SnTox1, a Parastagonospora nodorum necrotrophic effector, elicits PCD while binding chitin to protect the pathogen from wheat chitinases

Parastagonospora nodorum (Synonym: Stagonospora nodorum) is a destructive pathogen of wheat that induces yield and quality losses by causing necrosis on the leaves and glumes of wheat. P. nodorum is a necrotrophic specialist pathogen that secretes an arsenal of necrotrophic effectors (NEs) involved in inducing necrosis. SnTox1 was the first of seven NEs to be reported from P. nodorum and interacts directly or indirectly with the single dominant susceptibility gene Snn1. SnTox1 is recognized by Snn1 followed by the induction of a classical defense response involving programmed cell death (PCD), an oxidative burst, DNA laddering, and up regulation of several PR proteins including chitinases. However, this recognition results in wheat being susceptible to P. nodorum rather than resistant. Interestingly, the C-terminus of SnTox1 has homology to several plant chitin binding proteins and we have shown that SnTox1 does bind chitin. Therefore, we have expressed two wheat chitinases that are able to degrade the fungal cell wall in vitro to show that P. nodorum transformed other plant pathogens and non-pathogens with SnTox1 including Neurospora crassa (saprotroph), Pyrenophora teres f. teres (necrotrophic barley pathogen), and Cercospora beticola (hemi-biotrophic sugarbeet pathogen) and show that not only did some of these fungi become pathogens of wheat lines harboring Snn1, but all had increased protection from the wheat chitinases in vitro, exposing a secondary or possibly the primary function of SnTox1. The dual function of this protein explains the high prevalence of SnTox1, relative to other NEs in the P. nodorum global population and shows that necrotrophs harbor chitin binding proteins for their protection during pathogenesis.