SnTox1, a Parastagonospora nodorum necrotrophic effector, is a dual‐function protein that facilitates infection while protecting from wheat‐produced chitinases

Abstract

Summary SnTox1 induces programmed cell death and the up‐regulation of pathogenesis‐related genes including chitinases. Additionally, SnTox1 has structural homology to several plant chitin‐binding proteins. Therefore, we evaluated SnTox1 for chitin binding and localization. We transformed an avirulent strain of Parastagonospora nodorum as well as three nonpathogens of wheat (Triticum aestivum), including a necrotrophic pathogen of barley, a hemibiotrophic pathogen of sugar beet and a saprotroph, to evaluate the role of SnTox1 in infection and in protection from wheat chitinases. SnTox1 bound chitin and an SnTox1‐green fluorescent fusion protein localized to the mycelial cell wall. Purified SnTox1 induced necrosis in the absence of the pathogen when sprayed on the leaf surface and appeared to remain on the leaf surface while inducing both epidermal and mesophyll cell death. SnTox1 protected the different fungi from chitinase degradation. SnTox1 was sufficient to change the host range of a necrotrophic pathogen but not a hemibiotroph or saprotroph. Collectively, this work shows that SnTox1 probably interacts with a receptor on the outside of the cell to induce cell death to acquire nutrients, but SnTox1 accomplishes a second role in that it protects against one aspect of the defense response, namely the effects of wheat chitinases.

Characterization of an antimicrobial and phytotoxic ribonuclease secreted by the fungal wheat pathogen Zymoseptoria tritici

“…), it suggests that the Zt6 protein is unlikely to penetrate the waxy leaf cuticle to gain access to the exterior of leaf epidermal cells. This distinguishes Zt6 from, for example, the SnTox1 effector protein from P. nodorum , which has recently been shown to be capable of direct penetration of the wheat leaf cuticle to elicit cell death in sensitive cultivars (Liu et al ., ). Therefore, at this point, we hypothesize that the function of Zt6 may be to clear the immediate area around the germinating spore of other potentially harmful or competing microorganisms.…”

“…In contrast with the examples above, a new concept of effector multifunctionality has recently gained traction based on data from other systems. The effector SnTox1 from the necrotrophic wheat pathogen Parastagonospora nodorum has recently been demonstrated to show dual functionality during wheat leaf infection (Liu et al ., ). First, it induces a cell death pathway on wheat cultivars harbouring the Snn1 sensitivity gene (Liu et al ., ; Shi et al ., ) and can then subsequently protect fungal hyphae from digestion by plant chitinases (Liu et al ., ), presumably activated as a consequence of the wheat cell death reaction.…”

“…The effector SnTox1 from the necrotrophic wheat pathogen Parastagonospora nodorum has recently been demonstrated to show dual functionality during wheat leaf infection (Liu et al ., ). First, it induces a cell death pathway on wheat cultivars harbouring the Snn1 sensitivity gene (Liu et al ., ; Shi et al ., ) and can then subsequently protect fungal hyphae from digestion by plant chitinases (Liu et al ., ), presumably activated as a consequence of the wheat cell death reaction. It has been speculated that pathogen effectors may have additional roles apart from direct host interactions, specifically with regard to the manipulation of local microbial communities (microbiomes) (Rovenich et al ., ).…”

The hijacking of a receptor kinase–driven pathway by a wheat fungal pathogen leads to disease

“…This is perhaps not surprising, given that Snn1 spans the plasma membrane and contains extracellular binding domains and that SnTox1 does not enter the plant cell ( 17 ). This is in contrast to the other well-characterized wheat– P. nodorum interaction involving the NB-LRR gene Tsn1 and the P. nodorum –produced NE SnToxA, which do not interact directly in yeast ( 5 ).…”

Chitin and chitin-related compounds in plant–fungal interactions

“…Additionally, SnTox1 has structural homology to several plant chitin-binding proteins. Therefore, SnTox1 protected the different fungi from chitinase degradation (Liu et al 2016). …”