Distinct modes of derepression of an
            <i>Arabidopsis</i>
            immune receptor complex by two different bacterial effectors

Ma, Yan; Guo, Hailong; Hu, Lanxi; Martinez, Paula Pons; Moschou, Panagiotis N.; Çevik, Volkan; Ding, Pingtao; Duxbury, Zane; Sarris, Panagiotis F.; Jones, Jonathan D. G.

doi:10.1073/pnas.1811858115

Cited by 91 publications

(127 citation statements)

References 39 publications

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“…In rice, the BIK1 orthologs OsRLCK176 and OsRLCK185 were shown to associate with OsCERK1 to mediate the chitin and peptidoglycan‐triggered immune signaling (Couto and Zipfel 2016; Li et al 2017). In addition to the RLCK group VII members, Arabidopsis RLCK group XII members BR‐SIGNALING KINASE 1 (BSK1) and BSK5 have also been reported to play a crucial role in PTI by interacting with PRRs directly (Shi et al 2013; Majhi et al 2019; Zhao et al 2019).…”

Section: Recent Discoveries Of the Activation Of Immunity Mediated Bymentioning

confidence: 99%

Plant immune signaling: Advancing on two frontiers

Wang

Feng

Zhou

et al. 2020

JIPB

176

144

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Plants have evolved multiple defense strategies to cope with pathogens, among which plant immune signaling that relies on cell-surface localized and intracellular receptors takes fundamental roles. Exciting breakthroughs were made recently on the signaling mechanisms of pattern recognition receptors (PRRs) and intracellular nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domain receptors (NLRs). This review summarizes the current view of PRRs activation, emphasizing the most recent discoveries about PRRs' dynamic regulation and signaling mechanisms directly leading to downstream molecular events including mitogen-activated protein kinase (MAPK) activation and calcium (Ca 2+ ) burst. Plants also have evolved intracellular NLRs to perceive the presence of specific pathogen effectors and trigger more robust immune responses. We also discuss the current understanding of the mechanisms of NLR activation, which has been greatly advanced by recent breakthroughs including structures of the first full-length plant NLR complex, findings of NLR sensor-helper pairs and novel biochemical activity of Toll/interleukin-1 receptor (TIR) domain.

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Section: Recent Discoveries Of the Activation Of Immunity Mediated Bymentioning

confidence: 99%

Plant immune signaling: Advancing on two frontiers

Wang

Feng

Zhou

et al. 2020

JIPB

176

144

View full text Add to dashboard Cite

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“…Some regions appear to be the source of major Cf loci, like MW, which are able to generate multiple effector-specific RLPs (RIVAS AND THOMAS 2005;DE WIT et al 2009). Although distinct recognition of multiple effectors by one or more R proteins is known (MACKEY et al 2002;MA et al 2018), the opposite has only been observed as convergent evolution in different species (ASHFIELD et al 2014;SAUCET et al 2015;CARTER et al 2018) with only one recent example in closely related species (AGUILERA-GALVEZ et al 2018). However, considering the monomorphic nature of Ecp5 and level of genetic complexity observed amongst Cf-Ecp5 genes in this study, we have to address this slight paradox in terms of evolution.…”

Section: Discussionmentioning

confidence: 92%

Genes encoding recognition of theCladosporium fulvumeffector protein Ecp5 are encoded at several loci in the tomato genome

