Analysis of <i><scp>T</scp></i><i>omato spotted wilt virus</i> <scp>NSs</scp> protein indicates the importance of the <scp>N</scp>‐terminal domain for avirulence and <scp>RNA</scp> silencing suppression

Ronde, Dryas de; Pasquier, Adrien; Shen, Ying; Butterbach, P.B.E.; Lohuis, Dick; Kormelink, Richard

doi:10.1111/mpp.12082

Cited by 79 publications

(109 citation statements)

References 42 publications

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“…The suppressor function of both the CP of Turnip crinkle virus and the NSs protein of Tomato spotted wilt virus appears to be independent of its role in elicitation of the resistance response mediated by HRT and Tsw R genes, respectively (53,54). However, other studies support the idea that triggering of the corresponding R genes requires VSR activity of the avr determinant.…”

Section: Discussionmentioning

confidence: 66%

The P25 Protein of Potato Virus X (PVX) Is the Main Pathogenicity Determinant Responsible for Systemic Necrosis in PVX-Associated Synergisms

Aguilar

Almendral

Allende

et al. 2015

J Virol

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Most plant viruses counter the RNA silencing-based antiviral defense by expressing viral suppressors of RNA silencing (VSRs). In this sense, VSRs may be regarded as virulence effectors that can be recognized by the host as avirulence (avr) factors to induce R-mediated resistance. We made use of Agrobacterium-mediated transient coexpression of VSRs in combination with Potato virus X (PVX) to recapitulate in local tissues the systemic necrosis (SN) caused by PVX-potyvirus synergistic infections in Nicotiana benthamiana. The hypersensitive response (HR)-like response was associated with an enhanced accumulation of PVX subgenomic RNAs. We further show that expression of P25, the VSR of PVX, in the presence of VSR from different viruses elicited an HR-like response in Nicotiana spp. Furthermore, the expression of P25 by a Plum pox virus (PPV) vector was sufficient to induce an increase of PPV pathogenicity that led to necrotic mottling. A frameshift mutation in the P25 open reading frame (ORF) of PVX did not lead to necrosis when coexpressed with VSRs. These findings indicate that P25 is the main PVX determinant involved in eliciting a systemic HR-like response in PVX-associated synergisms. Moreover, we show that silencing of SGT1 and RAR1 attenuated cell death in both PVX-potyvirus synergistic infection and the HR-like response elicited by P25. Our study underscores that P25 variants that have impaired ability to suppress RNA silencing cannot act as elicitors when synergized by the presence of other VSRs. These findings highlight the importance of RNA silencing suppression activity in the HR-like response elicited by VSRs in certain hosts. IMPORTANCEThe work presented here describes how the activity of the PVX suppressor P25 elicits an HR-like response in Nicotiana spp. when overexpressed with other VSR proteins. This finding suggests that the SN response caused by PVX-associated synergisms is a delayed immune response triggered by P25, once it reaches a threshold level by the action of other VSRs. Moreover, this work supports the contention that the silencing suppressor activity of PVX P25 protein is a prerequisite for HR elicitation. We propose that unidentified avr determinants could be involved in other cases of viral synergisms in which heterologous "helper" viruses encoding strong VSRs exacerbate the accumulation of the avr-encoding virus. I n host-virus interactions, RNA silencing triggered by viral double-stranded RNA (dsRNA) is a general mechanism involved in immunity against viruses (1). By analogy with the zigzag model that describes plant-microbe interactions, dsRNA and RNA silencing could be regarded as a viral pathogen-associated molecular pattern (PAMP) and PAMP-triggered immunity, respectively (2). Most viruses counter the RNA silencing-based antiviral defense by expressing viral suppressors of RNA silencing (VSRs). Therefore, VSRs may be regarded as virulence effectors that facilitate viral infection in plants. As suggested by the zigzag model, plants may have developed a countermeasure agai...

