Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance

Varden, Freya A.; Saitoh, Hiromasa; Yoshino, Kae; Franceschetti, Marina; Kamoun, Sophien; Terauchi, Ryohei; Banfield, Mark J.

doi:10.1101/530675

Cited by 3 publications

(4 citation statements)

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“…This raises the possibility that an HMA domain could be engineered to bind and respond to multiple effectors (27). Recently, the Pikp-HMA domain was shown to interact with AVR-Pia at the same interface as used by the RGA5-HMA domain, and this likely underpins partial resistance to M. oryzae expressing AVR-Pia in planta (31). This presents a starting point for using Pikp as a chassis for such studies.…”

Section: Discussionmentioning

confidence: 99%

Protein engineering expands the effector recognition profile of a rice NLR immune receptor

Concepcion

Franceschetti

Terauchi

et al. 2019

Preprint

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22Plant NLR receptors detect pathogen effectors and initiate an immune response. Since 23 their discovery, NLRs have been the focus of protein engineering to improve disease 24 resistance. However, this has proven challenging, in part due to their narrow response 25 specificity. Here, we used structure-guided engineering to expand the response 26 profile of the rice NLR Pikp to variants of the rice blast pathogen effector AVR-Pik. A 27 mutation located within an effector binding interface of the integrated Pikp-HMA 28 domain increased the binding affinity for AVR-Pik variants in vitro and in vivo. This 29 translates to an expanded cell death response to AVR-Pik variants previously 30 unrecognized by Pikp in planta. Structures of the engineered Pikp-HMA in complex 31 with AVR-Pik variants revealed the mechanism of expanded recognition. These 32 results provide a proof-of-concept that protein engineering can improve the utility of 33 plant NLR receptors where direct interaction between effectors and NLRs is 34 established, particularly via integrated domains. 35 36Protein engineering offers opportunities to develop new or improved molecular 37 recognition capabilities that have applications in basic research, health and 38 agricultural settings. Protein resurfacing, where the properties of solvent-exposed 39 regions are changed (often by mutation), has been used extensively in diverse areas 40 from antibody engineering for clinical use, to production of more stable, soluble 41 proteins for biotechnology applications (1). 42

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Section: Discussionmentioning

confidence: 99%

Protein engineering expands the effector recognition profile of a rice NLR immune receptor

Concepcion

Franceschetti

Terauchi

et al. 2019

Preprint

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“…Truncation mutants may serve to validate this hypothesis, however mutations within or truncations of a priori unfolded protein regions may have deleterious effects not only on the structure stability, as shown for N-terminal truncations of AVR-PikD (pages 87-88 in ref. [49]) but also and more specifically on the overall folding process of the protein. Recently, we used HP-NMR (high Hydrostatic Pressure NMR) [50,51] to study the folding/unfolding of AVR-Pia, AVR-Pib [52] and MAX60 [53].…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, AvrPiz-t displays a positively charged surface partially involving lysine residues that are required for AvrPiz-t avirulence and virulence functions in rice [14]. Inversely, while the surface of MAX86 (AVR1-CO39) is strongly negative, that of MAX93 (AVR-Pia) is neutral, yet both AVR1-CO39 and AVR-Pia interact similarly through their ß2 strand with the HMA domain from the rice immune receptors RGA5 [36] and Pikp-1 [37], respectively.…”

Section: Max Domains Exhibit Very Variegated Surface Propertiesmentioning

confidence: 99%

The structural landscape and diversity ofPyricularia oryzaeMAX effectors revisited

