TYMV and TRV infect Arabidopsis thaliana by expressing weak suppressors of RNA silencing and inducing host RNASE THREE LIKE1

• Published in: PLoS pathogens 2023-01, Vol.19 (1), p.e1010482-e1010482
• Main Authors: Sehki, Hayat, Yu, Agnès, Elmayan, Taline, Vaucheret, Hervé
• Format: Article
• Language: English
• Subjects: Accumulation; Amplification; Analysis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Argonaute 2 protein; Biology and life sciences; Defense industry; Defense mechanisms; Disease susceptibility; Diseases and pests; Engineering and Technology; Enzymes; Flowers & plants; Gene expression; Gene silencing; Genetic engineering; Genetic transcription; Health aspects; Hypotheses; Identification and classification; Infection; Infections; Life Sciences; Microbiology and Parasitology; Mutants; Mutation; Nucleic acids; Pathogens; Plant Diseases - genetics; Plant Diseases - virology; Plant virus diseases; Plant viruses; Plant-pathogen relationships; Post-transcription; Proteins; Repressor Proteins - genetics; Repressor Proteins - metabolism; Research and Analysis Methods; Ribonuclease; Ribonuclease III - genetics; Ribonuclease III - metabolism; Ribonucleic acid; RNA; RNA Interference; RNA polymerase; RNA viruses; RNA, Small Interfering - genetics; RNA, Small Interfering - metabolism; RNA-mediated interference; Scientific equipment and supplies industry; siRNA; Suppressors; Tobacco; Transgenes; Transgenic plants; Transposons; Tymovirus - genetics; Tymovirus - metabolism; Virology; Virus diseases of plants; Viruses
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1010482

Post-Transcriptional Gene Silencing (PTGS) is a defense mechanism that targets invading nucleic acids of endogenous (transposons) or exogenous (pathogens, transgenes) origins. During plant infection by viruses, virus-derived primary siRNAs target viral RNAs, resulting in both destruction of single-stranded viral RNAs (execution step) and production of secondary siRNAs (amplification step), which maximizes the plant defense. As a counter-defense, viruses express proteins referred to as Viral Suppressor of RNA silencing (VSR). Some viruses express VSRs that totally inhibit PTGS, whereas other viruses express VSRs that have limited effect. Here we show that infection with the Turnip yellow mosaic virus (TYMV) is enhanced in Arabidopsis ago1, ago2 and dcl4 mutants, which are impaired in the execution of PTGS, but not in dcl2, rdr1 and rdr6 mutants, which are impaired in the amplification of PTGS. Consistently, we show that the TYMV VSR P69 localizes in siRNA-bodies, which are the site of production of secondary siRNAs, and limits PTGS amplification. Moreover, TYMV induces the production of the host enzyme RNASE THREE-LIKE 1 (RTL1) to further reduce siRNA accumulation. Infection with the Tobacco rattle virus (TRV), which also encodes a VSR limiting PTGS amplification, induces RTL1 as well to reduce siRNA accumulation and promote infection. Together, these results suggest that RTL1 could be considered as a host susceptibility gene that is induced by viruses as a strategy to further limit the plant PTGS defense when VSRs are insufficient.