Population genomic analyses of the chocolate tree, Theobroma cacao L., provide insights into its domestication process

Authors: CORNEJO, OMAR - Washington State University; YEE, MUH-CHING - Stanford University; DOMINGEZ, VICTOR - Indiana University; ANDREWS, MARY - Indiana University; SOCKELL, ALEXANDRA - Stanford University; STRANDBERG, ERIKA - Stanford University; LIVINGSTONE, DONALD - Mars, Inc; STACK, CONRAD - Mars, Inc; ROMERO, ALBERTO - Mars, Inc; UMAHARAN, PATHMANATHAN - University Of The West Indies; ROYAERT, STEFAN - Mars, Inc; TAWARI, NILESH - Genome Institute Of Singapore; NG, PAULINE - Genome Institute Of Singapore; Gutierrez, Osman; PHILLIPS, WILBERT - Catie Tropical Agricultural Research; MOCKAITIS, KEITHANNE - Indiana University; BUSTAMANTE, CARLOS - Stanford University; MOTAMAYOR, JUAN - Mars, Inc

Submitted to: Communications Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/14/2018
Publication Date: 10/16/2018
Citation: Cornejo, O.E., Yee, M., Domingez, V., Andrews, M., Sockell, A., Strandberg, E., Livingstone, D., Stack, C., Romero, A., Umaharan, P., Royaert, S., Tawari, N.R., Ng, P., Gutierrez, O.A., Phillips, W., Mockaitis, K., Bustamante, C.D., Motamayor, J.C. 2018. Population genomic analyses of the chocolate tree, Theobroma cacao L., provide insights into its domestication process. Communications Biology. 1:16. https://doi.org/10.1038/s42003-018-0168-6.
DOI: https://doi.org/10.1038/s42003-018-0168-6

Interpretive Summary: Since the early days, crop domestication has been associated with the development of early civilizations. Cacao (Theobroma cacao L.), a main cash crop for tropical regions worldwide because it is the source of the raw material to produce chocolate, was domesticated in Mesoamerica by the Olmecs, whom are accredited with the development of the Criollo genetic group of cacao. An interdisciplinary research team participated in the sequence of 200 cacao accessions to investigate the domestication of the Criollo cacao populations. Sequencing results indicated that a sole Criollo population experienced a robust domestication process that included the selection of genes that are involved in disease resistance mechanisms as well as anthocyanins and theobromine metabolism. Finally, a consequence of the domestication process, the accumulation of deleterious alleles, caused a high level of inbreeding depression in the Criollo population.

Technical Abstract: Domestication has had a strong impact on the development of modern societies. We sequenced 200 genomes of the chocolate plant Theobroma cacao L. to show for the first time to our knowledge that a single population underwent strong domestication approximately 3,600 years (95% CI: 2481 – 13,806 years ago) ago, the Criollo population. We also show that during the process of domestication, there was strong selection for genes involved in the metabolism of the colored protectants anthocyanins and the stimulant theobromine, as well as disease resistance genes. Our analyses show that domesticated populations of T. cacao (Criollo) maintain a higher proportion of high frequency deleterious mutations. We also show for the first time the negative consequences of the increase accumulation of deleterious mutations during domestication on the fitness of individuals (significant reduction in Kg of beans per hectare per year as Criollo ancestry increases as estimated from a GLM, P = 0.000425).