Turnip crinkle virus-encoded suppressor of RNA silencing suppresses mRNA decay by interacting with Arabidopsis XRN4.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
11 2023
Historique:
revised: 06 07 2023
received: 14 04 2023
accepted: 17 07 2023
medline: 23 10 2023
pubmed: 31 7 2023
entrez: 31 7 2023
Statut: ppublish

Résumé

Plant cells employ intricate defense mechanisms, including mRNA decay pathways, to counter viral infections. Among the RNA quality control (RQC) mechanisms, nonsense-mediated decay (NMD), no-go decay (NGD), and nonstop decay (NSD) pathways play critical roles in recognizing and cleaving aberrant mRNA molecules. Turnip crinkle virus (TCV) is a plant virus that triggers mRNA decay pathways, but it has also evolved strategies to evade this antiviral defense. In this study, we investigated the activation of mRNA decay during TCV infection and its impact on TCV RNA accumulation. We found that TCV infection induced the upregulation of essential mRNA decay factors, indicating their involvement in antiviral defense and the capsid protein (CP) of TCV, a well-characterized viral suppressor of RNA silencing (VSR), also compromised the mRNA decay-based antiviral defense by targeting AtXRN4. This interference with mRNA decay was supported by the observation that TCV CP stabilized a reporter transcript with a long 3' untranslated region (UTR). Moreover, TCV CP suppressed the decay of known NMD target transcripts, further emphasizing its ability to modulate host RNA control mechanisms. Importantly, TCV CP physically interacted with AtXRN4, providing insight into the mechanism of viral interference with mRNA decay. Overall, our findings reveal an alternative strategy employed by TCV, wherein the viral coat protein suppresses the mRNA decay pathway to facilitate viral infection.

Identifiants

pubmed: 37522642
doi: 10.1111/tpj.16402
doi:

Substances chimiques

RNA 63231-63-0
Antiviral Agents 0
RNA, Viral 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

