The Role of Plant Secondary Metabolites in Plant Cross-Kingdom Interactions

Land plants have been associated with microorganisms across their five hundred million year evolution. Horizontal gene transfer that occurred during symbiosis with soil microorganisms enabled plants to produce phenylpropanoids and lignin, both essential in withstanding environmental and physical conditions outside an aquatic habitat. New secondary metabolites like terpenoids, derived from the polyketide metabolism, dramatically enriched the already existing stock of plant derived secondary compounds. This required extensive gene duplication and enzyme (neo)functionalization and resulted in the currently observed diversification of secondary metabolites: among them alkaloids, heterocyclic compounds, unusual and highly substituted flavonoids, betalains, and many other classes of chemicals. To date, several hundred thousand of these plant made secondary metabolites have been identified in higher plants. Many of them are highly toxic, while others are beneficial to the health of a more or less narrow range of target organisms. Allelochemicals, secondary metabolites with a role in plant-plant interactions, have been recognized as important modifiers of biodiversity and as factors driving the success of invasive plants, thus influencing the ecology of plant communities in constantly changing environments.

The expansion and diversification of angiosperms in the Cretaceous led to the evolution of new ecological interactions: among plants, between plants and insects, and between plants and the then expanding class of mammals. In all these organismal interactions, microorganisms were of utmost importance. As endophytes, microorganisms can alter the secondary metabolism of the host plant or establish alliances with the plant to complete the biosynthesis of plant secondary metabolites. In turn, plant secondary metabolites influence the biodiversity and community structure of associated plants and microbiomes.

There is increasing evidence that plant secondary metabolites cause qualitative and quantitative shifts in favor of microorganisms that can fulfill defined functions. This Research Topic addresses ecological and evolutionary aspects of plant secondary metabolite in plant interactions and the roles endogenous and exogenous microbes may play in preferentially symbiotic interactions, other than mycorrhizal partnerships or rhizobial nodulation. As an emerging topic, we consider microbiome-plant interactions, attempting to give a representative overview of the current knowledge on the connections between plant secondary metabolites and plant cross-kingdom interactions while simultaneously trying to integrate this knowledge into an evolutionary and ecological framework.