Identification of Host Factors Interacting with a γ-Shaped RNA Element from a Plant Virus-Associated Satellite RNA

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2023 Oct 28

PMID 37896816

Authors

Mengjiao Li

Xiaobei Zhang

Kaiyun Huang

Zhiyou Du

Affiliations

Soon will be listed here.

Abstract

Previously, we identified a highly conserved, γ-shaped RNA element (γRE) from satellite RNAs of cucumber mosaic virus (CMV), and we determined γRE to be structurally required for satRNA survival and the inhibition of CMV replication. It remains unknown how γRE biologically functions. In this work, pull-down assays were used to screen candidates of host factors from plants using biotin-labeled γRE as bait. Nine host factors were found to interact specifically with γRE. Then, all of these host factors were down-regulated individually in plants via tobacco rattle virus-induced gene silencing and tested with infection by GFP-expressing CMV (CMV-gfp) and the isolate T1 of satRNA (sat-T1). Out of nine candidates, three host factors, namely histone H3, GTPase Ran3, and eukaryotic translation initiation factor 4A, were extremely important for infection by CMV-gfp and sat-T1. Moreover, we found that cytosolic glyceraldehyde-3-phosphate dehydrogenase 2 contributed to the replication of CMV and sat-T1, but also negatively regulated CMV 2b activity. Collectively, our work provides essential clues for uncovering the mechanism by which satRNAs inhibit CMV replication.

Citing Articles

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References

Piazzolla P, Tousignant M, Kaper J . Cucumber mosaic virus-associated RNA 5. IX. The overtaking of viral RNA synthesis by CARNA 5 and dsCARNA 5 in tobacco. Virology. 1982; 122(1):147-57. DOI: 10.1016/0042-6822(82)90384-1. View

Kaper J, Waterworth H . Cucumber mosaic virus associated RNA 5: causal agent for tomato necrosis. Science. 1977; 196(4288):429-31. DOI: 10.1126/science.196.4288.429. View

Hamera S, Song X, Su L, Chen X, Fang R . Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. Plant J. 2011; 69(1):104-15. DOI: 10.1111/j.1365-313X.2011.04774.x. View

Nakahara K, Masuta C, Yamada S, Shimura H, Kashihara Y, Wada T . Tobacco calmodulin-like protein provides secondary defense by binding to and directing degradation of virus RNA silencing suppressors. Proc Natl Acad Sci U S A. 2012; 109(25):10113-8. PMC: 3382489. DOI: 10.1073/pnas.1201628109. View

Gao Y, Yang J, Zhang X, Chen A, Gu Z, Du Z . The Weak Small RNA-Binding Activity of the 2b Proteins of Subgroup II Cucumber Mosaic Virus Strains Is Insufficient for RNA Silencing Suppression. Front Microbiol. 2021; 12:760937. PMC: 8569468. DOI: 10.3389/fmicb.2021.760937. View

Huang Y, Hou P, Chen I, Hsu Y, Tsai C, Cheng C . Dissecting the role of a plant-specific Rab5 small GTPase NbRabF1 in Bamboo mosaic virus infection. J Exp Bot. 2020; 71(22):6932-6944. DOI: 10.1093/jxb/eraa422. View

Zhang X, Yuan Y, Pei Y, Lin S, Tuschl T, Patel D . Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006; 20(23):3255-68. PMC: 1686603. DOI: 10.1101/gad.1495506. View

Han S, Wang Y, Zheng X, Jia Q, Zhao J, Bai F . Cytoplastic Glyceraldehyde-3-Phosphate Dehydrogenases Interact with ATG3 to Negatively Regulate Autophagy and Immunity in Nicotiana benthamiana. Plant Cell. 2015; 27(4):1316-31. PMC: 4558687. DOI: 10.1105/tpc.114.134692. View

Gonzalez I, Martinez L, Rakitina D, Lewsey M, Atencio F, Llave C . Cucumber mosaic virus 2b protein subcellular targets and interactions: their significance to RNA silencing suppressor activity. Mol Plant Microbe Interact. 2010; 23(3):294-303. DOI: 10.1094/MPMI-23-3-0294. View

10.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

11.

Hou W, Wang S, Wu H, Xue L, Wang B, Wang S . Small GTPase-A Key Role in Host Cell for Coronavirus Infection and a Potential Target for Coronavirus Vaccine Adjuvant Discovery. Viruses. 2022; 14(9). PMC: 9504349. DOI: 10.3390/v14092044. View

12.

Palukaitis P . Satellite RNAs and Satellite Viruses. Mol Plant Microbe Interact. 2015; 29(3):181-6. DOI: 10.1094/MPMI-10-15-0232-FI. View

13.

Gao S, Lu J, Cheng X, Gu Z, Liao Q, Du Z . Heterologous Replicase from Cucumoviruses can Replicate Viral RNAs, but is Defective in Transcribing Subgenomic RNA4A or Facilitating Viral Movement. Viruses. 2018; 10(11). PMC: 6265798. DOI: 10.3390/v10110590. View

14.

Diaz-Pendon J, Li F, Li W, Ding S . Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell. 2007; 19(6):2053-63. PMC: 1955711. DOI: 10.1105/tpc.106.047449. View

15.

Lewsey M, Robertson F, Canto T, Palukaitis P, Carr J . Selective targeting of miRNA-regulated plant development by a viral counter-silencing protein. Plant J. 2007; 50(2):240-52. DOI: 10.1111/j.1365-313X.2007.03042.x. View

16.

Yuan J, Wang D, Stewart Jr C . Statistical methods for efficiency adjusted real-time PCR quantification. Biotechnol J. 2007; 3(1):112-23. DOI: 10.1002/biot.200700169. View

17.

He L, Wang Q, Gu Z, Liao Q, Palukaitis P, Du Z . A conserved RNA structure is essential for a satellite RNA-mediated inhibition of helper virus accumulation. Nucleic Acids Res. 2019; 47(15):8255-8271. PMC: 6735963. DOI: 10.1093/nar/gkz564. View

18.

Xu K, Nagy P . Enrichment of Phosphatidylethanolamine in Viral Replication Compartments via Co-opting the Endosomal Rab5 Small GTPase by a Positive-Strand RNA Virus. PLoS Biol. 2016; 14(10):e2000128. PMC: 5070881. DOI: 10.1371/journal.pbio.2000128. View

19.

Ding S, Li W, Symons R . A novel naturally occurring hybrid gene encoded by a plant RNA virus facilitates long distance virus movement. EMBO J. 1995; 14(23):5762-72. PMC: 394695. DOI: 10.1002/j.1460-2075.1995.tb00265.x. View

20.

Taliansky M, Robinson D . Trans-acting untranslated elements of groundnut rosette virus satellite RNA are involved in symptom production. J Gen Virol. 1997; 78 ( Pt 6):1277-85. DOI: 10.1099/0022-1317-78-6-1277. View