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서울대학교

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Plant Commun., 2023 Apr 23;100606 | https://doi.org/10.1016/j.xplc.2023.100606 The Phytophthora nucleolar effector Pi23226 targets host ribosome biogenesis to induce necrotrophic cell death

Soeui Lee ^{1 2}, Jaehwan Kim ^{1 2}, Myung-Shin Kim ^{1 3 5}, Cheol Woo Min ⁴, Sun Tae Kim ⁴, Sang-Bong Choi ⁵, Joo Hyun Lee ^{1 *}, Doil Choi ^{1 2 *}

¹Plant Immunity Research Center, Seoul National University, Seoul 08826, Republic of Korea
²Plant Genomics and Breeding Institute, Department of Agriculture, Forestry and Bioresources, College of Agriculture and Life Science, Seoul National University, Seoul 08826, Republic of Korea
³Interdisciplinary Programs in Agricultural Genomics, College of Agriculture and Life Science, Seoul National University, Seoul 08826, Republic of Korea
⁴Department of Plant Bioscience, Life and Industry Convergence Research Institute, Pusan National University, Miryang 50463, Republic of Korea
⁵Division of Bioscience and Bioinformatics, Myongji University, Yongin 449-728, Republic of Korea

^*Corresponding author: correspondence to Joo Hyun Lee or Doil Choi

Abstract

Pathogen effectors target diverse subcellular organelles to manipulate the plant immune system. Although the nucleolus has emerged as a stress marker and several effectors are localized in the nucleolus, the roles of nucleolar-targeted effectors remain elusive. In this study, we showed that Phytophthora infestans infection of Nicotiana benthamiana results in nucleolar inflation during the transition from the biotrophic to the necrotrophic phase. Multiple P. infestans effectors were localized in the nucleolus: Pi23226 induced cell death in N. benthamiana and nucleolar inflation similar to that observed in the necrotrophic stage of infection, whereas its homolog Pi23015 and a deletion mutant (Pi23226ΔC) did not induce cell death or affect nucleolar size. RNA immunoprecipitation and individual-nucleotide-resolution UV crosslinking and immunoprecipitation sequencing analysis indicated that Pi23226 bound to the 3′ end of 25S rRNA precursors, resulting in accumulation of unprocessed 27S pre-rRNAs. The nucleolar stress marker NAC082 was strongly upregulated under Pi23226-expressing conditions. Pi23226 subsequently inhibited global protein translation in host cells by interacting with ribosomes. Pi23226 enhanced P. infestans pathogenicity, indicating that Pi23226-induced ribosome malfunction and cell death were beneficial for pathogenesis in the host. Our results provide evidence for the molecular mechanism underlying RNA-binding effector activity in host ribosome biogenesis and lead to new insights into the nucleolar action of effectors in pathogenesis.

논문정보

형식Research article
게재일2023년 04월 (BRIC 등록일 2023-07-13)
연구진국내 연구진
분야 생명과학 > 식량작물 및 원예작물

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