Kee Hoon Sohn

Plants encounter diverse pathogens and have evolved a 2-layered innate immune system to detect pathogen molecules and activate defense mechanisms that restrict infection. Most cloned plant Resistance (R) genes encode NLR immune receptors. NLR genes are often found in clusters of paralogs with sequence and copy number variation; whether these NLR clusters evolve in response to single or multiple pathogens has been unclear. We report here the isolation of a Phytophthora capsici resistance gene, Rpc2, along with a novel P. infestans resistance gene, Rpi-amr5, from 2 Solanum americanum accessions. These orthologous genes reside in the Rpi-amr1 cluster, which has previously been associated with resistance to P. infestans. By screening RXLR effector libraries of P. infestans and P. capsici, we identified multiple effectors recognized by both NLRs. Our findings highlight the complexity of NLR clusters and evolution driven by interactions with multiple pathogens. This work will underpin efforts to elevate resistance against Phytophthora pathogens and enhances our understanding of NLR evolution.

Potato late blight, caused by the oomycete pathogen Phytophthora infestans , remains one of the most serious threats to global food security. Plants rely on a sophisticated intracellular immune system centered on nucleotide-binding leucine-rich repeat (NLR) receptors to perceive pathogen effectors. However, the rapid evolution of these effectors often renders individual resistance ( R ) genes ineffective within a short time frame. In a recent study, Wang et al . (Nature, 2025, https://doi.org/10.1038/s41586-025-09678-5 ) addressed this long-standing challenge by constructing a section-wide NLRome for potato. This comprehensive resource enabled cloning three previously unknown late blight R genes and led to the proposal of a ‘plug-in’ strategy for modular and precision resistance engineering.

Pathogens deploy effector proteins to manipulate host physiology and promote infection. YopJ family effectors are highly conserved across bacterial genera that cause crop diseases. Nucleotide‐binding leucine‐rich repeat receptors (NLRs) play a central role in direct or indirect recognition of effectors and trigger immune responses, including hypersensitive cell death (HR). Two NLRs, Nicotiana benthamiana homologues of Pseudomonas tomato race 1 (NbPtr1) and HOPZ‐ACTIVATED RESISTANCE 1 (NbZAR1), were recently identified as independently recognising two YopJ family effectors, HopZ5 and AvrBsT/XopJ2. NbZAR1 also detects XopJ4 via the receptor‐like cytoplasmic kinase XOPJ4 IMMUNITY 2 (JIM2). Here, we conducted Agrobacterium ‐mediated transient expression assays with 20 YopJ family effectors from five phytopathogenic bacterial genera and identified 12 YopJ family effectors that are recognised either by NbZAR1 or independently by NbZAR1 and NbPtr1. Furthermore, we show that YopJ family effector‐induced HR is differentially suppressed by the deacetylase SUPPRESSOR OF AVRBST‐ELICITED RESISTANCE 1, suggesting more than one mechanism for YopJ family effector recognition. This work provides the genetic basis of the recognition of YopJ family effectors in N. benthamiana and lays a foundation for the mechanistic study of NbZAR1/JIM2 and NbPtr1 mode of activation.

Plants encounter diverse pathogens and have evolved a two-layered innate immune system to detect pathogen molecules and activate defense mechanisms that restrict infection. Most cloned plant Resistance ( R ) genes encode NLR immune receptors. NLR genes are often found in clusters of paralogs with sequence and copy number variation; whether these NLR clusters evolve in response to single or multiple pathogens has been unclear. We report here the isolation of a Phytophthora capsici resistance gene, Rpc2 , along with a novel P. infestans resistance gene, Rpi-amr5 , from two Solanum americanum accessions. These orthologous genes reside in the Rpi-amr1 cluster, which has previously been associated with resistance to P. infestans . By screening RXLR effector libraries of P. infestans and P. capsici , we identified multiple effectors recognized by both NLRs. Our findings highlight the complexity of NLR clusters and evolution driven by interactions with multiple pathogens. This work will underpin efforts to elevate resistance against Phytophthora pathogens and enhances our understanding of NLR evolution.

SUMMARY: Wild plant species are threatened by diverse pathogens, but disease symptoms are rarely observed in nature. This suggests that wild plants harbor valuable sources of resistance. In this study, we show that the model bacterial pathogen Pseudomonas syringae pv. tomato ( Pto ) DC3000 triggered defense responses in all tested accessions of a wild Solanaceae species, Solanum americanum . Pto DC3000‐triggered immunity in S. americanum required a type III secretion system. We show that seven Pto DC3000 effectors (AvrPto, HopAD1, HopAM1, HopC1, HopAA1‐1, HopM1, and AvrE1) triggered hypersensitive responses (HR) in S. americanum accession SP2273. Significantly, sequential deletion of the HR‐triggering effectors from Pto DC3000 resulted in enhanced virulence in S. americanum . However, the well‐conserved effectors, HopM1 and AvrE1, were indispensable for virulence. We conclude that the immunity triggered by multiple effectors contributes to nonhost resistance in S. americanum against P. syringae . We propose that the identification of the corresponding disease resistance genes for HopM1 and AvrE1 in S. americanum would accelerate the development of durable immunity to P. syringae pathogens in Solanaceae crops.

