A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility
RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we sho...
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| Published in | Cell host & microbe Vol. 25; no. 1; pp. 153 - 165.e5 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
09.01.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens.
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•Phytophthora infection increases production of a pool of secondary siRNAs in Arabidopsis•Secondary siRNAs from a PPR gene cluster contribute to defense against Phytophthora•PPR-siRNAs potentially silence Phytophthora transcripts to confer resistance•Phytophthora effector PSR2 suppresses the biogenesis of PPR-siRNAs to promote infection
The role of plant RNAi in defense against eukaryotic pathogens is unclear. Hou et al. report that Arabidopsis produces a reservoir of secondary siRNAs that confer resistance against the notorious pathogen Phytophthora, likely through trans-kingdom gene silencing. However, a Phytophthora effector defeats this defense by specifically inhibiting secondary siRNA biogenesis. |
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| AbstractList | RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens. RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens. [Display omitted] •Phytophthora infection increases production of a pool of secondary siRNAs in Arabidopsis•Secondary siRNAs from a PPR gene cluster contribute to defense against Phytophthora•PPR-siRNAs potentially silence Phytophthora transcripts to confer resistance•Phytophthora effector PSR2 suppresses the biogenesis of PPR-siRNAs to promote infection The role of plant RNAi in defense against eukaryotic pathogens is unclear. Hou et al. report that Arabidopsis produces a reservoir of secondary siRNAs that confer resistance against the notorious pathogen Phytophthora, likely through trans-kingdom gene silencing. However, a Phytophthora effector defeats this defense by specifically inhibiting secondary siRNA biogenesis. RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens.RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens. RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi (PSRs), which enhance plant susceptibility. However, the role of small RNAs in defense against eukaryotic pathogens is unclear. Here, we show that Phytophthora infection of Arabidopsis leads to increased production of a diverse pool of secondary small interfering RNAs (siRNAs). Instead of regulating endogenous plant genes, these siRNAs are found in extracellular vesicles and likely silence target genes in Phytophthora during natural infection. Introduction of a plant siRNA in Phytophthora leads to developmental deficiency and abolishes virulence, while Arabidopsis mutants defective in secondary siRNA biogenesis are hypersusceptible. Notably, Phytophthora effector PSR2 specifically inhibits secondary siRNA biogenesis in Arabidopsis and promotes infection. These findings uncover the role of siRNAs as antimicrobial agents against eukaryotic pathogens and highlight a defense/counter-defense arms race centered on trans-kingdom gene silencing between hosts and pathogens. The role of plant RNAi in defense against eukaryotic pathogens is unclear. Hou et al. report that Arabidopsis produces a reservoir of secondary siRNAs that confer resistance against the notorious pathogen Phytophthora , likely through trans-kingdom gene silencing. However, a Phytophthora effector defeats this defense by specifically inhibiting secondary siRNA biogenesis. |
| Author | Zhai, Jixian Chen, Xuemei Gu, Weifeng Zeng, Liping Choi, Du Seok Ma, Wenbo Rutter, Brian D. Zhai, Yi Innes, Roger W. Feng, Li Ye, Wenwu Karimi, Hana Z. Zhang, Bailong Hou, Yingnan |
| AuthorAffiliation | 1 Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA 5 Department of Botany and Plant Science, University of California, Riverside, Riverside, CA 92521, USA 7 Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China 4 Department of Biology, Indiana University, Bloomington, IN 47405, USA 2 Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA 3 Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China 6 Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521, USA 8 These authors contributed equally 9 Lead Contact |
| AuthorAffiliation_xml | – name: 9 Lead Contact – name: 3 Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China – name: 6 Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521, USA – name: 7 Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China – name: 8 These authors contributed equally – name: 5 Department of Botany and Plant Science, University of California, Riverside, Riverside, CA 92521, USA – name: 2 Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA – name: 1 Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA – name: 4 Department of Biology, Indiana University, Bloomington, IN 47405, USA |
