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Plant-Virus Interactions

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Viruses of Plants, Fungi and Protozoa".

Deadline for manuscript submissions: closed (31 July 2018) | Viewed by 68005

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Dr. Jeanmarie Verchot

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Plant Virology, Texas A&M AgriLife Research, Dallas, TX, USA
Interests: potexvirus; potyvirus; protein–membrane interactions; ER stress regulation; cellular interactions
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

I am very grateful for this opportunity to host a Special Issue on “Plant–Virus Interactions”. Through my career, I have focused on virus cell-to-cell movement, and how viral proteins interact with the membrane compartment. In recent years, plant cell biologists have begun to shine a light on the extensive cross talk that occurs between organelles, the nucleus, and plasmodesmata. These advances in cell biology help to make sense of how and why plant viruses interact with organelles and how plant viruses can divert cellular communication. My goal in hosting this Special Issue is to invite primary research articles, reviews or opinion articles that highlight recent advances in how viruses depend on cell intercellular or intracellular communication strategies. Our goal is to explore the most advanced topics in virus cell biology. I want to invite my colleagues in the plant virology community to present their most recent and favorite discoveries.

Dr. Jeanmarie Verchot
Guest Editor

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Keywords

Virus-induced gene silencing
intracellular communication
chloroplast
nuclear signalling
endoplasmic reticulum
plasmodesmata
signal transduction
plant virus

Published Papers (13 papers)

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Research

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15 pages, 2824 KiB

Open AccessArticle

Molecular Co-Chaperone SGT1 Is Critical for Cell-to-Cell Movement and Systemic Infection of Tomato Spotted Wilt Virus in Nicotiana benthamiana

by Xin Qian, Qing Xiang, Tongqing Yang, Hongyu Ma, Xin Shun Ding and Xiaorong Tao

Viruses 2018, 10(11), 647; https://doi.org/10.3390/v10110647 - 17 Nov 2018

Cited by 10 | Viewed by 4161

Abstract

Tospovirus is a tripartite negative stranded RNA virus and is considered as one of the most devastating plant viruses. Successful virus infection in plant requires many host factors. To date, very few host factors have been identified as important in Tospovirus infection in plants. We reported earlier that NSm protein encoded by Tomato spotted wilt virus (TSWV), a type species of the genus Orthotospovirus, plays critical roles in viral cell-to-cell and long-distance movement. In this study, we determined that molecular co-chaperone NbSGT1 interacted with TSWV NSm in Nicotiana benthamiana. TSWV infection significantly upregulated the expression of NbSGT1 gene and transient overexpression of NbSGT1 in N. benthamiana leaves accelerated TSWV infection. In contrast, silencing the NbSGT1 gene expression using a virus-induced gene silencing (VIGS) approach strongly inhibited TSWV NSm cell-to-cell movement, as well as TSWV local and systemic infection in N. benthamiana plants. Furthermore, NbSGT1 was found to regulate the infection of both American and Euro/Asia type tospoviruses in N. benthamiana plant. Collectively, our findings presented in this paper and the results published previously indicated that molecular co-chaperone NbSGT1 plays important roles in modulating both positive stranded and tripartite negative stranded RNA virus infection in plants. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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15 pages, 4478 KiB

Open AccessArticle

CMV2b-Dependent Regulation of Host Defense Pathways in the Context of Viral Infection

by Jian-Hua Zhao, Xiao-Lan Liu, Yuan-Yuan Fang, Rong-Xiang Fang and Hui-Shan Guo

Viruses 2018, 10(11), 618; https://doi.org/10.3390/v10110618 - 09 Nov 2018

Cited by 13 | Viewed by 3785

Abstract

RNA silencing (or RNA interference, RNAi) plays direct roles in plant host defenses against viruses. Viruses encode suppressors of RNAi (VSRs) to counteract host antiviral defenses. The generation of transgenic plants expressing VSRs facilitates the understanding of the mechanisms of VSR-mediated interference with the endogenous silencing pathway. However, studying VSRs independent of other viral components simplifies the complex roles of VSRs during natural viral infection. While suppression of transgene silencing by the VSR 2b protein encoded by cucumber mosaic virus (CMV) requires 2b-small RNA (sRNA) binding activity, suppression of host antiviral defenses requires the binding activity of both sRNAs and AGOs proteins. This study, aimed to understand the functions of 2b in the context of CMV infection; thus, we performed genome-wide analyses of differential DNA methylation regions among wild-type CMV-infected, CMVΔ2b-infected, and 2b-transgenic Arabidopsis plants. These analyses, together with transcriptome sequencing and RT-qPCR analyses, show that while the majority of induced genes in 2b-transgenic plants were involved in extensive metabolic pathways, CMV-infection 2b-dependent induced genes were enriched in plant immunity pathways, including salicylic acid (SA) signaling. Together with infection with CMV mutants that expressed the 2b functional domains of sRNA or AGO binding, our data demonstrate that CMV-accelerated SA signaling depends on 2b-sRNA binding activity which is also responsible for virulence. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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12 pages, 1838 KiB

