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

Pacheco, Remedios; García-Marcos, Alberto; Manzano, Aránzazu; Lacoba, Mario Garcı́a de; Camañes, Gemma; García‐Agustín, Pilar; Díaz-Ruíz, José Ramón; Tenllado, Francisco

doi:10.1094/mpmi-11-11-0305

Cited by 58 publications

(60 citation statements)

References 59 publications

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“…Total RNA was extracted from infiltrated leaves at 3 and 6 dpa and from upper leaves at 6 and 9 dpa as described previously (10). RNA samples were separated on 1% agarose formaldehyde gels and transferred to Hybond-N membranes (Roche Molecular Biochemicals).…”

Section: Binarymentioning

confidence: 99%

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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: Binarymentioning

confidence: 99%

“…Several studies have postulated that systemic necrosis (SN) shares HR attributes, as a consequence of the delayed occurrence of biochemical and physiological events that are associated with programmed cell death (PCD) (8)(9)(10). Moreover, R proteins have been involved in some cases of SN responses associated with compatible virus interactions (6,11).…”

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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“…Leaves for autofluorescence experiments were prepared as described previously (37). The terminal deoxynucleotidyltransferasemediated dUTP nick end labeling (TUNEL) assay was performed using the in situ cell death detection kit with fluorescein (Roche Diagnostics), as described by Pacheco et al (38). Consecutive slides were treated with 4=,6-diamidino-2-phenylindole (DAPI) for nuclear staining.…”

Section: Methodsmentioning

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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“…To decipher systemic necrosis responses, Pacheco et al (2012) performed global analysis of gene expression of N. benthamiana plants after systemic necrosis was triggered by the recombinant PVX-HC-Pro virus. Comparisons of transcriptional changes associated with HR-associated necrosis during an incompatible interaction revealed striking similarities among the altered gene expression profiles in systemic necrosis and HRassociated necrosis.…”

Section: Systemic Necrosis Responsesmentioning

confidence: 99%

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?

2013

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Plants respond to pathogens using elaborate networks of genetic interactions. Recently, significant progress has been made in understanding RNA silencing and how viruses counter this apparently ubiquitous antiviral defense. In addition, plants also induce hypersensitive and systemic acquired resistance responses, which together limit the virus to infected cells and impart resistance to the noninfected tissues. Molecular processes such as the ubiquitin proteasome system and DNA methylation are also critical to antiviral defenses. Here, we provide a summary and update of advances in plant antiviral immune responses, beyond RNA silencing mechanisms-advances that went relatively unnoticed in the realm of RNA silencing and nonviral immune responses. We also document the rise of Brachypodium and Setaria species as model grasses to study antiviral responses in Poaceae, aspects that have been relatively understudied, despite grasses being the primary source of our calories, as well as animal feed, forage, recreation, and biofuel needs in the 21st century. Finally, we outline critical gaps, future prospects, and considerations central to studying plant antiviral immunity. To promote an integrated model of plant immunity, we discuss analogous viral and nonviral immune concepts and propose working definitions of viral effectors, effector-triggered immunity, and viral pathogen-triggered immunity.

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

Cited by 58 publications

References 59 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

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?

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