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Plant Immunity to Virus Infections

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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 (30 April 2019) | Viewed by 56880

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Dr. Feng Qu

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Guest Editor

Department of Plant Pathology, The Ohio State University, Wooster, OH, USA
Interests: plant antiviral defenses; including RNA silencing and resistance gene-mediated defense
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

I am honored to have this opportunity to guest-edit a Special Issue on “Plant Immunity to Virus Infections”. Plant antiviral defense mechanisms have always been a field of unabated research interest, as they offer both the thrill of basic research discovery and the promise of improved control of crop virus diseases.

Thanks to the relentless pursuit by generations of plant virologists, we now know that plant viruses encounter a wide array of host defenses, including RNA silencing, immunity conferred by single dominant (e.g., resistance genes or R genes) or recessive (e.g., eukaryotic translational initiation factors) plant genes, protein or virion destruction by autophagy and/or proteasome, defense augmentation through plant hormones and reactive oxygen species, and many more. Strikingly, nearly all of the defense mechanisms are counteracted by viruses with a steadily evolving arsenal of defense-mitigating or -evading tools.

With this Special Issue, I hope to highlight the latest progresses in the field of plant immunity to virus infection by inviting plant virologists worldwide to tell their most exciting stories in the form of original research articles, reviews, or opinion/hypothesis essays. Contributions from all branches of this field are equally and enthusiastically appreciated.

Dr. Feng Qu
Guest Editor

Manuscript Submission Information

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Keywords

Plant anti-viral defense
Resistance gene
RNA silencing
Autopahgy
Defense regulation by plant hormones
Crop virus diseases

Published Papers (12 papers)

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Research

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17 pages, 2281 KiB

Open AccessArticle

Tracing the Lineage of Two Traits Associated with the Coat Protein of the Tombusviridae: Silencing Suppression and HR Elicitation in Nicotiana Species

by Mustafa Adhab, Carlos Angel, Andres Rodriguez, Mohammad Fereidouni, Lóránt Király, Kay Scheets and James E. Schoelz

Viruses 2019, 11(7), 588; https://doi.org/10.3390/v11070588 - 28 Jun 2019

Cited by 9 | Viewed by 3119

Abstract

In this paper we have characterized the lineage of two traits associated with the coat proteins (CPs) of the tombusvirids: Silencing suppression and HR elicitation in Nicotiana species. We considered that the tombusvirid CPs might collectively be considered an effector, with the CP of each CP-encoding species comprising a structural variant within the family. Thus, a phylogenetic analysis of the CP could provide insight into the evolution of a pathogen effector. The phylogeny of the CP of tombusvirids indicated that CP representatives of the family could be divided into four clades. In two separate clades the CP triggered a hypersensitive response (HR) in Nicotiana species of section Alatae but did not have silencing suppressor activity. In a third clade the CP had a silencing suppressor activity but did not have the capacity to trigger HR in Nicotiana species. In the fourth clade, the CP did not carry either function. Our analysis illustrates how structural changes that likely occurred in the CP effector of progenitors of the current genera led to either silencing suppressor activity, HR elicitation in select Nicotiana species, or neither trait. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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17 pages, 3169 KiB

Open AccessArticle

Wheat streak mosaic virus P1 Binds to dsRNAs without Size and Sequence Specificity and a GW Motif Is Crucial for Suppression of RNA Silencing

