Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana.

Si Liu; Meijuan Chen; Ruidong Li; Wan-Xiang Li; Amit Gal-On; Zhenyu Jia; Shou-Wei Ding

doi:10.1038/s41467-022-30771-0

Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana.

Si Liu, Meijuan Chen, Ruidong Li, Wan-Xiang Li, Amit Gal-On, Zhenyu Jia, Shou-Wei Ding

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

Virus-host coevolution often drives virus immune escape. However, it remains unknown whether natural variations of plant virus resistance are enriched in genes of RNA interference (RNAi) pathway known to confer essential antiviral defense in plants. Here, we report two genome-wide association study screens to interrogate natural variation among wild-collected Arabidopsis thaliana accessions in quantitative resistance to the endemic cucumber mosaic virus (CMV). We demonstrate that the highest-ranked gene significantly associated with resistance from both screens acts to regulate antiviral RNAi in ecotype Columbia-0. One gene, corresponding to Reduced Dormancy 5 (RDO5), enhances resistance by promoting amplification of the virus-derived small interfering RNAs (vsiRNAs). Interestingly, the second gene, designated Antiviral RNAi Regulator 1 (VIR1), dampens antiviral RNAi so its genetic inactivation by CRISPR/Cas9 editing enhances both vsiRNA production and CMV resistance. Our findings identify positive and negative regulators of the antiviral RNAi defense that may play important roles in virus-host coevolution.

Original language	English (US)
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30771-0
State	Published - May 30 2022
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2022-06-06
Acknowledged KAUST grant number(s): OSR-2015-CRG4-2647
Acknowledgements: We wish to thank Drs. Daoxin Xie and Xueping Zhou for sharing materials. This project was supported by funding from the Agricultural Experimental Station and College of Natural and Agricultural Sciences, the University of California, Riverside (to S.-W.D.) and by grants from the US-Israel Binational Agricultural Research and Development Fund (no. IS-5027-17C to A.G.O. and S.-W.D.) and Office of Sponsored Research of the King Abdullah University of Science and Technology, Saudi Arabia (no. OSR-2015-CRG4-2647 to Drs. Magdy Mahfouz and S.-W.D.).
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology
General Chemistry
General Physics and Astronomy

Access to Document

10.1038/s41467-022-30771-0

Cite this

@article{d352201de0824ca1b9375269836d8a2d,

title = "Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana.",

abstract = "Virus-host coevolution often drives virus immune escape. However, it remains unknown whether natural variations of plant virus resistance are enriched in genes of RNA interference (RNAi) pathway known to confer essential antiviral defense in plants. Here, we report two genome-wide association study screens to interrogate natural variation among wild-collected Arabidopsis thaliana accessions in quantitative resistance to the endemic cucumber mosaic virus (CMV). We demonstrate that the highest-ranked gene significantly associated with resistance from both screens acts to regulate antiviral RNAi in ecotype Columbia-0. One gene, corresponding to Reduced Dormancy 5 (RDO5), enhances resistance by promoting amplification of the virus-derived small interfering RNAs (vsiRNAs). Interestingly, the second gene, designated Antiviral RNAi Regulator 1 (VIR1), dampens antiviral RNAi so its genetic inactivation by CRISPR/Cas9 editing enhances both vsiRNA production and CMV resistance. Our findings identify positive and negative regulators of the antiviral RNAi defense that may play important roles in virus-host coevolution.",

author = "Si Liu and Meijuan Chen and Ruidong Li and Wan-Xiang Li and Amit Gal-On and Zhenyu Jia and Shou-Wei Ding",

note = "KAUST Repository Item: Exported on 2022-06-06 Acknowledged KAUST grant number(s): OSR-2015-CRG4-2647 Acknowledgements: We wish to thank Drs. Daoxin Xie and Xueping Zhou for sharing materials. This project was supported by funding from the Agricultural Experimental Station and College of Natural and Agricultural Sciences, the University of California, Riverside (to S.-W.D.) and by grants from the US-Israel Binational Agricultural Research and Development Fund (no. IS-5027-17C to A.G.O. and S.-W.D.) and Office of Sponsored Research of the King Abdullah University of Science and Technology, Saudi Arabia (no. OSR-2015-CRG4-2647 to Drs. Magdy Mahfouz and S.-W.D.). This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

year = "2022",

month = may,

day = "30",

doi = "10.1038/s41467-022-30771-0",

language = "English (US)",

volume = "13",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

TY - JOUR

T1 - Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana.

