Phytophthora species are destructive plant pathogens that cause significant crop losses worldwide. To understand plant susceptibility to oomycete pathogens and to explore novel disease resistance strategies, we employed the Arabidopsis thaliana–Phytophthora parasitica model pathosystem and screened for A. thaliana T‐DNA insertion mutant lines resistant to P. parasitica. This led to the identification of the resistant mutant 267‐31, which carries two T‐DNA insertion sites in the promoter region of the ethylene‐responsive factor 19 gene (ERF019). Quantitative reverse transcription PCR (RT‐qPCR) assays showed that the expression of ERF019 was induced during P. parasitica infection in the wild type, which was suppressed in the 267‐31 mutant. Additional erf019 mutants were generated using CRISPR/Cas9 technology and were confirmed to have increased resistance to P. parasitica. In contrast, ERF019 overexpression lines were more susceptible. Transient overexpression assays in Nicotiana benthamiana showed that the nuclear localization of ERF019 is crucial for its susceptible function. RT‐qPCR analyses showed that the expression of marker genes for multiple defence pathways was significantly up‐regulated in the mutant compared with the wild type during infection. Flg22‐induced hydrogen peroxide accumulation and reactive oxygen species burst were impaired in ERF019 overexpression lines, and flg22‐induced MAPK activation was enhanced in erf019 mutants. Moreover, transient overexpression of ERF019 strongly suppressed INF‐triggered cell death in N. benthamiana. These results reveal the importance of ERF019 in mediating plant susceptibility to P. parasitica through suppression of pathogen‐associated molecular pattern‐triggered immunity.

Mitochondrial function depends on the RNA processing of mitochondrial gene transcripts by nucleus-encoded proteins. This posttranscriptional 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.

Proteases secreted by pathogens have been shown to be important virulence factors modifying plant immunity, and cysteine proteases have been demonstrated to participate in different pathosystems. However, the virulence functions of the cysteine proteases secreted by Phytophthora parasitica are poorly understood. Using a publicly available genome database, we identified 80 cysteine proteases in P. parasitica , 21 of which were shown to be secreted. Most of the secreted cysteine proteases are conserved among different P. parasitica strains and are induced during infection. The secreted cysteine protease proteins PpCys44/45 (proteases with identical protein sequences) and PpCys69 triggered cell death on the leaves of different Nicotiana spp. A truncated mutant of PpCys44/45 lacking a signal peptide failed to trigger cell death, suggesting that PpCys44/45 functions in the apoplastic space. Analysis of three catalytic site mutants showed that the enzyme activity of PpCys44/45 is required for its ability to trigger cell death. A virus‐induced gene silencing assay showed that PpCys44/45 does not induce cell death on NPK1 ( Nicotiana Protein Kinase 1 )‐silenced Nicotiana benthamiana plants, indicating that the cell death phenotype triggered by PpCys44/45 is dependent on NPK1 . PpCys44‐ and PpCys45‐deficient double mutants showed decreased virulence, suggesting that PpCys44 and PpCys45 positively promote pathogen virulence during infection. PpCys44 and PpCys45 are important virulence factors of P. parasitica and trigger NPK1‐ dependent cell death in various Nicotiana spp.

The late blight caused by Phytophthora infestans (P. infestans) has been a major constraint for worldwide sustainable potato production. Chinese potato cultivar Qingshu 9 has shown excellent field performance against late blight. To understand the mechanism underlying its resistance, the transcriptomic dynamics of Qingshu 9 infected with P. infestans was systematically investigated to identify the resistance-related genes. In total, 2027 shared differentially expressed genes (DEGs) were identified when infected with P. infestans at 24, 48 and 72 h post-inoculation. Based on k-mean cluster analysis, the DEGs showed four types of expression patterns, suggesting their divergent functions in response to P. infestans infection. KEGG enrichment analysis showed that the significantly enriched DEGs were involved in the biosynthesis of secondary metabolites, plant–pathogen interaction, and photosynthesis. Furthermore, 980 transcription factor genes belonging to 68 families were found in the DEGs, of which AP2-EREBP and MYB genes were the most abundant. Moreover, many genes related to disease resistance showed differential expression during infection. Finally, the expression of nine DEGs was validated by quantitative real-time PCR. These results provide valuable information for understanding late resistance in potato cultivar Qingshu 9.

Reactive oxygen species (ROS) are key signaling molecules in plant development and immunity, but current understanding is primarily focused on apoplastic and chloroplastic ROS. Mitochondria are also a key source of intracellular ROS, yet their contribution to plant immunity is poorly characterized. Here, we studied mitochondrial ROS (mROS) function in plant-pathogen interactions, deploying genetically encoded sensors, assorted fluorescent markers, and genetic approaches to track mROS, specifically H ₂ O ₂ , dynamics and identify interorganelle contact sites. We unexpectedly found a mitochondria–endoplasmic reticulum (ER) ROS signal cascade functioning independently of apoplastic and chloroplastic ROS in plant immunity. mROS initiate immune responses induced by the oomycete pathogen Phytophthora parasitica and promote mitochondria-ER association. These enhanced mitochondria-ER membrane associations are required for transfer of mROS signals and initiation of extensive unfolded protein responses. We conclude that mROS transfer via mitochondria-ER membranes to the ER lumen is an underappreciated yet essential component in plant defense.

Nonhost resistance refers to resistance of a plant species to all genetic variants of a non-adapted pathogen. Such resistance has the potential to become broad-spectrum and durable crop disease resistance. We previously employed Arabidopsis thaliana and a forward genetics approach to identify plant mutants susceptible to the nonhost pathogen Phytophthora sojae, which resulted in identification of the T-DNA insertion mutant esp1 (enhanced susceptibility to Phytophthora). In this study, we report the identification of VQ motif-containing protein 28 (VQ28), whose expression was highly up-regulated in the mutant esp1. Stable transgenic A. thaliana plants constitutively overexpressing VQ28 compromised nonhost resistance (NHR) against P. sojae and P. infestans, and supported increased infection of P. parasitica. Transcriptomic analysis showed that overexpression of VQ28 resulted in six differentially expressed genes (DEGs) that are involved in the response to abscisic acid (ABA). High performance liquid chromatography-mass spectrometry (HPLC-MS) detection showed that the contents of endogenous ABA, salicylic acid (SA), and jasmonate (JA) were enriched in VQ28 overexpression lines. These findings suggest that overexpression of VQ28 may lead to an imbalance in plant hormone homeostasis. Furthermore, transient overexpression of VQ28 in Nicotiana benthamiana rendered plants more susceptible to Phytophthora pathogens. Deletion mutant analysis showed that the C-terminus and VQ-motif were essential for plant susceptibility. Taken together, our results suggest that VQ28 negatively regulates plant NHR to Phytophthora pathogens.