by Adarsh K. Gupta and Satyanarayana Tatineni

Viruses 2019, 11(5), 472; https://doi.org/10.3390/v11050472 - 24 May 2019

Cited by 9 | Viewed by 3735

Abstract

Wheat streak mosaic virus (WSMV; genus Tritimovirus; family Potyviridae) is an economically important virus infecting wheat in the Great Plains region of the USA. Previously, we reported that the P1 protein of WSMV acts as a viral suppressor of RNA silencing. In this study, we delineated the minimal region of WSMV P1 and examined its mechanisms in suppression of RNA silencing. We found that the 25 N-terminal amino acids are dispensable, while deletion of a single amino acid at the C-terminal region completely abolished the RNA silencing suppression activity of P1. Electrophoretic mobility shift assays with in vitro expressed P1 revealed that the P1 protein formed complexes with green fluorescent protein-derived 180-nt dsRNA and 21 and 24-nt ds-siRNAs, and WSMV coat protein-specific 600-nt dsRNA. These data suggest that the P1 protein of WSMV binds to dsRNAs in a size- and sequence-independent manner. Additionally, in vitro dicing assay with human Dicer revealed that the P1 protein efficiently protects dsRNAs from processing by Dicer into siRNAs, by forming complexes with dsRNA. Sequence comparison of P1-like proteins from select potyvirid species revealed that WSMV P1 harbors a glycine-tryptophan (GW) motif at the C-terminal region. Disruption of GW motif in WSMV P1 through W303A mutation resulted in loss of silencing suppression function and pathogenicity enhancement, and abolished WSMV viability. These data suggest that the mechanisms of suppression of RNA silencing of P1 proteins of potyvirid species appear to be broadly conserved in the family Potyviridae. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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21 pages, 5602 KiB

Open AccessArticle

Identification and Analysis of Potential Genes Regulated by an Alphasatellite (TYLCCNA) that Contribute to Host Resistance against Tomato Yellow Leaf Curl China Virus and Its Betasatellite (TYLCCNV/TYLCCNB) Infection in Nicotiana benthamiana

by Chaohu Luo, Zhan Qi Wang, Xianan Liu, Liling Zhao, Xueping Zhou and Yan Xie

Viruses 2019, 11(5), 442; https://doi.org/10.3390/v11050442 - 15 May 2019

Cited by 18 | Viewed by 3353

Abstract

Recently, begomovirus/betasatellite disease complexes were found to be associated with alphasatellites, and their presence modulated disease symptoms and/or viral DNA accumulation in infected plants. However, the biological functions of alphasatellites during begomovirus/betasatellite infections remain unclear. Tomato yellow leaf curl China virus (TYLCCNV) associated with a betasatellite (TYLCCNB) is a widespread monopartite begomovirus in China. In the Yunnan province of China, the TYLCCNV/TYLCCNB disease complex is found in association with an alphasatellite (TYLCCNA). In this study, in order to explain the mechanisms underlying TYLCCNV/TYLCCNB infection and reductions in viral DNA accumulation caused by TYLCCNA, we analyzed the transcriptome profiles of Nicotiana benthamiana seedlings challenged by TYLCCNV/TYLCCNB or TYLCCNV/TYLCCNB/TYLCCNA using RNA sequencing. In total, 2272 and 1207 differentially expressed genes (DEGs) were identified to respond to TYLCCNV/TYLCCNB and TYLCCNV/TYLCCNB/TYLCCNA infections, respectively. Compared with the DEGs in the TYLCCNV/TYLCCNB-infected N. benthamiana seedlings, the number of DEGs in plants co-infected with TYLCCNV/TYLCCNB + TYLCCNA was significantly reduced. Additionally, 36 DEGs were identified to be regulated by TYLCCNA, six of which were further analyzed using the virus-induced gene silencing (VIGS) approach. Silencing of these six TYLCCNA responsive DEGs caused more severe disease symptoms and higher viral DNA accumulation levels, suggesting that TYLCCNA responsive DEGs may attenuate TYLCCNV/TYLCCNB infection. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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23 pages, 3797 KiB

Open AccessArticle

A Long Non-Coding RNA of Citrus tristeza virus: Role in the Virus Interplay with the Host Immunity

by Sung-Hwan Kang, Yong-Duo Sun, Osama O. Atallah, Jose Carlos Huguet-Tapia, Jerald D. Noble and Svetlana Y. Folimonova

