TAS2R20 variants confer dietary adaptation to high-quercitrin bamboo leaves in Qinling giant pandas.

Xiangxu Hu,Guan Wang,Yibo Hu,Lei Shan,Fuwen Wei,Shuyan Sun

doi:10.1002/ece3.6327

Abstract

Sensitivity to bitter tastes provides animals with an important means of interacting with their environment and thus, influences their dietary preferences. Genetic variants encoding functionally distinct receptor types contribute to variation in bitter taste sensitivity. Our previous study showed that two nonsynonymous sites, A52V and Q296H, in the TAS2R20 gene are directionally selected in giant pandas from the Qinling Mountains, which are speculated to be the causative base‐pair changes of Qinling pandas for the higher preference for bamboo leaves in comparison with other pandas. Here, we used functional expression in engineered cells to identify agonists of pTAS2R20 (i.e., giant panda's TAS2R20) and interrogated the differences in perception in the in vitro responses of pTAS2R20 variants to the agonists. Our results show that pTAS2R20 is specifically activated by quercitrin and that pTAS2R20 variants exhibit differences in the sensitivity of their response to the agonist. Compared with pTAS2R20 in pandas from other areas, the receptor variant with A52V and Q296H, which is most commonly found in Qinling pandas, confers a significantly decreased sensitivity to quercitrin. We subsequently quantified the quercitrin content of the leaves of bamboo distributed in the Qinling Mountains, which was found to be significantly higher than that of the leaves of bamboo from panda habitats in other areas. Our results suggest that the decreased sensitivity to quercitrin in Qinling pandas results in higher‐quercitrin‐containing bamboo leaves to be tasting less bitter to them and thus, influences their dietary preference. This study illustrates the genetic adaptation of Qinling pandas to their environments and provides a fine example of the functional effects of directional selection in the giant panda.

Highlights

Animals taste receptor genes evolve in response to species-specific diets (Jiang et al, 2012; Li et al, 2005; Liu et al, 2016; Sato & Wolsan, 2012; Shan, Wu, Wang, Zhang, & Wei, 2018; Zhao, Yang, Xu, & Zhang, 2010)
We hypothesized that the two nonsynonymous sites in TAS2R20 encode receptor variants that may decrease Qinling pandas’ taste sensitivity to bitter compounds, causing bamboo leaves to taste less bitter to the pandas
We showed that two directionally selected nonsynonymous sites, A52V and Q296H, are associated with decreased sensitivity to quercitrin in Qinling pandas, which confers upon the pandas a dietary preference for high-quercitrin bamboo leaves

Summary

| INTRODUCTION

Animals taste receptor genes evolve in response to species-specific diets (Jiang et al, 2012; Li et al, 2005; Liu et al, 2016; Sato & Wolsan, 2012; Shan, Wu, Wang, Zhang, & Wei, 2018; Zhao, Yang, Xu, & Zhang, 2010). TAS2R49 is designated as TAS2R20 according to the last Gene Nomenclature Committee of the Human Genome Organization (http://www.genenames.org/, last accessed April 30, 2016), and this gene has been directionally selected at two nonsynonymous sites A52V and Q296H in the panda population from the Qinling Mountains (Qinling pandas) (Shan et al, 2018; Zhao et al, 2013) Consistent with this finding, field observations showed that Qinling pandas consume more bamboo leaves than pandas in other areas (Pan et al, 2001; Schaller, Hu, Pan, & Zhu, 1985); population genetic data indicated their divergence from other pandas ~0.3 million years ago and showed genetic adaptation to their environments (Wei et al, 2014; Zhao et al, 2013). We hypothesized that the two nonsynonymous sites in TAS2R20 encode receptor variants that may decrease Qinling pandas’ taste sensitivity to bitter compounds, causing bamboo leaves to taste less bitter to the pandas To address this hypothesis, we first challenged pTAS2R20 with several common bitter substances (caffeine, sesquiterpene lactone, denatonium benzoate, chloroquine, picrotoxinin, cycloheximide, and nicotine), and some known bamboo-derived bitter chemicals (quercitrin, tannin, salicin, aloin, coumarin, amygdalin, and galangin) in a heterologous expression system. The changes in fluorescence were observed by fluorescence microscopy and measured with ImageJ

| MATERIALS AND METHODS

Findings

| DISCUSSION