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Viruses
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Plant Viruses: Pirates of Cellular Pathways
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Plant Viruses: Pirates of Cellular Pathways

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 May 2023) | Viewed by 20302

Special Issue Editors

Prof. Dr. Michael Taliansky

E-Mail Website
Guest Editor
The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
Interests: plant–virus interactions; cell nucleus and subnuclear structures; bionanotechnology
Special Issues, Collections and Topics in MDPI journals
Prof. Dr. Andrew J. Love

E-Mail Website
Guest Editor
Cell and Molecular Sciences, The James Hutton Institute, Errol Road, Invergowrie, Dundee DD2 5DA, UK
Interests: biotechnology; plant–virus interactions; cell nucleus; defence signalling pathways
Special Issues, Collections and Topics in MDPI journals
Dr. Alex M. Murphy

E-Mail Website
Guest Editor
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, UK
Interests: plant pathology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

We would like to invite you to submit review and original research articles to the Special Issue of Viruses, “Plant Viruses: Pirates of Cellular Pathways” (IF 5.048). Although viruses are very constrained with regard to genome size and number of proteins they encode relative to other pathogens, they are remarkably efficient at subverting host cellular processes to control their own replication, spread and dissemination in the environment. At the molecular level, it is astonishing that the few genes encoded by viruses and associated untranslated regions can trigger profound alterations in host cell signalling pathways, modulate the turnover/stability of host proteins, change the profiles of regulatory RNA species, vary cellular metabolic processes and induce the redistribution of cellular components. Understanding these orchestrated programmed events triggered by virus infection are key to uncovering interventions, which may reduce or block the invasion by these pirates of cellular processes. We also welcome papers related to molecular, genetic and biochemical bases controlling the virus manipulation of host–virus–vector interactions. Since there is a high degree of cross-kingdom functional similarities between plant and animal viruses and both manipulate cellular repertoires to promote virulence and spread, contributions from the animal side are also invited.

Prof. Dr. Michael Taliansky
Dr. Andrew J. Love
Dr. Alex M. Murphy
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • virus–plant interactions
  • virus–host–vector interactions
  • virus replication
  • virus movement
  • virus evolution

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Published Papers (11 papers)