Viruses 2019, 11(5), 436; https://doi.org/10.3390/v11050436 - 14 May 2019

Cited by 24 | Viewed by 4143

Abstract

During infection, Citrus tristeza virus (CTV) produces a non-coding subgenomic RNA referred to as low-molecular-weight tristeza 1 (LMT1), which for a long time has been considered as a by-product of the complex CTV replication machinery. In this study, we investigated the role of LMT1 in the virus infection cycle using a CTV variant that does not produce LMT1 (CTV-LMT1d). We showed that lack of LMT1 did not halt virus ability to replicate or form proper virions. However, the mutant virus demonstrated significantly reduced invasiveness and systemic spread in Nicotiana benthamiana as well as an inability to establish infection in citrus. Introduction of CTV-LMT1d into the herbaceous host resulted in elevation of the levels of salicylic acid (SA) and SA-responsive pathogenesis-related genes beyond those upon inoculation with wild-type (WT) virus (CTV-WT). Further analysis showed that the LMT1 RNA produced by CTV-WT or via ectopic expression in the N. benthamiana leaves suppressed SA accumulation and up-regulated an alternative oxidase gene, which appeared to mitigate the accumulation of reactive oxygen species. To the best of our knowledge, this is the first report of a plant viral long non-coding RNA being involved in counter-acting host response by subverting the SA-mediated plant defense. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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19 pages, 3209 KiB

Open AccessArticle

Nitric Oxide as a Downstream Signaling Molecule in Brassinosteroid-Mediated Virus Susceptibility to Maize Chlorotic Mottle Virus in Maize

by Ning Cao, Binhui Zhan and Xueping Zhou

Viruses 2019, 11(4), 368; https://doi.org/10.3390/v11040368 - 22 Apr 2019

Cited by 15 | Viewed by 3246

Abstract

Maize chlorotic mottle virus (MCMV) infection causes growth abnormalities in maize. Transcriptome sequencing was conducted to compare the global gene expression of MCMV-inoculated plants with that of mock-inoculated plants. Data analyses showed that brassinosteroid (BR)-associated genes were upregulated after MCMV infection. Exogenous 2,4-epibrassinolide (BL) or brassinazole (BRZ) applications indicated that BR pathway was involved in the susceptibility to MCMV infection. In addition, treatment of BL on maize induced the accumulation of nitric oxide (NO), and the changes of NO content played positive roles in the disease incidence of MCMV. Moreover, MCMV infection was delayed when the BL-treated plants were applied with NO scavenger, which suggested that BR induced the susceptibility of maize to MCMV infection in a NO-dependent manner. Further investigation showed the maize plants with knock-down of DWARF4 (ZmDWF4, a key gene of BR synthesis) and nitrate reductase (ZmNR, a key gene of NO synthesis) by virus-induced gene silencing displayed higher resistance to MCMV than control plants. Taken together, our results suggest that BR pathway promotes the susceptibility of maize to MCMV in a NO-dependent manner. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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16 pages, 3341 KiB

Open AccessArticle

The Three Essential Motifs in P0 for Suppression of RNA Silencing Activity of Potato leafroll virus Are Required for Virus Systemic Infection

by Mamun-Or Rashid, Xiao-Yan Zhang, Ying Wang, Da-Wei Li, Jia-Lin Yu and Cheng-Gui Han

Viruses 2019, 11(2), 170; https://doi.org/10.3390/v11020170 - 20 Feb 2019

Cited by 11 | Viewed by 4554

Abstract

Higher plants exploit posttranscriptional gene silencing as a defense mechanism against virus infection by the RNA degradation system. Plant RNA viruses suppress posttranscriptional gene silencing using their encoded proteins. Three important motifs (F-box-like motif, G139/W140/G141-like motif, and C-terminal conserved region) in P0 of Potato leafroll virus (PLRV) were reported to be essential for suppression of RNA silencing activity. In this study, Agrobacterium-mediated transient experiments were carried out to screen the available amino acid substitutions in the F-box-like motif and G139/W140/G141-like motif that abolished the RNA silencing suppression activity of P0, without disturbing the P1 amino acid sequence. Subsequently, four P0 defective mutants derived from a full-length cDNA clone of PLRV (L76F and W87R substitutions in the F-box-like motif, G139RRR substitution in the G139/W140/G141-like motif, and F220R substitution in the C-terminal conserved region) were successfully generated by reverse PCR and used to investigate the impact of these substitutions on PLRV infectivity. The RT-PCR and western blot analysis revealed that these defective mutants affected virus accumulation in inoculated leaves and systemic movement in Nicotiana benthamiana as well as in its natural hosts, potato and black nightshade. These results further demonstrate that the RNA silencing suppressor of PLRV is required for PLRV accumulation and systemic infection. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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11 pages, 1990 KiB

