The evolution of disease resistance is typically evaluated in terms of the effect of a single natural enemy on a host, but hosts are often, if not always, subject to attack by multiple enemies. This thesis employs the defense system of the genetic model plant Arabidopsis thaliana to elucidate mechanisms and consequences of three-way species interactions among plants, microbial pathogens and insect herbivores. These studies uncover complex signaling interactions constraining optimal expression of plant defense in the context of simultaneous attack, including constraints arising from 'hard-wired' trade-offs in inducible resistance responses and pathogen manipulation of plant defense signaling.

Chapter 1 introduces the plant defense system from a historical perspective, focusing on the discovery of induced resistance and prior evidence for crosstalk among signaling pathways encoding resistance to pathogens and herbivores.

Chapter 2 interrogates the mechanism by which a virulent strain of the phytopathogen Pseudomonas syringae induces systemic Arabidopsis susceptibility to herbivory by the insect Trichoplusia ni. Molecular genetic and hormone treatment experiments rule out the P. syringae-derived virulence factor coronatine (COR) as the cause of susceptibility. Rather, consistent with a previously described role in mimicking the phytohormone jasmonic acid (JA)—a major inducer of herbivore resistance in plants—, COR is shown to induce systemic plant resistance to herbivory. Thus, multiple competing signaling interactions modulate pathogen manipulation of plant resistance to herbivory.

Chapter 3 conducts gene expression profiling of Arabidopsis following infection with a COR-deficient P. syringae mutant to identify host genes whose expression is correlated with P. syringae-induced susceptibility to herbivory. Among the genes down-regulated after pathogen infection were two trypsin protease inhibitors (TIs), defense proteins known in other plants to inhibit digestion in the herbivore midgut. Preliminary genetic and biochemical experiments suggest that an Arabidopsis homologue of the soybean Kunitz-type TI may be one of the downstream targets of P. syringae manipulation resulting in increased susceptibility to herbivory. Moreover, pathogen manipulation in this case is independent of JA signaling.

Chapter 4 measures environment-dependent costs and benefits of inducing two major defense pathways, the JA pathway encoding resistance to herbivory and the salicylic acid (SA) pathway encoding resistance to pathogenesis. Plants induced with JA suffered less seed loss to herbivory due to increased resistance and tolerance, highlighting the fitness benefit of inducing appropriate resistance. In contrast, although no cost of induced resistance (measured as reduced seed set) was observed in the absence of attack, plants induced with SA suffered relatively higher seed loss to herbivory compared with uninduced plants, consistent with a previously-described antagonistic interaction between SA and JA signaling. In addition to effects on seed set, JA and SA elicited subtle, opposite effects on Arabidopsis flowering time (SA hastened and JA delay flowering date). Together, these results uncover novel pleiotropic costs of induced resistance due to modulation of life-history traits.

Chapter 5 examines the correlation between induced resistance and delayed flowering time elicited by JA. JA treatment of key JA signaling mutants demonstrates that induced resistance and delayed flowering time are underpinned by a common network and, hence, may be a coordinated response to balance the costs and benefits of resistance with reproductive timing.