Non-canonical fungal G-protein coupled receptors promote Fusarium head blight on wheat

Fusarium Head Blight (FHB) is the number one floral disease of cereals and poses a serious health hazard by contaminating grain with the harmful mycotoxin deoxynivalenol (DON). Fungi adapt to fluctuations in their environment, coordinating development and metabolism accordingly. G-protein coupled receptors (GPCRs) communicate changes in the environment to intracellular G-proteins that direct the appropriate biological response, suggesting that fungal GPCR signalling may be key to virulence. Here we describe the expansion of non-classical GPCRs in the FHB causing pathogen, Fusarium graminearum, and show that class X receptors are highly expressed during wheat infection. We identify class X receptors that are required for FHB disease on wheat, and show that the absence of a GPCR can cause an enhanced host response that restricts the progression of infection. Specific receptor sub-domains are required for virulence. These non-classical receptors physically interact with intracellular G-proteins and are therefore bona fide GPCRs. Disrupting a class X receptor is shown to dysregulate the transcriptional coordination of virulence traits during infection. This amounts to enhanced wheat defensive responses, including chitinase and plant cell wall biosynthesis, resulting in apoplastic and vascular occlusions that impede infection. Our results show that GPCR signalling is important to FHB disease establishment.

赤霉病（Fusarium Head Blight, FHB）是谷类作物最主要的花部病害，其产生的有毒真菌毒素脱氧雪腐镰刀菌烯醇（deoxynivalenol, DON）会污染谷物，对人体健康造成严重威胁。真菌可适应环境波动，并据此协调自身发育与代谢过程。G蛋白偶联受体（G-protein coupled receptors, GPCRs）可将环境变化传递至细胞内G蛋白，由后者调控相应的生物学应答，这提示真菌GPCR信号通路可能是其致病力的关键调控因素。本研究阐明了引发赤霉病的病原菌禾谷镰孢菌（Fusarium graminearum）中非经典GPCRs的扩增情况，并发现X类受体在小麦侵染过程中呈高表达状态。我们鉴定出了小麦赤霉病致病所必需的X类受体，并证实缺失某一GPCR可触发宿主增强型免疫应答，从而限制病原菌侵染进程。致病力依赖于特定的受体亚结构域。这类非经典受体可与细胞内G蛋白发生物理性相互作用，因此属于真正的GPCRs。研究表明，敲除X类受体会失调侵染过程中致病相关性状的转录调控网络。这会增强小麦的防御反应，包括几丁质酶活性与植物细胞壁生物合成，最终引发质外体与维管束堵塞，阻碍病原菌侵染。本研究结果证实，GPCR信号通路对于赤霉病的定殖至关重要。