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Section: Discussionmentioning

confidence: 66%

The P25 Protein of Potato Virus X (PVX) Is the Main Pathogenicity Determinant Responsible for Systemic Necrosis in PVX-Associated Synergisms

Aguilar

Almendral

Allende

et al. 2015

J Virol

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“…Analysis of nucleotide sequences of the S segment from WT and TBR isolates suggested several substitutions in TSWV NSs protein could be responsible for Tsw resistance-breakdown [19,29] and transient expression confirmed that NSs is the avirulence protein triggering resistance in pepper cultivars carrying the gene Tsw [3,5].…”

mentioning

confidence: 99%

Complete sequence of three different biotypes of tomato spotted wilt virus (wild type, tomato Sw-5 resistance-breaking and pepper Tsw resistance-breaking) from Spain

Debreczeni

López

Aramburu³

et al. 2015

Arch Virol

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The 5'-and 3'-terminal sequences were determined using the 5'/3' RACE Kit 2ndGeneration (Roche). To avoid errors associated with RT-PCR and sequencing, each genomic region was amplified and sequenced at least twice in both directions. Table 2.The complete sequences of isolates LL-N.05, Pujol1TL3 and PVR were aligned and compared with all complete sequences available for TSWV retrieved from GenBank (Table 1) Phylogenetic trees of the nucleotide sequences of the five TSWV ORFs were inferred by the maximum likelihood (ML) method with the nucleotide substitution model best fit for each ORF and 1000 bootstrap replicates to estimate the statistical significance of each node, using the program MEGA V6.0. The phylogenetic relationships of the Spanish TSWV isolates changed for the three genomic segments, but they were very similar for the two ORFs within each segment (Fig. 1) The genetic distances among TSWV isolates were uncorrelated to biotypes (resistancebreakdown ability) or plant hosts (Fig. 1) isolates [16,19,29]. The probable cause is that resistance-breakdown seems to have occurred several times independently and involve a few nucleotide changes as for other plant viruses [4].With respect to plant hosts, some TSWV isolates were more closely related to isolates from other plant species than isolates from the same plant host. E.g isolate TSWV-4 from pepper was closely related to isolate TSWV-10 from Stellaria aquatica, and isolate TSWV-16 from tomato, but distantly related to isolate CY-CN1 from pepper ( Fig. 1). This could be due to that TSWV has similar fitness in different hosts or that only a few nucleotide changes are involved in host adaptation (fitness increase).The complete genome sequences of TSWV isolates with different ability to overcome resistance in tomato and pepper are useful for further studies to understand emergence and evolution of TSWV adaptation to new hosts genotypes which can be applied in breeding programs to develop durable and efficient resistance cultivars against TSWV.

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“…Moreover, the NSs-silencing suppressor of TSWV was shown to be critical for the induction of HR in Tsw-gene resistance pepper. However, the RNAsilencing-suppressor activity of this protein could be separated from its Avr activity (de Ronde et al, 2014). In this study, we showed that the cell-to-cell movement function of NSm could be separated from its function for HR induction.…”

Section: Tomato Spotted Wilt Virus (Tswv) Is the Type Species Ofmentioning

confidence: 74%

Plasmodesmata targeting and intercellular trafficking of Tomato spotted wilt tospovirus movement protein NSm is independent of its function in HR induction

Zhao

Jiang

Feng

et al. 2016

Journal of General Virology

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Analysis of Tomato spotted wilt virus NSs protein indicates the importance of the N‐terminal domain for avirulence and RNA silencing suppression

Cited by 79 publications

References 42 publications

The P25 Protein of Potato Virus X (PVX) Is the Main Pathogenicity Determinant Responsible for Systemic Necrosis in PVX-Associated Synergisms

The P25 Protein of Potato Virus X (PVX) Is the Main Pathogenicity Determinant Responsible for Systemic Necrosis in PVX-Associated Synergisms

Complete sequence of three different biotypes of tomato spotted wilt virus (wild type, tomato Sw-5 resistance-breaking and pepper Tsw resistance-breaking) from Spain

Plasmodesmata targeting and intercellular trafficking of Tomato spotted wilt tospovirus movement protein NSm is independent of its function in HR induction

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