Effect of temperature on the pathogenesis, accumulation of viral and satellite RNAs and on plant proteome in peanut stunt virus and satellite RNA-infected plants

Peanut stunt virus (PSV) is a widespread pathogen infecting legumes. The PSV strains are classified into four subgroups and some are defined by the association of satellite RNAs (satRNAs). In the case of PSV, the presence of satRNAs alters the symptoms of disease in infected plants. In this study, we elucidated the plant response to PSV-G strain, which occurs in natural conditions without satRNA. However, it was found that it might easily acquire satRNA, which exacerbated pathogenesis in Nicotiana benthamiana. To explain the mechanisms underlying PSV infection and symptoms exacerbation caused by satRNA, we carried out transcriptome profiling of N. benthamiana challenged by PSV-G and satRNA using species-specific microarrays. Co-infection of plants with PSV-G + satRNA increased the number of identified differentially expressed genes (DEGs) compared with the number identified in PSV-G-infected plants. In both treatments, the majority of up-regulated DEGs were engaged in translation, ribosome biogenesis, RNA metabolism, and response to stimuli, while the down-regulated DEGs were required for photosynthesis. The presence of satRNA in PSV-G-infected plants caused different trends in expression of DEGs associated with phosphorylation, ATP binding, and plasma membrane.

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How can plant virus satellite RNAs alter the effects of plant virus infection? A study of the changes in the Nicotiana benthamiana proteome after infection by Peanut stunt virus in the presence or absence of its satellite RNA

PROTEOMICS ◽

10.1002/pmic.201200056 ◽

2013 ◽

Vol 13 (14) ◽

pp. 2162-2175 ◽

Cited By ~ 13

Author(s):

Aleksandra Obrępalska-Stęplowska ◽

Przemysław Wieczorek ◽

Marta Budziszewska ◽

Arnika Jeszke ◽

Jenny Renaut

Keyword(s):

Virus Infection ◽

Nicotiana Benthamiana ◽

Plant Virus ◽

Satellite Rna ◽

Satellite Rnas ◽

Peanut Stunt Virus

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Multiple cellular compartments engagement in Nicotiana benthamiana-peanut stunt virus-satRNA interactions revealed by systems biology approach

Plant Cell Reports ◽

10.1007/s00299-021-02706-4 ◽

2021 ◽

Author(s):

Barbara Wrzesińska ◽

Agnieszka Zmienko ◽

Lam Dai Vu ◽

Ive De Smet ◽

Aleksandra Obrępalska-Stęplowska

Keyword(s):

Virus Infection ◽

Nicotiana Benthamiana ◽

Cellular Localization ◽

Plant Interactions ◽

Satellite Rna ◽

Functional Connections ◽

Cell Compartments ◽

Wide Range ◽

Peanut Stunt Virus ◽

Cellular Compartments

Abstract Key message PSV infection changed the abundance of host plant’s transcripts and proteins associated with various cellular compartments, including ribosomes, chloroplasts, mitochondria, the nucleus and cytosol, affecting photosynthesis, translation, transcription, and splicing. Abstract Virus infection is a process resulting in numerous molecular, cellular, and physiological changes, a wide range of which can be analyzed due to development of many high-throughput techniques. Plant RNA viruses are known to replicate in the cytoplasm; however, the roles of chloroplasts and other cellular structures in the viral replication cycle and in plant antiviral defense have been recently emphasized. Therefore, the aim of this study was to analyze the small RNAs, transcripts, proteins, and phosphoproteins affected during peanut stunt virus strain P (PSV-P)–Nicotiana benthamiana interactions with or without satellite RNA (satRNA) in the context of their cellular localization or functional connections with particular cellular compartments to elucidate the compartments most affected during pathogenesis at the early stages of infection. Moreover, the processes associated with particular cell compartments were determined. The ‘omic’ results were subjected to comparative data analyses. Transcriptomic and small RNA (sRNA)–seq data were obtained to provide new insights into PSV-P–satRNA–plant interactions, whereas previously obtained proteomic and phosphoproteomic data were used to broaden the analysis to terms associated with cellular compartments affected by virus infection. Based on the collected results, infection with PSV-P contributed to changes in the abundance of transcripts and proteins associated with various cellular compartments, including ribosomes, chloroplasts, mitochondria, the nucleus and the cytosol, and the most affected processes were photosynthesis, translation, transcription, and mRNA splicing. Furthermore, sRNA-seq and phosphoproteomic analyses indicated that kinase regulation resulted in decreases in phosphorylation levels. The kinases were associated with the membrane, cytoplasm, and nucleus components.

