Leafminer attack induces plant-mediated facilitation of conspecific pupae in the soil

Plants and herbivores are engaged in intimate antagonistic interactions, with plants trying to mount effective defense responses and herbivores attempting to manipulate plants for their own benefit. Here we report on a new mechanism by which herbivores can facilitate their own development. We show that tomato (Solanum lycopersicum) leaf attack by the American serpentine leafminer Lyriomiza trifolii accelerates the development of conspecific pupae in the soil adjacent to the plant. This pattern was reversed in the jasmonate-signaling deficient tomato mutant def-1. Chemical analyses revealed that L. trifolii leaf attack changes the production of root volatiles in a def-1 dependent manner. Thus, leaf-feeding herbivores can interact with their soil-dwelling pupae, and jasmonates and root volatiles likely play relevant roles in this phenomenon. This study expands the repertoire of plant-herbivore interactions to herbivory-induced modulation of metamorphosis.

Root volatiles in plant-plant interactions I: Characterization of root sesquiterpene emissions from Centaurea stoebe and their effects on other plants

Volatile organic compounds (VOCs) emitted by plant leaves can influence the physiology of neighboring plants. In contrast to interactions above ground, little is known about the role of VOCs in belowground plant-plant interactions. Here, we characterize constitutive root volatile emissions of the spotted knapweed (Centaurea stoebe) and explore the impact of these volatiles on the germination and growth of different sympatric plant species. We show that C. stoebe roots emit high amounts of sesquiterpenes, with estimated release rates of (E)-β-caryophyllene above 3 μg g−1 dw h−1. Sesquiterpene emissions show little variation between different C. stoebe populations, but vary substantially between different Centaurea species. Through root transcriptome sequencing, we identify six root-expressed sesquiterpene synthases (TPSs). Two root-specific TPSs, CsTPS4 and CsTPS5, are sufficient to produce the full blend of emitted root sesquiterpenes. Volatile exposure experiments demonstrate that C. stoebe root volatiles have neutral to positive effects on the germination and growth of different sympatric neighbors. Thus, constitutive root sesquiterpenes produced by two C. stoebe TPSs are associated with facilitation of sympatric neighboring plants. The release of root VOCs may thus influence C. stoebe abundance and plant community structure in nature.