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.

Mitochondrial function depends on the RNA processing of mitochondrial gene transcripts by nucleus-encoded proteins. This post-transcriptional processing involves the large group of nuclear-encoded pentatricopeptide repeat (PPR) proteins. Mitochondrial processes represent a crucial part in animal immunity, but whether mitochondria play similar roles in plants remains unclear. Here, we report the identification of RESISTANCE TO PHYTOPHTHORA PARASITICA 7 (AtRTP7), a P-type PPR protein, in Arabidopsis thaliana and its conserved function in immunity to diverse pathogens across distantly related plant species. RTP7 affects the levels of mitochondrial reactive oxygen species (mROS) by participating in RNA splicing of nad7, which encodes a critical subunit of the mitochondrial respiratory chain Complex I, the largest of the four major components of the mitochondrial oxidative phosphorylation system. The enhanced resistance of rtp7 plants to Phytophthora parasitica is dependent on an elevated mROS burst, but might be independent from the ROS burst associated with plasma membrane-localized NADPH oxidases. Our study reveals the immune function of RTP7 and the defective processing of Complex I subunits in rtp7 plants resulted in enhanced resistance to both biotrophic and necrotrophic pathogens without affecting overall plant development.