Molecular Plant-Virus Interactions

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 January 2022) | Viewed by 32445

Special Issue Editors


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Guest Editor
Sveriges lantbruksuniversitet, Uppsala, Sweden
Interests: plant–virus interactions; virus long-distance movement; viral suppressors of RNA silencing; nuclear-localised viral proteins; virus interference with phytohormone signalling; virus-induced transcriptomic changes.

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Guest Editor
Sveriges lantbruksuniversitet, Uppsala, Sweden

Special Issue Information

Dear Colleagues,

Plant viruses—with more than a thousand known species—are a fascinating group of viruses, providing complex plant–virus interactions as a model for pathogenesis, plant defence, virus counter-defence, cell-to-cell and systemic movement, and transmission by vectors.  Molecular plant–virus interaction is a rather complex and dynamic process, involving numerous interactions with cellular and molecular components of the plant. In the infection–defence equilibrium, plant viruses are able to subvert plant development, defence responses, and phytohormone signalling for the benefit of the virus, often resulting in disease. With the advent of High-Throughput Sequencing (HTS), ‘omic’ technologies, genome editing techniques, and advanced microscopy and imaging techniques, it is now cost and time efficient to decipher the most intimate and intricate interplay between plant viruses and their hosts. Hence, next-generation technologies help us to dissect the molecular networks of plant–virus interactions in order to advance our understanding of the viral infection process with the aim of assisting with the development of novel antiviral strategies. Another aim is to expand the pool of genetic resources for breeding-for-resistance in order to reduce crop losses caused by viral diseases.

Dr. Eugene Savenkov
Dr. Katalin Nemes
Guest Editors

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Keywords

  • plant virus
  • RNA silencing
  • viral suppressor of RNA silencing
  • intracellular communication
  • phytohormone signalling
  • cell-to-cell movement
  • nuclear signalling
  • high-throughput sequencing
  • plasmodesmata
  • virus systemic movement.

Published Papers (10 papers)

