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

Abstract

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 (HMA) 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.