Pangenomic exploration of Theobroma cacao: new insights into gene content diversity and selection during domestication

Abstract

The Cacao tree (Theobroma cacao L.) is a major cash crop and an important source of income for millions of farmers across Africa, Asia and Latin America. However, cacao farmers and producing countries are facing multiple challenges including pest and disease management, sustainable production under threat of climate changes and diversification of cocoa flavor profiles. Addressing these challenging requires a deeper understanding of the existing genetic diversity of the species. Yet, very little is known about the intraspecific gene content variation. In this study, we used the genome of 216 accessions of T. cacao (including 185 newly re-sequenced) covering a broad genetic diversity of the species to construct the first pan-genome of the cacao tree. As a result, we predicted a total of 30,489 pan-genes, enriching the reference Criollo genome with 1,407 new genes. Our analysis revealed that only a small fraction of these genes (9.2%) is dispensable, being absent in some individuals. However, these genes could represent a valuable resource for breeding efforts aimed at improving disease resistance in the species. We used this new pangenome resource to gain insights into how diversification and domestication processes have influenced genomic variability within the species. Notably, we observed a significant loss of genes within the domesticated Criollo genetic group. Furthermore, we found evidences suggesting that domestication processes have had an impact on the vigor and disease tolerance of Criollo accessions. In summary, our research has contributed to a better understanding of the cacao trees genome diversity. These findings offer new avenues for biological discovery and breeding, ultimately addressing the challenges faced by cacao farmers and producing countries.