Wheat PR‐1 proteins are targeted by necrotrophic pathogen effector proteins

Abstract

Recent studies have identified that proteinaceous effectors secreted by Parastagonospora nodorum are required to cause disease on wheat. These effectors interact in a gene-for-gene manner with host-dominant susceptibilty loci, resulting in disease. However, whilst the requirement of these effectors for infection is clear, their mechanisms of action remain poorly understood. A yeast-two-hybrid library approach was used to search for wheat proteins that interacted with the necrotrophic effector SnTox3. Using this strategy we indentified an interaction between SnTox3 and the wheat pathogenicity-related protein TaPR-1-1, and confirmed it by in-planta co-immunprecipitation. PR-1 proteins represent a large family (23 in wheat) of proteins that are upregulated early in the defence response; however, their function remains ellusive. Interestingly, the P. nodorum effector SnToxA has recently been shown to interact specifically with TaPR-1-5. Our analysis of the SnTox3-TaPR-1 interaction demonstrated that SnTox3 can interact with a broader range of TaPR-1 proteins. Based on these data we utilised homology modeling to predict, and validate, regions on TaPR-1 proteins that are likely to be involved in the SnTox3 interaction. Precipitating from this work, we identified that a PR-1-derived defence signalling peptide from the C-terminus of TaPR-1-1, known as CAPE1, enhanced the infection of wheat by P. nodorum in an SnTox3-dependent manner, but played no role in ToxA-mediated disease. Collectively, our data suggest that P. nodorum has evolved unique effectors that target a common host-protein involved in host defence, albeit with different mechanisms and potentially outcomes.

The global regulator of pathogenesis PnCon7 positively regulates Tox3 effector gene expression through direct interaction in the wheat pathogen Parastagonospora nodorum

“…Tox1 is a chitin binding protein which is localised to the surface of mycelia and to protect the fungus from wheat chitinases during defence response (Liu et al ., ). Tox3 and ToxA have recently been shown to interact with wheat PR‐1 proteins and that this interaction influences pathogen growth during infection (Lu et al ., ; Breen et al ., ).…”

Targeting pathogen sterols: Defence and counterdefence?

“…tritici repentis , the causative agent of the tan spot disease in wheat, interacts with the basic PR1 protein TaPR-1-5 [30]. Similarly, SnTox3, another toxin effector secreted by Parastogonospora nodorum , the causative agent of the wheat glume blotch disease, binds not only the basic PR1 protein TaPR-1-1 but also other acidic and basic members of the PR1 gene family that contains more than 60 members in the genome of hexaploid wheat [31]. However, it is currently unknown if binding by these effectors abolishes the antifungal mode of action of PR1 by interfering with the sterol/ergosterol binding activity of wheat PR1 proteins (Fig 1E).…”

“…Although both TaPR-1-5 and TaPR-1-1 belong to the group 1 basic PR1 proteins and share high sequence similarity, TaPR-1-5 and TaPR-1-1 CAP domain residues required for either ToxA or SnTox3 interactions seem to be different [30,31]. Also, the asparagine (N) 141 residue in the PR-1-5 protein, which interacts with the N102 residue in ToxA, is not a conserved part of the CAP domain.…”

“…CAPE1 activates defence responses, suggesting that it may serve as a damage-associated molecular pattern (DAMP) molecule [32]. One intriguing possibility proposed by Breen et al [31] is that effector (e.g., SnTox3) binding triggers the release of CAPE1 from PR1, which can then contribute to the development of tissue necrosis. Indeed, infection experiments conducted on wheat plants previously infiltrated with CAPE1 showed that this peptide can amplify the necrosis caused by SnTox3 in plants carrying the cognate susceptibility gene Snn3 [31].…”

“…One intriguing possibility proposed by Breen et al [31] is that effector (e.g., SnTox3) binding triggers the release of CAPE1 from PR1, which can then contribute to the development of tissue necrosis. Indeed, infection experiments conducted on wheat plants previously infiltrated with CAPE1 showed that this peptide can amplify the necrosis caused by SnTox3 in plants carrying the cognate susceptibility gene Snn3 [31]. Similarly, a mutant form of TaPR-1-5 (N141A) unable to interact with ToxA triggers reduced necrosis when infiltrated into wheat plants carrying the cognate susceptibility gene Tsn1 [30].…”