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I04-Macromolecular Crystallography	Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities Adam R. Bentham , Juan Carlos De La Concepcion , Javier Vega Benjumea , Jiorgos Kourelis , Sally Jones , Melanie Mendel , Jack Stubbs , Clare E. M. Stevenson , Josephine H. R. Maidment , Mark Youles , Rafal Zdrzalek , Sophien Kamoun , Mark J. Banfield The Plant Cell DOI: 10.1093/plcell/koad204 Diamond Proposal Number(s): [25108] Open Access Show Abstract ▼ Abstract: 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 (NLR) superfamily for expanded recognition of pathogen virulence proteins (effectors) is a promising approach for engineering 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. The sensor and helper NLRs of the rice (Oryza sativa) NLR pair Pik have co-evolved, and mismatching between non-co-evolved alleles triggers constitutive activation and cell death. This limits the extent to which protein modifications can be used to engineer pathogen recognition and enhance disease resistance mediated by these NLRs. Here, we dissected incompatibility determinants in the Pik pair in Nicotiana benthamiana and found that heavy metal-associated (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 domains with novel and enhanced recognition specificities. Taken together, our results reveal a strategy for engineering NLRs, which has the potential to allow an expanded set of integrations and therefore new disease resistance specificities in plants.	Jul 2023

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I04-Macromolecular Crystallography

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

Adam R. Bentham , Juan Carlos De La Concepcion , Javier Vega Benjumea , Jiorgos Kourelis , Sally Jones , Melanie Mendel , Jack Stubbs , Clare E. M. Stevenson , Josephine H. R. Maidment , Mark Youles , Rafal Zdrzalek , Sophien Kamoun , Mark J. Banfield

The Plant Cell

DOI: 10.1093/plcell/koad204

Diamond Proposal Number(s): [25108]

Open Access

Show Abstract ▼

Abstract: 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 (NLR) superfamily for expanded recognition of pathogen virulence proteins (effectors) is a promising approach for engineering 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. The sensor and helper NLRs of the rice (Oryza sativa) NLR pair Pik have co-evolved, and mismatching between non-co-evolved alleles triggers constitutive activation and cell death. This limits the extent to which protein modifications can be used to engineer pathogen recognition and enhance disease resistance mediated by these NLRs. Here, we dissected incompatibility determinants in the Pik pair in Nicotiana benthamiana and found that heavy metal-associated (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 domains with novel and enhanced recognition specificities. Taken together, our results reveal a strategy for engineering NLRs, which has the potential to allow an expanded set of integrations and therefore new disease resistance specificities in plants.

Jul 2023

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