22 Oral - Platform Session #2 Genetics of Adaptation
Wednesday June 08, 4:15 PM - 4:30 PM
Deciphering the mystery of sorghum tannin domestication in Africa: coevolution among sorghum, human, and bird
Authors: Yueyu Wu 1; Tingting Guo 2; Qi Mu 2; Jinyu Wang 2; Xin Li 2; Yun Wu 2; Bin Tian 1; Ming Li Wang 3; Guihua Bai 3; Ramasamy Perumal 1; Harold Trick 1; Scott Bean 3; Ismail Dweikat 4; Mitchell Tuinstra 5; Geoffrey Morris 1; Tesfaye Tesso 1; Jianming Yu 2; Xianran Li 2,3
Affiliations: 1) Kansas State University; 2) Iowa State University; 3) USDA-ARS; 4) University of Nebraska, Lincoln; 5) Purdue University
Keywords: Coevolution
A crucial step of domesticating cereal crops is reducing bitter substances in the edible seeds. After domestication, condensed tannins, potent secondary metabolites inducing an unpleasant taste perception, are purged from seeds of major cereals, except sorghum. Half of sorghum cultivars (domesticated in Africa) have condensed tannings in grains, which presents an evolutionary mystery. With a serendipity field observation in Iowa, we parsed the harmonic relationships among the domesticate-triad in the evolution of African agroecosystems at the continental scale.
Started from the observation of sparrows’ feed preference on sorghum seeds from a mapping population, we uncovered that condensed tannins deterred sparrows and identified two interacting genes (Tannin1 and Tannin2) controlling for tannin presence. Geographic distributions of the functional polymorphisms suggested that smallholders in different African regions independently domesticated non-tannin sorghum for palatable food like other cereals.
Tannin sorghum cultivars are predominantly grown in East & South Africa, while non-tannin in West Africa. The parallel geographic distribution of the world’s most abundant wild bird, Quelea quelea, to tannin sorghum distribution supported that Q. quelea is the key biotic factor driving this differential at the continental scale. Smallholders in East & South Africa selected tannins to fight against the severe herbivore threats.
Using condensed tannins to fight against biotic threats is a smart strategy, however, how African smallholders can take “bad taste” tannin sorghum as a staple food needed to be reconciled. As the bad taste is induced by bitter taster receptors (TAS2Rs), mutations in TAS2Rs may lead varied sensitivity for condensed tannins. Analyzing African genomes uncovered a parallel geographic distribution of a non-synonymous SNP in TAS2R5 to the tannin sorghum distribution. The ancestral non-taste allele is predominantly observed in East & South Africa, while the derived taste allele sensitive to tannins is observed mainly from West Africa.
Three geographic distributions of domesticator, domesticate, and environment depict harmonic interactions in African agroecosystems. In East & South Africa, smallholders (perceiving less bitterness from tannins because of non-taster TAS2R5) selected tannin to fight against the pest Q. quelea; in West Africa with mild threats from Q. quelea, smallholders (carrying taster TAS2R5) selected non-tannin sorghum for better food.
Reference: Allelochemicals targeted to balance competing selections in African agroecosystems (https://doi.org/10.1038/s41477-019-0563-0)