Diversity and Divergence: Evolution of defense chemistry in the tropical tree genus Inga

Plants are widely recognized as chemical factories, with each species producing dozens to hundreds of unique secondary metabolites. These compounds shape the interactions between plants and their natural enemies. Here we explore how plants generate chemical diversity, and what evolutionary processes have led to novel compounds and unique chemical profiles. We comprehensively characterized the chemical profile of one-third of the species of tropical rainforest trees in the genus Inga (~ 100, Fabaceae) and applied phylogenetic comparative methods to understand the mode of chemical defense evolution. We show that: 1) Each Inga species produces exceptionally high levels of phytochemical diversity, despite costs, tradeoffs and biosynthetic constraints. 2) Closely related species have highly divergent defense profiles, with individual compounds, major compound classes and complete profiles showing little to no phylogenetic signal. 3) We show that the evolution of a species' chemical profile shows a signature of divergent adaptation, implying that it is advantageous for a species to have distinct chemistry from close relatives to avoid shared natural enemies. 4) Finally, we hypothesize a model where deep homology of biosynthetic pathways and rapid changes in regulatory mechanisms may better explain the observed large shifts in defense chemicals between closely related taxa.

Effects of root-colonizing fluorescent Pseudomonas on Arabidopsis resistance against a pathogen and an herbivore

Rhizobacteria in the genus Pseudomonas can enhance plant resistance to a range of pathogens and herbivores. However, resistance to these different classes of plant antagonists is mediated by different molecular mechanisms, and the extent to which induced systemic resistance by Pseudomonas can simultaneously protect plants against both pathogens and herbivores remains unclear. We screened 12 root-colonizing Pseudomonas strains to assess their ability to induce resistance in Arabidopsis thaliana against a foliar pathogen (Pseudomonas syringae DC3000) and a chewing herbivore (Spodoptera littoralis). None of our 12 strains increased plant resistance against herbivory; however, four strains enhanced pathogen resistance, and one of these (Pseudomonas strain P97-38) also made plants more susceptible to herbivory. Phytohormone analyses revealed stronger SA induction in plants colonized by P97-38 (vs controls) following subsequent pathogen infection but weaker induction of JA-mediated defenses following herbivory. We found no effects of P97-38 inoculation on herbivore-relevant nutrients such as sugars and protein, suggesting that the observed enhancement of susceptibility to S. littoralis is due to effects on plant defense chemistry rather than nutrition. These findings suggest that Pseudomonas strains that enhance plant resistance to pathogens may have neutral or negative effects on resistance to herbivores and provide insight into potential mechanisms associated with effects on different classes of plant antagonists. Improved understanding of these effects has potentially important implications for the use of rhizobacteria inoculation in agriculture. Importance Plant-associated microbes have significant potential to enhance agricultural production, for example by enhancing plant resistance to pathogens and pests. Efforts to identify beneficial microbial strains typically focus on a narrow range of desirable plant traits; however, microbial symbionts can have complex effects on plant phenotypes, including susceptibility and resistance to different classes of plant antagonists. We examined the effects of 12 strains of Pseudomonas rhizobacteria on plant (Arabidopsis) resistance to a Lepidopteran herbivore and a foliar pathogen. None of our strains increased plant resistance against herbivory; however, four strains enhanced pathogen resistance, and one of these made plants more susceptible to herbivory (likely via effects on plant defense chemistry). These findings indicate that microbial strains that enhance plant resistance to pathogens can have neutral or negative effects on resistance to herbivores, highlighting potential pitfalls in the application of beneficial rhizobacteria as biocontrol agents.