<i>Cauliflower mosaic virus</i>, a Compatible Pathogen of Arabidopsis, Engages Three Distinct Defense-Signaling Pathways and Activates Rapid Systemic Generation of Reactive Oxygen Species

Love, Andrew J.; Yun, Byung‐Wook; Laval, Valérie; Loake, Gary J.; Milner, Joel J.

doi:10.1104/pp.105.066803

Cited by 178 publications

(172 citation statements)

References 69 publications

(89 reference statements)

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“…On the other hand, in plants, during tobacco mosaic virus infection, ROS signaling was found to initiate plant defense hypersensitive response (Allan et al, 2001;Yoda et al, 2003;Love et al, 2005). Interestingly, chlorella virus, a close relative of EhV within the nucleo-cytoplasmic large DNA virus family, was found to encode a superoxide dismutase protein (Kang et al, 2014).…”

Section: Modulation Of Host Ros Metabolismmentioning

confidence: 99%

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

et al. 2016

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The cosmopolitan coccolithophore Emiliania huxleyi is a unicellular eukaryotic alga responsible for vast blooms in the ocean. These blooms have immense impact on large biogeochemical cycles and are terminated by a specific large double-stranded DNA E. huxleyi virus (EhV, Phycodnaviridae). EhV infection is accompanied by induction of hallmarks of programmed cell death and production of reactive oxygen species (ROS). Here we characterized alterations in ROS metabolism and explored its role during infection. Transcriptomic analysis of ROS-related genes predicted an increase in glutathione (GSH) and H 2 O 2 production during infection. In accordance, using biochemical assays and specific fluorescent probes we demonstrated the overproduction of GSH during lytic infection. We also showed that H 2 O 2 production, rather than superoxide, is the predominant ROS during the onset of the lytic phase of infection. Using flow cytometry, confocal microscopy and multispectral imaging flow cytometry, we showed that the profound co-production of H 2 O 2 and GSH occurred in the same subpopulation of cells but at different subcellular localization. Positively stained cells for GSH and H 2 O 2 were highly infected compared with negatively stained cells. Inhibition of ROS production by application of a peroxidase inhibitor or an H 2 O 2 scavenger inhibited host cell death and reduced viral production. We conclude that viral infection induced remodeling of the host antioxidant network that is essential for a successful viral replication cycle. This study provides insight into viral replication strategy and suggests the use of specific cellular markers to identify and quantify the extent of active viral infection during E. huxleyi blooms in the ocean.

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Section: Modulation Of Host Ros Metabolismmentioning

confidence: 99%

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

et al. 2016

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“…For CaMV DNA quantitation, total DNA was isolated from four replicates using the NucleoSpin Plant II Kit (MachereyNagel), followed by qPCR with ribosomal DNA as reference essentially as described in ref. 46.…”

Section: Methodsmentioning

confidence: 99%

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

Hafrén

Macia

Love

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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232

308

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Autophagy plays a paramount role in mammalian antiviral immunity including direct targeting of viruses and their individual components, and many viruses have evolved measures to antagonize or even exploit autophagy mechanisms for the benefit of infection. In plants, however, the functions of autophagy in host immunity and viral pathogenesis are poorly understood. In this study, we have identified both anti-and proviral roles of autophagy in the compatible interaction of cauliflower mosaic virus (CaMV), a double-stranded DNA pararetrovirus, with the model plant Arabidopsis thaliana. We show that the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1) targets nonassembled and virus particle-forming capsid proteins to mediate their autophagy-dependent degradation, thereby restricting the establishment of CaMV infection. Intriguingly, the CaMV-induced virus factory inclusions seem to protect against autophagic destruction by sequestering capsid proteins and coordinating particle assembly and storage. In addition, we found that virus-triggered autophagy prevents extensive senescence and tissue death of infected plants in a largely NBR1-independent manner. This survival function significantly extends the timespan of virus production, thereby increasing the chances for virus particle acquisition by aphid vectors and CaMV transmission. Together, our results provide evidence for the integration of selective autophagy into plant immunity against viruses and reveal potential viral strategies to evade and adapt autophagic processes for successful pathogenesis. A utophagy is a conserved intracellular pathway that engages specialized double-membrane vesicles, called "autophagosomes," to enclose and transport cytoplasmic content to lytic compartments for degradation and subsequent recycling (1). Autophagosome formation relies on extensive membrane rearrangements and is mediated by the concerted action of a core set of autophagy-related proteins (ATGs) (2, 3). At basal levels, autophagy serves mainly housekeeping functions in cellular homeostasis, whereas stimulated autophagy activity facilitates adaptation to developmental and environmental stress conditions including starvation, aging, and pathogen infection (1, 4). Ample evidence now indicates that autophagy, initially recognized as a mainly bulk catabolic process, is able specifically to target and degrade a multitude of cellular structures ranging from individual and aggregated proteins to entire organelles and invading microbes (5, 6). Selectivity is provided by a growing number of autophagic adaptor or receptor proteins identified in eukaryotic organisms that recruit the cargo to the developing autophagosome through interaction with membrane-associated ATG8/LC3 proteins (7, 8). Several mammalian autophagy receptors have been implicated in the targeting of intracellular bacterial and viral pathogens in a process called "xenophagy" (8-10). For instance, the cargo receptor p62 (SQSTM1) was shown to bind directly to and mediate autophagic clearance of different viral capsid pr...

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“…Accumulation of ROS in the apoplast/cell wall compartments takes place early after the activation of the hypersensitive response (HR) (Sagi and Fluhr, 2001). Accumulation of ROS was also observed during viral compatible interactions (Riedle-Bauer, 2000;Love et al, 2005;Inaba et al, 2011;Manacorda et al, 2013). Moreover, in some plantvirus interactions, necrotic symptoms are associated with an increase of hydrogen peroxide (H 2 O 2 ) production (Inaba et al, 2011;Manacorda et al, 2013).…”

Section: Rna Interference-mediated Resistancementioning

confidence: 92%

Modulation of host plant immunity by Tobamovirus proteins

Conti

Rodríguez

Venturuzzi

et al. 2016

Ann Bot

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Background To establish successful infection, plant viruses produce profound alterations of host physiology, disturbing unrelated endogenous processes and contributing to the development of disease. In tobamoviruses, emerging evidence suggests that viral-encoded proteins display a great variety of functions beyond the canonical roles required for virus structure and replication. Among these, their modulation of host immunity appears to be relevant in infection progression.Scope In this review, some recently described effects on host plant physiology of Tobacco mosaic virus (TMV)-encoded proteins, namely replicase, movement protein (MP) and coat protein (CP), are summarized. The discussion is focused on the effects of each viral component on the modulation of host defense responses, through mechanisms involving hormonal imbalance, innate immunity modulation and antiviral RNA silencing. These effects are described taking into consideration the differential spatial distribution and temporality of viral proteins during the dynamic process of replication and spread of the virus.Conclusion In discussion of these mechanisms, it is shown that both individual and combined effects of viralencoded proteins contribute to the development of the pathogenesis process, with the host plant's ability to control infection to some extent potentially advantageous to the invading virus.

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Cauliflower mosaic virus, a Compatible Pathogen of Arabidopsis, Engages Three Distinct Defense-Signaling Pathways and Activates Rapid Systemic Generation of Reactive Oxygen Species

Cited by 178 publications

References 69 publications

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

Modulation of host ROS metabolism is essential for viral infection of a bloom-forming coccolithophore in the ocean

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

Modulation of host plant immunity by Tobamovirus proteins

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