<scp>TGB</scp>p3 triggers the unfolded protein response and <scp>SKP</scp>1‐dependent programmed cell death

Ye, Changming; Chen, Shaorong; Payton, Mark E.; Dickman, Martin B.; Verchot, Jeanmarie

doi:10.1111/mpp.12000

Cited by 53 publications

(67 citation statements)

References 94 publications

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“…The plant UPR comprises two branches, one mediated by IRE1 and the other by ATF6-like receptors, which involves the transcription factors bZIP17 and 28 (Howell, 2013). Viral infection in plants is known to induce the IRE1 arm of UPR, which involves IRE1-mediated splicing of bZIP60 mRNA, resulting in the synthesis of a functional bZIP protein that can activate ER stress-inducible promoters in the nucleus (Ye et al, , 2013Verchot 2014). Examples include induction of bZIP60 and UPR chaperone gene expression by the ER associated movement protein of potato virus X and the turnip mosaic virus 6K2 protein-induced splicing of bZIP60 mRNA .…”

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confidence: 99%

The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

et al. 2016

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The biochemical function of the potyviral P3 protein is not known, although it is known to regulate virus replication, movement, and pathogenesis. We show that P3, the putative virulence determinant of soybean mosaic virus (SMV), targets a component of the translation elongation complex in soybean. Eukaryotic elongation factor 1A (eEF1A), a well-known host factor in viral pathogenesis, is essential for SMV virulence and the associated unfolded protein response (UPR). Silencing GmEF1A inhibits accumulation of SMV and another ER-associated virus in soybean. Conversely, endoplasmic reticulum (ER) stress-inducing chemicals promote SMV accumulation in wild-type, but not GmEF1A-knockdown, plants. Knockdown of genes encoding the eEF1B isoform, which is important for eEF1A function in translation elongation, has similar effects on UPR and SMV resistance, suggesting a link to translation elongation. P3 and GmEF1A promote each other's nuclear localization, similar to the nuclearcytoplasmic transport of eEF1A by the Human immunodeficiency virus 1 Nef protein. Our results suggest that P3 targets host elongation factors resulting in UPR, which in turn facilitates SMV replication and place eEF1A upstream of BiP in the ER stress response during pathogen infection.

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confidence: 99%

The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

et al. 2016

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“…, ; Ye et al. , ). Similarly, we propose that co‐infections of PVX with other viruses expressing strong VSRs could mimic HC‐Pro action on P25, allowing P25 to accumulate to very high levels with a detrimental effect on ER homeostasis, subsequently leading to necrosis in systemic leaves.…”

Section: Discussionmentioning

confidence: 99%

“…Previous investigations have shown that the TGB3 protein of PVX triggers UPR and elicits PCD when expressed from TMV or under the control of the CaMV 35S promoter and delivered by agroinfiltration into N. benthamiana (Ye et al. , ). These findings argue that PVX encodes at least two protein products, TGB3 and P25, capable of inducing a UPR and cell death when overexpressed by either a viral vector or in the presence of a strong VSR.…”

Section: Discussionmentioning

confidence: 99%

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Cell death triggered by the P25 protein in Potato virus X‐associated synergisms results from endoplasmic reticulum stress in Nicotiana benthamiana

Aguilar

Toro

Brosseau

et al. 2018

Molecular Plant Pathology

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The synergistic interaction of Potato virus X (PVX) with a number of potyviruses results in systemic necrosis in Nicotiana spp. Previous investigations have indicated that the viral suppressor of RNA silencing (VSR) protein P25 of PVX triggers systemic necrosis in PVX-associated synergisms in a threshold-dependent manner. However, little is still known about the cellular processes that lead to this necrosis, and whether the VSR activity of P25 is involved in its elicitation. Here, we show that transient expression of P25 in the presence of VSRs from different viruses, including the helper component-proteinase (HC-Pro) of potyviruses, induces endoplasmic reticulum (ER) stress and the unfolded protein response (UPR), which ultimately lead to ER collapse. However, the host RNA silencing pathway was dispensable for the elicitation of cell death by P25. Confocal microscopy studies in leaf patches co-expressing P25 and HC-Pro showed dramatic alterations in ER membrane structures, which correlated with the up-regulation of bZIP60 and several ER-resident chaperones, including the ER luminal binding protein (BiP). Overexpression of BiP alleviated the cell death induced by the potexviral P25 protein when expressed together with VSRs derived from different viruses. Conversely, silencing of the UPR master regulator, bZIP60, led to an increase in cell death elicited by the P25/HC-Pro combination as well as by PVX-associated synergism. In addition to its role as a negative regulator of P25-induced cell death, UPR partially restricted PVX infection. Thus, systemic necrosis caused by PVX-associated synergistic infections is probably the effect of an unmitigated ER stress following the overaccumulation of a viral protein, P25, with ER remodelling activity.

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“…Silencing SKP1 directly alters the level of virus accumulation and systemic necrosis in tobacco plants. While the role of ubiquitin in this process is not established, the role of the proteasome in viral protein turnover is inferred [48,50]. These examples of TYMV, TMV and PVX demonstrate that the UPS can be subverted by some viruses to ensure cellular homeostasis and cell survival needed by both the plant and the virus to co-exist.…”

Section: Ubiquitin Proteasome System Supporting Virus Replication mentioning

confidence: 99%

Plant Virus Infection and the Ubiquitin Proteasome Machinery: Arms Race along the Endoplasmic Reticulum

Verchot

2016

Viruses

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The endoplasmic reticulum (ER) is central to plant virus replication, translation, maturation, and egress. Ubiquitin modification of ER associated cellular and viral proteins, alongside the actions of the 26S proteasome, are vital for the regulation of infection. Viruses can arrogate ER associated ubiquitination as well as cytosolic ubiquitin ligases with the purpose of directing the ubiquitin proteasome system (UPS) to new targets. Such targets include necessary modification of viral proteins which may stabilize certain complexes, or modification of Argonaute to suppress gene silencing. The UPS machinery also contributes to the regulation of effector triggered immunity pattern recognition receptor immunity. Combining the results of unrelated studies, many positive strand RNA plant viruses appear to interact with cytosolic Ub-ligases to provide novel avenues for controlling the deleterious consequences of disease. Viral interactions with the UPS serve to regulate virus infection in a manner that promotes replication and movement, but also modulates the levels of RNA accumulation to ensure successful biotrophic interactions. In other instances, the UPS plays a central role in cellular immunity. These opposing roles are made evident by contrasting studies where knockout mutations in the UPS can either hamper viruses or lead to more aggressive diseases. Understanding how viruses manipulate ER associated post-translational machineries to better manage virus–host interactions will provide new targets for crop improvement.

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TGBp3 triggers the unfolded protein response and SKP1‐dependent programmed cell death

Cited by 53 publications

References 94 publications

The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

The Potyviral P3 Protein Targets Eukaryotic Elongation Factor 1A to Promote the Unfolded Protein Response and Viral Pathogenesis

Cell death triggered by the P25 protein in Potato virus X‐associated synergisms results from endoplasmic reticulum stress in Nicotiana benthamiana

Plant Virus Infection and the Ubiquitin Proteasome Machinery: Arms Race along the Endoplasmic Reticulum

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