Multiple pairs of allelic MLA immune receptor-powdery mildew AVR_A effectors argue for a direct recognition mechanism.

Abstract

Nucleotide-binding domain and leucine-rich repeat (NLR)-containing proteins in plants and animals mediate intracellular pathogen sensing. Plant NLRs typically detect strain-specific pathogen effectors and trigger immune responses often linked to localized host cell death. The barley <i>Mla</i> disease resistance locus has undergone extensive functional diversification in the host population and encodes numerous allelic NLRs each detecting a matching isolate-specific avirulence effector (AVR_A) of the fungal pathogen <i>Blumeria graminis</i> f. sp. <i>hordei</i> (<i>Bgh</i>). We report here the isolation of <i>Bgh AVR_a7</i>, <i>AVR_a9</i>, <i>AVR_a10</i>, and <i>AVR_a22</i>, which encode small secreted proteins recognized by allelic MLA7, MLA9, MLA10, and MLA22 receptors, respectively. These effectors are sequence-unrelated, except for allelic <i>AVR_a10</i> and <i>AVR_a22</i> that are co-maintained in pathogen populations in the form of a balanced polymorphism. Contrary to numerous examples of indirect recognition of bacterial effectors by plant NLRs, co-expression experiments with matching <i>Mla-AVR_a</i> pairs indicate direct detection of the sequence-unrelated fungal effectors by MLA receptors.