Resurrection of plant disease resistance proteins via helper NLR bioengineering

Contreras, Mauricio P; Pai, Hsuan; Selvaraj, Manikandan; Toghani, AmirAli; Lawson, David M; Tümtaş, Yasin; Duggan, Cian; Yuen, Enoch Lok Him; Stevenson, Clare E. M.; Harant, Adeline; Wu, Chih‐Hang; Bozkurt, Tolga O.; Kamoun, Sophien; Derevnina, Lida

doi:10.1101/2022.12.11.519957

Cited by 9 publications

(30 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Examples of effector targeting NLR come from the P. infestans effector AVRcap1b and the cyst nematode effector SS15, which suppress Solanaceae-specific helper NLRs NRC2 and NRC3 either by affecting their negative regulator NbTOL9a or by preventing their oligomerization and activation 22,23 . We add to these insights, by revealing not only that helper NLRs ADR1-L1 and ADR1-L2 are targeted by P. syringae effector AvrPtoB, but also that AvrPtoB-induced degradation of ADR1-L1 and ADR1-L2 is monitored by the sensor NLR SNC1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…either by affecting their negative regulator NbTOL9a or by preventing their oligomerization and activation 22,23 . We add to these insights, by revealing not only that helper NLRs ADR1-L1 and ADR1-L2 are targeted by P. syringae effector AvrPtoB, but also that AvrPtoB-induced degradation of ADR1-L1 and ADR1-L2 is monitored by the sensor NLR SNC1 (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…For example, HopI1 greatly dampens HR triggered by several other effectors by unknown mechanisms 21 . A recent reverse genetic screen identified five effectors from oomycetes and nematodes that suppress cell death triggered by NLRs Prf or Rpi-blb2 in N. benthamiana 22 .Among these effectors, SS15 exerts its effects by inhibiting the intramolecular rearrangements of NRC2, which prevents its oligomerization and activation 23 , while AVRcap1b dampens NRC2 and NRC3 function through the membrane trafficking-associated protein NbTOL9a (Target of Myb 1-like protein 9a) 22 . From these studies it is clear that much is still to be learned about how pathogens suppress ETI and how plants in turn counteract such suppression.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The immune receptor SNC1 monitors helper NLRs targeted by a bacterial effector

Wang

Chen

et al. 2023

Preprint

View full text Add to dashboard Cite

Plants deploy intracellular receptors to counteract pathogen effectors that suppress cell-surface receptor-mediated immunity. To what extent pathogens manipulate also immunity mediated by intracellular receptors, and how plants tackle such manipulation, remains unknown. Arabidopsis thaliana encodes three very similar ADR1 class helper NLRs (ADR1, ADR1-L1 and ADR1-L2), which play key roles in plant immunity initiated by intracellular receptors. Here, we report that Pseudomonas syringae AvrPtoB, an effector with E3 ligase activity, can suppress ADR1-L1- and ADR1-L2-mediated cell death. ADR1, however, evades such suppression by diversification of two ubiquitination sites targeted by AvrPtoB. The intracellular sensor NLR SNC1 interacts with and guards the CCR domains of ADR1-L1 and ADR-L2. Removal of ADR1-L1 and ADR1-L2 or delivery of AvrPtoB activates SNC1, which then signals through ADR1 to trigger immunity. Our work not only uncovers the long sought-after physiological function of SNC1 in pathogen defense,but also that reveals how plants can use dual strategies, sequence diversification and a multiple layered guard-guardee system, to counteract pathogen attack on core immunity functions.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The immune receptor SNC1 monitors helper NLRs targeted by a bacterial effector

Wang

Chen

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Two studies on the SS15 effector from the potato cyst nematode Globodera rostochiensis (Derevnina et al, 2021;Contreras et al, 2023a) revealed that SS15 can inhibit cell death triggered by the helper NLRs NRC2 and NRC3, as well as the tomato (Solanum Pathogen effectors can suppress NLR signaling via diverse strategies. Some effectors can target downstream components required for NLR signaling to suppress immune signaling (Table 1) (A), while others can suppress immune responses by directly targeting NLRs (B).…”

