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  1. Abstract

    Basic helix–loop–helix (bHLH) transcription factors constitute a superfamily in eukaryotes, but their roles in plant immunity remain largely uncharacterized. We found that the transcript abundance in tomato (Solanum lycopersicum) leaves of one bHLH transcription factor-encoding gene, negative regulator of resistance to DC3000 1 (Nrd1), increased significantly after treatment with the immunity-inducing flgII-28 peptide. Plants carrying a loss-of-function mutation in Nrd1 (Δnrd1) showed enhanced resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 although early pattern-triggered immunity responses, such as generation of reactive oxygen species and activation of mitogen-activated protein kinases after treatment with flagellin-derived flg22 and flgII-28 peptides, were unaltered compared to wild-type plants. RNA-sequencing (RNA-seq) analysis identified a gene, Arabinogalactan protein 1 (Agp1), whose expression is strongly suppressed in an Nrd1-dependent manner. Agp1 encodes an arabinogalactan protein, and overexpression of the Agp1 gene in Nicotiana benthamiana led to ∼10-fold less Pst growth compared to the control. These results suggest that the Nrd1 protein promotes tomato susceptibility to Pst by suppressing the defense gene Agp1. RNA-seq also revealed that the loss of Nrd1 function has no effect on the transcript abundance of immunity-associated genes, including AvrPtoB tomato-interacting 9 (Bti9), Cold-shock protein receptor (Core), Flagellin sensing 2 (Fls2), Flagellin sensing (Fls3),more »and Wall-associated kinase 1 (Wak1) upon Pst inoculation, suggesting that the enhanced immunity observed in the Δnrd1 mutants is due to the activation of key PRR signaling components as well as the loss of Nrd1-regulated suppression of Agp1.

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  2. Summary

    Some nucleotide‐binding and leucine‐rich repeat receptors (NLRs) indirectly detect pathogen effectors by monitoring their host targets. InArabidopsis thaliana, RIN4 is targeted by multiple sequence‐unrelated effectors and activates immune responses mediated by RPM1 and RPS2. These effectors trigger cell death inNicotiana benthamiana, but the corresponding NLRs have yet not been identified. To identifyN. benthamianaNLRs (NbNLRs) that recognize Arabidopsis RIN4‐targeting effectors, we conducted a rapid reverse genetic screen using an NbNLR VIGS library.

    We identified that theN. benthamianahomolog of Ptr1 (Pseudomonas tomato race 1) recognizes thePseudomonaseffectors AvrRpt2, AvrRpm1, and AvrB.

    We demonstrated that recognition of theXanthomonaseffector AvrBsT and thePseudomonaseffector HopZ5 is conferred independently by theN. benthamianahomolog of Ptr1 and ZAR1. Interestingly, the recognition of HopZ5 and AvrBsT is contributed unequally by Ptr1 and ZAR1 inN. benthamianaandCapsicum annuum. In addition, we showed that the RLCK XII family protein JIM2 is required for the NbZAR1‐dependent recognition of AvrBsT and HopZ5.

    The recognition of sequence‐unrelated effectors by NbPtr1 and NbZAR1 provides an additional example of convergently evolved effector recognition. Identification of key components involved in Ptr1 and ZAR1‐mediated immunity could reveal unique mechanisms of expanded effector recognition.

    Free, publicly-accessible full text available June 19, 2024
  3. Abstract

    Solanum pimpinellifolium(SP) is the wild progenitor of cultivated tomato. Because of its remarkable stress tolerance and intense flavor, SP has been used as an important germplasm donor in modern tomato breeding. Here, we present a high-quality chromosome-scale genome sequence of SP LA2093. Genome comparison identifies more than 92,000 structural variants (SVs) between LA2093 and the modern cultivar, Heinz 1706. Genotyping these SVs in ~600 representative tomato accessions identifies alleles under selection during tomato domestication, improvement and modern breeding, and discovers numerous SVs overlapping genes known to regulate important breeding traits such as fruit weight and lycopene content. Expression quantitative trait locus (eQTL) analysis detects hotspots harboring master regulators controlling important fruit quality traits, including cuticular wax accumulation and flavonoid biosynthesis, and SVs contributing to these complex regulatory networks. The LA2093 genome sequence and the identified SVs provide rich resources for future research and biodiversity-based breeding.


    Wild relatives of tomato are a valuable source of natural variation in tomato breeding, as many can be hybridized to the cultivated species (Solanum lycopersicum). Several, includingSolanum lycopersicoides, have been crossed toS. lycopersicumfor the development of ordered introgression lines (ILs), facilitating breeding for desirable traits. Despite the utility of these wild relatives and their associated ILs, few finished genome sequences have been produced to aid genetic and genomic studies. Here we report a chromosome‐scale genome assembly forS. lycopersicoidesLA2951, which contains 37 938 predicted protein‐coding genes. With the aid of this genome assembly, we have precisely delimited the boundaries of theS. lycopersicoidesintrogressions in a set ofS. lycopersicumcv. VF36 × LA2951 ILs. We demonstrate the usefulness of the LA2951 genome by identifying several quantitative trait loci for phenolics and carotenoids, including underlying candidate genes, and by investigating the genome organization and immunity‐associated function of the clusteredPtogene family. In addition, syntenic analysis of R2R3MYB genes sheds light on the identity of theAuberginelocus underlying anthocyanin production. The genome sequence and IL map provide valuable resources for studying fruit nutrient/quality traits, pathogen resistance, and environmental stress tolerance. We present a new genome resource for the wild speciesS. lycopersicoides, which we use to shed light on theAuberginelocus responsiblemore »for anthocyanin production. We also provide IL boundary mappings, which facilitated identifying novel carotenoid quantitative trait loci of which one was likely driven by an uncharacterized lycopene β‐cyclase whose function we demonstrate.

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  5. Summary

    The interaction between tomato andPseudomonas syringaepv tomato (Pst) is a well‐developed model for investigating the molecular basis of the plant immune system. There is extensive natural variation inSolanum lycopersicum(tomato) but it has not been fully leveraged to enhance our understanding of the tomato–Pstpathosystem. We screened 216 genetically diverse accessions of cultivated tomato and a wild tomato species for natural variation in their response to three strains ofPst.

    The host response toPstwas investigated using multiplePststrains, tomato accessions with available genome sequences, reactive oxygen species (ROS) assays, reporter genes and bacterial population measurements.

    The screen uncovered a broad range of previously unseen host symptoms in response toPst, and one of these, stem galls, was found to be simply inherited. The screen also identified tomato accessions that showed enhanced responses to flagellin in bacterial population assays and in ROS assays upon exposure to flagellin‐derived peptides, flg22 and flgII‐28. Reporter genes confirmed that the host responses were due primarily to pattern recognition receptor‐triggered immunity.

    This study revealed extensive natural variation in tomato for susceptibility and resistance toPstand will enable elucidation of the molecular mechanisms underlying these host responses.