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

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