744-755

Informations de copyright

© 2023 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Arciga-Reyes, L., Wootton, L., Kieffer, M. & Davies, B. (2006) UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. The Plant Journal: For Cell and Molecular Biology, 47(3), 480-489.
Balistreri, G., Bognanni, C. & Mühlemann, O. (2017) Virus escape and manipulation of cellular nonsense-mediated mRNA decay. Viruses, 9(1), 24.
Cao, M., Ye, X., Willie, K., Lin, J., Zhang, X., Redinbaugh, M.N. et al. (2010) The capsid protein of turnip crinkle virus overcomes two separate defense barriers to facilitate systemic movement of the virus in Arabidopsis. Journal of Virology, 84(15), 7793-7802.
Cheng, C.P., Jaag, H.M., Jonczyk, M., Serviene, E. & Nagy, P.D. (2007) Expression of the Arabidopsis Xrn4p 5′-3′ exoribonuclease facilitates degradation of tombusvirus RNA and promotes rapid emergence of viral variants in plants. Virology, 368(2), 238-248.
Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C. & Voinnet, O. (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science, 313(5783), 68-71.
Garcia, D., Garcia, S. & Voinnet, O. (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host & Microbe, 16(3), 391-402.
Ge, Z., Quek, B.L., Beemon, K.L. & Hogg, J.R. (2016) Polypyrimidine tract binding protein 1 protects mRNAs from recognition by the nonsense-mediated mRNA decay pathway. eLife, 5, e11155.
Gloggnitzer, J., Akimcheva, S., Srinivasan, A., Kusenda, B., Riehs, N., Stampfl, H. et al. (2014) Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host & Microbe, 16(3), 376-390.
Gunawardene, C.D., Im, J. & White, K.A. (2021) RNA structure protects the 5′ end of an uncapped tombusvirus RNA genome from Xrn digestion. Journal of Virology, 95(20), e0103421.
Gunawardene, C.D., Newburn, L.R. & White, K.A. (2019) A 212-nt long RNA structure in the tobacco necrosis virus-D RNA genome is resistant to Xrn degradation. Nucleic Acids Research, 47(17), 9329-9342.
Gutierrez, R.A., Ewing, R.M., Cherry, J.M. & Green, P.J. (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes. Proceedings of the National Academy of Sciences of the United States of America, 99(17), 11513-11518.
Hogg, J.R. (2016) Viral evasion and manipulation of host RNA quality control pathways. Journal of Virology, 90(16), 7010-7018.
Jaag, H.M. & Nagy, P.D. (2009) Silencing of Nicotiana benthamiana Xrn4p exoribonuclease promotes tombusvirus RNA accumulation and recombination. Virology, 386(2), 344-352.
Jiang, S., Jiang, L., Yang, J., Peng, J., Lu, Y., Zheng, H. et al. (2018) Over-expression of Oryza sativa Xrn4 confers plant resistance to virus infection. Gene, 639, 44-51.
Kerényi, Z., Mérai, Z., Hiripi, L., Benkovics, A., Gyula, P., Lacomme, C. et al. (2008) Inter-kingdom conservation of mechanism of nonsense-mediated mRNA decay. The EMBO Journal, 27(11), 1585-1595.
Kertész, S., Kerényi, Z., Mérai, Z., Bartos, I., Pálfy, T., Barta, E. et al. (2006) Both introns and long 3'-UTRs operate as cis-acting elements to trigger nonsense-mediated decay in plants. Nucleic Acids Research, 34(21), 6147-6157.
Kishor, A., Fritz, S.E. & Hogg, J.R. (2019) Nonsense-mediated mRNA decay: the challenge of telling right from wrong in a complex transcriptome. Wiley Interdisciplinary Reviews. RNA, 10(6), e1548.
Kurosaki, T., Popp, M.W. & Maquat, L.E. (2019) Quality and quantity control of gene expression by nonsense-mediated mRNA decay. Nature Reviews. Molecular Cell Biology, 20(7), 406-420.
Li, F. & Wang, A. (2018) RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors. PLoS Pathogens, 14(8), e1007228.
Li, F. & Wang, A. (2019) RNA-targeted antiviral immunity: more than just RNA silencing. Trends in Microbiology, 27(9), 792-805.
Li, W.Z., Qu, F. & Morris, T.J. (1998) Cell-to-cell movement of turnip crinkle virus is controlled by two small open reading frames that function in trans. Virology, 244(2), 405-416.
Liu, L., Wang, H., Tang, W., Zhao, P., Ren, Y., Liu, Z. et al. (2023) Turnip crinkle virus-encoded suppressor of RNA silencing interacts with Arabidopsis SGS3 to enhance virus infection. Molecular Plant Pathology, 24(2), 154-166.
Lukhovitskaya, N. & Ryabova, L.A. (2019) Cauliflower mosaic virus transactivator protein (TAV) can suppress nonsense-mediated decay by targeting VARICOSE, a scaffold protein of the decapping complex. Scientific Reports, 9(1), 7042.
Mailliot, J., Vivoli-Vega, M. & Schaffitzel, C. (2022) No-nonsense: insights into the functional interplay of nonsense-mediated mRNA decay factors. The Biochemical Journal, 479(9), 973-993.
May, J.P., Johnson, P.Z., Ilyas, M., Gao, F. & Simon, A.E. (2020) The multifunctional long-distance movement protein of pea enation mosaic virus 2 protects viral and host transcripts from nonsense-mediated decay. MBio, 11(2), e00204-e00220.
May, J.P. & Simon, A.E. (2021) Targeting of viral RNAs by Upf1-mediated RNA decay pathways. Current Opinion in Virology, 47, 1-8.
May, J.P., Yuan, X., Sawicki, E. & Simon, A.E. (2018) RNA virus evasion of nonsense-mediated decay. PLoS Pathogens, 14(11), e1007459.
Molleston, J.M. & Cherry, S. (2017) Attacked from all sides: RNA decay in antiviral defense. Viruses, 9(1), 2.
Peng, J., Yang, J., Yan, F., Lu, Y., Jiang, S., Lin, L. et al. (2011) Silencing of NbXrn4 facilitates the systemic infection of Tobacco mosaic virus in Nicotiana benthamiana. Virus Research, 158(1-2), 268-270.
Qu, F., Ren, T. & Morris, T.J. (2003) The coat protein of turnip crinkle virus suppresses posttranscriptional gene silencing at an early initiation step. Journal of Virology, 77(1), 511-522.
Qu, F., Ye, X. & Morris, T.J. (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proceedings of the National Academy of Sciences of the United States of America, 105(38), 14732-14737.
Rayson, S., Arciga-Reyes, L., Wootton, L., De Torres Zabala, M., Truman, W., Graham, N. et al. (2012) A role for nonsense-mediated mRNA decay in plants: pathogen responses are induced in Arabidopsis thaliana NMD mutants. PLoS One, 7(2), e31917.
Ruan, M.B., Guo, X., Wang, B., Yang, Y.L., Li, W.Q., Yu, X.L. et al. (2017) Genome-wide characterization and expression analysis enables identification of abiotic stress-responsive MYB transcription factors in cassava (Manihot esculenta). Journal of Experimental Botany, 68(13), 3657-3672.
Shoemaker, C.J. & Green, R. (2012) Translation drives mRNA quality control. Nature Structural & Molecular Biology, 19(6), 594-601.
Souret, F.F., Kastenmayer, J.P. & Green, P.J. (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Molecular Cell, 15(2), 173-183.
van Hoof, A. & Green, P.J. (1996) Premature nonsense codons decrease the stability of phytohemagglutinin mRNA in a position-dependent manner. The Plant Journal: For Cell and Molecular Biology, 10(3), 415-424.
Voelker, T.A., Moreno, J. & Chrispeels, M.J. (1990) Expression analysis of a pseudogene in transgenic tobacco: a frameshift mutation prevents mRNA accumulation. The Plant Cell, 2(3), 255-261.
Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. The Plant Journal, 33(5), 949-956.
Wu, K., Wu, Y., Zhang, C., Fu, Y., Liu, Z. & Zhang, X. (2021) Simultaneous silencing of two different Arabidopsis genes with a novel virus-induced gene silencing vector. Plant Methods, 17(1), 6. Available from: 10.1186/s13007-020-00701-6
Xu, J. & Chua, N.H. (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. The Plant Cell, 21(10), 3270-3279.
Xu, J., Yang, J.Y., Niu, Q.W. & Chua, N.H. (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. The Plant Cell, 18(12), 3386-3398.
Zhang, X., Zhang, X., Singh, J., Li, D. & Qu, F. (2012) Temperature-dependent survival of Turnip crinkle virus-infected arabidopsis plants relies on an RNA silencing-based defense that requires dcl2, AGO2, and HEN1. Journal of Virology, 86, 6847-6854.
Zhang, X., Zhang, X., Wu, K., Liu, Z., Li, D. & Qu, F. (2016) Incomplete DRB4-dependence of the DCL4-mediated antiviral defense. Scientific Reports, 6, 39244.

