Identification of the domains of cauliflower mosaic virus protein P6 responsible for suppression of RNA silencing and salicylic acid signalling

Laird, Janet; McInally, Carol; Carr, Craig; Doddiah, Sowjanya; Yates, Gary; Chrysanthou, Elina; Khattab, Ahmed; Love, Andrew J.; Geri, C.; Sadanandom, Ari; Smith, Brian O.; Kobayashi, Kappei; Milner, Joel J.

doi:10.1099/vir.0.057729-0

Cited by 50 publications

(61 citation statements)

References 68 publications

(134 reference statements)

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“…CaMV Tav has been well studied not only as a translational transactivator and the major component of CaMV (Hohn and Rothnie 2013), but also as a pathogenesis factor that determines the viral host range (Hapiak et al 2008;Schoelz et al 1986;Wintermantel et al 1993) and symptom expression (Kobayashi and Hohn 2004), most likely through the regulation of host innate immunity (Love et al 2012) and RNA silencing (Haas et al 2008;Laird et al 2013;Love et al 2007a). In transgenic Arabidopsis thaliana, Tav enhances the expression of jasmonic acid (JA) responsive genes and resistance to necrotrophic fungi and suppresses the salicylic acid (SA) response, basal resistance and gene-for-gene resistance to hemibiotrophic bacteria and SA-dependent, Tomato bushy stunt virus (TBSV) P19-mediated cell death, probably by affecting NPR1 function (Love et al 2012).…”

Section: Introductionmentioning

confidence: 98%

Cauliflower mosaic virus Tav protein induces leaf chlorosis in transgenic tobacco through a host response to virulence function of Tav

et al. 2015

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To study the precise mechanisms underlying the chlorosis caused by plant viruses, we previously established a synchronous experimental system using transgenic plants expressing Cauliflower mosaic virus multifunctional protein, Tav (transactivator/viroplasmin), under the control of an artificially inducible promoter. Shortly after the induction of Tav expression, pathogenesis-related protein (PR) 1a gene expression is upregulated in the transgenic tobacco lines, which show visible chlorosis within a week. The present study showed that the expression of Tav also induces some salicylic acid (SA)-and ethylene-responsive PR genes. In contrast to transiently expressed Tav, which suppressed Agrobacterium-induced and SA-induced PR1a expression, the artificial induction of Tav from the transgene did not affect SAinduced PR1a expression, rather it alone induced PR1a expression. In a deletion analysis, chlorosis and PR1a induction function in transgenic tobacco were mapped to a region in Tav that had been shown to have a role in pathogenesis in a susceptible host, elicitation of the hypersensitive response in a resistant host, suppression of RNA silencing, and the suppression of Tomato bushy stunt virus P19-mediated cell death in tobacco. The results suggest that Tav-induced chlorosis results from a host response, which accompanies PR1a induction, to pathogenic function of Tav.

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Section: Introductionmentioning

confidence: 98%

Cauliflower mosaic virus Tav protein induces leaf chlorosis in transgenic tobacco through a host response to virulence function of Tav

et al. 2015

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“…P6 and P4 of CaMV (Cabb B-JI) were cloned into pENTR/D-TOPO and further recombined into pGWB5 (P6) and pGWB606 (P4), resulting in the fusion constructs 35S:P6-GFP (as described previously in ref. 42) and 35S:GFP-P4, respectively. The binary plasmids were electroporated into Agrobacterium tumefaciens strain GV3101 and were transformed into Col-0 WT or atg5 plants using the floral dip method (43).…”

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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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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“…In systemically infected leaves, cells contain one or a few, very large CaMV IBs (Shalla et al, 1980), and the infection front would have already moved through that tissue. By contrast, upon agroinfiltration of P6-GFP, plant cells contain numerous, small I-LBs that are capable of moving on microfilaments (Harries et al, 2009a;Angel et al, 2013;Laird et al, 2013). Larger P6-GFP I-LBs are also present in the cell, but they tend to be stationary (Angel et al, 2013).…”

