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      Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

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          Abstract

          Some pathogens and pests deliver small RNAs (sRNAs) into host cells to suppress host immunity. Conversely, hosts also transfer sRNAs into pathogens and pests to inhibit their virulence. Although sRNA trafficking has been observed in a wide variety of interactions, how sRNAs are transferred, especially from hosts to pathogens and pests, is still unknown. Here, we show that host Arabidopsis cells secrete exosome-like extracellular vesicles to deliver sRNAs into fungal pathogen Botrytis cinerea. These sRNA-containing vesicles accumulate at the infection sites and are taken up by the fungal cells. Transferred host sRNAs induce silencing of fungal genes critical for pathogenicity. Thus, Arabidopsis has adapted exosome-mediated cross-kingdom RNA interference as part of its immune responses during the evolutionary arms race with the pathogen.

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          RNA silencing in plants.

          David Baulcombe (2004)
          There are at least three RNA silencing pathways for silencing specific genes in plants. In these pathways, silencing signals can be amplified and transmitted between cells, and may even be self-regulated by feedback mechanisms. Diverse biological roles of these pathways have been established, including defence against viruses, regulation of gene expression and the condensation of chromatin into heterochromatin. We are now in a good position to investigate the full extent of this functional diversity in genetic and epigenetic mechanisms of genome control.
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            Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways.

            Arne Weiberg, Ming Wang, Feng-Mao Lin … (2013)
            Botrytis cinerea, the causative agent of gray mold disease, is an aggressive fungal pathogen that infects more than 200 plant species. Here, we show that some B. cinerea small RNAs (Bc-sRNAs) can silence Arabidopsis and tomato genes involved in immunity. These Bc-sRNAs hijack the host RNA interference (RNAi) machinery by binding to Arabidopsis Argonaute 1 (AGO1) and selectively silencing host immunity genes. The Arabidopsis ago1 mutant exhibits reduced susceptibility to B. cinerea, and the B. cinerea dcl1 dcl2 double mutant that can no longer produce these Bc-sRNAs displays reduced pathogenicity on Arabidopsis and tomato. Thus, this fungal pathogen transfers "virulent" sRNA effectors into host plant cells to suppress host immunity and achieve infection, which demonstrates a naturally occurring cross-kingdom RNAi as an advanced virulence mechanism.
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              The structure and synthesis of the fungal cell wall.

              Shaun M Bowman, Stephen Free (2006)
              The fungal cell wall is a dynamic structure that protects the cell from changes in osmotic pressure and other environmental stresses, while allowing the fungal cell to interact with its environment. The structure and biosynthesis of a fungal cell wall is unique to the fungi, and is therefore an excellent target for the development of anti-fungal drugs. The structure of the fungal cell wall and the drugs that target its biosynthesis are reviewed. Based on studies in a number of fungi, the cell wall has been shown to be primarily composed of chitin, glucans, mannans and glycoproteins. The biosynthesis of the various components of the fungal cell wall and the importance of the components in the formation of a functional cell wall, as revealed through mutational analyses, are discussed. There is strong evidence that the chitin, glucans and glycoproteins are covalently cross-linked together and that the cross-linking is a dynamic process that occurs extracellularly. (c) 2006 Wiley Periodicals, Inc.
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                Author and article information

                Journal
                Journal ID (nlm-journal-id): 0404511
                Journal ID (pubmed-jr-id): 7473
                Journal ID (nlm-ta): Science
                Journal ID (iso-abbrev): Science
                Title: Science (New York, N.Y.)
                ISSN (Print): 0036-8075
                ISSN (Electronic): 1095-9203
                Publication date Nihms-submitted: 24 March 2019
                Publication date (Electronic): 17 May 2018
                Publication date (Print): 08 June 2018
                Publication date PMC-release: 01 April 2019
                Volume: 360
                Issue: 6393
                Pages: 1126-1129
                Affiliations
                [1 ]Department of Microbiology and Plant Pathology, Center for Plant Cell Biology, Institute for Integrative Genome Biology, University of California, Riverside, 900 University Avenue, Riverside, CA 92521, USA.
                [2 ]Department of Plant Protection, Nanjing Agriculture University, Nanjing, 210095, China.
                [3 ]Department of Biological Science and Technology, National Chiao Tung University, Hsin-Chu 300, Taiwan.
                Author notes

                Author contributions: H.J. conceived the idea, designed the experiments, and supervised the project. Q.C. performed the majority of the experiments and analyzed data. L.Q., M.W., B.H., and J.P. contributed to the functional analysis of the fungal target genes. F.-M.L. and S.-D.H. performed bioinformatics analysis. Q.C. and H.J. wrote the manuscript.

                [* ]Corresponding author. hailingj@ucr.edu
                Article
                Accession ID: PMC6442475 Pmcid ID: PMC6442475 Pmc-uid ID: 6442475 Manuscript ID: nihpa1019813
                DOI: 10.1126/science.aar4142
                PMC ID: 6442475
                PubMed ID: 29773668
                SO-VID: f4b55912-adc0-4dbc-9385-cc8f5bdfe3c1
                License:

                exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. The title Science is a registered trademark of AAAS.

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