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Sohn, K. H.

Publications and source records attributed to Sohn, K. H..

8 recordsLinked to original sources

Solanum americanum Bs2 and ZAR1 homologs recognize Xanthomonas euvesicatoria effectors essential for infection.

Multiple recognition events of pathogen-secreted effectors by immune receptors confer robust disease resistance in plants. Understanding the underlying mechanisms facilitates the discovery and deployment of valuable resistance genes for crop protection. Xanthomonas euvesicatoria causes devastating bacterial spot disease in solanaceous crops but cannot infect the wild relative Solanum americanum. Here, we identified X. euvesicatoria type III effectors (T3Es) that induce cell death in S. americanum when transiently expressed in leaf. By quantifying immune responses of the S. americanum SP2273 accession to X. euvesicatoria multiple-T3E knockout mutants, we demonstrated that at least nine T3Es (AvrBs2, XopAP, XopAU, XopE1, XopJ3, XopM, XopN, XopX, and XopZ1) collectively contribute to effector-triggered immunity (ETI). Among these, AvrBs2 and XopJ3 were the primary drivers of ETI, eliciting robust cell death and defense gene expression when naturally delivered into plant cells. We next generated S. americanum lines concomitantly edited at the corresponding immune receptor loci, SaBs2 and SaZAR1 (SP2273-bz). Genetic complementation of SP2273-bz confirmed that AvrBs2 and XopJ3 are specifically recognized by each of the four SaBs2 homologs and by SaZAR1, respectively. Moreover, enhanced growth of X. euvesicatoria on the characterized SP2273-bz line indicated that both effectors are required for bacterial multiplication in S. americanum. Together, our findings provide a framework for understanding the mechanisms of ETI-mediated resistance and establish a genetic foundation for resistance breeding in solanaceous crops.

plant biology↗

Diverse haplotypes at a complex Solanum americanum locus confer resistance to Phytophthora infestans and P. capsici

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.

plant biology↗

The recognition of YopJ family effectors depends on ZAR1/JIM2 immune complex in Nicotiana benthamiana.

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 homologs of Pseudomonas tomato race 1 (NbPtr1) and HOPZ-ACTIVATED RESISTANCE 1 (NbZAR1) were recently identified as independently recognizing 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 recognized either by NbZAR1 or independently by NbZAR1 and NbPtr1. Furthermore, we show that YopJ family effector-induced HR was 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.

plant biology↗

Multiple effectors trigger nonhost resistance in Solanum americanum against Pseudomonas syringae

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.

plant biology↗

Rapid dissemination of host-metabolism-manipulating transposon-like entities via integrative and conjugative elements

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, yet ICEs that carry accessory genes encoding functions other than antimicrobial resistance remain poorly characterized. Recent observation of the 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 among a diverse array of P. syringae. Fifty-three unique ICE types were identified across multiple phylogroups. These ICEs display distinct evolutionary histories compared to their bacterial hosts, are highly recombinogenic, exhibit a conserved structure and are punctuated by hotspots of accessory gene integration. Many carry a 16 kb transposon-like entity (Tn6212) that shows little polymorphism indicating recent dissemination. Deletion of Tn6212 did not alter pathogen growth in planta, but mutants displayed significant fitness defects when grown on TCA cycle intermediates. These were largely attributable to a single LysR regulator. RNA-seq analysis of a set of nested Tn6212 deletions confirmed a central role of LysR in enhanced expression of more than 300 genes and down-regulation of genes controlling expression of energetically demanding loci. Together the transcriptional data indicate a major role for Tn6212 in manipulation of bacterial metabolism with primary effects on RNA degradation, protein synthesis and potential diversion of ATP to growth.

microbiology↗

The Ralstonia pseudosolanacearum effector RipE1 is recognized at the plasma membrane by NbPtr1, Nicotiana benthamiana homolog of Pseudomonas tomato race 1.