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20 pages, 8185 KiB  
Article
Plant Poly(ADP-Ribose) Polymerase 1 Is a Potential Mediator of Cross-Talk between the Cajal Body Protein Coilin and Salicylic Acid-Mediated Antiviral Defence
by Nadezhda Spechenkova, Viktoriya O. Samarskaya, Natalya O. Kalinina, Sergey K. Zavriev, S. MacFarlane, Andrew J. Love and Michael Taliansky
Viruses 2023, 15(6), 1282; https://doi.org/10.3390/v15061282 - 30 May 2023
Cited by 3 | Viewed by 1842
Abstract
The nucleolus and Cajal bodies (CBs) are sub-nuclear domains with well-known roles in RNA metabolism and RNA-protein assembly. However, they also participate in other important aspects of cell functioning. This study uncovers a previously unrecognised mechanism by which these bodies and their components [...] Read more.
The nucleolus and Cajal bodies (CBs) are sub-nuclear domains with well-known roles in RNA metabolism and RNA-protein assembly. However, they also participate in other important aspects of cell functioning. This study uncovers a previously unrecognised mechanism by which these bodies and their components regulate host defences against pathogen attack. We show that the CB protein coilin interacts with poly(ADP-ribose) polymerase 1 (PARP1), redistributes it to the nucleolus and modifies its function, and that these events are accompanied by substantial increases in endogenous concentrations of salicylic acid (SA), activation of SA-responsive gene expression and callose deposition leading to the restriction of tobacco rattle virus (TRV) systemic infection. Consistent with this, we also find that treatment with SA subverts the negative effect of the pharmacological PARP inhibitor 3-aminobenzamide (3AB) on plant recovery from TRV infection. Our results suggest that PARP1 could act as a key molecular actuator in the regulatory network which integrates coilin activities as a stress sensor for virus infection and SA-mediated antivirus defence. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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16 pages, 2507 KiB  
Article
Differential Effects of RNA-Dependent RNA Polymerase 6 (RDR6) Silencing on New and Old World Begomoviruses in Nicotiana benthamiana
by Emanuela Noris, Mattia Pegoraro, Sandra Palzhoff, Catalina Urrejola, Nicolai Wochner, Sigi Kober, Kerstin Ruoff, Slavica Matić, Vera Schnepf, Nina Weisshaar and Christina Wege
Viruses 2023, 15(4), 919; https://doi.org/10.3390/v15040919 - 05 Apr 2023
Cited by 1 | Viewed by 1639
Abstract
RNA-dependent RNA polymerases (RDRs) are key players in the antiviral defence mediated by RNA silencing in plants. RDR6 is one of the major components of the process, regulating the infection of certain RNA viruses. To better clarify its function against DNA viruses, we [...] Read more.
RNA-dependent RNA polymerases (RDRs) are key players in the antiviral defence mediated by RNA silencing in plants. RDR6 is one of the major components of the process, regulating the infection of certain RNA viruses. To better clarify its function against DNA viruses, we analyzed the effect of RDR6 inactivation (RDR6i) in N. benthamiana plants on two phloem-limited begomoviruses, the bipartite Abutilon mosaic virus (AbMV) and the monopartite tomato yellow leaf curl Sardinia virus (TYLCSV). We observed exacerbated symptoms and DNA accumulation for the New World virus AbMV in RDR6i plants, varying with the plant growth temperature (ranging from 16 °C to 33 °C). However, for the TYLCSV of Old World origin, RDR6 depletion only affected symptom expression at elevated temperatures and to a minor extent; it did not affect the viral titre. The accumulation of viral siRNA differed between the two begomoviruses, being increased in RDR6i plants infected by AbMV but decreased in those infected by TYLCSV compared to wild-type plants. In situ hybridization revealed a 6.5-fold increase in the number of AbMV-infected nuclei in RDR6i plants but without egress from the phloem tissues. These results support the concept that begomoviruses adopt different strategies to counteract plant defences and that TYLCSV evades the functions exerted by RDR6 in this host. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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24 pages, 3694 KiB  
Article
Effects of Poty-Potexvirus Synergism on Growth, Photosynthesis and Metabolite Status of Nicotiana benthamiana
by Maija Pollari, Nina Sipari, Sylvain Poque, Kristiina Himanen and Kristiina Mäkinen
Viruses 2023, 15(1), 121; https://doi.org/10.3390/v15010121 - 30 Dec 2022
Cited by 2 | Viewed by 2037
Abstract
Mixed virus infections threaten crop production because interactions between the host and the pathogen mix may lead to viral synergism. While individual infections by potato virus A (PVA), a potyvirus, and potato virus X (PVX), a potexvirus, can be mild, co-infection leads to [...] Read more.