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Complete nucleotide sequence of a Polish strain of Peanut stunt virus (PSV-P) that is related to but not a typical member of subgroup I.

Acta Biochimica Polonica ◽

10.18388/abp.2008_3034 ◽

2008 ◽

Vol 55 (4) ◽

pp. 731-739 ◽

Cited By ~ 8

Author(s):

Aleksandra Obrepalska-Steplowska ◽

Marta Budziszewska ◽

Henryk Pospieszny

Keyword(s):

Phylogenetic Analyses ◽

The Other ◽

Full Genome Sequence ◽

Full Genome ◽

Satellite Rna ◽

Protein Coding ◽

Typical Member ◽

Rna Analysis ◽

Nucleotide Homology ◽

Peanut Stunt Virus

Peanut stunt virus (PSV) is a common legume pathogen present worldwide. It is also infectious for many other plants including peanut and some vegetables. Viruses of this species are classified at present into three subgroups based on their serology and nucleotide homology. Some of them may also carry an additional subviral element - satellite RNA. Analysis of the full genome sequence of a Polish strain - PSV-P - associated with satRNA was performed and showed that it may be classified as a derivative of the subgroup I sharing 83.9-87.9% nucleotide homology with other members of this subgroup. A comparative study of sequenced PSV strains indicates that PSV-P shows the highest identity level with PSV-ER or PSV-J depending on the region used for analysis. Phylogenetic analyses, on the other hand, have revealed that PSV-P is related to representatives of the subgroup I to the same degree, with the exception of the coat protein coding sequence where PSV-P is clustered together with PSV-ER.

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Viral Satellite RNAs for the Prevention of Cucumber Mosaic Virus (CMV) Disease in Field-Grown Pepper and Melon Plants

Plant Disease ◽

10.1094/pdis.1998.82.12.1298 ◽

1998 ◽

Vol 82 (12) ◽

pp. 1298-1303 ◽

Cited By ~ 20

Author(s):

M. S. Montasser ◽

M. E. Tousignant ◽

J. M. Kaper

Keyword(s):

Cucumber Mosaic Virus ◽

Mosaic Virus ◽

Plant Viruses ◽

Yield Reduction ◽

Satellite Rna ◽

Time Intervals ◽

Mild Strain ◽

Challenge Inoculation ◽

Satellite Rnas ◽

Cmv Disease

A benign viral satellite RNA, in combination with a mild strain of cucumber mosaic virus (CMV-S), was used as a “vaccine” or “preinoculum” to demonstrate the feasibility of protecting pepper (Capsicum annuum cv. California Wonder) and melon (Cucurbita melo cv. Janus des Canaries) against two severe CMV strains, CMV-D and CMV-16, in the final 2 years of a 4-year pilot field and greenhouse experiment. In the field, healthy pepper and melon seedlings challenged with CMV-D and CMV-16 reduced yields by 33 to 60%; CMV-S caused only limited yield reduction in pepper and had no effect on the yield of melon. Different time intervals between preinoculation of pepper and melon seedlings with CMV-S and challenge inoculation with the severe CMV strains were tested. All plants challenged 3 weeks after vaccination showed nearly complete protection from subsequent infection by severe strains. The yield from preinoculated and challenged pepper plants was 80% that of untreated plants, while the yield from preinoculated and challenged melon plants was increased slightly over the untreated control plants. The use of this technology for biological control of plant viruses is discussed.

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Peanut stunt virus satellite RNA: Analysis of sequences that affect symptom attenuation in tobacco

Virology ◽

10.1016/0042-6822(92)90590-l ◽

1992 ◽

Vol 189 (2) ◽

pp. 668-677 ◽

Cited By ~ 15

Author(s):

R.A. Naidu ◽

G.B. Collins ◽

S.A. Ghabrial

Keyword(s):

Satellite Rna ◽

Rna Analysis ◽

Peanut Stunt Virus

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Satellite RNAs and Satellite Viruses

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-10-15-0232-fi ◽

2016 ◽

Vol 29 (3) ◽

pp. 181-186 ◽

Cited By ~ 27

Author(s):

Peter Palukaitis

Keyword(s):