Open AccessArticle

Virus-Derived Small Interfering RNAs Affect the Accumulations of Viral and Host Transcripts in Maize

by Zihao Xia, Zhenxing Zhao, Zhiyuan Jiao, Tengzhi Xu, Yuanhua Wu, Tao Zhou and Zaifeng Fan

Viruses 2018, 10(12), 664; https://doi.org/10.3390/v10120664 - 23 Nov 2018

Cited by 12 | Viewed by 3417

Abstract

RNA silencing is a conserved surveillance mechanism against invading viruses in plants, which involves the production of virus-derived small interfering RNAs (vsiRNAs) that play essential roles in the silencing of viral RNAs and/or specific host transcripts. However, how vsiRNAs function to target viral and/or host transcripts is poorly studied, especially in maize (Zea mays L.). In this study, a degradome library constructed from Sugarcane mosaic virus (SCMV)-inoculated maize plants was analyzed to identify the cleavage sites in viral and host transcripts mainly produced by vsiRNAs. The results showed that 42 maize transcripts were possibly cleaved by vsiRNAs, among which several were involved in chloroplast functions and in biotic and abiotic stresses. In addition, more than 3000 cleavage sites possibly produced by vsiRNAs were identified in positive-strand RNAs of SCMV, while there were only four cleavage sites in the negative-strand RNAs. To determine the roles of vsiRNAs in targeting viral RNAs, six vsiRNAs were expressed in maize protoplast based on artificial microRNAs (amiRNAs), of which four could efficiently inhibit the accumulations of SCMV RNAs. These results provide new insights into the genetic manipulation of maize with resistance against virus infection by using amiRNA as a more predictable and useful approach. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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17 pages, 6047 KiB

Open AccessArticle

Non-Structural Protein NSm of Tomato Spotted Wilt Virus Is an Avirulence Factor Recognized by Resistance Genes of Tobacco and Tomato via Different Elicitor Active Sites

by Changjun Huang, Yong Liu, Haiqin Yu, Cheng Yuan, Jianmin Zeng, Lu Zhao, Zhijun Tong and Xiaorong Tao

Viruses 2018, 10(11), 660; https://doi.org/10.3390/v10110660 - 21 Nov 2018

Cited by 19 | Viewed by 4780

Abstract

Tomato spotted wilt virus (TSWV) is one of the most destructive viral pathogens of plants. Recently, a single dominant gene conferring complete resistance to TSWV (RTSW) was identified in Nicotina alata and introgressed into cultivated tobacco (N. tabacum). However, whether the TSWV carries an avirulence (Avr) factor directed against RTSW remains obscure. In the present study, we identified the non-structural protein (NSm), the movement protein of TSWV, which is an RTSW-specific Avr factor, by using two different transient expression systems. Using amino acid (aa) substitution mutants, we demonstrated the ability to induce RTSW-mediated hypersensitive response (HR) of NSm is independent of its movement function. Moreover, key substitutions (C118Y and T120N), a 21-aa viral effector epitope, and different truncated versions of NSm, which are responsible for the recognition of the Sw-5b resistance gene of tomato, were tested for their ability to trigger HR to TSWV in tobacco. Together, our results demonstrated that RTSW-mediated resistance is triggered by NSm in the same way as by Sw-5b, however, via different elicitor active sites. Finally, an Avr gene-based diagnostic approach was established and used to determine the presence and effectiveness of resistance genes in tobacco. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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Review

