Format: ORAL

Federico Roda1; Ronald A. Pardo1; Sofía Rojas-Contreras1; Saleh Alseekh2,3; Pablo Perez Mesa1; Andrés Orejuela1; D. Estevan García1,4; Liliana Lopez-Kleine4; Gina P. Sierra1; Alisdair R. Fernie2,3

1 Max Planck Tandem Group GEME, Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, 11321, Colombia. 2 Max-Planck-Institute of Molecular Plant Physiology, Am Muhlenberg 1, 14476. Potsdam-Golm, Germany. 3 Center of Plant Systems Biology and Biotechnology, 4000 Plovdiv, Bulgaria. 4 Departamento de Estadística, Universidad Nacional de Colombia, Bogotá, 111321, Colombia.

Plant species that produce tropane alkaloids (TAs) have been used by humans for millennia as medicines, stimulants, and for mystical-divinatory purposes. We ignore how the longstanding interaction with humans has shaped the genomes and metabolism of these sacred plants. We studied the evolution of TAs in members of the Solanaceae family, which includes multiple TA-producing species that are sacred to cultures around the world. We conducted a search for regulatory networks associated with TA evolution by integrating transcriptomic and metabolomic variation in hundreds of Solanaceae species. Our findings show that TAs are produced by independent phylogenetic clades, indicating the independent acquisition or loss of the TA pathway. Notably, TA genes are components of the same co-expression networks as genes involved in the production of other alkaloids, steroidal glycoalkaloids (SGAs), implying a regulatory tradeoff linking the two pathways. We identified candidate alkaloid genes whose expression shows a correlation with SGA and TA levels across samples. These genes could play a role in metabolic switching between TAs and SGAs during the evolution of the Solanaceae. A genomic analysis of the distribution of TA genes across the Solanaceae phylogeny highlights the significance of genomic clustering, gene duplication, and gene loss in the evolution of alkaloid pathways. Finally, we found that viruses and endophytes have shaped the use of TA-producing species by humans. Our study provides a unique view of the evolution of medicinal plants with potential applications for metabolic engineering of TAs.