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.

Antibiosis is a key feature widely exploited to develop biofungicides based on the ability of biological control agents (BCAs) to produce fungitoxic compounds. A less recognised attribute of plant-associated beneficial microorganisms is their ability to stimulate the plant immune system, which may provide long-term, systemic self-protection against different types of pathogens. By using conventional antifungal in vitro screening coupled with in planta assays, we found antifungal and non-antifungal Bacillus strains that protected the ornamental plant Kalanchoe against the soil-borne pathogen Fusarium oxysporum in experimental and commercial production settings. Further examination of one antifungal and one non-antifungal strain indicated that high protection efficacy in planta did not correlate with antifungal activity in vitro. Whole-genome sequencing showed that the non-antifungal strain EC9 lacked the biosynthetic gene clusters associated with typical antimicrobial compounds. Instead, this bacterium triggers the expression of marker genes for the jasmonic and salicylic acid defence pathways, but only after pathogen challenge, indicating that this strain may protect Kalanchoe plants by priming immunity. We suggest that the stimulation of the plant immune system is a promising mode of action of BCAs for the development of novel biological crop protection products.

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.

Oomycetes, particularly Phytophthora species, cause destructive plant diseases that severely threaten sustainable crop production. Due to the loss of genotype-specific disease resistance, it is important to identify and understand immune factors that mediate plant susceptibility. Loss-of-function of the susceptibility factor resistance to Phytophthora parasitica 1 (RTP1) leads to broad-spectrum disease resistance in Arabidopsis thaliana (A. thaliana (L.) Heynh.). Through RNA-seq analysis, we determined that CYP71B3, encoding an uncharacterized P450 enzyme, is significantly upregulated in rtp1 mutant plants infected with P. parasitica. Loss-of-function of CYP71B3 led to abolished pathogen-associated molecular pattern (PAMP)–triggered oxidative burst and rendered Arabidopsis more susceptible to diverse pathogens, including the oomycete P. parasitica and bacterial Pseudomonas syringae. Conversely, overexpression of CYP71B3 enhanced plant resistance and PAMP-triggered oxidative burst. CYP71B3 localized in the endoplasmic reticulum and was destabilized by interacting with RTP1 via the I-38 residue, which is essential for its immune function and P450 enzyme activity. The expression of CYP71B3 was regulated by transcription factor bZIP60, which is required for rtp1-mediated resistance to P. parasitica. Our studies indicate that RTP1 mediates plant susceptibility by destabilizing the downstream positive immune factor CYP71B3.

The symbiotic fungus Serendipita indica confers broad-spectrum beneficial effects on diverse plant hosts. Its key effector SIE141 elicits immunity against Phytophthora and salt tolerance by binding and relocalizing thioredoxin CDSP32 from chloroplast to the nucleus. Here, we show that this functionally essential nuclear transfer process of the SIE141-CDSP32 complex is mediated by the host NTF2 proteins. NTF2 family proteins are direct targets of SIE141, whose knockdown abolished nuclear accumulation of both SIE141 and CDSP32, leading to their rendered accumulation to chloroplasts. The glutamine residue at position 40 of NbNTF2A is critical for its interaction with both SIE141 and Ran-GTPase 1. SIE141 modulates NbNTF2-NbRan1 interaction in a dose-dependent manner, without impairing nuclear accumulation of NbRan1 and the NTF2-mediated positive immune function of Ran1. Our results reveal a previously unknown mechanism where a beneficial symbiotic fungal effector utilizes the conserved NTF2 rather than other core nuclear import machinery components to traffic an immune complex and enhance disease resistance. These findings provide a potential strategy for engineering plant immunity by manipulating NTF2–Ran-GTPase dependent nucleocytoplasmic transport.

Plant-colonizing mutualistic symbionts confer beneficial effects to their hosts, which often includes increased growth as well as biotic and abiotic stress resilience. How these benefits are activated on a molecular level is mostly unknown. Here, we describe effector candidates of the fungal symbiont Serendipita indica (Si), which modulate plant stress signaling pathways. By analyzing the Si effector interactome, we reveal frequent targeting of stress-related host proteins, which are linked to the identified effector signaling functions. Moreover, functional data indicate that Si effectors modulate abiotic stress response of Arabidopsis, as well as resistance to pathogen infection. Analysis of symbiont effectors might not only uncover previously unreported molecular mechanisms that increase plant fitness but might also be used to identify potential genetic traits for crop improvement under changing climates.