Wild plant species are threatened by diverse pathogens, but disease symptoms are rarely observed in nature. This suggests that wild plants harbor valuable sources of resistance. In this study, we show that a model bacterial pathogen Pseudomonas syringae pv. tomato ( Pto ) DC3000 triggered defense responses in all tested accessions of a wild Solanaceae species, Solanum americanum . Pto DC3000-triggered immunity in S. americanum required type III secretion system. We show that seven Pto DC3000 effectors (AvrPto, HopAD1, HopAM1, HopC1, HopAA1-1, HopM1, and AvrE1) triggered hypersensitive responses (HR) in S. americanum accession SP2273. Significantly, sequential deletion of the HR-triggering effectors from Pto DC3000 resulted in enhanced virulence in S. americanum . However, the well-conserved effectors, HopM1 and AvrE1 were indispensable for virulence. We conclude that the immunity triggered by multiple effectors contributes to nonhost resistance in S. americanum against P. syringae . We propose that the identification of the corresponding disease resistance genes for HopM1 and AvrE1 in S. americanum would accelerate development of durable immunity to P. syringae pathogens in Solanaceae crops.

In plants, balancing growth and environmental responses is crucial for maximizing fitness. Close proximity among plants and canopy shade, which negatively impacts reproduction, elicits morphological adjustments such as hypocotyl growth and leaf hyponasty, mainly through changes in light quality and auxin levels. However, how auxin, synthesized from a shaded leaf blade, distally induces elongation of hypocotyl and petiole cells remains to be elucidated. We demonstrated that ASYMMETRIC LEAVES1 (AS1) promotes leaf hyponasty through the regulation of auxin biosynthesis, polar auxin transport, and auxin signaling genes in Arabidopsis (Arabidopsis thaliana). AS1 overexpression leads to elongation of the abaxial petiole cells with auxin accumulation in the petiole, resulting in hyponastic growth, which is abolished by the application of an auxin transport inhibitor to the leaf blade. In addition, the as1 mutant exhibits reduced hypocotyl growth under shade conditions. We observed that AS1 protein accumulates in the nucleus in response to shade or far-red light. Chromatin immunoprecipitation analysis identified the association of AS1 with the promoters of YUCCA8 (YUC8) and INDOLE-3-ACETIC ACID INDUCIBLE 19 (IAA19). In addition, AS1 forms complexes with PHYTOCHROME INTERACTING FACTORs in the nucleus and synergistically induces YUC8 and IAA19 expression. Our findings suggest that AS1 plays a crucial role in facilitating phenotypic plasticity to the surroundings by connecting light and phytohormone action.

Integrative and conjugative elements (ICEs) are self-transmissible mobile elements that transfer functional genetic units across broad phylogenetic distances. Accessory genes shuttled by ICEs can make significant contributions to bacterial fitness. Most ICEs characterized to date encode readily observable phenotypes contributing to symbiosis, pathogenicity, and antimicrobial resistance, yet the majority of ICEs carry genes of unknown function. Recent observations of rapid acquisition of ICEs in a pandemic lineage of Pseudomonas syringae pv. actinidae led to investigation of the structural and functional diversity of these elements. Fifty-three unique ICE types were identified across the P. syringae species complex. Together they form a distinct family of ICEs (PsICEs) that share a distant relationship to ICEs found in Pseudomonas aeruginosa . PsICEs are defined by conserved backbone genes punctuated by an array of accessory cargo genes, are highly recombinogenic, and display distinct evolutionary histories compared to their bacterial hosts. The most common cargo is a recently disseminated 16-kb mobile genetic element designated Tn 6212 . Deletion of Tn 6212 did not alter pathogen growth in planta, but mutants displayed fitness defects when grown on tricarboxylic acid (TCA) cycle intermediates. RNA-seq analysis of a set of nested deletion mutants showed that a Tn 6212 -encoded LysR regulator has global effects on chromosomal gene expression. We show that Tn 6212 responds to preferred carbon sources and manipulates bacterial metabolism to maximize growth.

SUMMARY: Arabidopsis thaliana WRKY proteins are potential targets of pathogen‐secreted effectors. RESISTANT TO RALSTONIA SOLANACEARUM 1 (RRS1; AtWRKY52) is a well‐studied Arabidopsis nucleotide‐binding and leucine‐rich repeat (NLR) immune receptor carrying a C‐terminal WRKY domain that functions as an integrated decoy. RRS1‐R recognizes the effectors AvrRps4 from Pseudomonas syringae pv. pisi and PopP2 from Ralstonia pseudosolanacearum by direct interaction through its WRKY domain. AvrRps4 and PopP2 were previously shown to interact with several AtWRKYs. However, how these effectors selectively interact with their virulence targets remains unknown. Here, we show that several members of subgroup IIIb of the AtWRKY family are targeted by AvrRps4 and PopP2. We demonstrate that several AtWRKYs induce cell death when transiently expressed in Nicotiana benthamiana, indicating the activation of immune responses. AtWRKY54 was the only cell death‐inducing AtWRKY that interacted with both AvrRps4 and PopP2. We found that AvrRps4 and PopP2 specifically suppress AtWRKY54‐induced cell death. We also demonstrate that the amino acid residues required for the avirulence function of AvrRps4 and PopP2 are critical for suppressing AtWRKY54‐induced cell death. AtWRKY54 residues predicted to form a binding interface with AvrRps4 were predominantly located in the DNA binding domain and necessary for inducing cell death. Notably, one AtWRKY54 residue, E164, contributes to affinity with AvrRps4 and is exclusively present among subgroup IIIb AtWRKYs, yet is located outside of the DNA‐binding domain. Surprisingly, AtWRKY54 mutated at E164 evaded AvrRps4‐mediated cell death suppression. Taking our observations together, we propose that AvrRp4 and PopP2 specifically target AtWRKY54 to suppress plant immune responses.