Cucumber Mosaic Virus Infection in : A Conditional Mutualistic Symbiont?

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2022 Jan 24

PMID 35069476

Authors

Hideki Takahashi

Midori Tabara

Shuhei Miyashita

Sugihiro Ando

Shuichi Kawano

Yoshinori Kanayama

Toshiyuki Fukuhara

Richard Kormelink

Affiliations

Soon will be listed here.

Abstract

A cucumber mosaic virus isolate, named Ho [CMV(Ho)], was isolated from a symptomless field sample containing low virus titers. An analysis of CMV(Ho) RNA molecules indicated that the virus isolate, besides the usual cucumovirus tripartite RNA genome, additionally contained defective RNA3 molecules and a satellite RNA. To study the underlying mechanism of the persistent CMV(Ho) infection in perennial , infectious cDNA clones were generated for all its genetic elements. CMV, which consists of synthetic transcripts from the infectious tripartite RNA genomes, and designated CMV(Ho)tr, multiplied in and annual Col-0 to a similar level as the virulent strain CMV(Y), but did not induce any symptoms in them. The response of Col-0 to a series of reassortant CMVs between CMV(Ho)tr and CMV(Y) suggested that the establishment of an asymptomatic phenotype of CMV(Ho) infection was due to the gene of CMV RNA2, but not due to the presence of the defective RNA3 and satellite RNA. The accumulation of CMV(Ho) 2b protein tagged with the FLAG epitope (2b.Ho-FLAG) in -transformed Col-0 did not induce any symptoms, suggesting a 2b-dependent persistency of CMV(Ho)tr infection in . The 2b protein interacted with Argonaute 4, which is known to regulate the cytosine methylation levels of host genomic DNA. Whole genomic bisulfite sequencing analysis of CMV(Ho)tr- and mock-inoculated Col-0 revealed that cytosine hypomethylation in the promoter regions of 82 genes, including two genes encoding transcriptional regulators ( and ), was induced in response to CMV(Ho)tr infection. Moreover, the increased levels of hypomethylation in the promoter region of both genes, during CMV(Ho)tr infection, were correlated with the up- or down-regulation of their expression. Taken altogether, the results indicate that during persistent CMV(Ho) infection in , host gene expression may be epigenetically modulated resulting from a 2b-mediated cytosine hypomethylation of host genomic DNA.

Citing Articles

A resilient mutualistic interaction between cucumber mosaic virus and its natural host to adapt to an excess zinc environment and drought stress.

Tabara M, Uraguchi S, Kiyono M, Watanabe I, Takeda A, Takahashi H J Plant Res. 2024; 137(6):1151-1164.

PMID: 39190237 DOI: 10.1007/s10265-024-01573-w.

Strain-specific differences in the interactions of the cucumber mosaic virus 2b protein with the viral 1a and host Argonaute 1 proteins.

Crawshaw S, Watt L, Murphy A, Carr J J Virol. 2024; 98(9):e0099324.

PMID: 39162432 PMC: 11406993. DOI: 10.1128/jvi.00993-24.

A single amino acid at position 31 in the N-terminus of the coat protein of cucumber mosaic virus determines its avirulence function for RCY1-conferred virus resistance.

Takahashi H, Ando Y, Kanayama Y, Miyashita S Arch Virol. 2024; 169(3):61.

PMID: 38441697 DOI: 10.1007/s00705-024-05961-4.

References

Xu P, Chen F, Mannas J, Feldman T, Sumner L, Roossinck M . Virus infection improves drought tolerance. New Phytol. 2008; 180(4):911-21. DOI: 10.1111/j.1469-8137.2008.02627.x. View

Pagan I, Alonso-Blanco C, Garcia-Arenal F . The relationship of within-host multiplication and virulence in a plant-virus system. PLoS One. 2007; 2(8):e786. PMC: 1950075. DOI: 10.1371/journal.pone.0000786. View

Le Hir R, Bellini C . The plant-specific dof transcription factors family: new players involved in vascular system development and functioning in Arabidopsis. Front Plant Sci. 2013; 4:164. PMC: 3665933. DOI: 10.3389/fpls.2013.00164. View

Ji L, Ding S . The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact. 2001; 14(6):715-24. DOI: 10.1094/MPMI.2001.14.6.715. View

