Inoue Yoshihiro, Phuong Vy Trinh Thi, Singkaravanit-Ogawa Suthitar, Zhang Ru, Yamada Kohji, Ogawa Taiki, Ishizuka Junya, Narusaka Yoshihiro, Takano Yoshitaka
Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan.
Graduate School of Technology, Industrial and Social Sciences, Tokushima University, Tokushima, 770-8513, Japan.
New Phytol. 2023 May;238(4):1578-1592. doi: 10.1111/nph.18790. Epub 2023 Mar 20.
The hemibiotrophic fungal plant pathogen Colletotrichum orbiculare is predicted to secrete hundreds of effector proteins when the pathogen infects cucurbit crops, such as cucumber and melon, and tobacco (Nicotiana benthamiana), a distantly related Solanaceae species. Here, we report the identification of sets of C. orbiculare effector genes that are differentially required for fungal virulence to two phylogenetically distant host species. Through targeted gene knockout screening of C. orbiculare 'core' effector candidates defined based on in planta gene expression, we identified: four host-specific virulence effectors (named effector proteins for cucurbit infection, or EPCs) that are required for full virulence of C. orbiculare to cucurbit hosts, but not to the Solanaceae host N. benthamiana; and five host-nonspecific virulence effectors, which collectively contribute to fungal virulence to both hosts. During host infection, only a small subset of genes, including the host-specific EPC effector genes, showed preferential expression on one of the hosts, while gene expression profiles of the majority of other genes, including the five host-nonspecific effector genes, were common to both hosts. This work suggests that C. orbiculare adopts a host-specific effector deployment strategy, in addition to general host-blind virulence mechanisms, for adaptation to cucurbit hosts.
半活体营养型真菌植物病原菌圆形炭疽菌在侵染葫芦科作物（如黄瓜和甜瓜）以及烟草（本氏烟草，一种亲缘关系较远的茄科植物）时，预计会分泌数百种效应蛋白。在此，我们报告了圆形炭疽菌效应子基因集的鉴定结果，这些基因对于真菌在两种系统发育关系较远的宿主物种上的致病性具有不同的需求。通过对基于植物体内基因表达定义的圆形炭疽菌“核心”效应子候选基因进行靶向基因敲除筛选，我们鉴定出：四种宿主特异性致病效应子（命名为葫芦科感染效应蛋白，即EPCs），它们是圆形炭疽菌对葫芦科宿主具有完全致病性所必需的，但对茄科宿主本氏烟草则不是必需的；以及五种宿主非特异性致病效应子，它们共同促进真菌对两种宿主的致病性。在宿主感染过程中，只有一小部分基因，包括宿主特异性EPC效应子基因，在其中一种宿主上表现出优先表达，而大多数其他基因，包括五种宿主非特异性效应子基因，在两种宿主上的基因表达谱是相同的。这项工作表明，除了一般的宿主非特异性致病机制外，圆形炭疽菌还采用宿主特异性效应子部署策略来适应葫芦科宿主。