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16 pages, 1367 KiB

Open AccessReview

Roles of Small RNAs in Virus-Plant Interactions

by Baogang Zhang, Wenji Li, Jialin Zhang, Lu Wang and Jianguo Wu

Viruses 2019, 11(9), 827; https://doi.org/10.3390/v11090827 - 05 Sep 2019

Cited by 28 | Viewed by 5139

Abstract

Small RNAs (sRNAs), including microRNAs (miRNAs) and short interfering RNAs (siRNAs), are non-coding but powerful RNA molecules of 20–30 nucleotides in length. sRNAs play crucial regulatory roles in diverse plant biological processes. Recently, many studies on sRNAs have been reported. We summarize new findings of sRNAs in virus-plant interactions to accelerate the function analysis of sRNAs. The main content of this review article includes three parts: virus-responsive sRNAs, function analysis of sRNAs in virus pathogenicity or host resistance, and some sRNAs-mediated underlying mechanisms in virus-plant interactions. New findings of sRNAs deepen our understanding about sRNAs’ roles, which might contribute to the design of novel control measures against plant viruses. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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17 pages, 280 KiB

Open AccessReview

A New Era for Mild Strain Cross-Protection

by Katrin Pechinger, Kar Mun Chooi, Robin M. MacDiarmid, Scott J. Harper and Heiko Ziebell

Viruses 2019, 11(7), 670; https://doi.org/10.3390/v11070670 - 23 Jul 2019

Cited by 54 | Viewed by 6373

Abstract

Societal and environmental pressures demand high-quality and resilient cropping plants and plant-based foods grown with the use of low or no synthetic chemical inputs. Mild strain cross-protection (MSCP), the pre-immunization of a plant using a mild strain of a virus to protect against subsequent infection by a severe strain of the virus, fits with future-proofing of production systems. New examples of MSCP use have occurred recently. New technologies are converging to support the discovery and mechanism(s) of action of MSCP strains thereby accelerating the popularity of their use. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

12 pages, 491 KiB

Open AccessReview

Arbuscular Mycorrhizal Symbiosis Affects Plant Immunity to Viral Infection and Accumulation

by Zhipeng Hao, Wei Xie and Baodong Chen

Viruses 2019, 11(6), 534; https://doi.org/10.3390/v11060534 - 08 Jun 2019

Cited by 35 | Viewed by 6791

Abstract

Arbuscular mycorrhizal (AM) fungi, as root symbionts of most terrestrial plants, improve plant growth and fitness. In addition to the improved plant nutritional status, the physiological changes that trigger metabolic changes in the root via AM fungi can also increase the host ability to overcome biotic and abiotic stresses. Plant viruses are one of the important limiting factors for the commercial cultivation of various crops. The effect of AM fungi on viral infection is variable, and considerable attention is focused on shoot virus infection. This review provides an overview of the potential of AM fungi as bioprotection agents against viral diseases and emphasizes the complex nature of plant–fungus–virus interactions. Several mechanisms, including modulated plant tolerance, manipulation of induced systemic resistance (ISR), and altered vector pressure are involved in such interactions. We propose that using “omics” tools will provide detailed insights into the complex mechanisms underlying mycorrhizal-mediated plant immunity. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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25 pages, 1015 KiB

Open AccessReview

The Tug-of-War between Plants and Viruses: Great Progress and Many Remaining Questions

by Xiaoyun Wu, Adrian Valli, Juan Antonio García, Xueping Zhou and Xiaofei Cheng

Viruses 2019, 11(3), 203; https://doi.org/10.3390/v11030203 - 28 Feb 2019

Cited by 57 | Viewed by 7209

Abstract

Plants are persistently challenged by various phytopathogens. To protect themselves, plants have evolved multilayered surveillance against all pathogens. For intracellular parasitic viruses, plants have developed innate immunity, RNA silencing, translation repression, ubiquitination-mediated and autophagy-mediated protein degradation, and other dominant resistance gene-mediated defenses. Plant viruses have also acquired diverse strategies to suppress and even exploit host defense machinery to ensure their survival. A better understanding of the defense and counter-defense between plants and viruses will obviously benefit from the development of efficient and broad-spectrum virus resistance for sustainable agriculture. In this review, we summarize the cutting edge of knowledge concerning the defense and counter-defense between plants and viruses, and highlight the unexploited areas that are especially worth investigating in the near future. Full article

(This article belongs to the Special Issue Plant Immunity to Virus Infections)

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