Cucumber Mosaic Virus ◽

Mosaic Virus ◽

Rna Silencing ◽

Noncoding Rnas ◽

Turnip Crinkle Virus ◽

Satellite Rna ◽

Satellite Rnas ◽

Satellite Viruses

Satellite RNAs and satellite viruses are extraviral components that can affect either the pathogenicity, the accumulation, or both of their associated viruses while themselves being dependent on the associated viruses as helper viruses for their infection. Most of these satellite RNAs are noncoding RNAs, and in many cases, have been shown to alter the interaction of their helper viruses with their hosts. In only a few cases have the functions of these satellite RNAs in such interactions been studied in detail. In particular, work on the satellite RNAs of Cucumber mosaic virus and Turnip crinkle virus have provided novel insights into RNAs functioning as noncoding RNAs. These effects are described and potential roles for satellite RNAs in the processes involved in symptom intensification or attenuation are discussed. In most cases, models describing these roles involve some aspect of RNA silencing or its suppression, either directly or indirectly involving the particular satellite RNA.

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Tomato Cell Death Mediated By Complementary Plant Viral Satellite RNA Sequences

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.1998.11.12.1214 ◽

1998 ◽

Vol 11 (12) ◽

pp. 1214-1222 ◽

Cited By ~ 17

Author(s):

Michael E. Taliansky ◽

Eugene V. Ryabov ◽

David J. Robinson ◽

Peter Palukaitis

Keyword(s):

Cell Death ◽

Secondary Structure ◽

Potato Virus X ◽

Computer Assisted ◽

Satellite Rna ◽

Rna Sequences ◽

Virus Particles ◽

Tomato Seedlings ◽

Secondary Structure Analysis ◽

Satellite Rnas

Cell death (necrosis) and severe yellowing (chlorosis) in tomato are induced by cucumber mosaic virus (CMV) supporting particular satellite RNAs. To determine whether CMV RNA sequences also are needed to induce necrosis or chlorosis, tomato seedlings were infected with the potato virus X vector expressing either a necrogenic or chlorosis-inducing satellite RNA of CMV. The infected plants did not develop chlorosis, although they did develop necrosis, but only when all or part of a 335-nucleotide necrogenic satellite RNA was expressed in the (-) polarity; i.e., the strand not packaged in virus particles. Computer-assisted secondary structure analysis suggests that the necrogenicity domain is an octanucleotide loop and adjacent base-paired stem of a thermodynamically stable hairpin structure.

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Peanut Stunt Virus and Its Satellite RNA Trigger Changes in Phosphorylation in N. benthamiana Infected Plants at the Early Stage of the Infection

International Journal of Molecular Sciences ◽

10.3390/ijms19103223 ◽

2018 ◽

Vol 19 (10) ◽

pp. 3223 ◽

Cited By ~ 4

Author(s):

Barbara Wrzesińska ◽

Lam Dai Vu ◽

Kris Gevaert ◽

Ive De Smet ◽

Aleksandra Obrępalska-Stęplowska

Keyword(s):

Host Plants ◽

Early Stage ◽

Disease Process ◽

Proteome Analysis ◽

Infection Process ◽

Satellite Rna ◽

Data Set ◽

Phosphorylated Proteins ◽

Successful Infection ◽

Peanut Stunt Virus

Signaling in host plants is an integral part of a successful infection by pathogenic RNA viruses. Therefore, identifying early signaling events in host plants that play an important role in establishing the infection process will help our understanding of the disease process. In this context, phosphorylation constitutes one of the most important post-translational protein modifications, regulating many cellular signaling processes. In this study, we aimed to identify the processes affected by infection with Peanut stunt virus (PSV) and its satellite RNA (satRNA) in Nicotiana benthamiana at the early stage of pathogenesis. To achieve this, we performed proteome and phosphoproteome analyses on plants treated with PSV and its satRNA. The analysis of the number of differentially phosphorylated proteins showed strong down-regulation in phosphorylation in virus-treated plants (without satRNA). Moreover, proteome analysis revealed more down-regulated proteins in PSV and satRNA-treated plants, which indicated a complex dependence between proteins and their modifications. Apart from changes in photosynthesis and carbon metabolism, which are usually observed in virus-infected plants, alterations in proteins involved in RNA synthesis, transport, and turnover were observed. As a whole, this is the first community (phospho)proteome resource upon infection of N. benthamiana with a cucumovirus and its satRNA and this resource constitutes a valuable data set for future studies.

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