HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities

Ballut, Lionel; Drucker, Martin; Pugnière, Martine; Cambon, Florence; Blanc, Stéphane; Roquet, Françoise; Candresse, Thierry; Schmid, Hans Peter; Nicolas, P.; Gall, Olivier Le; Badaoui, Saloua

doi:10.1099/vir.0.81107-0

Cited by 92 publications

(85 citation statements)

References 56 publications

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“…Interestingly, a countereffect has been uncovered by the finding that the multifunctional HcPro viral protein (Helper component Protein), a potent suppressor of RNA silencing, associates with different 20S proteasomal subunits and interferes with the RNase activity of the 20S proteasome (Ballut et al, 2005;Jin et al, 2007;Dielen et al, 2011). Moreover, Arabidopsis mutants knocked out for each of the two At-PAE genes encoding the a5 subunit of the 20S proteasome were more susceptible to infection by Lettuce mosaic potyvirus (Dielen et al, 2011).…”

Section: Viral E3 Ubiquitin Ligasesmentioning

confidence: 99%

Ubiquitination during Plant Immune Signaling

2012

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Section: Viral E3 Ubiquitin Ligasesmentioning

confidence: 99%

Ubiquitination during Plant Immune Signaling

2012

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“…HC-Pro also participates in symptom development, genome replication, and virus movement (Maia et al, 1996;Syller, 2006), whereas these capacities should be derived from its ability to suppress RNA silencing (Kasschau and Carrington, 2001;Díaz-Pendón and Ding, 2008). Furthermore, HC-Pros from different viruses have been reported to interact with various host factors and affect their functions, such as the ubiquitin/26S proteasome system (Ballut et al, 2005), the chloroplast precursor of ferredoxin-5 (Cheng et al, 2008), and chloroplast protein 1-deoxy-D-xylulose-5-phosphate synthase (Li et al, 2015).…”

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confidence: 99%

A Violaxanthin Deepoxidase Interacts with a Viral Suppressor of RNA Silencing to Inhibit Virus Amplification

et al. 2017

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RNA silencing plays a critical role against viral infection. To counteract this antiviral silencing, viruses have evolved various RNA silencing suppressors. Meanwhile, plants have evolved counter-counter defense strategies against RNA silencing suppression (RSS). In this study, the violaxanthin deepoxidase protein of maize (Zea mays), ZmVDE, was shown to interact specifically with the helper component-proteinase (HC-Pro; a viral RNA silencing suppressor) of Sugarcane mosaic virus (SCMV) via its mature protein region by yeast two-hybrid assay, which was confirmed by coimmunoprecipitation in Nicotiana benthamiana cells. It was demonstrated that amino acids 101 to 460 in HC-Pro and the amino acid glutamine-292 in ZmVDE mature protein were essential for this interaction. The mRNA levels of ZmVDE were down-regulated 75% to 65% at an early stage of SCMV infection. Interestingly, ZmVDE, which normally localized in the chloroplasts and cytoplasm, could relocalize to HC-Pro-containing aggregate bodies in the presence of HC-Pro alone or SCMV infection. In addition, ZmVDE could attenuate the RSS activity of HC-Pro in a specific protein interaction-dependent manner. Subsequently, transient silencing of the ZmVDE gene facilitated SCMV RNA and coat protein accumulation. Taken together, our results suggest that ZmVDE interacts with SCMV HC-Pro and attenuates its RSS activity, contributing to decreased SCMV accumulation. This study demonstrates that a host factor can be involved in secondary defense responses against viral infection in monocot plants.

