The evolution of Pseudomonas syringae host specificity and type III effector repertoires

Abstract

The discovery 45 years ago that many Pseudomonas syringae pathovars elicit the hypersensitive response in plant species other than their hosts fostered the use of these bacteria as experimental models. However, the basis for host specificity and the corresponding resistance of nonhosts remain unclear. Pseudomonas syringae is now known to inject into the host cytoplasm, via the type III secretion system, effector proteins that suppress basal innate immunity, but may be recognized by cognate resistance (R) proteins in a second level of defence. The identification and manipulation of complete repertoires of type III effectors have revealed the highly polymorphic nature of effector repertoires and their potential to limit the host range. However, the maintenance of compatible effector repertoires may be driven by adaptations to life in a given plant species involving many factors. Tools are now available to test several hypotheses for the nature and evolution of P. syringae host specificity and nonhost resistance.

Figure 1

Model for the role of type III effector repertoires as highly polymorphic, qualitative limiters of Pseudomonas syringae host range at the pathovar–species level (nonhost resistance) and race–cultivar level (host resistance). The model presents several examples of P. syringae strains interacting with resistant plants. Host vs. nonhost resistance and type I vs. type II nonhost resistance are represented as outcomes of a continuum of processes, shown in the next column, contributing to these interaction types. The model postulates that host specialization may evolve through adaptation to quantitative effects of polymorphisms among plant species involving nutrients, antimicrobials, pathogen‐associated molecular pattern (PAMP) perception and PAMP‐triggered immunity (PTI) suppression. However, effector repertoires co‐evolving to evade effector‐triggered immunity (ETI)‐mediated host resistance will accumulate many incompatibilities with the ETI systems of other plant species. The ETI system is presented in bold because the recognition of a single effector by highly polymorphic resistance (R) protein repertoires can produce qualitative resistance. Because of the apparent conservation of several components of the PTI system and potential redundancies in the effectors targeting them, we postulate that nonadapted strains will be only quantitatively penalized at the PTI suppression step. Pseudomonas syringae pathovar abbreviations: Pph, phaseolicola; Psg, glycinea; Pto, tomato.