The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat

Abstract

The wheat Pm3 resistance gene against the powdery mildew pathogen occurs as an allelic series encoding functionally different immune receptors which induce resistance upon recognition of isolate-specific avirulence (AVR) effectors from the pathogen. Here, we describe the identification of five effector proteins from the mildew pathogens of wheat, rye, and the wild grass Dactylis glomerata , specifically recognized by the PM3B, PM3C and PM3D receptors. Together with the earlier identified AVRPM3 A2/F2 , the recognized AVRs of PM3B/C, (AVRPM3 B2/C2 ), and PM3D (AVRPM3 D3 ) belong to a large group of proteins with low sequence homology but predicted structural similarities. AvrPm3 b2/c2 and AvrPm3 d3 are conserved in all tested isolates of wheat and rye mildew, and non-host infection assays demonstrate that Pm3b , Pm3c , and Pm3d are also restricting the growth of rye mildew on wheat. Furthermore, divergent AVR homologues from non-adapted rye and Dactylis mildews are recognized by PM3B, PM3C, or PM3D, demonstrating their involvement in host specificity.

Mechanisms of powdery mildew resistance of wheat – a review of molecular breeding

“…This finding acknowledged the contribution of major R genes to nonhost resistance, suggesting overlap between defence pathways in the two‐layered zigzag model. Moreover, conservation of the same effectors in the nonadapted powdery mildews of grass relatives to wheat, as demonstrated in both AvrPm3 – Pm3 (Bourras et al , 2019) and AvrPm2–Pm2 (Praz et al , 2017) interactions, provides molecular evidence for successful introgression of Pm genes from wheat wild and cultivated relatives.…”

“…The presence of Svr in mildew will, together with the avirulence allele and R allele, regulate plant resistance in the cereal–powdery mildew pathosystem, suggesting additional layers of a simple gene‐for‐gene model controlling Avr – R interactions in the wheat–powdery mildew system. The recent follow‐up work on the AvrPm3–Pm3 model (Bourras et al , 2019) further established the role of Pm3 NLR receptors in simultaneously determining host‐specificity for grass mildews and race‐specific resistance to wheat powdery mildew. This finding acknowledged the contribution of major R genes to nonhost resistance, suggesting overlap between defence pathways in the two‐layered zigzag model.…”

Cross-Kingdom RNAi of Pathogen Effectors Leads to Quantitative Adult Plant Resistance in Wheat

“…We also present the generation, selection, and characterization of stable wheat lines expressing a HIGS construct targeting the suppressor of avirulence gene SvrPm3 a1/f 1 . This wheat powdery mildew effector is involved in the suppression of several allelic Pm3 resistance gene variants in wheat (Bourras et al, 2015(Bourras et al, , 2019Parlange et al, 2015). We also show that SvrPm3 a1/f 1 is expressed at significantly lower levels in B.g.…”

A holistic view on plant effector-triggered immunity presented as an iceberg model

“…Based on a genetic segregation study of the wheat powdery mildew fungus, another 2nd ETS effector was uncovered. Here, "suppressor of Avr", SVRPM3 A1/F1 suppressed distinct resistances mediated five PM3 NLRs encoded by an allelic series of R-genes and triggered by distantly related AVRPM3s [8,123,124]. Leptosphaeria maculans effector AvrLm4-7 suppresses resistance mediated by R-protein, Rlm3, after recognition of AvrLm3 in oil seed rape [125].…”

“…Indeed, this may in broad sense be the case for many necrotrophic pathogens, where no NLR-type R-genes have been found [127]. However, even though SVRPM3 A1/F1 suppresses ETI activated by closely related NLRs, other R-genes can confer resistance against wheat powdery mildew isolates expressing SVRPM3 A1/F1 , showing that this is not a silver bullet effector [8,123,124]. This and other examples above, in turn indicates that 2nd ETS effectors function at the stage of effector target monitoring.…”