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Research

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16 pages, 3042 KiB  
Article
The Potyviral Protein 6K1 Reduces Plant Proteases Activity during Turnip mosaic virus Infection
by Sayanta Bera, Gabriella D. Arena, Swayamjit Ray, Sydney Flannigan and Clare L. Casteel
Viruses 2022, 14(6), 1341; https://doi.org/10.3390/v14061341 - 20 Jun 2022
Cited by 9 | Viewed by 2510
Abstract
Potyviral genomes encode just 11 major proteins and multifunctionality is associated with most of these proteins at different stages of the virus infection cycle. Some potyviral proteins modulate phytohormones and protein degradation pathways and have either pro- or anti-viral/insect vector functions. Our previous [...] Read more.
Potyviral genomes encode just 11 major proteins and multifunctionality is associated with most of these proteins at different stages of the virus infection cycle. Some potyviral proteins modulate phytohormones and protein degradation pathways and have either pro- or anti-viral/insect vector functions. Our previous work demonstrated that the potyviral protein 6K1 has an antagonistic effect on vectors when expressed transiently in host plants, suggesting plant defenses are regulated. However, to our knowledge the mechanisms of how 6K1 alters plant defenses and how 6K1 functions are regulated are still limited. Here we show that the 6K1 from Turnip mosaic virus (TuMV) reduces the abundance of transcripts related to jasmonic acid biosynthesis and cysteine protease inhibitors when expressed in Nicotiana benthamiana relative to controls. 6K1 stability increased when cysteine protease activity was inhibited chemically, showing a mechanism to the rapid turnover of 6K1 when expressed in trans. Using RNAseq, qRT-PCR, and enzymatic assays, we demonstrate TuMV reprograms plant protein degradation pathways on the transcriptional level and increases 6K1 stability at later stages in the infection process. Moreover, we show 6K1 decreases plant protease activity in infected plants and increases TuMV accumulation in systemic leaves compared to controls. These results suggest 6K1 has a pro-viral function in addition to the anti-insect vector function we observed previously. Although the host targets of 6K1 and the impacts of 6K1-induced changes in protease activity on insect vectors are still unknown, this study enhances our understanding of the complex interactions occurring between plants, potyviruses, and vectors. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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23 pages, 4441 KiB  
Article
Severe Stunting Symptoms upon Nepovirus Infection Are Reminiscent of a Chronic Hypersensitive-like Response in a Perennial Woody Fruit Crop
by Isabelle R. Martin, Emmanuelle Vigne, Amandine Velt, Jean-Michel Hily, Shahinez Garcia, Raymonde Baltenweck, Véronique Komar, Camille Rustenholz, Philippe Hugueney, Olivier Lemaire and Corinne Schmitt-Keichinger
Viruses 2021, 13(11), 2138; https://doi.org/10.3390/v13112138 - 22 Oct 2021
Cited by 10 | Viewed by 2552
Abstract
Virus infection of plants can result in various degrees of detrimental impacts and disparate symptom types and severities. Although great strides have been made in our understanding of the virus–host interactions in herbaceous model plants, the mechanisms underlying symptom development are poorly understood [...] Read more.
Virus infection of plants can result in various degrees of detrimental impacts and disparate symptom types and severities. Although great strides have been made in our understanding of the virus–host interactions in herbaceous model plants, the mechanisms underlying symptom development are poorly understood in perennial fruit crops. Grapevine fanleaf virus (GFLV) causes variable symptoms in most vineyards worldwide. To better understand GFLV-grapevine interactions in relation to symptom development, field and greenhouse trials were conducted with a grapevine genotype that exhibits distinct symptoms in response to a severe and a mild strain of GFLV. After validation of the infection status of the experimental vines by high-throughput sequencing, the transcriptomic and metabolomic profiles in plants infected with the two viral strains were tested and compared by RNA-Seq and LC-MS, respectively, in the differentiating grapevine genotype. In vines infected with the severe GFLV strain, 1023 genes, among which some are implicated in the regulation of the hypersensitive-type response, were specifically deregulated, and a higher accumulation of resveratrol and phytohormones was observed. Interestingly, some experimental vines restricted the virus to the rootstock and remained symptomless. Our results suggest that GFLV induces a strain- and cultivar-specific defense reaction similar to a hypersensitive reaction. This type of defense leads to a severe stunting phenotype in some grapevines, whereas others are resistant. This work is the first evidence of a hypersensitive-like reaction in grapevine during virus infection. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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31 pages, 45048 KiB  
Article
WRKY Transcription Factors in Cassava Contribute to Regulation of Tolerance and Susceptibility to Cassava Mosaic Disease through Stress Responses
by Warren Freeborough, Nikki Gentle and Marie E.C. Rey
Viruses 2021, 13(9), 1820; https://doi.org/10.3390/v13091820 - 13 Sep 2021
Cited by 10 | Viewed by 2657
Abstract
Among the numerous biological constraints that hinder cassava (Manihot esculenta Crantz) production, foremost is cassava mosaic disease (CMD) caused by virus members of the family Geminiviridae, genus Begomovirus. The mechanisms of CMD tolerance and susceptibility are not fully understood; however, [...] Read more.
