Host‐dependent differences during synergistic infection by Potyviruses with potato virus X

González-Jara, Pablo; Tenllado, Francisco; Martínez‐García, Belén; Atencio, Félix A.; Barajas, Daniel; Vargas, Marisol; Díaz-Ruíz, José Ramón

doi:10.1111/j.1364-3703.2004.00202.x

Cited by 73 publications

(45 citation statements)

References 33 publications

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“…Synergy is often manifested by a remarkable increase in both virus accumulation and symptom expression, compared to single infections. The beststudied synergistic interaction involves Potato virus X (PVX) with a number of potyviruses in tobacco (Nicotiana tabacum) plants, in which the level of PVX is enhanced severalfold compared to its level in singly infected plants (16,17). Potyvirus-associated synergistic diseases have been suggested to result from suppression of the host defense mechanism based on RNA silencing by the potyviral VSR, helper component-proteinase (HC) protein (18).…”

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confidence: 99%

“…Potyvirus-associated synergistic diseases have been suggested to result from suppression of the host defense mechanism based on RNA silencing by the potyviral VSR, helper component-proteinase (HC) protein (18). However, the accumulation of PVX genomic RNA (gRNA) did not increase greatly in N. benthamiana when doubly infected with PVX and either Plum pox virus (PPV) or Tobacco etch virus (TEV), despite the extreme enhancement of symptoms in this host that lead to SN, i.e., synergism in pathology (16,19). PVX-mediated expression of viral genes to determine whether a protein would function as a pathogenicity determinant is a wellestablished technique (17,20).…”

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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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confidence: 99%

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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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“…Previous studies showed an increase of PVX in mixed infection of PVY and PVX compared to the single inoculations [32,40]. Whereas, González-Jara et al [11] reported that PVY and PVX mixed infection did not cause a considerable increase in the accumulation of PVX in N. benthamiana though the severe symptoms like necrosis of leaves and stems leading up to the death of plants. Similar observations were also reported for PVX in mixed infections with O and NTN strain of PVY [29].…”

Section: Discussionmentioning

confidence: 88%

Expression of symptoms, viral coat protein and silencing suppressor gene during mixed infection of a N–Wi strain of potato virus Y and an asymptomatic strain of potato virus X

Senanayake

Mandal

2014

VirusDis.

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Potato virus Y (PVY) and potato virus X (PVX), the RNA viruses of two different genera results into synergistic interactions on mixed infection. In this study, a N-Wi strain of PVY and a PVX strain that is asymptomatic on potato were used to study their interactions during mixed infection in Nicotiana benthamiana and Nicotiana tabacum with reference to symptom expression, level of coat protein (CP) using ELISA and suppressor gene using real time PCR under high temperature (26-40°C) and low temperature (5-25°C) conditions. Both mixed and single infection caused severe necrosis and death of N. benthamiana plants. Single infection of these viruses in N. tabacum showed mild symptoms but mixed infection caused more severe symptoms. Synergistic symptoms were more pronounced under low temperature conditions than at high temperature. In low temperature conditions, the CP level of PVX in N. benthamiana was twofold higher than PVY and both the viruses reached at peak at 28 dpi in single virus infection. When PVY and PVX inoculated together, the CP levels of both the viruses increased and reached to the peak earlier (within 7-14 days) than that in the single virus inoculation. Although, the CP level of PVX was higher than PVY in mixed infection, at later stage (28 dpi) both the CP level declined to the similar level. The level of p25 suppressor gene was higher than HCPro in single inoculation. However, under mixed inoculation of PVY and PVX, expression of p25 was declined to the level of HC-Pro when the CP levels of both the virus also were observed to decline. The expression pattern of CP and suppressor gene was different in plants when mixed infection was created by inoculation of one virus followed by the other. This study showed the level of CP and suppressor gene of specific strain of PVY and PVX during their mixed infection in tobacco.

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“…N. benthamiana plants were grown in a growth chamber with a 16-h-light/8-h-dark cycle at 25°C. Four-week-old N. benthamiana plants were inoculated by rubbing plant sap infected with PVX, PVY, or Tomato spotted wilt virus (TSWV) onto two fully expanded leaves as described previously (33). Mixed inoculations were performed separately on opposite halves of the same leaves.…”

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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Host‐dependent differences during synergistic infection by Potyviruses with potato virus X

Cited by 73 publications

References 33 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

Expression of symptoms, viral coat protein and silencing suppressor gene during mixed infection of a N–Wi strain of potato virus Y and an asymptomatic strain of potato virus X

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

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