Mixed virus infections threaten crop production because interactions between the host and the pathogen mix may lead to viral synergism. While individual infections by potato virus A (PVA), a potyvirus, and potato virus X (PVX), a potexvirus, can be mild, co-infection leads to synergistic enhancement of PVX and severe symptoms. We combined image-based phenotyping with metabolite analysis of single and mixed PVA and PVX infections and compared their effects on growth, photosynthesis, and metabolites in Nicotiana benthamiana. Viral synergism was evident in symptom severity and impaired growth in the plants. Indicative of stress, the co-infection increased leaf temperature and decreased photosynthetic parameters. In contrast, singly infected plants sustained photosynthetic activity. The host’s metabolic response differed significantly between single and mixed infections. Over 200 metabolites were differentially regulated in the mixed infection: especially defense-related metabolites and aromatic and branched-chain amino acids increased compared to the control. Changes in the levels of methionine cycle intermediates and a low S-adenosylmethionine/S-adenosylhomocysteine ratio suggested a decline in the methylation potential in co-infected plants. The decreased ratio between reduced glutathione, an important scavenger of reactive oxygen species, and its oxidized form, indicated that severe oxidative stress developed during co-infection. Based on the results, infection-associated oxidative stress is successfully controlled in the single infections but not in the synergistic infection, where activated defense pathways are not sufficient to counter the impact of the infections on plant growth. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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15 pages, 4968 KiB  
Article
Cucumber Mosaic Virus-Induced Systemic Necrosis in Arabidopsis thaliana: Determinants and Role in Plant Defense
by Israel Pagán and Fernando García-Arenal
Viruses 2022, 14(12), 2790; https://doi.org/10.3390/v14122790 - 14 Dec 2022
Cited by 3 | Viewed by 1669 | Correction
Abstract
Effector-triggered immunity (ETI) is one of the most studied mechanisms of plant resistance to viruses. During ETI, viral proteins are recognized by specific plant R proteins, which most often trigger a hypersensitive response (HR) involving programmed cell death (PCD) and a restriction of [...] Read more.
Effector-triggered immunity (ETI) is one of the most studied mechanisms of plant resistance to viruses. During ETI, viral proteins are recognized by specific plant R proteins, which most often trigger a hypersensitive response (HR) involving programmed cell death (PCD) and a restriction of infection in the initially infected sites. However, in some plant–virus interactions, ETI leads to a response in which PCD and virus multiplication are not restricted to the entry sites and spread throughout the plant, leading to systemic necrosis. The host and virus genetic determinants, and the consequences of this response in plant–virus coevolution, are still poorly understood. Here, we identified an allelic version of RCY1—an R protein—as the host genetic determinant of broad-spectrum systemic necrosis induced by cucumber mosaic virus (CMV) infection in the Arabidopsis thaliana Co-1 ecotype. Systemic necrosis reduced virus fitness by shortening the infectious period and limiting virus multiplication; thus, this phenotype could be adaptive for the plant population as a defense against CMV. However, the low frequency (less than 1%) of this phenotype in A. thaliana wild populations argues against this hypothesis. These results expand current knowledge on the resistance mechanisms to virus infections associated with ETI in plants. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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17 pages, 6224 KiB  
Article
The Secret Life of the Inhibitor of Virus Replication
by Peter Palukaitis, Masoud Akbarimotlagh, Eseul Baek and Ju-Yeon Yoon
Viruses 2022, 14(12), 2782; https://doi.org/10.3390/v14122782 - 14 Dec 2022
Cited by 2 | Viewed by 1706
Abstract
The inhibitor of virus replication (IVR) is an inducible protein that is not virus-target-specific and can be induced by several viruses. The GenBank was interrogated for sequences closely related to the tobacco IVR. Various RNA fragments from tobacco, tomato, and potato and their [...] Read more.
The inhibitor of virus replication (IVR) is an inducible protein that is not virus-target-specific and can be induced by several viruses. The GenBank was interrogated for sequences closely related to the tobacco IVR. Various RNA fragments from tobacco, tomato, and potato and their genomic DNA contained IVR-like sequences. However, IVRs were part of larger proteins encoded by these genomic DNA sequences, which were identified in Arabidopsis as being related to the cyclosome protein designated anaphase-promoting complex 7 (APC7). Sequence analysis of the putative APC7s of nine plant species showed proteins of 558-561 amino acids highly conserved in sequence containing at least six protein-binding elements of 34 amino acids called tetratricopeptide repeats (TPRs), which form helix–turn–helix structures. The structures of Arabidopsis APC7 and the tobacco IVR proteins were modeled using the AlphaFold program and superimposed, showing that IVR had the same structure as the C-terminal 34% of APC7, indicating that IVR was a product of the APC7 gene. Based on the presence of various transcription factor binding sites in the APC7 sequences upstream of the IVR coding sequences, we propose that IVR could be expressed by these APC7 gene sequences involving the transcription factor SHE1. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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17 pages, 7220 KiB  
Article
Interaction between Movement Proteins of Hibiscus green spot virus
by Anastasia K. Atabekova, Ekaterina A. Lazareva, Alexander A. Lezzhov, Anna D. Solovieva, Sergei A. Golyshev, Boris I. Skulachev, Ilya D. Solovyev, Alexander P. Savitsky, Manfred Heinlein, Sergey Y. Morozov and Andrey G. Solovyev
