Taxonomically Restricted Wheat Genes Interact With Small Secreted Fungal Proteins and Enhance Resistance to Septoria Tritici Blotch Disease.

Ciarán J Brennan,Angela Feechan,Ewen Mullins,Aoife O’Driscoll,Harriet R Benbow,Binbin Zhou,Sobia Ajaz,Sujit J Karki,James Gerard Hehir,Fiona M Doohan

doi:10.3389/fpls.2020.00433

Abstract

Understanding the nuances of host/pathogen interactions are paramount if we wish to effectively control cereal diseases. In the case of the wheat/Zymoseptoria tritici interaction that leads to Septoria tritici blotch (STB) disease, a 10,000-year-old conflict has led to considerable armaments being developed on both sides which are not reflected in conventional model systems. Taxonomically restricted genes (TRGs) have evolved in wheat to better allow it to cope with stress caused by fungal pathogens, and Z. tritici has evolved specialized effectors which allow it to manipulate its’ host. A microarray focused on the latent phase response of a resistant wheat cultivar (cv. Stigg) and susceptible wheat cultivar (cv. Gallant) to Z. tritici infection was mined for TRGs within the Poaceae. From this analysis, we identified two TRGs that were significantly upregulated in response to Z. tritici infection, Septoria-responsive TRG6 and 7 (TaSRTRG6 and TaSRTRG7). Virus induced silencing of these genes resulted in an increased susceptibility to STB disease in cvs. Gallant and Stigg, and significantly so in the latter (2.5-fold increase in STB disease). In silico and localization studies categorized TaSRTRG6 as a secreted protein and TaSRTRG7 as an intracellular protein. Yeast two-hybrid analysis and biofluorescent complementation studies demonstrated that both TaSRTRG6 and TaSRTRG7 can interact with small proteins secreted by Z. tritici (potential effector candidates). Thus we conclude that TRGs are an important part of the wheat-Z. tritici co-evolution story and potential candidates for modulating STB resistance.

Highlights

Septoria tritici blotch (STB) is a foliar disease of wheat caused by the haploid, pathogenic fungus Zymoseptoria tritici
Stigg only exhibiting
Using a galactose-responsive transcription factor GAL4 (GAL4)-based Y2H system, we deduced that TaSRTRG6 interacted with three of 27 Z. tritici SSPs (Zt11, Zt19, and Zt24) and TaSRTRG7 interacted with two of the 27 Z. tritici SSPs tested (Zt16 and Zt18) (Figure 7)

Summary

Introduction

Septoria tritici blotch (STB) is a foliar disease of wheat caused by the haploid, pathogenic fungus Zymoseptoria tritici (formally known as Mycosphaerella graminicola; anamorph: Septoria tritici). Severe epidemics of STB have historically been reported to cause yield losses of up to 50% (Eyal, 1987). More contemporary estimates in the United Kingdom have placed losses closer to 20% when STB resistant varieties are used in conjunction with a viable fungicide management plan (Fones and Gurr, 2015). A hallmark of Z. tritici infection in wheat is the prolonged asymptomatic latent phase that occurs after infection takes place. This latent phase varies dramatically between cultivars, inoculum and environmental conditions Prolonging this phase further can help to mitigate the effects of STB due to prolonged photosynthesis and a reduction in fungal inoculum (Hehir et al, 2017)

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Results

Conclusion