Commission and Chinese Academy of Medical Sciences Key Laboratory of Medical Neurobiology, Zhejiang University School of Medicine, Hangzhou, Zhejiang Province, China.
⁶ Department of Physiology and Membrane Biology, University of California, Davis, Davis, California, United States of America.
⁷ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, Yunnan, China.

Abstract

Spicy foods elicit a pungent or hot and painful sensation that repels almost all mammals. Here, we observe that the tree shrew (Tupaia belangeri chinensis), which possesses a close relationship with primates and can directly and actively consume spicy plants. Our genomic and functional analyses reveal that a single point mutation in the tree shrew's transient receptor potential vanilloid type-1 (TRPV1) ion channel (tsV1) lowers its sensitivity to capsaicinoids, which enables the unique feeding behavior of tree shrews with regards to pungent plants. We show that strong selection for this residue in tsV1 might be driven by Piper boehmeriaefolium, a spicy plant that geographically overlaps with the tree shrew and produces Cap2, a capsaicin analog, in abundance. We propose that the mutation in tsV1 is a part of evolutionary adaptation that enables the tree shrew to tolerate pungency, thus widening the range of its diet for better survival.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adaptation, Physiological
Amino Acids / genetics
Animals
Capsaicin / pharmacology
Capsicum
Conserved Sequence
Mutation / genetics
Nociceptors / metabolism
Spices*
TRPV Cation Channels / agonists
TRPV Cation Channels / metabolism
Tupaia / physiology*

Substances

Amino Acids
TRPV Cation Channels
Capsaicin

Grants and funding

National Science Foundation of China http://www.nsfc.gov.cn/ (grant number 21761142, 31640071, 31770835). Grant number 21761142 to RL; Grant number 31640071 and 31770835 to SY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Chinese Academy of Sciences http://www.cas.cn/ (grant number 21761142002, SAJC201606, "Light of West China" Program and Youth Innovation Promotion Association). Grant number 21761142002 and SAJC201606 to RL; “Light of West China” Program to SY; Youth Innovation Promotion Association to SY and GDW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Yunnan Province http://www.ynstc.gov.cn/ (grant number 2015HA023, 2017FB037). Grant number 2015HA023 to RL; Grant number 2017FB037 to SY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Central Organization Department http://1000plan.org/qrjh/article/69239 (grant number The Young Thousand Talents Plan of China). The Young Thousand Talents Plan of China to FY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.