Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection

Zhou, Tao; Murphy, Alex M.; Lewsey, Mathew G.; Westwood, Jack H.; Zhang, Heng-Mu; González, Inmaculada; Canto, Tomás; Carr, John P.

doi:10.1099/vir.0.063461-0

Cited by 39 publications

(35 citation statements)

References 40 publications

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“…Systemic infection of susceptible plants by certain compatible viruses, for example during the infection of nn genotype tobacco by TMV, does not result in increased SA biosynthesis by the host (Malamy et al ., ). However, cauliflower mosaic virus (CaMV) (Love et al ., ), cucumber mosaic virus (Zhou et al ., ), potato virus Y (Krečič‐Stres et al ., ) and turnip mosaic virus (Whitham et al ., ) induce increased SA accumulation and SA‐responsive gene expression as they spread through their susceptible hosts. SCMV infection was previously reported to cause SA accumulation in maize inbred lines (Wu et al ., ), but the role of SA in SCMV–maize interactions was not clarified.…”

Section: Resultsmentioning

confidence: 99%

“…SCMV infection induced endogenous SA accumulation in maize plants and increased expression of the SA‐regulated genes ZmPR1 and ZmPR5 . Increases in SA accumulation have been observed in several compatible plant–virus interactions (Krečič‐Stres et al ., ; Love et al ., ; Whitham et al ., ; Wu et al ., ; Zhou et al ., ). Results of a previous study suggested an increase in SA in maize infected by SCMV (Wu et al ., ) but the role of SA in SCMV infection remains unclear.…”

Section: Discussionmentioning

confidence: 97%

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Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

Wen

Jiang

et al. 2019

Molecular Plant Pathology

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Summary Sugarcane mosaic virus (SCMV) is a pathogen of worldwide importance that causes dwarf mosaic disease on maize (Zea mays). Until now, few maize genes/proteins have been shown to be involved in resistance to SCMV. In this study, we characterized the role of maize phenylalanine ammonia‐lyases (ZmPALs) in accumulation of the defence signal salicylic acid (SA) and in resistance to virus infection. SCMV infection significantly increased SA accumulation and expression of SA‐responsive pathogenesis‐related protein genes (PRs). Interestingly, exogenous SA treatment decreased SCMV accumulation and enhanced resistance. Both reverse transcription‐coupled quantitative PCR and RNA‐Seq data confirmed that expression levels of at least four ZmPAL genes were significantly up‐regulated upon SCMV infection. Knockdown of ZmPAL expression led to enhanced SCMV infection symptom severity and virus multiplication, and simultaneously resulted in decreased SA accumulation and PR gene expression. Intriguingly, application of exogenous SA to SCMV‐infected ZmPAL‐silenced maize plants decreased SCMV accumulation, showing that ZmPALs are required for SA‐mediated resistance to SCMV infection. In addition, lignin measurements and metabolomic analysis showed that ZmPALs are also involved in SCMV‐induced lignin accumulation and synthesis of other secondary metabolites via the phenylpropanoid pathway. In summary, our results indicate that ZmPALs are required for SA accumulation in maize and are involved in resistance to virus infection by limiting virus accumulation and moderating symptom severity.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 97%

Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

Wen

Jiang

et al. 2019

Molecular Plant Pathology

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“…It was shown that CaMV P6 suppressor inhibits SA-induced gene expression through NPR1 (Laird et al, 2013;Love et al, 2012). Upon CMV but not CMVΔ2b suppressor mutant strain infection the SA levels accumulated Zhou et al, 2014). 2b was shown to have a dual action: it inhibited expression of few SA-regulated genes but in the same time enhanced the effect of SA on others.…”

Section: Connecting Antiviral Silencing To Hormone Signalingmentioning

confidence: 97%

viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

2015

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RNA silencing is a homology-dependent gene inactivation mechanism that regulates a wide range of biological processes including antiviral defense. To deal with host antiviral responses viruses evolved mechanisms to avoid or counteract this, most notably through expression of viral suppressors of RNA silencing. Besides working as silencing suppressors, these proteins may also fulfill other functions during infection. In many cases the interplay between the suppressor function and other "unrelated" functions remains elusive. We will present host factors implicated in antiviral pathways and summarize the current status of knowledge about the diverse viral suppressors' strategies acting at various steps of antiviral silencing in plants. Besides, we will consider the multi-functionality of these versatile proteins and related biochemical processes in which they may be involved in fine-tuning the plant-virus interaction. Finally, we will present the current applications and discuss perspectives of the use of these proteins in molecular biology and biotechnology.

