Point mutations in helper component protease of clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean

Yambao, M. L. M.; Yagihashi, Haruka; Sekiguchi, Hiroshi; Sekiguchi, T.; Sasaki, Takashi; Sato, Mitsuru; Atsumi, Go; Tacahashi, Yoko; Nakahara, Kenji; Uyeda, Ichiro

doi:10.1007/s00705-007-1073-3

Cited by 56 publications

(51 citation statements)

References 37 publications

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“…This condition is amply fulfilled by viral silencing suppressors. For example, 1 focusing only on potyviruses, it has been shown that two amino acid replacements in the HC-Pro suppressor of Clover yellow vein virus are sufficient to attenuate the symptoms and reduce virus accumulation (Yambao et al 2008), whereas a single mutation in Plum pox virus HCPro had a similar effect (González-Jara et al 2005). As a final example, mutations in the conserved motifs of Zucchini yellow mosaic virus HC-Pro also produced attenuated viruses on the natural host squash and also abolished the ability to elicit hypersensitive responses in other local lesion hosts (Lin et al 2007).…”

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confidence: 99%

From Hypo- to Hypersuppression: Effect of Amino Acid Substitutions on the RNA-Silencing Suppressor Activity of the Tobacco etch potyvirus HC-Pro

et al. 2008

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RNA silencing participates in several important functions: from the regulation of cell metabolism and organism development to sequence-specific antiviral defense. Most plant viruses have evolved proteins that suppress RNA silencing and that in many cases are multifunctional. Tobacco etch potyvirus (TEV) HCPro protein suppresses RNA silencing and participates in aphid-mediated transmission, polyprotein processing, and genome amplification. In this study, we have generated 28 HC-Pro amino acid substitution mutants and quantified their capacity as suppressors of RNA silencing in a transient expression assay. Most mutations either had no quantitative effect or completely abolished silencing suppression (10 in each class), 3 caused a significant decrease in the activity, and 5 significantly increased it, revealing an unexpected high frequency of mutations conferring hypersuppressor activity. A representative set of the mutant alleles, containing both hypo-and hypersuppressors, was further analyzed for their effect on TEV accumulation and the strength of induced symptoms. Whereas TEV variants with hyposuppressor mutants were far less virulent than wild-type TEV, those with hypersuppressor alleles induced symptoms that were not more severe than those characteristic of the wild-type virus, suggesting that there is not a perfect match between suppression and virulence. S MALL RNAs, including micro RNAs (miRNAs) and short interfering RNAs (siRNAs), are key components of an evolutionarily conserved RNA-based gene regulation system documented in fungi, plants, and animals that is implicated in various biological processes from development to antiviral defenses (Ratcliff et al. 1997;Waterhouse et al. 2001;Baulcombe 2002;Voinnet 2002;Ding et al. 2004;Chen et al. 2005;Wilkins et al. 2005;Kim and Nam 2006;Ding and Voinnet 2007). The silencing pathway is triggered by the presence of double-stranded RNAs (dsRNA) or single-stranded RNAs with stem-loop structures that are processed by several Dicer proteins into $21-to 24-nt short RNAs, including siRNAs, miRNAs, and others, which are incorporated into an RNA-induced silencing complex (RISC) to promote a sequence-specific cleavage or translation arrest of transcripts of complementary sequence (Hammond et al.

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confidence: 99%

From Hypo- to Hypersuppression: Effect of Amino Acid Substitutions on the RNA-Silencing Suppressor Activity of the Tobacco etch potyvirus HC-Pro

et al. 2008

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“…1G). In previous studies, we revealed that the HC-Pro gene is indirectly involved in the induction of lethal systemic cell death in PI 118501 (20,22,32). We found that a Cl-No.30 mutant with a D-to-Y substitution at amino acid position 193 of HC-Pro (Cl-D193Y) loses the ability to induce cell death in PI 118501 (20).…”

Section: Discussionmentioning

confidence: 93%

“…Extremely high virulence of ClYVV has been observed for many pea cultivars: ClYVV systemically induces cell death, resulting in plant death within 2 weeks when used to infect young plants (20)(21)(22) (Table 1). We previously reported that cell death induced by Cl-No.30 in pea cultivar PI 118501 is a form of an HR-like response accompanied by the activation of the salicylic acid (SA) pathway, which is one of the hallmarks of an HR (20).…”

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confidence: 99%

P3N-PIPO, a Frameshift Product from the P3 Gene, Pleiotropically Determines the Virulence of Clover Yellow Vein Virus in both Resistant and Susceptible Peas