Iakovidis

Soumpourou

Anderson

et al. 2019

Preprint

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The molecular interactions between tomato and Cladosporium fulvum have been an important model for molecular plant pathology. Complex genetic loci on tomato chromosomes 1 and 6 harbor genes for resistance to Cladosporium fulvum, encoding receptor like-proteins that perceive distinct Cladosporium fulvum effectors and trigger plant defenses. Here, we report classical mapping strategies for loci in tomato accessions that respond to Cladosporium fulvum effector Ecp5, which is very sequencemonomorphic. We screened 139 wild tomato accessions for an Ecp5-induced hypersensitive response, and in five accessions, the Ecp5-induced hypersensitive response segregated as a monogenic trait, mapping to distinct loci in the tomato genome. We identified at least three loci on chromosomes 1, 7 and 12 that harbor distinct Cf-Ecp5 genes in four different accessions. Our mapping showed that the Cf-Ecp5 in Solanum pimpinellifolium G1.1161 is located at the Milky Way locus. The Cf-Ecp5 in Solanum pimpinellifolium LA0722 was mapped to the bottom arm of chromosome 7, while the Cf-Ecp5 genes in Solanum lycopersicum Ontario 7522 and Solanum pimpinellifolium LA2852 were mapped to the same locus on the top arm of chromosome 12. Bi-parental crosses between accessions carrying distinct Cf-Ecp5 genes revealed putative genetically unlinked suppressors of the Ecp5-induced hypersensitive response. Our mapping also showed that Cf-11 is located on chromosome 11, close to the Cf-3 locus. The Ecp5-induced hypersensitive response is widely distributed within tomato species and is variable in strength. This novel example of convergent evolution could be used for choosing different functional Cf-Ecp5 genes according to individual plant breeding needs.Cf-Ecp4 or Cf-Ecp5 genes that could be used in future studies. We found that Cf-Ecp5 was distributed in a wider geographical region than Cf-Ecp4. Lastly, we report the chromosomal locations of Cf-11, which maps to the top arm of chromosome 11, close to the previously reported Cf-3 gene (KANWAR et al. 1980). All in all, this study revealed a unique example of multiple convergently evolved tomato loci in different accessions 7 associated with the HR to C. fulvum Ecp5 effector that have not been previously reported in plant-pathogen interactions. MATERIALS AND METHODSPlant and fungal materials. Seeds from core collections of wild and domesticated tomato species were obtained from the C.M. Rick Tomato Genetics Resource Center, University of California, Davis, USA. These species included Solanum arcanum, Solanum cheesmaniae, Solanum chilense, Solanum chmielewskii, Solanum corneliomulleri, Solanum galapagense, Solanum habrochaites, Solanum huaylasense, Solanum lycopersicoides, Solanum lycopersicum, Solanum neorickii, Solanum ochranthum, Solanum pennellii, Solanum peruvianum and Solanum sitiens. Additional stocks containing previously characterised Cf-Ecp genes were obtained from Dr M. H. A. J. Joosten and Dr P. Lindhout (University of Wageningen) including the accessions S. pimpinellifolium LA1683 (Cf-Ecp4) and S. ...

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“…It is notable that there are differences in the mechanistic basis of AvrRps4 and PopP2 recognition (Sarris et al ., ; Ma et al ., ). RRS1‐R/RPS4 appears to be an exquisitely coevolved NLR pair; whether autoimmunity and ETI can be uncoupled in other NLRs remains to be seen.…”

Section: Discussionmentioning

confidence: 97%

“…It is notable that there are differences in the mechanistic basis of AvrRps4 and PopP2 recognition Ma et al, 2018). RRS1-R/RPS4 appears to be an exquisitely coevolved 6 The SUSHI mutations in the RRS1B Toll/interleukin-1 receptor (TIR) domain do not affect AvrRps4 recognition.…”

Section: Researchmentioning

confidence: 99%

Autoimmunity and effector recognition in Arabidopsis thaliana can be uncoupled by mutations in the RRS1‐R immune receptor

et al. 2019

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Summary Plant nucleotide‐binding leucine‐rich repeat (NLR) disease resistance proteins recognize specific pathogen effectors and activate a cellular defense program. In Arabidopsis thaliana (Arabidopsis), Resistance to Ralstonia solanacearum 1 (RRS1‐R) and Resistance to Pseudomonas syringae 4 (RPS4) function together to recognize the unrelated bacterial effectors PopP2 and AvrRps4. In the plant cell nucleus, the RRS1‐R/RPS4 complex binds to and signals the presence of AvrRps4 or PopP2. The exact mechanism underlying NLR signaling and immunity activation remains to be elucidated. Using genetic and biochemical approaches, we characterized the intragenic suppressors of sensitive to low humidity 1 (slh1), a temperature‐sensitive autoimmune allele of RRS1‐R. Our analyses identified five amino acid residues that contribute to RRS1‐RSLH1 autoactivity. We investigated the role of these residues in the RRS1‐R allele by genetic complementation, and found that C15 in the Toll/interleukin‐1 receptor (TIR) domain and L816 in the LRR domain were also important for effector recognition. Further characterization of the intragenic suppressive mutations located in the RRS1‐R TIR domain revealed differing requirements for RRS1‐R/RPS4‐dependent autoimmunity and effector‐triggered immunity. Our results provide novel information about the mechanisms which, in turn, hold an NLR protein complex inactive and allow adequate activation in the presence of pathogens.

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Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors

Cited by 91 publications

References 39 publications

Plant immune signaling: Advancing on two frontiers

Plant immune signaling: Advancing on two frontiers

Genes encoding recognition of theCladosporium fulvumeffector protein Ecp5 are encoded at several loci in the tomato genome

Autoimmunity and effector recognition in Arabidopsis thaliana can be uncoupled by mutations in the RRS1‐R immune receptor

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