Colletotrichum fructicola is emerging as a devastating pathogenic fungus causing anthracnose in a wide range of horticultural crops, particularly fruits. Exploitation of nonhost resistance (NHR) represents a robust strategy for plant disease management. Perception of core effectors from phytopathogens frequently leads to hypersensitive cell death and resistance in nonhost plants, however, such core effectors in C. fructicola and their signaling components in non-hosts remain elusive. Here, we found a virulent C. fructicola strain isolated from pear exhibits non-adaptation in the model plant N. benthamiana. Perception of secreted molecules from C. fructicola appears to be a dominant factor in NHR, and four novel core effectors CfCE4, CfCE25, CfCE61 and CfCE66 detected by N. benthamiana were accordingly identified. These core effectors exhibit cell death-inducing activity in N. benthamiana and accumulate in the apoplast. With a series of CRISPR/Cas9-edited mutants or gene-silenced plants, we found the coreceptor BAK1 and helper NLRs including ADR1, NRG1 and NRCs mediate perceptions of these core effectors in N. benthamiana. Concurrently, multiple N. benthamiana genes encoding cell surface immune receptors and intracellular immune receptors were greatly induced by C. fructicola. This work represents the first characterization of the repertoire of C. fructicola core effectors responsible for NHR. Significantly, the novel core effectors and their signaling components unveiled in this study offered insights into a continuum of layered immunity during NHR, and will be helpful for anthracnose disease management in diverse horticultural crops.

中文翻译：

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非宿主本塞姆氏烟草中广泛宿主范围的梨炭疽病菌炭疽菌中多个新型核心效应子的细胞外感知

果炭疽病 (Colletotrichum fructicola) 正在成为一种毁灭性的病原真菌，可在多种园艺作物（尤其是水果）中引起炭疽病。利用非寄主抗性（NHR）代表了植物病害管理的强有力策略。对植物病原体核心效应子的感知经常导致非寄主植物中过敏性细胞死亡和抗性，然而，C. fructicola 中的此类核心效应子及其在非寄主中的信号传导成分仍然难以捉摸。在这里，我们发现从梨中分离出的有毒 C. fructicola 菌株在模式植物 N. Benthamiana 中表现出不适应。对 C. fructicola 分泌分子的感知似乎是 NHR 的主导因素，并且相应地鉴定了本塞姆氏烟草检测到的四个新的核心效应子 CfCE4、CfCE25、CfCE61 和 CfCE66。这些核心效应子在本塞姆氏烟草中表现出细胞死亡诱导活性，并在质外体中积累。通过一系列 CRISPR/Cas9 编辑的突变体或基因沉默植物，我们发现本塞姆氏烟草中的辅助受体 BAK1 和辅助 NLR（包​​括 ADR1、NRG1 和 NRC）介导这些核心效应子的感知。同时，编码细胞表面免疫受体和细胞内免疫受体的多个本塞姆氏烟草基因被 C. fructicola 极大地诱导。这项工作代表了负责 NHR 的 C. fructicola 核心效应子的首次表征。值得注意的是，本研究中揭示的新型核心效应器及其信号成分为 NHR 期间分层免疫的连续体提供了见解，并将有助于多种园艺作物的炭疽病管理。