Genetic basis of alkaloid divergence in the Solanaceae

Abstract

Plant lineages produce distinctive alkaloids, suggesting the existence of evolutionary mechanisms preventing the simultaneous metabolism of multiple alkaloid types in the same species. Tribes in the Solanaceae family produce either tropane alkaloids (TAs) or steroidal glycoalkaloids (SGAs). We integrated genomic, transcriptomic, and metabolomic variation across tens of species representing most Solanaceae tribes to evaluate three possible genetic causes of this mutually exclusive distribution, namely (1) loss of biosynthetic genes, (2) genomic clustering, and (3) regulatory changes. We found that both pathways are produced by multiple phylogenetic clades, suggesting that the differential loss of the biosynthetic pathways across lineages could explain their patchy distributions in the phylogeny. However, TA and SGA genes show contrasting patterns of genomic presence and distribution: SGA genes are grouped in large and dynamic biosynthetic clusters but are present across most species whereas TA genes are sparsely distributed and almost exclusively present in TA-producing species genomes. Additionally, SGA and TA genes are preferentially expressed in species that produce SGAs and TAs respectively, suggesting that expression differences were crucial for the divergence of the two pathways. Our results highlight the asymmetric significance of gene loss, genomic clustering, and gene expression differences in the divergence of TAs and SGAs.