Viruses 2022, 14(12), 2742; https://doi.org/10.3390/v14122742 - 08 Dec 2022
Cited by 3 | Viewed by 1482
Abstract
Movement proteins (MPs) of plant viruses enable the translocation of viral genomes from infected to healthy cells through plasmodesmata (PD). The MPs functions involve the increase of the PD permeability and routing of viral genome both to the PD entrance and through the [...] Read more.
Movement proteins (MPs) of plant viruses enable the translocation of viral genomes from infected to healthy cells through plasmodesmata (PD). The MPs functions involve the increase of the PD permeability and routing of viral genome both to the PD entrance and through the modified PD. Hibiscus green spot virus encodes two MPs, termed BMB1 and BMB2, which act in concert to accomplish virus cell-to-cell transport. BMB1, representing an NTPase/helicase domain-containing RNA-binding protein, localizes to the cytoplasm and the nucleoplasm. BMB2 is a small hydrophobic protein that interacts with the endoplasmic reticulum (ER) membranes and induces local constrictions of the ER tubules. In plant cells, BMB2 localizes to PD-associated membrane bodies (PAMBs) consisting of modified ER tubules and directs BMB1 to PAMBs. Here, we demonstrate that BMB1 and BMB2 interact in vitro and in vivo, and that their specific interaction is essential for BMB2-directed targeting of BMB1 to PAMBs. Using mutagenesis, we show that the interaction involves the C-terminal BMB1 region and the N-terminal region of BMB2. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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15 pages, 14546 KiB  
Article
Comprehensive Analysis of Ubiquitome Changes in Nicotiana benthamiana after Rice Stripe Virus Infection
by Yu Liu, Chenyang Li, Yaqin Wang, Yi Xu, Jianxiang Wu and Xueping Zhou
Viruses 2022, 14(11), 2349; https://doi.org/10.3390/v14112349 - 26 Oct 2022
Viewed by 1710
Abstract
Rice stripe virus (RSV) is one of the most devastating viruses affecting rice production. During virus infection, ubiquitination plays an important role in the dynamic regulation of host defenses. We combined the ubiquitomics approach with the label-free quantitation proteomics approach to investigate potential [...] Read more.
Rice stripe virus (RSV) is one of the most devastating viruses affecting rice production. During virus infection, ubiquitination plays an important role in the dynamic regulation of host defenses. We combined the ubiquitomics approach with the label-free quantitation proteomics approach to investigate potential ubiquitination status changes of Nicotiana benthamiana infected with RSV. Bioinformatics analyses were performed to elucidate potential associations between proteins with differentially ubiquitinated sites (DUSs) and various cellular components/pathways during virus infection. In total, 399 DUSs in 313 proteins were identified and quantified, among them 244 ubiquitinated lysine (Kub) sites in 186 proteins were up-regulated and 155 Kub sites in 127 proteins were down-regulated at 10 days after RSV infection. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathway enrichment analyses indicated that proteins with up-regulated Kub sites were significantly enriched in the ribosome. Silencing of 3-isopropylmalate dehydratase large subunit through virus-induced gene silencing delayed RSV infection, while silencing of mRNA-decapping enzyme-like protein promoted RSV symptom in the late stage of infection. Moreover, ubiquitination was observed in all seven RSV-encoded proteins. Our study supplied the comprehensive analysis of the ubiquitination changes in N. benthamiana after RSV infection, which is helpful for understanding RSV pathogenesis and RSV-host interactions. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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11 pages, 2030 KiB  
Article
The P3N-PIPO Protein Encoded by Wheat Yellow Mosaic Virus Is a Pathogenicity Determinant and Promotes Its Pathogenicity through Interaction with NbRLK6 in Nicotiana benthamiana
by Runpu Miao, Zhuangxin Ye, Stuart MacFarlane, Yanjun Li, Qianzhuo Mao, Yanzhen Tian, Zhiping Deng, Zongtao Sun, Jian Yang, Junmin Li, Fei Yan, Jianping Chen and Chulang Yu
Viruses 2022, 14(10), 2171; https://doi.org/10.3390/v14102171 - 30 Sep 2022
Cited by 2 | Viewed by 1610
Abstract
Similarly to other potyvirids, the bymovirus wheat yellow mosaic virus (WYMV) encodes a P3N-PIPO protein that is expressed by frameshifting occurring within the open reading frame of the P3 protein. P3N-PIPO is known to be essential for the cell-to-cell movement of several potyviruses, [...] Read more.
Similarly to other potyvirids, the bymovirus wheat yellow mosaic virus (WYMV) encodes a P3N-PIPO protein that is expressed by frameshifting occurring within the open reading frame of the P3 protein. P3N-PIPO is known to be essential for the cell-to-cell movement of several potyviruses, but this has not yet been confirmed for the WYMV. Here, we show that the WYMV P3N-PIPO protein influences disease symptom formation. Infection of Nicotiana benthamiana plants with a potato virus X (PVX)-based vector carrying the WYMV P3N-PIPO gene induced more severe disease symptoms and resulted in higher virus accumulation levels than did infection with PVX lacking the P3N-PIPO gene. N. benthamiana P3N-PIPO-interacting proteins were identified through co-immunoprecipitation (Co-IP) coupled with LC-MS/MS (mass spectrometry), and the interaction between P3N-PIPO and the N. benthamiana receptor-like kinase NbRLK6 was further verified by Co-IP and bimolecular fluorescence complementation (BiFC) of transiently-expressed proteins. Furthermore, our investigation showed that the disease symptom severity and accumulation level of PVX-P3N-PIPO were decreased in N. benthamiana plants when NbRLK6 expression was reduced by tobacco rattle virus-induced gene silencing. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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19 pages, 4241 KiB  