Among the numerous biological constraints that hinder cassava (Manihot esculenta Crantz) production, foremost is cassava mosaic disease (CMD) caused by virus members of the family Geminiviridae, genus Begomovirus. The mechanisms of CMD tolerance and susceptibility are not fully understood; however, CMD susceptible T200 and tolerant TME3 cassava landraces have been shown to exhibit different large-scale transcriptional reprogramming in response to South African cassava mosaic virus (SACMV). Recent identification of 85 MeWRKY transcription factors in cassava demonstrated high orthology with those in Arabidopsis, however, little is known about their roles in virus responses in this non-model crop. Significant differences in MeWRKY expression and regulatory networks between the T200 and TME3 landraces were demonstrated. Overall, WRKY expression and associated hormone and enriched biological processes in both landraces reflect oxidative and other biotic stress responses to SACMV. Notably, MeWRKY11 and MeWRKY81 were uniquely up and downregulated at 12 and 67 days post infection (dpi) respectively in TME3, implicating a role in tolerance and symptom recovery. AtWRKY28 and AtWRKY40 homologs of MeWRKY81 and MeWRKY11, respectively, have been shown to be involved in regulation of jasmonic and salicylic acid signaling in Arabidopsis. AtWRKY28 is an interactor in the RPW8-NBS resistance (R) protein network and downregulation of its homolog MeWRKY81 at 67 dpi in TME3 suggests a negative role for this WRKY in SACMV tolerance. In contrast, in T200, nine MeWRKYs were differentially expressed from early (12 dpi), middle (32 dpi) to late (67 dpi) infection. MeWRKY27 (homolog AtWRKY33) and MeWRKY55 (homolog AtWRKY53) were uniquely up-regulated at 12, 32 and 67 dpi in T200. AtWRKY33 and AtWRKY53 are positive regulators of leaf senescence and oxidative stress in Arabidopsis, suggesting MeWRKY55 and 27 contribute to susceptibility in T200. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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21 pages, 4418 KiB  
Article
R-BPMV-Mediated Resistance to Bean pod mottle virus in Phaseolus vulgaris L. Is Heat-Stable but Elevated Temperatures Boost Viral Infection in Susceptible Genotypes
by Chouaïb Meziadi, Julie Lintz, Masoud Naderpour, Charlotte Gautier, Sophie Blanchet, Alicia Noly, Ariane Gratias-Weill, Valérie Geffroy and Stéphanie Pflieger
Viruses 2021, 13(7), 1239; https://doi.org/10.3390/v13071239 - 26 Jun 2021
Cited by 4 | Viewed by 2675
Abstract
In the context of climate change, elevated temperature is a major concern due to the impact on plant–pathogen interactions. Although atmospheric temperature is predicted to increase in the next century, heat waves during summer seasons have already become a current problem. Elevated temperatures [...] Read more.
In the context of climate change, elevated temperature is a major concern due to the impact on plant–pathogen interactions. Although atmospheric temperature is predicted to increase in the next century, heat waves during summer seasons have already become a current problem. Elevated temperatures strongly influence plant–virus interactions, the most drastic effect being a breakdown of plant viral resistance conferred by some major resistance genes. In this work, we focused on the R-BPMV gene, a major resistance gene against Bean pod mottle virus in Phaseolus vulgaris. We inoculated different BPMV constructs in order to study the behavior of the R-BPMV-mediated resistance at normal (20 °C) and elevated temperatures (constant 25, 30, and 35 °C). Our results show that R-BPMV mediates a temperature-dependent phenotype of resistance from hypersensitive reaction at 20 °C to chlorotic lesions at 35 °C in the resistant genotype BAT93. BPMV is detected in inoculated leaves but not in systemic ones, suggesting that the resistance remains heat-stable up to 35 °C. R-BPMV segregates as an incompletely dominant gene in an F2 population. We also investigated the impact of elevated temperature on BPMV infection in susceptible genotypes, and our results reveal that elevated temperatures boost BPMV infection both locally and systemically in susceptible genotypes. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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16 pages, 2930 KiB  
Article
The Resistance Responses of Potato Plants to Potato Virus Y Are Associated with an Increased Cellular Methionine Content and an Altered SAM:SAH Methylation Index
by Nadezhda Spechenkova, Igor A. Fesenko, Anna Mamaeva, Tatyana P. Suprunova, Natalia O. Kalinina, Andrew J. Love and Michael Taliansky
Viruses 2021, 13(6), 955; https://doi.org/10.3390/v13060955 - 21 May 2021
Cited by 10 | Viewed by 2578
Abstract
Plant-virus interactions are frequently influenced by elevated temperature, which often increases susceptibility to a virus, a scenario described for potato cultivar Chicago infected with potato virus Y (PVY). In contrast, other potato cultivars such as Gala may have similar resistances to PVY at [...] Read more.
Plant-virus interactions are frequently influenced by elevated temperature, which often increases susceptibility to a virus, a scenario described for potato cultivar Chicago infected with potato virus Y (PVY). In contrast, other potato cultivars such as Gala may have similar resistances to PVY at both normal (22 °C) and high (28 °C) temperatures. To elucidate the mechanisms of temperature-independent antivirus resistance in potato, we analysed responses of Gala plants to PVY at different temperatures using proteomic, transcriptional and metabolic approaches. Here we show that in Gala, PVY infection generally upregulates the accumulation of major enzymes associated with the methionine cycle (MTC) independently of temperature, but that temperature (22 °C or 28 °C) may finely regulate what classes accumulate. The different sets of MTC-related enzymes that are up-regulated at 22 °C or 28 °C likely account for the significantly increased accumulation of S-adenosyl methionine (SAM), a key component of MTC which acts as a universal methyl donor in methylation reactions. In contrast to this, we found that in cultivar Chicago, SAM levels were significantly reduced which correlated with the enhanced susceptibility to PVY at high temperature. Collectively, these data suggest that MTC and its major transmethylation function determines resistance or susceptibility to PVY. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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7 pages, 1382 KiB  