Open AccessArticle

Impact of Two Reoviruses and Their Coinfection on the Rice RNAi System and vsiRNA Production

by Zhanbiao Li, Tong Zhang, Xiuqin Huang and Guohui Zhou

Viruses 2018, 10(11), 594; https://doi.org/10.3390/v10110594 - 30 Oct 2018

Cited by 11 | Viewed by 3513

Abstract

Both Southern rice black-streaked dwarf virus (SRBSDV) and Rice ragged stunt virus (RRSV) belong to the family Reoviridae, and synergistic infection of these two viruses commonly occurs in the field. This study revealed that both SRBSDV and RRSV affect the RNA interference (RNAi) pathway and form different virus-derived interfering RNA (vsiRNA) profiles in rice. Co-infection of rice by SRBSDV and RRSV up-regulated the expression of rice DICER-like (DCL) proteins but down-regulated the expression of rice RNA-dependent RNA polymerases (RDRs), and the accumulation of vsiRNAs of either RBSDV or RRSV was decreased compared with that in singly infected plants. The majority of SRBSDV vsiRNAs were 21 nt or 22 nt in length, whether plants were singly infected with SRBSDV or co-infected with RRSV. On the other hand, the majority of RRSV vsiRNAs were 20 nt, 21 nt, or 22 nt in length, among which those 20 nt in length accounted for the largest proportion; co-infection with SRBSDV further increased the proportion of 20 nt vsiRNAs and decreased the proportion of 21 nt vsiRNAs. Co-infection had no effects on the strand favoritism and hot spots of the vsiRNAs, but changed the bias of the 5′ terminal nucleotide significantly. This study provides a reference for further study on the pathogenesis and synergistic mechanism of SRBSDV and RRSV. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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26 pages, 10775 KiB

Open AccessArticle

The Interaction Dynamics of Two Potato Leafroll Virus Movement Proteins Affects Their Localization to the Outer Membranes of Mitochondria and Plastids

by Stacy L. DeBlasio, Yi Xu, Richard S. Johnson, Ana Rita Rebelo, Michael J. MacCoss, Stewart M. Gray and Michelle Heck

Viruses 2018, 10(11), 585; https://doi.org/10.3390/v10110585 - 26 Oct 2018

Cited by 18 | Viewed by 6181

Abstract

The Luteoviridae is an agriculturally important family of viruses whose replication and transport are restricted to plant phloem. Their genomes encode for four proteins that regulate viral movement. These include two structural proteins that make up the capsid and two non-structural proteins known as P3a and P17. Little is known about how these proteins interact with each other and the host to coordinate virus movement within and between cells. We used quantitative, affinity purification-mass spectrometry to show that the P3a protein of Potato leafroll virus complexes with virus and that this interaction is partially dependent on P17. Bimolecular complementation assays (BiFC) were used to validate that P3a and P17 self-interact as well as directly interact with each other. Co-localization with fluorescent-based organelle markers demonstrates that P3a directs P17 to the mitochondrial outer membrane while P17 regulates the localization of the P3a-P17 heterodimer to plastids. Residues in the C-terminus of P3a were shown to regulate P3a association with host mitochondria by using mutational analysis and also varying BiFC tag orientation. Collectively, our work reveals that the PLRV movement proteins play a game of intracellular hopscotch along host organelles to transport the virus to the cell periphery. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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16 pages, 8322 KiB

Open AccessArticle

Elements Involved in the Rsv3-Mediated Extreme Resistance against an Avirulent Strain of Soybean Mosaic Virus

by Mazen Alazem, Kuan-Chieh Tseng, Wen-Chi Chang, Jang-Kyun Seo and Kook-Hyung Kim