AU - Liu, Si

AU - Chen, Meijuan

AU - Li, Ruidong

AU - Li, Wan-Xiang

AU - Gal-On, Amit

AU - Jia, Zhenyu

AU - Ding, Shou-Wei

N1 - KAUST Repository Item: Exported on 2022-06-06 Acknowledged KAUST grant number(s): OSR-2015-CRG4-2647 Acknowledgements: We wish to thank Drs. Daoxin Xie and Xueping Zhou for sharing materials. This project was supported by funding from the Agricultural Experimental Station and College of Natural and Agricultural Sciences, the University of California, Riverside (to S.-W.D.) and by grants from the US-Israel Binational Agricultural Research and Development Fund (no. IS-5027-17C to A.G.O. and S.-W.D.) and Office of Sponsored Research of the King Abdullah University of Science and Technology, Saudi Arabia (no. OSR-2015-CRG4-2647 to Drs. Magdy Mahfouz and S.-W.D.). This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2022/5/30

Y1 - 2022/5/30

N2 - Virus-host coevolution often drives virus immune escape. However, it remains unknown whether natural variations of plant virus resistance are enriched in genes of RNA interference (RNAi) pathway known to confer essential antiviral defense in plants. Here, we report two genome-wide association study screens to interrogate natural variation among wild-collected Arabidopsis thaliana accessions in quantitative resistance to the endemic cucumber mosaic virus (CMV). We demonstrate that the highest-ranked gene significantly associated with resistance from both screens acts to regulate antiviral RNAi in ecotype Columbia-0. One gene, corresponding to Reduced Dormancy 5 (RDO5), enhances resistance by promoting amplification of the virus-derived small interfering RNAs (vsiRNAs). Interestingly, the second gene, designated Antiviral RNAi Regulator 1 (VIR1), dampens antiviral RNAi so its genetic inactivation by CRISPR/Cas9 editing enhances both vsiRNA production and CMV resistance. Our findings identify positive and negative regulators of the antiviral RNAi defense that may play important roles in virus-host coevolution.

AB - Virus-host coevolution often drives virus immune escape. However, it remains unknown whether natural variations of plant virus resistance are enriched in genes of RNA interference (RNAi) pathway known to confer essential antiviral defense in plants. Here, we report two genome-wide association study screens to interrogate natural variation among wild-collected Arabidopsis thaliana accessions in quantitative resistance to the endemic cucumber mosaic virus (CMV). We demonstrate that the highest-ranked gene significantly associated with resistance from both screens acts to regulate antiviral RNAi in ecotype Columbia-0. One gene, corresponding to Reduced Dormancy 5 (RDO5), enhances resistance by promoting amplification of the virus-derived small interfering RNAs (vsiRNAs). Interestingly, the second gene, designated Antiviral RNAi Regulator 1 (VIR1), dampens antiviral RNAi so its genetic inactivation by CRISPR/Cas9 editing enhances both vsiRNA production and CMV resistance. Our findings identify positive and negative regulators of the antiviral RNAi defense that may play important roles in virus-host coevolution.

UR - http://hdl.handle.net/10754/678610

UR - https://www.nature.com/articles/s41467-022-30771-0

U2 - 10.1038/s41467-022-30771-0

DO - 10.1038/s41467-022-30771-0

M3 - Article

C2 - 35637208

SN - 2041-1723

VL - 13

JO - Nature communications

JF - Nature communications

IS - 1

ER -

Identification of positive and negative regulators of antiviral RNA interference in Arabidopsis thaliana.

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this