The bacterial wilt disease caused by soil-borne bacteria of the Ralstonia solanacearum species complex (RSSC) threatens important crops worldwide. Only a few immune receptors conferring resistance to this devastating disease are known so far. Individual RSSC strains deliver around 70 different type III secretion system effectors into host cells to manipulate the plant physiology and dampen immune responses. RipE1 is an effector conserved across RSSC isolated from diverse plant species and triggers immune responses in the model Solanaceae Nicotiana benthamiana. Here, we used multiplexed virus-induced gene silencing of the nucleotide-binding and leucine-rich repeat receptor family to identify the genetic basis of RipE1 recognition in N. benthamiana. Specific silencing of the N. benthamiana homolog of Solanum lycopersicoides Pseudomonas tomato race 1 gene (NbPtr1) completely abolished RipE1-induced hypersensitive response and immunity to Ralstonia pseudosolanacearum. In Nb-ptr1 knock-out plants, expression of the native NbPtr1 coding sequence was sufficient to restore RipE1 recognition. In addition to the putative catalytic triad Cys-His-Asp, RipE1 association with the host cell plasma membrane was found necessary for NbPtr1-dependent recognition. Furthermore, we found that NbPtr1-dependent recognition of RipE1 natural variants is polymorphic suggesting the coevolutionary nature of this interaction. This work hence provides an additional evidence for the indirect mode of activation of NbPtr1 and supports NbPtr1 relevance for resistance to bacterial wilt disease in Solanaceae.

plant biology↗

Ptr1 and ZAR1 immune receptors confer overlapping and distinct bacterial pathogen effector specificities

Nucleotide-binding and leucine-rich repeat receptors (NLRs) detect pathogen effectors inside the plant cell. To identify Nicotiana benthamiana NLRs (NbNLRs) with novel effector recognition specificity, we designed an NbNLR VIGS library and conducted a rapid reverse genetic screen. During the NbNLR VIGS library screening, we identified that N. benthamiana homolog of Ptr1 (PSEUDOMONAS SYRINGAE PV. TOMATO RACE 1 RESISTANCE) recognizes the Pseudomonas effectors AvrRpt2, AvrRpm1, and AvrB. We demonstrated that recognition of the Xanthomonas effector AvrBsT and the Pseudomonas effector HopZ5 in N. benthamiana is conferred independently by N. benthamiana homolog of Ptr1 and ZAR1 (HOPZ-ACTIVATED RESISTANCE 1). In addition, we showed that the RLCK XII family protein JIM2 (XOPJ4 IMMUNITY 2) physically interacts with AvrBsT and HopZ5 and is required for the NbZAR1-dependent recognition of AvrBsT and HopZ5. The recognition of multiple bacterial effectors by Ptr1 and ZAR1 in N. benthamiana demonstrates a convergent evolution of effector recognition across plant species. Identification of key components involved in Ptr1 and ZAR1 mediated immunity would reveal unique mechanisms of expanded effector recognition and be useful for engineering resistance in solanaceous crops.

plant biology↗

Direct acetylation of the conserved threonine of an immune regulator by bacterial effectors activates RPM1-dependent immunity in Arabidopsis

Plant pathogenic bacteria deliver effectors into plant cells to suppress immunity and promote pathogen survival (Buttner, 2016; Deslandes and Rivas, 2012); however, these effectors can be recognised by plant disease resistance (R) proteins to activate innate immunity (Jones and Dangl, 2006; Spoel and Dong, 2012). The bacterial acetyltransferase effectors HopZ5 and AvrBsT trigger immunity in Arabidopsis thaliana genotypes lacking SUPPRESSOR OF AVRBST-ELICITED RESISTANCE 1 (SOBER1) (Choi et al., 2018; Jayaraman et al., 2017). Using an Arabidopsis accession, Tscha-1, that naturally lacks functional SOBER1 but is unable to recognise HopZ5, we demonstrate that RESISTANCE TO P. SYRINGAE PV MACULICOLA 1 (RPM1) and RPM1-INTERACTING PROTEIN 4 (RIN4) are indispensable for HopZ5- or AvrBsT-triggered immunity. Remarkably, T166 of RIN4, the phosphorylation of which is induced by AvrB and AvrRpm1, was directly acetylated by HopZ5 and AvrBsT. Furthermore, we demonstrate that acetylation of RIN4 T166 is required and sufficient for activation of HopZ5- or AvrBsT-triggered defence. Finally, we show that SOBER1 interferes with HopZ5- or AvrBsT-triggered immunity by deacetylating RIN4 T166. Our findings indicate that multiple pathogen effectors with distinct biochemical properties modify a single residue in a guardee protein and activate a plant NLR immune receptor. We have thus elucidated detailed molecular mechanisms underlying the activation and suppression of plant innate immunity triggered by bacterial acetyltransferases.

plant biology↗