Viruses 2018, 10(11), 581; https://doi.org/10.3390/v10110581 - 24 Oct 2018

Cited by 23 | Viewed by 5059

Abstract

Extreme resistance (ER) is a type of R-gene-mediated resistance that rapidly induces a symptomless resistance phenotype, which is different from the phenotypical R-resistance manifested by the programmed cell death, accumulation of reactive oxygen species, and hypersensitive response. The Rsv3 gene in soybean cultivar L29 is responsible for ER against the avirulent strain G5H of soybean mosaic virus (SMV), but is ineffective against the virulent strain G7H. Rsv3-mediated ER is achieved through the rapid accumulation of callose, which arrests SMV-G5H at the point of infection. Callose accumulation, however, may not be the lone mechanism of this ER. Analyses of RNA-seq data obtained from infected soybean plants revealed a rapid induction of the abscisic acid pathway at 8 h post infection (hpi) in response to G5H but not to G7H, which resulted in the down-regulation of transcripts encoding β-1,3 glucanases that degrade callose in G5H-infected but not G7H-infected plants. In addition, parts of the autophagy and the small interfering (si) RNA pathways were temporally up-regulated at 24 hpi in response to G5H but not in response to G7H. The jasmonic acid (JA) pathway and many WRKY factors were clearly up-regulated only in G7H-infected plants. These results suggest that ER against SMV-G5H is achieved through the quick and temporary induction of ABA, autophagy, and the siRNA pathways, which rapidly eliminate G5H. The results also suggest that suppression of the JA pathway in the case of G5H is important for the Rsv3-mediated ER. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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15 pages, 3748 KiB

Open AccessArticle

Functional Scanning of Apple Geminivirus Proteins as Symptom Determinants and Suppressors of Posttranscriptional Gene Silencing

by Binhui Zhan, Wenyang Zhao, Shifang Li, Xiuling Yang and Xueping Zhou

Viruses 2018, 10(9), 488; https://doi.org/10.3390/v10090488 - 11 Sep 2018

Cited by 23 | Viewed by 4192

Abstract

Apple geminivirus (AGV) is a recently identified geminivirus which is isolated from the apple tree in China. We carried out functional scanning of apple geminivirus proteins as symptom determinants and suppressors of posttranscriptional gene silencing (PTGS). Our results indicated that AGV V2 is an important virulence factor localized to the nucleus and cytoplasm that suppresses PTGS and induces severe symptoms of crinkling and necrosis. AGV C1 is also a virulence determinant which elicits systemic necrosis when expressed from a PVX-based vector. The AGV C4 is targeted to cytoplasm, plasma membrane, nucleus, and chloroplasts. The inoculation of PVX-C4 on N. benthamiana induced severe upward leaf curling, which implied that AGV C4 also functions as a symptom determinant, and mutation analyses suggested that the acylated residues on Gly2 and Cys8 play important roles in its subcellular localization and symptom development. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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16 pages, 4716 KiB

Open AccessArticle

Identification of the Potential Virulence Factors and RNA Silencing Suppressors of Mulberry Mosaic Dwarf-Associated Geminivirus

by Xiuling Yang, Yanxiang Ren, Shaoshuang Sun, Dongxue Wang, Fanfan Zhang, Dawei Li, Shifang Li and Xueping Zhou

Viruses 2018, 10(9), 472; https://doi.org/10.3390/v10090472 - 03 Sep 2018

Cited by 25 | Viewed by 5269

Abstract

Plant viruses encode virulence factors or RNA silencing suppressors to reprogram plant cellular processes or to fine-tune host RNA silencing-mediated defense responses. In a previous study, Mulberry mosaic dwarf-associated virus (MMDaV), a novel, highly divergent geminivirus, has been identified from a Chinese mulberry tree showing mosaic and dwarfing symptoms, but the functions of its encoded proteins are unknown. In this study, all seven proteins encoded by MMDaV were screened for potential virulence and RNA silencing suppressor activities. We found that V2, RepA, and Rep affect the pathogenicity of a heterologous potato virus X. We showed that V2 could inhibit local RNA silencing and long-distance movement of the RNA silencing signal, but not short-range spread of the green fluorescent protein (GFP) silencing signal in Nicotiana benthamiana 16c plants. In addition, V2 localized to both subnuclear foci and the cytoplasm. Deletion mutagenesis of V2 showed that the basic motif from amino acids 61 to 76 was crucial for V2 to form subnuclear foci and for suppression of RNA silencing. Although the V2 protein encoded by begomoviruses or a curtovirus has been shown to have silencing suppressor activity, this is the first identification of an RNA silencing suppressor from a woody plant-infecting geminivirus. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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16 pages, 16755 KiB