| Author_xml | – sequence: 1 givenname: Yingnan surname: Hou fullname: Hou, Yingnan organization: Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 2 givenname: Yi surname: Zhai fullname: Zhai, Yi organization: Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 3 givenname: Li surname: Feng fullname: Feng, Li organization: Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China – sequence: 4 givenname: Hana Z. surname: Karimi fullname: Karimi, Hana Z. organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 5 givenname: Brian D. surname: Rutter fullname: Rutter, Brian D. organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 6 givenname: Liping surname: Zeng fullname: Zeng, Liping organization: Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 7 givenname: Du Seok surname: Choi fullname: Choi, Du Seok organization: Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 8 givenname: Bailong surname: Zhang fullname: Zhang, Bailong organization: Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 9 givenname: Weifeng surname: Gu fullname: Gu, Weifeng organization: Department of Cell Biology and Neuroscience, University of California, Riverside, Riverside, CA 92521, USA – sequence: 10 givenname: Xuemei surname: Chen fullname: Chen, Xuemei organization: Center for Plant Cell Biology, University of California, Riverside, Riverside, CA 92521, USA – sequence: 11 givenname: Wenwu surname: Ye fullname: Ye, Wenwu organization: Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China – sequence: 12 givenname: Roger W. surname: Innes fullname: Innes, Roger W. organization: Department of Biology, Indiana University, Bloomington, IN 47405, USA – sequence: 13 givenname: Jixian surname: Zhai fullname: Zhai, Jixian organization: Institute of Plant and Food Science, Department of Biology, Southern University of Science and Technology, Shenzhen 518055, China – sequence: 14 givenname: Wenbo surname: Ma fullname: Ma, Wenbo email: wenbo.ma@ucr.edu organization: Department of Microbiology and Plant Pathology, University of California, Riverside, Riverside, CA 92521, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30595554$$D View this record in MEDLINE/PubMed |
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| IngestDate | Thu Aug 21 14:01:32 EDT 2025 Tue Aug 05 11:32:27 EDT 2025 Fri Jul 11 03:22:52 EDT 2025 Thu Apr 03 07:08:07 EDT 2025 Tue Jul 01 02:44:21 EDT 2025 Thu Apr 24 22:53:14 EDT 2025 Fri Feb 23 02:31:04 EST 2024 |
| IsDoiOpenAccess | false |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1 |
| Keywords | pathogenesis RNA interference RNA-silencing suppressor microRNA host-induced gene silencing secondary small RNAs virulence factor plant immunity |
| Language | English |
| License | Copyright © 2018 Elsevier Inc. All rights reserved. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c554t-54b40eecb5f77a2ba84f249c71fe1d7383edb10e2b1966403e21a3903e309c53 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Y.H., Y.Z., H.Z.K., B.D.R., and D.S.C. did the experiments. L.F., L.Z., W.Y., and J.Z. did the sequencing analyses and sRNA target prediction. Y.H., Y.Z., H.Z.K., and B.Z. cultivated plants and harvested materials. W.M., Y.H., Y.Z., L.F., and J.Z. prepared figures and tables. W.M., R.W.I., X.C., and W.G. guided the execution of the experiments. W.M., Y.H., and R.W.I. analyzed the data. W.M. conceived the project. W.M. and Y.H. wrote the manuscript. J.Z., W.G., X.C., and R.W.I. revised the manuscript. |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/9208300 |
| PMID | 30595554 |
| PQID | 2161923173 |
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| PageCount | 13 |
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| PublicationCentury | 2000 |
| PublicationDate | 2019-01-09 |
| PublicationDateYYYYMMDD | 2019-01-09 |
| PublicationDate_xml | – month: 01 year: 2019 text: 2019-01-09 day: 09 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | Cell host & microbe |
| PublicationTitleAlternate | Cell Host Microbe |
| PublicationYear | 2019 |
| Publisher | Elsevier Inc |
| Publisher_xml | – name: Elsevier Inc |
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| Snippet | RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi... RNA silencing (RNAi) has a well-established role in anti-viral immunity in plants. The destructive eukaryotic pathogen Phytophthora encodes suppressors of RNAi... |
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| SubjectTerms | Arabidopsis Arabidopsis - genetics Arabidopsis - immunology Arabidopsis - microbiology Arabidopsis Proteins - genetics biogenesis disease susceptibility Disease Susceptibility - microbiology Gene Expression Regulation, Plant Gene Silencing genes Genes, Reporter - genetics host-induced gene silencing Host-Pathogen Interactions - genetics Host-Pathogen Interactions - immunology immunity microRNA MicroRNAs - genetics MicroRNAs - immunology Nicotiana pathogenesis pathogens Phosphoprotein Phosphatases - antagonists & inhibitors Phosphoprotein Phosphatases - metabolism Phytophthora Phytophthora - metabolism Phytophthora - pathogenicity Plant Diseases - immunology Plant Diseases - microbiology plant immunity Plant Immunity - genetics Plant Immunity - immunology Plant Leaves - immunology Plant Leaves - microbiology RNA interference RNA Interference - immunology RNA, Small Interfering - biosynthesis RNA, Small Interfering - drug effects RNA, Small Interfering - genetics RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism RNA-silencing suppressor secondary small RNAs Verticillium Virulence virulence factor Virulence Factors - genetics Virulence Factors - metabolism |
| Title | A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility |
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