Section: Pathogen Suppression Of Nlrs By Direct Inhibitionmentioning

confidence: 99%

“…lycopersicum) helper NLR NRC1 of the solanaceous NRC network (Fig 4C). SS15 acts as a proteinaceous inhibitor, directly binding to the HD1 region of the central NB-ARC domains of the helper NLRs (Derevnina et al, 2021;Contreras et al, 2023a). SS15 was proposed to immobilize a critical "hinge" loop in the NB-ARC domain, preventing intramolecular rearrangements required for activation and resistosome formation.…”

Section: Pathogen Suppression Of Nlrs By Direct Inhibitionmentioning

confidence: 99%

NLR receptors in plant immunity: making sense of the alphabet soup

Contreras,

Lüdke,

Pai

et al. 2023

EMBO Reports

Self Cite

View full text Add to dashboard Cite

Plants coordinately use cell‐surface and intracellular immune receptors to perceive pathogens and mount an immune response. Intracellular events of pathogen recognition are largely mediated by immune receptors of the nucleotide binding and leucine rich‐repeat (NLR) classes. Upon pathogen perception, NLRs trigger a potent broad‐spectrum immune reaction, usually accompanied by a form of programmed cell death termed the hypersensitive response. Some plant NLRs act as multifunctional singleton receptors which combine pathogen detection and immune signaling. However, NLRs can also function in higher order pairs and networks of functionally specialized interconnected receptors. In this article, we cover the basic aspects of plant NLR biology with an emphasis on NLR networks. We highlight some of the recent advances in NLR structure, function, and activation and discuss emerging topics such as modulator NLRs, pathogen suppression of NLRs, and NLR bioengineering. Multi‐disciplinary approaches are required to disentangle how these NLR immune receptor pairs and networks function and evolve. Answering these questions holds the potential to deepen our understanding of the plant immune system and unlock a new era of disease resistance breeding.

show abstract

TheNRC0gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants

Sakai,

Martinez-Anaya,

Contreras

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

NLR (nucleotide-binding domain and leucine-rich repeat-containing) proteins can form complex receptor networks to confer innate immunity. NRCs are phylogenetically related nodes that function downstream of a massively expanded network of disease resistance proteins that protect against multiple plant pathogens. Here, we used phylogenomic methods to reconstruct the macroevolution of the NRC family. One of the NRCs, we termed NRC0, is the only family member shared across asterid plants, leading us to investigate its evolutionary history and genetic organization. In several asterid species, NRC0 is genetically clustered to other NLRs that are phylogenetically related to NRC-dependent disease resistance genes. This prompted us to hypothesize that the ancestral state of the NRC network is an NLR helper-sensor gene cluster that was present early during asterid evolution. We validated this hypothesis by demonstrating that NRC0 is essential for the hypersensitive cell death induced by its genetically linked sensor NLR partners in four divergent asterid species: tomato, wild sweet potato, coffee and carrot. In addition, activation of a sensor NLR leads to high-order complex formation of its genetically linked NRC0 similar to other NRCs. Our findings map out contrasting evolutionary dynamics in the macroevolution of the NRC network over the last 125 million years from a functionally conserved NLR gene cluster to a massive genetically dispersed network.

show abstract

Resurrection of plant disease resistance proteins via helper NLR bioengineering

Cited by 9 publications

References 56 publications

The immune receptor SNC1 monitors helper NLRs targeted by a bacterial effector

The immune receptor SNC1 monitors helper NLRs targeted by a bacterial effector

NLR receptors in plant immunity: making sense of the alphabet soup

TheNRC0gene cluster of sensor and helper NLR immune receptors is functionally conserved across asterid plants

Contact Info

Product

Resources

About