Open AccessArticle

Two Crinivirus-Conserved Small Proteins, P5 and P9, Are Indispensable for Efficient Lettuce infectious yellows virus Infectivity in Plants

by Wenjie Qiao, Erin L. Helpio and Bryce W. Falk

Viruses 2018, 10(9), 459; https://doi.org/10.3390/v10090459 - 28 Aug 2018

Cited by 7 | Viewed by 3915

Abstract

Genomic analysis of Lettuce infectious yellows virus (LIYV) has revealed two short open reading frames (ORFs) on LIYV RNA2, that are predicted to encode a 5-kDa (P5) and a 9-kDa (P9) protein. The P5 ORF is part of the conserved quintuple gene block in the family Closteroviridae, while P9 orthologs are found in all Criniviruses. In this study, the expression of LIYV P5 and P9 proteins was confirmed; P5 is further characterized as an endoplasmic reticulum (ER)-localized integral transmembrane protein and P9 is a soluble protein. The knockout LIYV mutants presented reduced symptom severity and virus accumulation in Nicotiana benthamiana or lettuce plants, indicating their importance in efficient virus infection. The P5 mutant was successfully complemented by a dislocated P5 in the LIYV genome. The structural regions of P5 were tested and all were found to be required for the appropriate functions of P5. In addition, P5, as well as its ortholog P6, encoded by Citrus tristeza virus (CTV) and another ER-localized protein encoded by LIYV RNA1, were found to cause cell death when expressed in N. benthamiana plants from a TMV vector, and induce ER stress and the unfolded protein response (UPR). Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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23 pages, 7911 KiB

Open AccessArticle

The Defense Response of Nicotiana benthamiana to Peanut Stunt Virus Infection in the Presence of Symptom Exacerbating Satellite RNA

by Aleksandra Obrępalska-Stęplowska, Agnieszka Zmienko, Barbara Wrzesińska, Michal Goralski, Marek Figlerowicz, Joanna Zyprych-Walczak, Idzi Siatkowski and Henryk Pospieszny

Viruses 2018, 10(9), 449; https://doi.org/10.3390/v10090449 - 23 Aug 2018

Cited by 7 | Viewed by 5401

Abstract

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. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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15 pages, 1578 KiB

Open AccessArticle

Olive Mild Mosaic Virus Coat Protein and P6 Are Suppressors of RNA Silencing, and Their Silencing Confers Resistance against OMMV

by Carla MR Varanda, Patrick Materatski, Maria Doroteia Campos, Maria Ivone E. Clara, Gustavo Nolasco and Maria Do Rosário Félix

Viruses 2018, 10(8), 416; https://doi.org/10.3390/v10080416 - 09 Aug 2018

Cited by 11 | Viewed by 3410

Abstract

RNA silencing is an important defense mechanism in plants, yet several plant viruses encode proteins that suppress this mechanism. In this study, the genome of the Olive mild mosaic virus (OMMV) was screened for silencing suppressors. The full OMMV cDNA and 5 OMMV open reading frames (ORFs) were cloned into the Gateway binary vector pK7WG2, transformed into Agrobacterium tumefaciens, and agroinfiltrated into N. benthamiana 16C plants. CP and p6 showed suppressor activity, with CP showing significantly higher activity than p6, yet activity that was lower than the full OMMV, suggesting a complementary action of CP and p6. These viral suppressors were then used to induce OMMV resistance in plants based on RNA silencing. Two hairpin constructs targeting each suppressor were agroinfiltrated in N. benthamiana plants, which were then inoculated with OMMV RNA. When silencing of both suppressors was achieved, a significant reduction in viral accumulation and symptom attenuation was observed as compared to those of the controls, as well as to when each construct was used alone, proving them to be effective against OMMV infection. This is the first time that a silencing suppressor was found in a necrovirus, and that two independent proteins act as silencing suppressors in a virus member of the Tombusviridae family. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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16 pages, 2527 KiB

Open AccessArticle

Epigenetic Changes in the Regulation of Nicotiana tabacum Response to Cucumber Mosaic Virus Infection and Symptom Recovery through Single-Base Resolution Methylomes

by Chenguang Wang, Chaonan Wang, Wenjie Xu, Jingze Zou, Yanhong Qiu, Jun Kong, Yunshu Yang, Boyang Zhang and Shuifang Zhu