Atsumi

Suzuki

Miyashita

et al. 2016

J Virol

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IMPORTANCEControl of plant viral disease has relied on the use of resistant cultivars; however, emerging mutant viruses have broken many types of resistance. Recently, we revealed that Cl-90-1 Br2 breaks the recessive resistance conferred by cyv1, mainly by accumulating a higher level of P3N-PIPO than that of the nonbreaking isolate Cl-No.30. Here we show that a susceptible pea line recognized the increased amount of P3N-PIPO produced by Cl-90-1 Br2 and activated the salicylic acid-mediated defense pathway, inducing lethal systemic cell death. We found a gradation of virulence among ClYVV isolates in a cyv1-carrying pea line and two susceptible pea lines. This study suggests a trade-off between breaking of recessive resistance (cyv1) and host viability; the latter is presumably regulated by the dominant Cyn1 gene, which may impose evolutionary constraints upon P3N-PIPO for overcoming resistance. We propose a working model of the host strategy to sustain the durability of resistance and control fast-evolving viruses.H ost plants protect themselves from virus infection by activating defense systems mediated by immune receptors (e.g., nucleotide-binding-site-leucine-rich-repeat [NB-LRR] proteins) (1). Plants have many NB-LRR immune receptors, each of which recognizes specific viral proteins. The activated immune response is referred to as a hypersensitive response (HR) and is often accompanied by cell death. When an HR is induced, the virus is localized in and around the infection locus. NB-LRR immune receptors are encoded by resistance genes that are genetically dominant.Another important defense against plant virus infection is genetically recessive resistance (2). The viral life cycle totally relies on host cells, and viruses require host factors in order to multiply within cells and move to neighboring cells. Therefore, the lack of a specific host-coopted factor required for the viral life cycle leads to host resistance against the virus, which would be recessively inherited. Many natural recessive resistance genes against viruses have been identified in diverse crops (2). Extensive studies have been carried out on viruses belonging to the Potyvirus genus, the major genus of the Potyviridae family, which is one of the two largest plant virus genera and is found in most climatic regions worldwide (3). These viruses infect a broad range of host plants, including both monocots and dicots. They cause considerable crop damage, resulting in severe economic losses. Most of the recessive

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“…1c, there are also reports of attenuated potyviruses (Chiang et al 2007;Lin et al 2007b;Yambao et al 2008). When an attenuated strain (HA5-1) of PRSV was compared with its parent strain HA using an infectious cDNA clone, two amino acid substitutions among three in the C-terminal region of P1 at aa positions 309 and 481, and two of four in HC-Pro at aa positions 753 and 944 of HA5-1 appear to be critical in symptom attenuation in papaya (Chiang et al 2007).…”

Section: Potyvirusmentioning

confidence: 99%

“…When an attenuated strain (HA5-1) of PRSV was compared with its parent strain HA using an infectious cDNA clone, two amino acid substitutions among three in the C-terminal region of P1 at aa positions 309 and 481, and two of four in HC-Pro at aa positions 753 and 944 of HA5-1 appear to be critical in symptom attenuation in papaya (Chiang et al 2007). In a comparison of attenuated and severe strains of Clover yellow vein virus (ClYVV), two amino acid substitutions in HC-Pro were found to be responsible for symptom attenuation (Yambao et al 2008). Both mutations caused weaker RNA silencing suppression than the wild type did, suggesting a correlation between viral virulence and silencing suppression activity.…”

Section: Potyvirusmentioning

confidence: 99%

Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism

Nishiguchi

Kobayashi

2011

J Gen Plant Pathol

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Attenuated viruses have been isolated and studied not only as a practical means of controlling virus diseases but also to gain a molecular understanding of viral virulence and cross protection. They have been isolated from crop fields and generated through high/low temperature treatment or by mutagens such as nitrous acid and ultraviolet irradiation. Some viruses have been beneficially used in fields and evaluated for one or more decades. Molecular genetic studies on attenuated viruses have revealed that amino acid substitutions are located in replicase and the movement protein in tobamovirus, protein 2b for cucumovirus, and P1 and HC-Pro for potyvirus. In most cases, with a few exceptions, symptom attenuation is positively correlated with a reduced level of RNA silencing suppression. Molecular mechanisms underlying virus attenuation and cross protection and the rationale for practical use of attenuated viruses for effective virus disease control are discussed.

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Point mutations in helper component protease of clover yellow vein virus are associated with the attenuation of RNA-silencing suppression activity and symptom expression in broad bean

Cited by 56 publications

References 37 publications

From Hypo- to Hypersuppression: Effect of Amino Acid Substitutions on the RNA-Silencing Suppressor Activity of the Tobacco etch potyvirus HC-Pro

From Hypo- to Hypersuppression: Effect of Amino Acid Substitutions on the RNA-Silencing Suppressor Activity of the Tobacco etch potyvirus HC-Pro

P3N-PIPO, a Frameshift Product from the P3 Gene, Pleiotropically Determines the Virulence of Clover Yellow Vein Virus in both Resistant and Susceptible Peas

Attenuated plant viruses: preventing virus diseases and understanding the molecular mechanism

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