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“…The helper component protease (HcPro) of potato virus Y can interact with three Arabidopsis 20S proteasome subunits (39). Ballut et al found that lettuce mosaic virus HcPro could interact with the Arabidopsis thaliana ␣5 subunit of the 20S proteasome, and they suggested that HcPro may modulate its RNase activity, contributing to an antiviral response (40). Recently, it was found that the HcPro protein of papaya ringspot virus (PRSV) could inhibit the catalytic activity of the host proteasome and that the inhibition was achieved through interaction with the 20S proteasome subunit ␣1 (41).…”

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Rice Stripe Tenuivirus Nonstructural Protein 3 Hijacks the 26S Proteasome of the Small Brown Planthopper via Direct Interaction with Regulatory Particle Non-ATPase Subunit 3

et al. 2015

J Virol

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The ubiquitin/26S proteasome system plays a vital role in regulating host defenses against pathogens. Previous studies have highlighted different roles for the ubiquitin/26S proteasome in defense during virus infection in both mammals and plants, but their role in the vectors that transmit those viruses is still unclear. In this study, we determined that the 26S proteasome is present in the small brown planthopper (SBPH) (Laodelphgax striatellus) and has components similar to those in plants and mammals. There was an increase in the accumulation of Rice stripe virus (RSV) in the transmitting vector SBPH after disrupting the 26S proteasome, indicating that the SBPH 26S proteasome plays a role in defense against RSV infection by regulating RSV accumulation. Yeast two-hybrid analysis determined that a subunit of the 26S proteasome, named RPN3, could interact with RSV NS3. Transient overexpression of RPN3 had no effect on the RNA silencing suppressor activity of RSV NS3. However, NS3 could inhibit the ability of SBPH rpn3 to complement an rpn3 mutation in yeast. Our findings also indicate that the direct interaction between RPN3 and NS3 was responsible for inhibiting the complementation ability of RPN3. In vivo, we found an accumulation of ubiquitinated protein in SBPH tissues where the RSV titer was high, and silencing of rpn3 resulted in malfunction of the SBPH proteasome-mediated proteolysis. Consequently, viruliferous SBPH in which RPN3 was repressed transmitted the virus more effectively as a result of higher accumulation of RSV. Our results suggest that the RSV NS3 protein is able to hijack the 26S proteasome in SBPH via a direct interaction with the RPN3 subunit to attenuate the host defense response. IMPORTANCEWe show, for the first time, that the 26S proteasome components are present in the small brown planthopper and play a role in defense against its vectored plant virus (RSV). In turn, RSV encodes a protein that subverts the SBPH 26S proteasome via direct interaction with the 26S proteasome subunit RPN3. Our results imply that the molecular arms race observed in plant hosts can be extended to the insect vector that transmits those viruses. Rice stripe virus (RSV), one of the most destructive pathogens of rice production, has been responsible for numerous epidemics since it was first described in Japan in 1897 (1-3). RSV is the type member of the Tenuivirus genus, and the viral genome consists of four single-stranded RNA segments which range in size from approximately 8.9 to 2.1 kb (4, 5). RNA 1 is negative sense and encodes a putative RNA-dependent RNA polymerase. RNAs 2, 3, and 4 are ambisense, and each contains two open reading frames (ORFs), with one on the viral RNA strand (vRNA) and the second on the viral cRNA strand (vcRNA) (6). RSV vRNA 2 encodes a membrane-associated protein that reportedly is an RNA silencing suppressor and interacts with suppressor of gene silencing 3 (SGS3) (7). vcRNA 2 encodes a glycoprotein (NSvc2) which when expressed in insect cells is displayed on the membrane su...

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HcPro, a multifunctional protein encoded by a plant RNA virus, targets the 20S proteasome and affects its enzymic activities

Abstract: absen

Cited by 92 publications

References 56 publications

Ubiquitination during Plant Immune Signaling

Ubiquitination during Plant Immune Signaling

A Violaxanthin Deepoxidase Interacts with a Viral Suppressor of RNA Silencing to Inhibit Virus Amplification

Rice Stripe Tenuivirus Nonstructural Protein 3 Hijacks the 26S Proteasome of the Small Brown Planthopper via Direct Interaction with Regulatory Particle Non-ATPase Subunit 3

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