Abstract

Key messagePSV 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.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.

Highlights

  • The presence of a virus in a host cell interferes with host cell metabolism and utilizes cell structural elements, including membranous ones, for its multiplication and cell-to-cell movement

  • Results small RNA (sRNA) profiling of N. benthamiana infected with peanut stunt virus (PSV)‐P indicate changes in miRNAs and ta‐short interfering RNAs (siRNAs) associated mainly with the nucleus and cytoskeleton sRNA sequencing of N. benthamiana infected with peanut stunt virus strain P (PSV-P) and PSV-P + satellite RNA (satRNA) revealed that the majority of sRNAs belonged to the 24 nt size class followed by the 20 nt size class (Fig. S1)

  • A comparison of these miRNAs to known miRNAs allowing for up to 5 mismatches and no gaps resulted in 41 records, suggesting that a large fraction of the discovered miRNAs were novel; their identification might have been correct but was unexpected

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Summary

Introduction

The presence of a virus in a host cell interferes with host cell metabolism and utilizes cell structural elements, including membranous ones, for its multiplication and cell-to-cell movement. For their replication, viruses can use host proteins, membranes, lipids and metabolites to assemble viral replication complexes (VRCs), called viral factories, on subcellular membrane surfaces. Host plants dealing with cellular infection enter a new state as a result of the triggering of response reactions One such defense reaction is posttranscriptional gene silencing (PTGS), which is a crucial factor in the regulation of gene expression during development and genome stability maintenance. Plants utilize PTGS to efficiently and recognize and eliminate invading viruses (Baulcombe 2004; Wieczorek and Obrępalska-Stęplowska 2015)

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