Article
The Effects of Cucumber Mosaic Virus and Its 2a and 2b Proteins on Interactions of Tomato Plants with the Aphid Vectors Myzus persicae and Macrosiphum euphorbiae
by Warren Arinaitwe, Alex Guyon, Trisna D. Tungadi, Nik J. Cunniffe, Sun-Ju Rhee, Amjad Khalaf, Netsai M. Mhlanga, Adrienne E. Pate, Alex M. Murphy and John P. Carr
Viruses 2022, 14(8), 1703; https://doi.org/10.3390/v14081703 - 01 Aug 2022
Cited by 6 | Viewed by 3145
Abstract
Cucumber mosaic virus (CMV), a major tomato pathogen, is aphid-vectored in the non-persistent manner. We investigated if CMV-induced volatile organic compounds (VOCs) or other virus-induced cues alter aphid–tomato interactions. Y-tube olfactometry showed that VOCs emitted by plants infected with CMV (strain Fny) attracted [...] Read more.
Cucumber mosaic virus (CMV), a major tomato pathogen, is aphid-vectored in the non-persistent manner. We investigated if CMV-induced volatile organic compounds (VOCs) or other virus-induced cues alter aphid–tomato interactions. Y-tube olfactometry showed that VOCs emitted by plants infected with CMV (strain Fny) attracted generalist (Myzus persicae) and Solanaceae specialist (Macrosiphum euphorbiae) aphids. Myzus persicae preferred settling on infected plants (3 days post-inoculation: dpi) at 1h post-release, but at 9 and 21 dpi, aphids preferentially settled on mock-inoculated plants. Macrosiphum euphorbiae showed no strong preference for mock-inoculated versus infected plants at 3 dpi but settled preferentially on mock-inoculated plants at 9 and 21 dpi. In darkness aphids showed no settling or migration bias towards either mock-inoculated or infected plants. However, tomato VOC blends differed in light and darkness, suggesting aphids respond to a complex mix of olfactory, visual, and other cues influenced by infection. The LS-CMV strain induced no changes in aphid–plant interactions. Experiments using inter-strain recombinant and pseudorecombinant viruses showed that the Fny-CMV 2a and 2b proteins modified tomato interactions with Macrosiphum euphorbiae and Myzus persicae, respectively. The defence signal salicylic acid prevents excessive CMV-induced damage to tomato plants but is not involved in CMV-induced changes in aphid–plant interactions. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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1 pages, 412 KiB  
Correction
Correction: Pagán, I.; García-Arenal, F. Cucumber Mosaic Virus-Induced Systemic Necrosis in Arabidopsis thaliana: Determinants and Role in Plant Defense. Viruses 2022, 14, 2790
by Israel Pagán and Fernando García-Arenal
Viruses 2023, 15(4), 852; https://doi.org/10.3390/v15040852 - 27 Mar 2023
Viewed by 650
Abstract
In the original publication [...] Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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12 pages, 1772 KiB  
Perspective
ADP-Ribosylation and Antiviral Resistance in Plants
by Nadezhda Spechenkova, Natalya O. Kalinina, Sergey K. Zavriev, Andrew J. Love and Michael Taliansky
Viruses 2023, 15(1), 241; https://doi.org/10.3390/v15010241 - 14 Jan 2023
Cited by 2 | Viewed by 1732
Abstract
ADP-ribosylation (ADPRylation) is a versatile posttranslational modification in eukaryotic cells which is involved in the regulation of a wide range of key biological processes, including DNA repair, cell signalling, programmed cell death, growth and development and responses to biotic and abiotic stresses. Members [...] Read more.
ADP-ribosylation (ADPRylation) is a versatile posttranslational modification in eukaryotic cells which is involved in the regulation of a wide range of key biological processes, including DNA repair, cell signalling, programmed cell death, growth and development and responses to biotic and abiotic stresses. Members of the poly(ADP-ribosyl) polymerase (PARP) family play a central role in the process of ADPRylation. Protein targets can be modified by adding either a single ADP-ribose moiety (mono(ADP-ribosyl)ation; MARylation), which is catalysed by mono(ADP-ribosyl) transferases (MARTs or PARP “monoenzymes”), or targets may be decorated with chains of multiple ADP-ribose moieties (PARylation), via the activities of PARP “polyenzymes”. Studies have revealed crosstalk between PARylation (and to a lesser extent, MARylation) processes in plants and plant–virus interactions, suggesting that these tight links may represent a novel factor regulating plant antiviral immunity. From this perspective, we go through the literature linking PARylation-associated processes with other plant regulation pathways controlling virus resistance. Once unraveled, these links may serve as the basis of innovative strategies to improve crop resistance to viruses under challenging environmental conditions which could mitigate yield losses. Full article
(This article belongs to the Special Issue Plant Viruses: Pirates of Cellular Pathways)
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