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“…Since CMV infection has been reported to induce salicylic acid signaling in this study (Fig. 4) and previously (44,68,69), one may expect that rgs-CaM autoactivates its antiviral function for SAR during CMV infection via its perception of CMV 2b. However, rgs-CaM did not effectively inhibit CMV infection in relatively young plants (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…8A). CMV 2b has been reported to interfere with salicylic acid and jasmonic acid signaling (44,68,69). Ca 2ϩ influx induced by A23187 caused rgs-CaM protein accumulation in both wild-type and 2b-expressing transgenic plants (Fig.…”

Section: Discussionmentioning

confidence: 99%

rgs-CaM Detects and Counteracts Viral RNA Silencing Suppressors in Plant Immune Priming

Jeon

Tadamura

Murakami

et al. 2017

J Virol

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Primary infection of a plant with a pathogen that causes high accumulation of salicylic acid in the plant typically via a hypersensitive response confers enhanced resistance against secondary infection with a broad spectrum of pathogens, including viruses. This phenomenon is called systemic acquired resistance (SAR), which is a plant priming for adaption to repeated biotic stress. However, the molecular mechanisms of SAR-mediated enhanced inhibition, especially of virus infection, remain unclear. Here, we show that SAR against cucumber mosaic virus (CMV) in tobacco plants (Nicotiana tabacum) involves a calmodulin-like protein, rgs-CaM. We previously reported the antiviral function of rgs-CaM, which binds to and directs degradation of viral RNA silencing suppressors (RSSs), including CMV 2b, via autophagy. We found that rgs-CaM-mediated immunity is ineffective against CMV infection in normally growing tobacco plants but is activated as a result of SAR induction via salicylic acid signaling. We then analyzed the effect of overexpression of rgsCaM on salicylic acid signaling. Overexpressed and ectopically expressed rgs-CaM induced defense reactions, including cell death, generation of reactive oxygen species, and salicylic acid signaling. Further analysis using a combination of the salicylic acid analogue benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) and the Ca 2ϩ ionophore A23187 revealed that rgs-CaM functions as an immune receptor that induces salicylic acid signaling by simultaneously perceiving both viral RSS and Ca 2ϩ influx as infection cues, implying its autoactivation. Thus, secondary infection of SAR-induced tobacco plants with CMV seems to be effectively inhibited through 2b recognition and degradation by rgs-CaM, leading to reinforcement of antiviral RNA silencing and other salicylic acid-mediated antiviral responses.IMPORTANCE Even without an acquired immune system like that in vertebrates, plants show enhanced whole-plant resistance against secondary infection with pathogens; this so-called systemic acquired resistance (SAR) has been known for more than half a century and continues to be extensively studied. SAR-induced plants strongly and rapidly express a number of antibiotics and pathogenesis-related proteins targeted against secondary infection, which can account for enhanced resistance against bacterial and fungal pathogens but are not thought to control viral infection. This study showed that enhanced resistance against cucumber mosaic virus is caused by a tobacco calmodulin-like protein, rgs-CaM, which detects and counteracts the major viral virulence factor (RNA silencing suppressor) after SAR induction. rgs-CaM-mediated SAR illustrates the growth versus defense trade-off in plants, as it targets the major virulence factor only under specific biotic stress conditions, thus avoiding the cost of constitutive activation while reducing the damage from virus infection.

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Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection

Cited by 39 publications

References 40 publications

Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence

rgs-CaM Detects and Counteracts Viral RNA Silencing Suppressors in Plant Immune Priming

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