Molecular sources of monoterpenoid chemodiversity in the Asteraceae Tanacetum vulgare suggest a new model for the evolution of specialized metabolism

Abstract

Highly diversified specialized metabolism enables plant communication with pollinators, herbivores, and protectors1-4. Its chemodiversity, under which evenness, richness and variation is summarized5-7, includes many compounds without known function1-4 and presents an evolutionary conundrum about how and what is selected for8,9. Due to its complexity, it is frequently unknown how it is encoded in genomes. To produce population level chemodiversity, the traits need to allow for highly chemodiverse and highly specific individuals in the same population. Here we use metabolomics, transcriptomics, and genomics combined with field analyses and functional assays of monoterpene synthases in the Asteraceae Tanacetum vulgare (tansy) and identify forces which produce high population level chemodiversity: selection for product specificity in enzymes, loss-of-expression alleles, absence variation, and specialized metabolism islands drive individuals towards low chemodiversity while unlinked enzyme loci, expression variation alleles, presence variation, and de novo enzyme evolution enable high individual chemodiversity. Since the molecular data suggests selection for mechanisms that increase chemodiversity itself at the population level, the screening hypothesis which posited plants produce a reservoir of diverse chemicals prior to selection8 should be replaced by a chemodiversity selection hypothesis. The results demonstrate that, in addition to plant protection via individual chemicals with known targeting mechanisms for predators, being different from your neighbors even if you are closely related is likely an important element in plant protection.