Show me your ID: NLR immune receptors with integrated domains in plants

Marchal, Clémence; Michalopoulou, Vassiliki A.; Zou, Zhou; Çevik, Volkan; Sarris, Panagiotis F.

doi:10.1042/ebc20210084

Cited by 23 publications

(16 citation statements)

References 118 publications

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“…Effector recognition by NLRs often culminates in cell death that isolates the invading pathogen and confers resistance (Jones et al, 2016; Maruta et al, 2022). Due to their effective and specific responses to plant pathogens, engineering of NLRs to increase their effector recognition specificities is a promising approach to boost disease resistance (Marchal et al, 2022; Monteiro and Nishimura, 2018; Outram et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities

Bentham

Concepcion

Benjumea

et al. 2022

Preprint

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Engineering the plant immune system offers genetic solutions to mitigate crop diseases caused by diverse agriculturally significant pathogens and pests. Modification of intracellular plant immune receptors of the nucleotide-binding leucine rich repeat (NLRs) superfamily for expanded recognition of pathogen virulence proteins (effectors) is a promising approach for engineering novel disease resistance. However, engineering can cause NLR autoactivation, resulting in constitutive defence responses that are deleterious to the plant. This may be due to plant NLRs associating in highly complex signalling networks that co-evolve together, and changes through breeding or genetic modification can generate incompatible combinations, resulting in autoimmune phenotypes. We have previously shown how alleles of the rice NLR pair Pik have differentially co-evolved, and how sensor/helper mismatching between non-co-evolved alleles triggers constitutive activation and cell death (De la Concepcion et al., 2021b). Here, we dissect incompatibility determinants in the Pik pair and found that HMA domains integrated in Pik-1 not only evolved to bind pathogen effectors but also likely co-evolved with other NLR domains to maintain immune homeostasis. This explains why changes in integrated domains can lead to autoactivation. We then used this knowledge to facilitate engineering of new effector recognition specificities overcoming initial autoimmune penalties. We show that by mismatching alleles of the rice sensor and helper NLRs Pik-1 and Pik-2, we can enable the integration of synthetic HMA domains with novel and enhanced recognition of an effector from the rice blast fungus. Taken together, our results reveal a new strategy for engineering NLRs, which has the potential to allow an expanded set of integrations and therefore new disease resistance specificities in plants.

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Section: Introductionmentioning

confidence: 99%

Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities

Bentham

Concepcion

Benjumea

et al. 2022

Preprint

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“…Pii-2 indirectly recognizes the M. oryzae effector AVR-Pii via a complex between rice EXO70 (a subunit of the exocyst complex) and the NOI domain of Pii-2 [31,79,80]. The integrated domains of these rice sensor NLRs have been used for protein engineering to confer broadspectrum resistance [81][82][83][84][85][86][87][88][89].…”

Section: Introductionmentioning

confidence: 99%

Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector

Sugihara

Abe

Takagi

et al. 2022

Preprint

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Studies focused solely on single organisms can fail to identify the networks underlying host–pathogen gene-for-gene interactions. Here, we integrate genetic analyses of rice (Oryza sativa, host) and rice blast fungus (Magnaporthe oryzae, pathogen) and uncover a new pathogen recognition specificity of the rice nucleotide-binding domain and leucine-rich repeat protein (NLR) immune receptor Pik, which mediates resistance to M. oryzae expressing the avirulence effector gene AVR-Pik. Rice Piks-1, encoded by an allele of Pik-1, recognizes a previously unidentified effector encoded by the M. oryzae avirulence gene AVR-Mgk1, which is found on a mini-chromosome. AVR-Mgk1 has no sequence similarity to known AVR-Pik effectors, and is prone to deletion from the mini-chromosome mediated by repeated Inago2 retrotransposon sequences. AVR-Mgk1 is detected by Piks-1 and by other Pik-1 alleles known to recognize AVR-Pik effectors; recognition is mediated by AVR-Mgk1 binding to the integrated heavy metal-associated domain of Piks-1 and other Pik-1 alleles. Our findings highlight how complex gene-for-gene interaction networks can be disentangled by applying forward genetics approaches simultaneously to the host and pathogen. We demonstrate dynamic co-evolution between an NLR integrated domain and multiple families of effector proteins.

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“…The first layer of defense is the recognition of pathogen or microorganism-associated molecular patterns (PAMPs or MAMPs), resulting in the PAMP-triggered immunity (PTI) (Jones and Dangl, 2006). Subsequently, host can recognize the pathogen effectors via specialized immunity receptors known as nucleotide binding leucine-rich repeat receptors (NB-LRR or NLR), which triggers the effector-triggered immunity (ETI) (Marchal et al ., 2022; Mermigka and Sarris, 2019; Jones and Dangl, 2006). This two-layered system leads to a variety of responses, such as accumulation of oxygen species, callose deposition, mitogen activated protein kinase activation and pathogenesis related gene expression (Sertedakis et al ., 2022; Yuan et al ., 2021).…”

Section: Introductionmentioning

confidence: 99%

The functional and structural characterization ofXanthomonas campestrispv.campestriscore effector XopP revealed a new kinase activity

Kotsaridis

Michalopoulou

Tsakiri

et al. 2022

Preprint

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The exocyst complex subunit protein Exo70B1 plays a crucial role in a variety of cell mechanisms including immune responses against pathogens. The calcium dependent kinase 5 (CPK5) of Arapidopsis thaliana, phosphorylates AtExo70B1 upon functional disruption. We previously reported that, the Xanthomonas campestris pv. campestis effector XopP, compromises Exo70B1 and bypasses the host's hypersensitive response (HR), in a way that is still unclear. Herein we designed an experimental approach based on biophysical, biochemical and molecular assays, based on structural and functional predictions, as well as, utilizing Aplhafold and DALI online servers respectively, in order to characterize the in vivo XccXopP function. The interaction between AtExo70B1 and XccXopP is very stable in high temperatures, while the AtExo70B1 appeared to be phosphorylated at XccXopP expressing transgenic Arabidopsis. XccXopP reveals similarities with known mammalian kinases, and phosphorylates AtExo70B1 at Ser107, Ser111, Ser248, Thr309 and Thr364. Furthermore, XccXopP protects AtExo70B1 from AtCPK5 phosphorylation. Together these findings show that, XccXopP is an effector, which not only functions as a novel serine/threonine kinase upon its host's protein target AtExo70B1, but also protects the latter from the innate AtCPK5 phosphorylation, to bypass the host's immune responses.

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Show me your ID: NLR immune receptors with integrated domains in plants

Cited by 23 publications

References 118 publications

Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities

Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities

Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector

The functional and structural characterization ofXanthomonas campestrispv.campestriscore effector XopP revealed a new kinase activity

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