Khankhum S, Valverde R . Physiological traits of endornavirus-infected and endornavirus-free common bean (Phaseolus vulgaris) cv Black Turtle Soup. Arch Virol. 2018; 163(4):1051-1056. DOI: 10.1007/s00705-018-3702-4. View

Ruiz , Voinnet , Baulcombe . Initiation and maintenance of virus-induced gene silencing . Plant Cell. 1998; 10(6):937-46. PMC: 144041. DOI: 10.1105/tpc.10.6.937. View

Ye R, Chen Z, Lian B, Rowley M, Xia N, Chai J . A Dicer-Independent Route for Biogenesis of siRNAs that Direct DNA Methylation in Arabidopsis. Mol Cell. 2015; 61(2):222-35. PMC: 5110219. DOI: 10.1016/j.molcel.2015.11.015. View

Hu C, Hsu Y, Lin N . Satellite RNAs and Satellite Viruses of Plants. Viruses. 2011; 1(3):1325-50. PMC: 3185516. DOI: 10.3390/v1031325. View

Honjo M, Kudoh H . : a perennial model system for studying population differentiation and local adaptation. AoB Plants. 2019; 11(6):plz076. PMC: 6899346. DOI: 10.1093/aobpla/plz076. View

10.

Pagan I, Alonso-Blanco C, Garcia-Arenal F . Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathog. 2008; 4(8):e1000124. PMC: 2494869. DOI: 10.1371/journal.ppat.1000124. View

11.

Kreuze J, Perez A, Untiveros M, Quispe D, Fuentes S, Barker I . Complete viral genome sequence and discovery of novel viruses by deep sequencing of small RNAs: a generic method for diagnosis, discovery and sequencing of viruses. Virology. 2009; 388(1):1-7. DOI: 10.1016/j.virol.2009.03.024. View

12.

Westwood J, McCann L, Naish M, Dixon H, Murphy A, Stancombe M . A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana. Mol Plant Pathol. 2012; 14(2):158-70. PMC: 6638696. DOI: 10.1111/j.1364-3703.2012.00840.x. View

13.

Xi Y, Li W . BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics. 2009; 10:232. PMC: 2724425. DOI: 10.1186/1471-2105-10-232. View

14.

Wang C, Wang C, Xu W, Zou J, Qiu Y, Kong J . Epigenetic Changes in the Regulation of Response to Infection and Symptom Recovery through Single-Base Resolution Methylomes. Viruses. 2018; 10(8). PMC: 6115852. DOI: 10.3390/v10080402. View

15.

Bies-Etheve N, Pontier D, Lahmy S, Picart C, Vega D, Cooke R . RNA-directed DNA methylation requires an AGO4-interacting member of the SPT5 elongation factor family. EMBO Rep. 2009; 10(6):649-54. PMC: 2711833. DOI: 10.1038/embor.2009.31. View

16.

Alexander H . Disease in Natural Plant Populations, Communities, and Ecosystems: Insights into Ecological and Evolutionary Processes. Plant Dis. 2019; 94(5):492-503. DOI: 10.1094/PDIS-94-5-0492. View

17.

Lewsey M, Murphy A, MacLean D, Dalchau N, Westwood J, Macaulay K . Disruption of two defensive signaling pathways by a viral RNA silencing suppressor. Mol Plant Microbe Interact. 2010; 23(7):835-45. DOI: 10.1094/MPMI-23-7-0835. View

18.

Lewsey M, Surette M, Robertson F, Ziebell H, Choi S, Ryu K . The role of the Cucumber mosaic virus 2b protein in viral movement and symptom induction. Mol Plant Microbe Interact. 2009; 22(6):642-54. DOI: 10.1094/MPMI-22-6-0642. View

19.

Takahashi H, Nakaho K, Ishihara T, Ando S, Wada T, Kanayama Y . Transcriptional profile of tomato roots exhibiting Bacillus thuringiensis-induced resistance to Ralstonia solanacearum. Plant Cell Rep. 2013; 33(1):99-110. DOI: 10.1007/s00299-013-1515-1. View

20.

Tabara M, Nagashima Y, He K, Qian X, Crosby K, Jifon J . Frequent asymptomatic infection with tobacco ringspot virus on melon fruit. Virus Res. 2020; 293:198266. DOI: 10.1016/j.virusres.2020.198266. View