The fungal ribonuclease-like effector protein CSEP0064/BEC1054 represses plant immunity and interferes with degradation of host ribosomal RNA

Abstract

The biotrophic fungal pathogen Blumeria graminis causes the powdery mildew disease of cereals and grasses. We present the first crystal structure of a B . graminis effector of pathogenicity (CSEP0064/BEC1054), demonstrating it has a ribonuclease (RNase)-like fold. This effector is part of a group of RNase-like proteins (termed RALPHs) which comprise the largest set of secreted effector candidates within the B . graminis genomes. Their exceptional abundance suggests they play crucial functions during pathogenesis. We show that transgenic expression of RALPH CSEP0064/BEC1054 increases susceptibility to infection in both monocotyledonous and dicotyledonous plants. CSEP0064/BEC1054 interacts in planta with the pathogenesis-related protein PR10. The effector protein associates with total RNA and weakly with DNA. Methyl jasmonate (MeJA) levels modulate susceptibility to aniline-induced host RNA fragmentation. In planta expression of CSEP0064/BEC1054 reduces the formation of this RNA fragment. We propose CSEP0064/BEC1054 is a pseudoenzyme that binds to host ribosomes, thereby inhibiting the action of plant ribosome-inactivating proteins (RIPs) that would otherwise lead to host cell death, an unviable interaction and demise of the fungus.

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

“…An extension of this concept is the evolution of catalytically inactive variants of secreted proteins. Examples include the functional conversion of a glutathione synthetase in a plant-parasitic nematode (Lilley et al, 2018), enzymatically inactive fungal chitinases that sequester immunogenic chitin fragments (Fiorin et al, 2018), or the large family of catalytically inactive RNase-like effector proteins in cereal powdery mildews (Pennington et al, 2019).…”

Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity

“…Some of these putative effectors are expressed primarily in haustoria (Spanu, 2017). Recently, the first structure of an effector from Blumeria , that of BEC1054, was determined and showed structural similarities with ribonucleases; they were hence named RNase‐like proteins expressed in haustoria (RALPHs; Pennington et al , 2019; Fig. 2c).…”

“…Like MAX effectors, RALPHs are predicted to contain a disulfide bond, as do the ribonucleases they share structural homology with. BEC1054 is proposed to mediate virulence by functioning as a pseudoenzyme to impede host ribosome inactivating proteins (RIPs) and inhibit host cell death (Pennington et al , 2019).…”

Mildew Locus O facilitates colonization by arbuscular mycorrhiza in angiosperms

“…Notably, a role for mechanosensing has been proposed for the receptor kinase Feronia (Hamant & Haswell, 2017), which was shown to be required for proper re-localization of MLO7/NORTIA to the site of pollen tube contact in the synergid cell (Kessler et al, 2010;. However, other cues may activate MLO, for example, both Blumeria graminis and R. irregularis produce effectors that could target MLO (Kloppholz et al, 2011;Requena et al, 2018;Pennington et al, 2019;Saur et al, 2019).…”