Effector adaptation in a host-specialized lineage of Phytophthora

There are very few examples detailing how plant pathogen proteins have adapted to their host environments at the resolution of single amino acids, obscuring the molecular evolutionary steps that shape the process of host specialization. Here, we use closely related Phytophthoraspecies—Phytophthora infestans, a pathogen of Solanum plants, and Phytophthora mirabilis, a pathogen of four-o’-clock flower (Mirabilis jalapa)—as a molecular platform to study the specialization of a well-characterized secreted effector, PexRD54. Previously, it was shown that the P. infestansPexRD54 (PiPexRD54) targets the potato host selective autophagy protein ATG8CL during infection via a C-terminal ATG8-interacting motif (AIM), counteracting host defences and re-routing autophagosome traffic. The P. mirabilisPexRD54 ortholog (PmPexRD54) has a fixed amino-acid polymorphism in its AIM which significantly reduces binding to the M. jalapahost ATG8s (MjATG8s), as tested in both in planta co-immunoprecipitation and isothermal titration calorimetry experiments. We propose that the interaction between PmPexRD54 and the M. jalapahost ATG8s is deleterious for P. mirabilisinfection. Ongoing experiments will determine whether PmPexRD54 retains the capacity to modulate selective autophagy via other mechanisms, such as through association with host vesicle trafficking proteins.