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.

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

Grant support

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.