Communication
LAMP-Coupled CRISPR–Cas12a Module for Rapid and Sensitive Detection of Plant DNA Viruses
by Ahmed Mahas, Norhan Hassan, Rashid Aman, Tin Marsic, Qiaochu Wang, Zahir Ali and Magdy M. Mahfouz
Viruses 2021, 13(3), 466; https://doi.org/10.3390/v13030466 - 12 Mar 2021
Cited by 55 | Viewed by 6192
Abstract
One important factor for successful disease management is the ability to rapidly and accurately identify the causal agent. Plant viruses cause severe economic losses and pose a serious threat to sustainable agriculture. Therefore, optimization of the speed, sensitivity, feasibility, portability, and accuracy of [...] Read more.
One important factor for successful disease management is the ability to rapidly and accurately identify the causal agent. Plant viruses cause severe economic losses and pose a serious threat to sustainable agriculture. Therefore, optimization of the speed, sensitivity, feasibility, portability, and accuracy of virus detection is urgently needed. Here, we developed a clustered regularly interspaced short palindromic repeats (CRISPR)-based nucleic acid diagnostic method utilizing the CRISPR–Cas12a system for detecting two geminiviruses, tomato yellow leaf curl virus (TYLCV) and tomato leaf curl New Delhi virus (ToLCNDV), which have single-stranded DNA genomes. Our assay detected TYLCV and ToLCNDV in infected plants with high sensitivity and specificity. Our newly developed assay can be performed in ~1 h and provides easy-to-interpret visual readouts using a simple, low-cost fluorescence visualizer, making it suitable for point-of-use applications. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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14 pages, 30582 KiB  
Article
The 28 Ser Amino Acid of Cucumber Mosaic Virus Movement Protein Has a Role in Symptom Formation and Plasmodesmata Localization
by Réka Sáray, Attila Fábián, László Palkovics and Katalin Salánki
Viruses 2021, 13(2), 222; https://doi.org/10.3390/v13020222 - 31 Jan 2021
Cited by 4 | Viewed by 3048
Abstract
Cucumber mosaic virus (CMV, Cucumovirus, Bromoviridae) is an economically significant virus infecting important horticultural and field crops. Current knowledge regarding the specific functions of its movement protein (MP) is still incomplete. In the present study, potential post-translational modification sites of its MP [...] Read more.
Cucumber mosaic virus (CMV, Cucumovirus, Bromoviridae) is an economically significant virus infecting important horticultural and field crops. Current knowledge regarding the specific functions of its movement protein (MP) is still incomplete. In the present study, potential post-translational modification sites of its MP were assayed with mutant viruses: MP/S28A, MP/S28D, MP/S120A and MP/S120D. Ser28 was identified as an important factor in viral pathogenicity on Nicotiana tabacum cv. Xanthi, Cucumis sativus and Chenopodium murale. The subcellular localization of GFP-tagged movement proteins was determined with confocal laser-scanning microscopy. The wild type movement protein fused to green fluorescent protein (GFP) (MP-eGFP) greatly colocalized with callose at plasmodesmata, while MP/S28A-eGFP and MP/S28D-eGFP were detected as punctate spots along the cell membrane without callose colocalization. These results underline the importance of phosphorylatable amino acids in symptom formation and provide data regarding the essential factors for plasmodesmata localization of CMV MP. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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13 pages, 2039 KiB  
Article
The AC2 Protein of a Bipartite Geminivirus Stimulates the Transcription of the BV1 Gene through Abscisic Acid Responsive Promoter Elements
by Rong Sun, Junping Han, Limin Zheng and Feng Qu
Viruses 2020, 12(12), 1403; https://doi.org/10.3390/v12121403 - 07 Dec 2020
Cited by 3 | Viewed by 2097
Abstract
Geminiviruses possess single-stranded, circular DNA genomes and control the transcription of their late genes, including BV1 of many bipartite begomoviruses, through transcriptional activation by the early expressing AC2 protein. DNA binding by AC2 is not sequence-specific; hence, the specificity of AC2 activation is [...] Read more.
Geminiviruses possess single-stranded, circular DNA genomes and control the transcription of their late genes, including BV1 of many bipartite begomoviruses, through transcriptional activation by the early expressing AC2 protein. DNA binding by AC2 is not sequence-specific; hence, the specificity of AC2 activation is thought to be conferred by plant transcription factors (TFs) recruited by AC2 in infected cells. However, the exact TFs AC2 recruits are not known for most viruses. Here, we report a systematic examination of the BV1 promoter (PBV1) of the mungbean yellow mosaic virus (MYMV) for conserved promoter motifs. We found that MYMV PBV1 contains three abscisic acid (ABA)-responsive elements (ABREs) within its first 70 nucleotides. Deleting these ABREs, or mutating them all via site-directed mutagenesis, abolished the capacity of PBV1 to respond to AC2-mediated transcriptional activation. Furthermore, ABRE and other related ABA-responsive elements were prevalent in more than a dozen Old World begomoviruses we inspected. Together, these findings suggest that ABA-responsive TFs may be recruited by AC2 to BV1 promoters of these viruses to confer specificity to AC2 activation. These observations are expected to guide the search for the actual TF(s), furthering our understanding of the mechanisms of AC2 action. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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Review

