A Tilletia horrida-Secreted Cell Surface Protein ThCSP5 Functions as an Elicitor to Activate Plant Immunity and Enhance Resistance

Tilletia horrida is an important soilborne fungal pathogen that causes rice kernel smut (RKS) worldwide. We identified a secretory protein, ThCSP5, which encodes a cell surface protein (CSP) that induces cell death in Nicotiana benthamiana leaves. The predicted signal peptide (SP) of ThCSP5 has a secreting function and is required for its ability to induce cell death. The cysteine residues are necessary for ThCSP5 to trigger cell death in N. benthamiana. ThCSP5 is found in the cytoplasm, plasma membrane, and nucleus of plant cells, and its localization in the extranuclear is required to induce cell death. The ability of ThCSP5 to trigger cell death in N. benthamiana depends on RAR1 (required for Mla12 resistance), BAK1/SERK3 (somatic embryogenesis receptor-like kinase), and SGT1 (suppressor of the G2 allele of Skp1). Heterologous overexpression and transcriptome analysis showed that ThCSP5 triggered various defense-related pathways and enhanced resistance to T. horrida in rice. Further research revealed that ThCSP5 interacted with and degraded the rice RNA recognition motif (RRM) protein OsRRM1, which negatively regulates rice resistance against T. horrida. These findings suggest that ThCSP5 is a novel fungal elicitor in T. horrida that activates plant immunity and enhances resistance by degrading OsRRM1.

稻粒黑粉菌（Tilletia horrida）是一种重要的土传真菌病原菌，在全球范围内引发稻粒黑粉病（RKS）。本研究鉴定得到一种分泌蛋白ThCSP5，其编码一种可在本氏烟草（Nicotiana benthamiana）叶片中诱导细胞死亡的细胞表面蛋白（CSP）。ThCSP5的预测信号肽（SP）具备分泌功能，且是其诱导细胞死亡能力所必需的。半胱氨酸残基对于ThCSP5在本氏烟草中触发细胞死亡至关重要。ThCSP5可定位于植物细胞的细胞质、质膜与细胞核中，其核外定位是诱导细胞死亡的必要条件。ThCSP5在本氏烟草中触发细胞死亡的能力依赖于Mla12抗性必需因子RAR1、体细胞胚胎发生类受体激酶BAK1/SERK3以及Skp1的G2等位基因抑制因子SGT1。异源过表达与转录组分析结果显示，ThCSP5可激活多种防御相关通路，并增强水稻对稻粒黑粉菌的抗性。进一步研究发现，ThCSP5可与水稻RNA识别基序（RRM）蛋白OsRRM1相互作用并使其降解，而OsRRM1负调控水稻对稻粒黑粉菌的抗性。上述研究结果表明，ThCSP5是稻粒黑粉菌中一种新型真菌激发子，可通过降解OsRRM1激活植物免疫并增强水稻抗性。