Collaborative Research: Sticky sugars and lantern fruits: Investigating the convergent evolution of inflated calyces and chemical defenses in the tomatillo tribe (Physalideae)

Given that plants cannot outrun their predators, they often rely on chemical defenses to protect themselves and their offspring (seeds). These chemical defenses, often unique to particular plants or groups of plants, are valuable resources for developing natural pesticides that may carry fewer risks for ecosystems and for consumers. This project focuses on a group of plants in the tomato family that produce a promising class of natural insecticides called acylsugars. These sticky sugars are produced by gland-tipped hairs and act as traps for insect predators, but they are non-toxic to humans and degrade quickly in the environment. While most acylsugar research has examined their importance in leaf defense, this research will explore their role in protecting the fruit and its enclosed seeds, studying the tomatillos and their wild relatives. Many of these species cover their fruit in a balloon-like sac that develops from the outer organ of the flower (the calyx), and they decorate this inflated calyx with dense sticky acylsugar-coated hairs. This research will investigate the relationship between the repeated evolutionary origins of the inflated calyx across tomatillos and the production of insecticidal acylsugars, providing the foundation for developing novel natural insecticides. This project is built upon a collaborative network of tomatillo researchers from the U.S. and abroad and will advance international collaborations. It will provide training opportunities for early career researchers including high school students, undergraduates, graduate students, and a postdoctoral fellow. In order to trace the coordinated evolution of inflated fruiting calyces and acylsugar defenses, the research will build the first comprehensive phylogenetic tree for all 310 species in the tomatillo clade. The phylogeny will be estimated using target sequence capture relying on existing collections of DNAs and herbarium specimens as well as new field collections. The researchers will use recently described Solanaceae fruit fossils, including two in the tomatillo clade, to calibrate the tree, and apply methods including state-dependent diversification to estimate transition rates to and away from the inflated calyx state. They will specifically test the hypothesis that gains of inflation are irreversible and that they proceed via an intermediate stage in which the calyx expands to cover the fruit but does not inflate. Finally, the project will explore the coupling of this physical defense (calyx elongation and inflation) with chemical defenses. In particular, the researchers posit that independent gains of inflated fruiting calyces are correlated with increased production of glandular trichomes and sticky, insecticidal acylsugars. Together, these three aims will allow the researchers to trace the assembly of a complex plant defense syndrome, which like many trait syndromes, combines convergently-evolved morphological and biochemical innovations as an adaptive response to a shared ecological driver. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.