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11 pages, 1771 KiB  
Review
Geminivirus–Host Interactions: Action and Reaction in Receptor-Mediated Antiviral Immunity
by Marco Aurélio Ferreira, Ruan M. Teixeira and Elizabeth P. B. Fontes
Viruses 2021, 13(5), 840; https://doi.org/10.3390/v13050840 - 06 May 2021
Cited by 3 | Viewed by 2965
Abstract
In plant−virus interactions, the plant immune system and virulence strategies are under constant pressure for dominance, and the balance of these opposing selection pressures can result in disease or resistance. The naturally evolving plant antiviral immune defense consists of a multilayered perception system [...] Read more.
In plant−virus interactions, the plant immune system and virulence strategies are under constant pressure for dominance, and the balance of these opposing selection pressures can result in disease or resistance. The naturally evolving plant antiviral immune defense consists of a multilayered perception system represented by pattern recognition receptors (PRR) and resistance (R) proteins similarly to the nonviral pathogen innate defenses. Another layer of antiviral immunity, signaling via a cell surface receptor-like kinase to inhibit host and viral mRNA translation, has been identified as a virulence target of the geminivirus nuclear shuttle protein. The Geminiviridae family comprises broad-host range viruses that cause devastating plant diseases in a large variety of relevant crops and vegetables and hence have evolved a repertoire of immune-suppressing functions. In this review, we discuss the primary layers of the receptor-mediated antiviral immune system, focusing on the mechanisms developed by geminiviruses to overcome plant immunity. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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22 pages, 1167 KiB  
Review
Changes in Subcellular Localization of Host Proteins Induced by Plant Viruses
by Rosalba Rodriguez-Peña, Kaoutar El Mounadi and Hernan Garcia-Ruiz
Viruses 2021, 13(4), 677; https://doi.org/10.3390/v13040677 - 15 Apr 2021
Cited by 12 | Viewed by 3510
Abstract
Viruses are dependent on host factors at all parts of the infection cycle, such as translation, genome replication, encapsidation, and cell-to-cell and systemic movement. RNA viruses replicate their genome in compartments associated with the endoplasmic reticulum, chloroplasts, and mitochondria or peroxisome membranes. In [...] Read more.
Viruses are dependent on host factors at all parts of the infection cycle, such as translation, genome replication, encapsidation, and cell-to-cell and systemic movement. RNA viruses replicate their genome in compartments associated with the endoplasmic reticulum, chloroplasts, and mitochondria or peroxisome membranes. In contrast, DNA viruses replicate in the nucleus. Viral infection causes changes in plant gene expression and in the subcellular localization of some host proteins. These changes may support or inhibit virus accumulation and spread. Here, we review host proteins that change their subcellular localization in the presence of a plant virus. The most frequent change is the movement of host cytoplasmic proteins into the sites of virus replication through interactions with viral proteins, and the protein contributes to essential viral processes. In contrast, only a small number of studies document changes in the subcellular localization of proteins with antiviral activity. Understanding the changes in the subcellular localization of host proteins during plant virus infection provides novel insights into the mechanisms of plant–virus interactions and may help the identification of targets for designing genetic resistance to plant viruses. Full article
(This article belongs to the Special Issue Molecular Plant-Virus Interactions)
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