Lahfa,

Barthe,

De Guillen

et al. 2023

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Plant pathogenic fungi secrete a wide variety of small proteins, named effectors.MagnaportheAVRs and ToxB-like (MAX) effectors constitute a superfamily of secreted proteins widely distributed inPyricularia (syn. Magnaporthe) oryzae, a devastating fungus responsible for blast disease in cereals such as rice. In spite of high evolutionary sequence divergence, MAX effectors share a common fold characterized by a ß-sandwich core often stabilized by a conserved disulfide bond. In this study, we investigated the structural landscape and diversity within this effector family based on a previous phylogenetic analysis ofP. oryzaeprotein sequences that identified 94 ortholog groups (OG) of putative MAX effectors. Combining protein structure modeling approaches and experimental structure determination, we validated the prediction of the conserved MAX core domain for 77 OG clusters. Four novel MAX effector structures determined by NMR were in remarkably good agreement with AlphaFold2 (AF) predictions. Based on the comparison of the AF-generated 3D models we propose an updated classification of the MAX effectors superfamily in 20 structural groups that highlight variation observed in the canonical MAX fold, disulfide bond patterns and decorating secondary structures in N- and C-terminal extensions. About one-third of the MAX family members remain single, showing no obvious structural relationship with other MAX effectors. Analysis of the surface properties of the AF MAX models also highlights the very high variability remaining within the MAX family when examined at the structural level, probably reflecting the wide diversity of their virulence functions and host targets.Author summaryMAX effectors are a family of virulence proteins from the plant pathogenic fungusPyricularia (syn. Magnaporthe) oryzaethat share a similar 3D structure despite very low amino-acid sequence identity. Characterizing the function and evolution of these proteins requires a detailed understanding of their structural diversity. We used a combination of experimental structure determination and structural modeling to characterize in detail the MAX effector repertoire ofP. oryzae. A prediction pipeline based on similarity searches and structural modeling using the AlphaFold2 (AF) software were used to predict MAX effectors in a collection of 120P. oryzaegenomes. We then compared AF models with experimentally validated NMR structures. The resulting models and experimental structures revealed that the preserved MAX core coexists with extensive structural variability in terms of structured N- or C-terminal extensions. For each of the AF models, we also analyzed the surfaces of the canonical fold that may be involved in protein-protein interactions. This work constitutes a major step in mapping the functional network of MAX effectors through their structure by identifying possible recognition sites that may help focusing studies of their putative targets in infected plant hosts.

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“…Avr-Rmg7/8 of Magnaporthe grisea is recognized by the wheat resistance genes Rmg7 and Rmg8 , which are located in homeologous chromosomes 2B and 2A, respectively [38]. Furthermore, some rice R genes were recently found to interact with divergent Magnaporthe oryzae effectors via different binding surfaces [39, 40]. The effectors have evolved independently to unconventional R gene domains and target them with different binding-specificities [41].…”

Section: Discussionmentioning

confidence: 99%

TheRpi-mcq1resistance gene family recognizesAvr2ofPhytophthora infestansbut is distinct fromR2

Aguilera-Gálvez

Zhang

Haque

et al. 2020

Preprint

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Potato late blight, which is caused by the destructive oomycete pathogen Phytophthora infestans, is a major threat to global food security. Several nucleotide binding, leucine-rich repeat (NLR) Resistance to P. infestans (Rpi) genes have been introgressed into potato cultivars from wild Solanum species that are native to Mexico, but these were quickly defeated. Positional cloning in Solanum mochiquense, combined with allele mining in Solanum huancabambense, were used to identify a new family of Rpi genes from Peruvian Solanum species. Rpi-mcq1, Rpi-hcb1.1 and Rpi-hcb1.2 confer race-specific resistance to a panel of P. infestans isolates. Effector assays showed that the Rpi-mcq1 family mediates a hypersensitive response upon recognition of the RXLR effector AVR2, which had previously been found to be exclusively recognized by the family of R2 resistance proteins. The Rpi-mcq1 and R2 genes are distinct and reside on chromosome IX and IV, respectively. This is the first report of two unrelated R protein families that recognize the same AVR protein. We anticipate that this likely is a consequence of a geographically separated dynamic co-evolution of R gene families of Solanum with an important effector gene of P. infestans.Author summaryPotato is the largest non-grain staple crop and essential for food security world-wide. However, potato plants are continuously threatened by the notorious oomycete pathogen Phytophthora infestans that causes late blight. This devastating disease has led to the Irish famine more then 150 years ago, and is still a major threat for potato. Resistance against P. infestans can be found in wild relatives of potato, which carry resistance genes that belong to the nucleotide binding site-leucine-rich repeat (NLR) class. Known NLR proteins typically recognize a matching effector from Phytophthora, which leads to a hypersensitive resistance response (HR). For example, R2 from Mexican Solanum species recognizes AVR2 from P. infestans. So far, these R genes exclusively match to one Avr gene. Here, we identified a new class of NLR proteins that are different from R2, but also recognize the same effector AVR2. This new family of NLR occurs in South American Solanum species, and we anticipate that it is likely a product of a geographically separated co-evolution with AVR2. This is the first report of two unrelated R protein families that recognize the same AVR protein.

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Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance

Cited by 3 publications

References 45 publications

Protein engineering expands the effector recognition profile of a rice NLR immune receptor

Protein engineering expands the effector recognition profile of a rice NLR immune receptor

The structural landscape and diversity ofPyricularia oryzaeMAX effectors revisited

TheRpi-mcq1resistance gene family recognizesAvr2ofPhytophthora infestansbut is distinct fromR2

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