Viruses 2018, 10(8), 402; https://doi.org/10.3390/v10080402 - 29 Jul 2018

Cited by 31 | Viewed by 4630

Abstract

Plants have evolved multiple mechanisms to respond to viral infection. These responses have been studied in detail at the level of host immune response and antiviral RNA silencing (RNAi). However, the possibility of epigenetic reprogramming has not been thoroughly investigated. Here, we identified the role of DNA methylation during viral infection and performed reduced representation bisulfite sequencing (RRBS) on tissues of Cucumber mosaic virus (CMV)-infected Nicotiana tabacum at various developmental stages. Differential methylated regions are enriched with CHH sequence contexts, 80% of which are located on the gene body to regulate gene expression in a temporal style. The methylated genes depressed by methyltransferase inhibition largely overlapped with methylated genes in response to viral invasion. Activation in the argonaute protein and depression in methyl donor synthase revealed the important role of dynamic methylation changes in modulating viral clearance and resistance signaling. Methylation-expression relationships were found to be required for the immune response and cellular components are necessary for the proper defense response to infection and symptom recovery. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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14 pages, 2367 KiB

Open AccessArticle

Phytohormone Signaling of the Resistance to Plum pox virus (PPV, Sharka Disease) Induced by Almond (Prunus dulcis (Miller) Webb) Grafting to Peach (P. persica L. Batsch)

by Azam Nikbakht Dehkordi, Manuel Rubio, Nadali Babaeian, Alfonso Albacete and Pedro Martínez-Gómez

Viruses 2018, 10(5), 238; https://doi.org/10.3390/v10050238 - 03 May 2018

Cited by 17 | Viewed by 6170

Abstract

Plum pox virus (PPV, sharka) is a limiting factor for peach production, and no natural sources of resistance have been described. Recent studies, however, have demonstrated that grafting the almond cultivar “Garrigues” onto the “GF305” peach infected with Dideron-type (PPV-D) isolates progressively reduces disease symptoms and virus accumulation. Furthermore, grafting “Garrigues” onto “GF305” prior to PPV-D inoculation has been found to completely prevent virus infection, showing that resistance is constitutive and not induced by the virus. To unravel the phytohormone signaling of this mechanism, we analyzed the following phytohormones belonging to the principal hormone classes: the growth-related phytohormones cytokinin trans-zeatin (tZ) and the gibberellins GA₃ and GA₄; and the stress-related phytohormones ethylene acid precursor 1-aminocyclopropane-1-carboxylic acid (ACC), abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA). PPV inoculation produced a significant increase in GA₃ and ABA in peach, and these imbalances were related to the presence of chlorosis symptoms. However, grafting “Garrigues” almond onto the PPV-inoculated “GF305” peach produced the opposite effect, reducing GA₃ and ABA contents in parallel to the elimination of symptoms. Our results showed the significant implication of SA in this induced resistance in peach with an additional effect on tZ and JA concentrations. This SA-induced resistance based in the decrease in symptoms seems to be different from Systemic Acquired Resistance (SAR) and Induced Systemic Resistance (ISR), which are based in other reactions producing necrosis. Further studies are necessary, however, to validate these results against PPV-D isolates in the more aggressive Marcus-type (PPV-M) isolates. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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Review

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19 pages, 15201 KiB

Open AccessReview

Susceptibility Genes to Plant Viruses

by Hernan Garcia-Ruiz

Viruses 2018, 10(9), 484; https://doi.org/10.3390/v10090484 - 10 Sep 2018

Cited by 77 | Viewed by 10426

Abstract

Plant viruses use cellular factors and resources to replicate and move. Plants respond to viral infection by several mechanisms, including innate immunity, autophagy, and gene silencing, that viruses must evade or suppress. Thus, the establishment of infection is genetically determined by the availability of host factors necessary for virus replication and movement and by the balance between plant defense and viral suppression of defense responses. Host factors may have antiviral or proviral activities. Proviral factors condition susceptibility to viruses by participating in processes essential to the virus. Here, we review current advances in the identification and characterization of host factors that condition susceptibility to plant viruses. Host factors with proviral activity have been identified for all parts of the virus infection cycle: viral RNA translation, viral replication complex formation, accumulation or activity of virus replication proteins, virus movement, and virion assembly. These factors could be targets of gene editing to engineer resistance to plant viruses. Full article

(This article belongs to the Special Issue Plant-Virus Interactions)

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