Auteurs

Kunxin Wu (K)

National Key Laboratory for Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
Key Laboratory for Biology and Genetic Resources of Tropical Crops of Hainan Province, Hainan Institute for Tropical Agriculture Resources, Haikou, 571101, China.

Yan Fu (Y)

National Key Laboratory for Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
Key Laboratory for Biology and Genetic Resources of Tropical Crops of Hainan Province, Hainan Institute for Tropical Agriculture Resources, Haikou, 571101, China.

Yanli Ren (Y)

School of Biological and Geographical Sciences, Yili Normal University, Yili, 835000, China.

Linyu Liu (L)

National Key Laboratory for Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
Key Laboratory for Biology and Genetic Resources of Tropical Crops of Hainan Province, Hainan Institute for Tropical Agriculture Resources, Haikou, 571101, China.
School of Biological and Geographical Sciences, Yili Normal University, Yili, 835000, China.

Xiuchun Zhang (X)

National Key Laboratory for Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
Key Laboratory for Biology and Genetic Resources of Tropical Crops of Hainan Province, Hainan Institute for Tropical Agriculture Resources, Haikou, 571101, China.
Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya, 572025, China.

Mengbin Ruan (M)

National Key Laboratory for Tropical Crop Breeding, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.
Key Laboratory for Biology and Genetic Resources of Tropical Crops of Hainan Province, Hainan Institute for Tropical Agriculture Resources, Haikou, 571101, China.
Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Sanya, 572025, China.

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