A Nucleolar Effector of Phytophthora infestans , Pi23226, Binds to rRNA and Subverts Ribosome Biogenesis to Cell Death

Effectors from pathogens target diverse subcellular organelles to manipulate the plant immune system. Although quite a few effectors were reported to be localized in the nucleolus, their roles remain largely unknown. In this study, a nucleolar-localizing Phytophthora infestans effector (Pi23226), which induces cell death in a host plant, Nicotiana benthamiana, was characterized. Pi23226-induced cell death was accompanied by the inflation of the nucleolus and subverting protein translation by interfering with ribosome biogenesis, whereas its homolog Pi23015 and a deletion mutant (Pi23226ΔC) did not induce either cell death or subvert ribosome biogenesis. Although Pi23226, Pi23226ΔC, or Pi23015 highly accumulated mature 18S, 5.8S, and 25S rRNAs, only Pi23226 accumulated unprocessed 27S pre-rRNAs. Incomplete processing of 25S rRNA was caused by direct binding of Pi23226 to the 3’-end of 25S rRNA precursors. In addition, a nucleolar stress marker, a NAC082 transcription factor, was highly upregulated in Pi23226-expressing conditions. Subsequently, Pi23226 inhibits global protein translation in host cells by interacting with ribosomes. Considering that Pi23226 positively affects the pathogenicity of P. infestans, Pi23226-induced ribosome malfunction and cell death could be beneficial for colonization of the pathogen in the host plant. Our results provide the first evidence of RNA-binding effectors from plant pathogens as well as new insight into the nucleolar action of pathogen effectors.