Phytophthora pathogens secrete a large arsenal of effectors that manipulate host processes to create an environment conducive to pathogen colonization. However, the underlying mechanisms by which Phytophthora effectors manipulate host plant cells still remain largely unclear. In this study, we report that PcAvr3a12, a Phytophthora capsici RXLR effector and a member of the Avr3a effector family, suppresses plant immunity by targeting and inhibiting host plant peptidyl-prolyl cis-trans isomerase (PPIase). Overexpression of PcAvr3a12 in Arabidopsis thaliana enhanced plant susceptibility to P. capsici. FKBP15-2, an endoplasmic reticulum (ER)-localized protein, was identified as a host target of PcAvr3a12 during early P. capsici infection. Analyses of A. thaliana T-DNA insertion mutant (fkbp15-2), RNAi, and overexpression lines consistently showed that FKBP15-2 positively regulates plant immunity in response to Phytophthora infection. FKBP15-2 possesses PPIase activity essential for its contribution to immunity but is directly suppressed by PcAvr3a12. Interestingly, we found that FKBP15-2 is involved in ER stress sensing and is required for ER stress-mediated plant immunity. Taken together, these results suggest that P. capsici deploys an RXLR effector, PcAvr3a12, to facilitate infection by targeting and suppressing a novel ER-localized PPIase, FKBP15-2, which is required for ER stress-mediated plant immunity.

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In plants, recognition of small secreted peptides, such as damage/danger-associated molecular patterns (DAMPs), regulates diverse processes, including stress and immune responses. Here, we identified an SGPS (Ser-Gly-Pro-Ser) motif-containing peptide, Nicotiana tabacum NtPROPPI, and its two homologs in Nicotiana benthamiana, NbPROPPI1 and NbPROPPI2. Phytophthora parasitica infection and salicylic acid (SA) treatment induced NbPROPPI1/2 expression. Moreover, SignalP predicted that the 89-amino acid NtPROPPI includes a 24-amino acid N-terminal signal peptide and NbPROPPI1/2-GFP fusion proteins were mainly localized to the periplasm. Transient expression of NbPROPPI1/2 inhibited P. parasitica colonization, and NbPROPPI1/2 knockdown rendered plants more susceptible to P. parasitica. An eight-amino-acid segment in the NbPROPPI1 C-terminus was essential for its immune function and a synthetic 20-residue peptide, NbPPI1, derived from the C-terminus of NbPROPPI1 provoked significant immune responses in N. benthamiana. These responses led to enhanced accumulation of reactive oxygen species, activation of mitogen-activated protein kinases, and up-regulation of the defense genes Flg22-induced receptor-like kinase (FRK) and WRKY DNA-binding protein 33 (WRKY33). The NbPPI1-induced defense responses require Brassinosteroid insensitive 1-associated receptor kinase 1 (BAK1). These results suggest that NbPPI1 functions as a DAMP in N. benthamiana; this novel DAMP provides a potentially useful target for improving plant resistance to Pytophthora pathogens.

The interaction between Arabidopsis thaliana and the oomycete pathogen Phytophthora parasitica emerges as a model for exploring the molecular basis and evolution of recognition and host defense. Phenotypic variation and genetic analysis is essential to dissect the underlying mechanisms in plant–oomycete interaction. In this study, the reaction phenotypes of 28 A. thaliana accessions to P. parasitica strain Pp016 were examined using detached leaf infection assay. The results showed the presence of four distinct groups based on host response and disease development. Of all the accessions examined, Zurich (Zu-1) is highly resistant to P. parasitica. Microscopic characterization showed that rapid and severe hypersensitive response at the primary infection epidermal cells is associated with disease resistance. Furthermore, Zu-1 is resistant to a set of 20 diverse P. parasitica strains, which were collected from different host plants and exhibited differential specificities on a set of tobacco cultivars. However, Zu-1 is susceptible to P. parasitica when the root is inoculated, suggesting differential expression of associated resistance genes in the root and foliar tissues. Genetic analysis by crossing Zu-1 and the susceptible accession Landsberg (Ler) showed that the resistance in Zu-1 to P. parasitica is semi-dominant, as shown by infection assays of F1 progenies, and is likely conferred by a single locus, defined as RPPA1Zu-1 (for Resistance to P. parasitica 1), as shown by analysis of F2 segregating populations. By employing specific-locus amplified fragment sequencing (SLAF-seq) strategy to identify molecular markers potentially linked to the locus, the strongest associated region was determined to be located between 7.1 and 11.2 Mb in chromosome IV. The future cloning of RPPA1Zu-1 locus will facilitate improved understanding of plant broad-spectrum disease resistance to oomycete pathogens.