Mediation of plant–insect interactions in the wild by natural phyllosphere bacteria

Background/Question/Methods

Most herbivorous insects tend to consume only a few plant species, suggesting that host specialization is correlated with enormous ecological and evolutionary success. But specialized herbivores may be impacted by the outcome of interactions between their hosts and other species. Leaf-associated (i.e. phyllosphere) bacteria are a ubiquitous and diverse group of plant symbionts, but whose ecological impacts on plants and insects remain unexplored.

Laboratory studies indicate that bacteria alter plant susceptibility to herbivores through impacting plant defenses. Herbivores typically induce jasmonic acid (JA) defenses, while bacterial infection typically induces salicylate-acid (SA) defenses. Elicitation of either pathway tends to suppress the activity of the other. This trade-off in plant defense might have been present since the ancestor of flowering plants. SA–JA cross-talk may thus be a general mechanism by which phyllosphere bacteria indirectly influence insect herbivores.

Through field observations and manipulative experiments, we explore the structure and function of phyllosphere bacterial assemblages from the native plant Cardamine cordifolia (Brassicaceae; “bittercress”) in relation to insect herbivory by the specialist leaf-miner, Scaptomyza nigrita (Drosophilidae). We test the hypothesis that bacterial infection increases plant susceptibility to herbivory by this insect, and that these impacts arise from trade-offs between SA–JA plant defenses.

Results/Conclusions

In a native population of bittercress, we found a positive correlation between S. nigrita herbivory and the abundance of phyllosphere bacteria cultured from bittercress leaves. Of the major phyllosphere taxa recovered from a bittercress transect, bacteria from the genus Pseudomonas were most prevalent among leaves and showed the strongest positive correlation with S. nigrita herbivory. We found that S. nigrita avoids, and is negatively impacted by, feeding on bittercress treated with JA under laboratory and field conditions. Thus, the strength of anti-herbivore defenses modulates foraging behavior and fitness of this specialist insect. To examine whether bacteria may be facilitating S. nigrita by reducing anti-herbivore defenses, we experimentally infected bittercress with several Pseudomonas isolates. Infection increased rates of adult and larval S. nigrita foraging in laboratory choice tests, consistent with the expectations of a SA–JA plant defense trade-off.

Phyllosphere bacteria exist at the very interface of interactions between plants and herbivorous insects and therefore may be a crucial but cryptic third player in their mutual relations. By examining the ecological consequences of an evolutionarily conserved trade-off between plant defense pathways, this work helps illuminate the potential role of phyllosphere bacteria in shaping plant interactions with insect herbivores more generally.