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

Authors: LIU, ZHAOHUI - North Dakota State University; GAO, YUANYUAN - North Dakota State University; KIM, YONG MIN - North Dakota State University; Faris, Justin; Shelver, Weilin; DE WIT, PIERRE - Wageningen University; Xu, Steven; Friesen, Timothy

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/3/2016
Publication Date: 7/1/2016
Publication URL: http://handle.nal.usda.gov/10113/62881
Citation: Liu, Z., Gao, Y., Kim, Y.M., Faris, J.D., Shelver, W.L., de Wit, P.J.G.M., Xu, S.S., Friesen, T.L. 2016. SnTox1, a Parastagonospora nodorum necrotrophic effector, is a dual-function protein that facilitates infection while protecting from wheat-produced chitinases. New Phytologist. 211:1052-1064. doi: 10.1111/nph.13959.

Interpretive Summary: Plant pathogens all produce molecules that are useful in penetrating, colonizing and gaining nutrient from their plant hosts. Much is known about biotrophic pathogens such as the rusts and powdery mildews, however, less is known about how pathogens classified as necrotrophs successfully colonize their respective hosts. SnTox1 is a small molecule secreted by the fungal pathogen, Parastagonospora nodorum, the causal agent of Septoria nodorum blotch (SNB) of wheat. We previously reported that SnTox1 is used by the pathogen to induce plant cell death to cause disease. We also reported that the SnTox1 C-terminal region harbored structural homology to several plant chitin binding proteins. Because chitin is a main component of the cell wall and plants attack the cell wall by producing chitinases, we hypothesized that SnTox1 may have a secondary role in protection from components of the plant defense response. As hypothesized, SnTox1 binds multiple sources of chitin and localized to the fungal cell wall. We cloned and expressed two wheat chitinases to show that SnTox1 protects the pathogen from wheat chitinases roduced during infection.

Technical Abstract: All fungal plant pathogens produce effectors to manipulate the plant immune system to colonize and gain nutrients from the plant cell. Much is known about how fungal pathogens classified as biotrophs use effectors to interact with their hosts and how the host responds, however, less is known about how pathogens classified as necrotrophs use effectors to successfully colonize their respective hosts. SnTox1 is a small proteinaceous necrotrophic effector (NE) produced by the fungal pathogen, Parastagonospora nodorum, the causal agent of Septoria nodorum blotch (SNB) of wheat. We previously reported that SnTox1 induces several hallmarks of the defense response, most visibly programmed cell death (PCD) on wheat lines carrying the SnTox1 sensitivity gene Snn1. We show here that when applied to the leaf surface, SnTox1, but not other P. nodorum NEs, induces PCD in the epidermal cells as well as in the mesophyll, indicating host controlled cell-to-cell communication. We previously reported that the SnTox1 C-terminal region harbored structural homology to several plant chitin binding proteins. As predicted, SnTox1 binds multiple sources of chitin and a SnTox1-GFP fusion protein localized to the fungal cell wall. We cloned and expressed two wheat chitinases to show that, in vitro, SnTox1-expressing isolates are more fit in the presence of these wheat chitinases, showing that SnTox1 not only induces PCD to provide a source of nutrients, but also protects from the resulting increase in host chitinases.