Allelic variants of the NLR protein Rpi‐chc1 differentially recognize members of the Phytophthora infestans PexRD12/31 effector superfamily through the leucine‐rich repeat domain

• Published in: The Plant journal : for cell and molecular biology Vol. 107; no. 1; pp. 182 - 197
• Main Authors: Monino‐Lopez, Daniel, Nijenhuis, Maarten, Kodde, Linda, Kamoun, Sophien, Salehian, Hamed, Schentsnyi, Kyrylo, Stam, Remco, Lokossou, Anoma, Abd‐El‐Haliem, Ahmed, Visser, Richard G.F., Vossen, Jack H.
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.07.2021; John Wiley and Sons Inc
• Subjects: Alleles; Coils; Disease resistance; Domains; Evolution; Genes; Late blight; late blight resistance gene; Leucine; leucine‐rich repeat; NLR cluster; Nlr protein; Nucleotides; Original; Pathogens; Phytophthora infestans; potato; Proteins; RXLR effector; Solanum; Solanum species; Leucine rich repeat; NLR cluster; potato; Phytophthora infestans; RXLR effector; Late blight resistance gene; Solanum species
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.15284

SUMMARY Phytophthora infestans is a pathogenic oomycete that causes the infamous potato late blight disease. Resistance (R) genes from diverse Solanum species encode intracellular receptors that trigger effective defense responses upon the recognition of cognate RXLR avirulence (Avr) effector proteins. To deploy these R genes in a durable fashion in agriculture, we need to understand the mechanism of effector recognition and the way the pathogen evades recognition. In this study, we cloned 16 allelic variants of the Rpi‐chc1 gene from Solanum chacoense and other Solanum species, and identified the cognate P. infestans RXLR effectors. These tools were used to study effector recognition and co‐evolution. Functional and non‐functional alleles of Rpi‐chc1 encode coiled‐coil nucleotide‐binding leucine‐rich repeat (CNL) proteins, being the first described representatives of the CNL16 family. These alleles have distinct patterns of RXLR effector recognition. While Rpi‐chc1.1 recognized multiple PexRD12 (Avrchc1.1) proteins, Rpi‐chc1.2 recognized multiple PexRD31 (Avrchc1.2) proteins, both belonging to the PexRD12/31 effector superfamily. Domain swaps between Rpi‐chc1.1 and Rpi‐chc1.2 revealed that overlapping subdomains in the leucine‐rich repeat (LRR) domain are responsible for the difference in effector recognition. This study showed that Rpi‐chc1.1 and Rpi‐chc1.2 evolved to recognize distinct members of the same PexRD12/31 effector family via the LRR domain. The biased distribution of polymorphisms suggests that exchange of LRRs during host–pathogen co‐evolution can lead to novel recognition specificities. These insights will guide future strategies to breed durable resistant varieties. Significance statement In this manuscript the cloning of novel late blight resistance genes and their cognate effectors is described. The mechanism of recognition, host pathogen co‐evolution, and implications for deployment of the knowledge in agriculture are discussed.