The evolution of pyrrolizidine alkaloid diversity among and withinJacobaeaspecies

Plants produce many secondary metabolites showing considerable inter- and intraspecific diversity of concentration and composition as a strategy to cope with environmental stresses. The evolution of plant defenses against herbivores and pathogens can be unraveled by understanding the mechanisms underlying chemical diversity. Pyrrolizidine alkaloids are a class of secondary metabolites with high diversity. We performed a qualitative and quantitative analysis of 80 pyrrolizidine alkaloids with liquid chromatography-tandem mass spectrometry of leaves from 17Jacobaeaspecies including one to three populations per species with 4-10 individuals per population grown under controlled conditions in a climate chamber. We observed large inter- and intraspecific variation in pyrrolizidine alkaloid concentration and composition, which were both species-specific. Furthermore, we sequenced 11 plastid and three nuclear regions to reconstruct the phylogeny of the 17Jacobaeaspecies. Ancestral state reconstruction at the species level showed mainly random distributions of individual pyrrolizidine alkaloids. We found little evidence for phylogenetic signals, as nine out of 80 pyrrolizidine alkaloids showed a significant phylogenetic signal for Pagel's lambda statistics only, whereas no significance was detected for Blomberg'sKmeasure. We speculate that this high pyrrolizidine alkaloid diversity is the result of the upregulation and downregulation of specific pyrrolizidine alkaloids depending on ecological needs rather than gains and losses of particular pyrrolizidine alkaloid biosynthesis genes during evolution.

Automated summary

Plants produce diverse secondary metabolites as a strategy to cope with environmental stresses, and pyrrolizidine alkaloids are one class of such metabolites with high diversity. In this study, we analyzed the concentration and composition of pyrrolizidine alkaloids in leaves of 17 Jacobaea species and reconstructed their phylogeny. Our results revealed significant inter- and intraspecific variation in pyrrolizidine alkaloid diversity, suggesting species-specific patterns. Ancestral state reconstruction showed random distributions of individual alkaloids, indicating ecological regulation rather than genetic gains or losses during evolution.