Systemic Cell Death Is Elicited by the Interaction of a Single Gene in <i>Nicotiana clevelandii</i> and Gene VI of Cauliflower Mosaic Virus

Király, Lóránt; Cole, Anthony B.; Bourque, June E.; Schoelz, James E.

doi:10.1094/mpmi.1999.12.10.919

Cited by 54 publications

(24 citation statements)

References 44 publications

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“…Indeed, VSRs are recognized by R genes to trigger immune responses. For example, the Cauliflower mosaic virus VSR protein P6 is an avr determinant recognized by R genes in several plants (3,4). Similarly, the Tomato bushy stunt virus (TBSV) P19 silencing suppressor is also an elicitor of hypersensitive response (HR) in certain Nicotiana species (5).…”

mentioning

confidence: 99%

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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confidence: 99%

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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“…Although several studies have identified viral symptom determinants responsible for systemic necrosis, the mechanics of how they contribute to necrosis in infected plants remain poorly understood (52,53,54). Enhancement of several dioxygenase activities in response to fungal, bacterial, and viral pathogens appears to be a common feature occurring in several pathosystems (12).…”

Section: Discussionmentioning

confidence: 99%

Oxylipin Biosynthesis Genes Positively Regulate Programmed Cell Death during Compatible Infections with the Synergistic Pair Potato Virus X-Potato Virus Y and Tomato Spotted Wilt Virus

García-Marcos

Pacheco

Manzano

et al. 2013

J Virol

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One of the most severe symptoms caused by compatible plant-virus interactions is systemic necrosis, which shares common attributes with the hypersensitive response to incompatible pathogens. Although several studies have identified viral symptom determinants responsible for systemic necrosis, mechanistic models of how they contribute to necrosis in infected plants remain scarce. Here, we examined the involvement of different branches of the oxylipin biosynthesis pathway in the systemic necrosis response caused either by the synergistic interaction of Potato virus X with Potato virus Y (PVX-PVY) or by Tomato spotted wilt virus (TSWV) in Nicotiana benthamiana. Silencing either 9-lipoxygenase (LOX), 13-LOX, or ␣-dioxygenase-1 (␣-DOX-1) attenuated the programmed cell death (PCD)-associated symptoms caused by infection with either PVX-PVY or TSWV. In contrast, silencing of the jasmonic acid perception gene, COI1 (Coronatine insensitive 1), expedited cell death during infection with compatible viruses. This correlated with an enhanced expression of oxylipin biosynthesis genes and dioxygenase activity in PVX-PVY-infected plants. Moreover, the Arabidopsis thaliana double lox1 ␣-dox-1 mutant became less susceptible to TSWV infection. We conclude that oxylipin metabolism is a critical component that positively regulates the process of PCD during compatible plant-virus interactions but does not play a role in restraining virus accumulation in planta.

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“…Similarly, Atsumi and associates (2009) reported that a reduced ability to induce SN in plants infected by HC-Pro mutants of Clover yellow vein virus was accompanied by decreased virus accumulation, which correlated with a reduced suppressor activity of the mutated proteins. However, SN was not associated with enhanced levels of virus titers in N. clevelandii infected with Cauliflower mosaic virus (Király et al 1999). In plants, the proteasome harbors a ribonuclease activity which has been shown to specifically target viral RNAs (Ballut et al 2005;Dielen et al 2011).…”

Section: Pcd Is Involved In Pvx-potyvirus Synergismmentioning

confidence: 93%

“…Moreover, several studies have suggested that SN may result from a gene-for-gene interaction, in some cases through R gene recognition (Atsumi et al 2009;Kim et al 2010;Király et al 1999). In addition, perturbation of Avr-R recognition during incompatible interactions occasionally results in virus escape to distant tissues provoking systemic HR (SHR), a phenotype that resembles SN (Dinesh-Kumar et al 2000;Seo et al 2006).…”

mentioning

confidence: 99%

“…However, very little is known about how compatible viruses induce PCD-like processes, although several studies have identified viral symptom determinants responsible for SN (Burgyan et al 2000;Király et al 1999;Komatsu et al 2011). Because both types of necrosis responses share molecular and biochemical features, a comparative study could shed light on their similarities and differences.…”

mentioning

confidence: 99%

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Comparative Analysis of Transcriptomic and Hormonal Responses to Compatible and Incompatible Plant-Virus Interactions that Lead to Cell Death

Pacheco¹,

García-Marcos²,

Manzano³

et al. 2012

MPMI

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Hypersensitive response-related programmed cell death (PCD) has been extensively analyzed in various plantvirus interactions. However, little is known about the changes in gene expression and phytohormone levels associated with cell death caused by compatible viruses. The synergistic interaction of Potato virus X (PVX) with a number of Potyvirus spp. results in increased symptoms that lead to systemic necrosis (SN) in Nicotiana benthamiana. Here, we show that SN induced by a PVX recombinant virus expressing a potyviral helper componentproteinase (HC-Pro) gene is associated with PCD. We have also compared transcriptomic and hormonal changes that occur in response to a compatible synergistic virus interaction that leads to SN, a systemic incompatible interaction conferred by the Tobacco mosaic virus-resistance gene N, and a PCD response conditioned by depletion of proteasome function. Our analysis indicates that the SN response clusters with the incompatible response by the similarity of their overall gene expression profiles. However, the expression profiles of both defense-related genes and hormone-responsive genes, and also the relative accumulation of several hormones in response to SN, relate more closely to the response to depletion of proteasome function than to that elicited by the incompatible interaction. This suggests a potential contribution of proteasome dysfunction to the increased pathogenicity observed in PVX-Potyvirus mixed infections. Furthermore, silencing of coronatine insensitive 1, a gene involved in jasmonate perception, in N. benthamiana accelerated cell death induced by PVX expressing HC-Pro.

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Systemic Cell Death Is Elicited by the Interaction of a Single Gene in Nicotiana clevelandii and Gene VI of Cauliflower Mosaic Virus

Cited by 54 publications

References 44 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

Oxylipin Biosynthesis Genes Positively Regulate Programmed Cell Death during Compatible Infections with the Synergistic Pair Potato Virus X-Potato Virus Y and Tomato Spotted Wilt Virus

Comparative Analysis of Transcriptomic and Hormonal Responses to Compatible and Incompatible Plant-Virus Interactions that Lead to Cell Death

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