Section: Discussionmentioning

confidence: 98%

“…P6 functions as an avirulence determinant in some solanaceous and cruciferous species (Daubert et al, 1984;Schoelz et al, 1986;Hapiak et al, 2008) and is a chlorosis symptom determinant in susceptible hosts (Daubert et al, 1984;Baughman et al, 1988;Goldberg et al, 1991;Cecchini et al, 1997). Finally, P6 has the capacity to compromise host defenses, as it is a suppressor of RNA silencing and cell death (Love et al, 2007;Haas et al, 2008), and it modulates signaling by salicylic acid, jasmonic acid, ethylene, and auxin (Geri et al, 2004;Love et al, 2012;Laird et al, 2013). Domain D1 of P6 has been shown to be necessary but not sufficient for suppression of silencing and salicylic acid-mediated defenses (Laird et al, 2013).…”

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confidence: 99%

“…Finally, P6 has the capacity to compromise host defenses, as it is a suppressor of RNA silencing and cell death (Love et al, 2007;Haas et al, 2008), and it modulates signaling by salicylic acid, jasmonic acid, ethylene, and auxin (Geri et al, 2004;Love et al, 2012;Laird et al, 2013). Domain D1 of P6 has been shown to be necessary but not sufficient for suppression of silencing and salicylic acid-mediated defenses (Laird et al, 2013).…”

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Association of the P6 Protein of Cauliflower mosaic virus with Plasmodesmata and Plasmodesmal Proteins

et al. 2014

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The P6 protein of Cauliflower mosaic virus (CaMV) is responsible for the formation of inclusion bodies (IBs), which are the sites for viral gene expression, replication, and virion assembly. Moreover, recent evidence indicates that ectopically expressed P6 inclusion-like bodies (I-LBs) move in association with actin microfilaments. Because CaMV virions accumulate preferentially in P6 IBs, we hypothesized that P6 IBs have a role in delivering CaMV virions to the plasmodesmata. We have determined that the P6 protein interacts with a C2 calcium-dependent membrane-targeting protein (designated Arabidopsis [Arabidopsis thaliana] Soybean Response to Cold [AtSRC2.2]) in a yeast (Saccharomyces cerevisiae) two-hybrid screen and have confirmed this interaction through coimmunoprecipitation and colocalization assays in the CaMV host Nicotiana benthamiana. An AtSRC2.2 protein fused to red fluorescent protein (RFP) was localized to the plasma membrane and specifically associated with plasmodesmata. The AtSRC2.2-RFP fusion also colocalized with two proteins previously shown to associate with plasmodesmata: the host protein Plasmodesmata-Localized Protein1 (PDLP1) and the CaMV movement protein (MP). Because P6 I-LBs colocalized with AtSRC2.2 and the P6 protein had previously been shown to interact with CaMV MP, we investigated whether P6 I-LBs might also be associated with plasmodesmata. We examined the colocalization of P6-RFP I-LBs with PDLP1-green fluorescent protein (GFP) and aniline blue (a stain for callose normally observed at plasmodesmata) and found that P6-RFP I-LBs were associated with each of these markers. Furthermore, P6-RFP coimmunoprecipitated with PDLP1-GFP. Our evidence that a portion of P6-GFP I-LBs associate with AtSRC2.2 and PDLP1 at plasmodesmata supports a model in which P6 IBs function to transfer CaMV virions directly to MP at the plasmodesmata.Through the years, numerous studies have focused on the characterization of viral replication sites within the cell, as well as how plant virus movement proteins (MPs) modify the plasmodesmata to facilitate cell-tocell movement (for review, see Benitez-Alfonso et al.,

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Identification of the domains of cauliflower mosaic virus protein P6 responsible for suppression of RNA silencing and salicylic acid signalling

Cited by 50 publications

References 68 publications

Cauliflower mosaic virus Tav protein induces leaf chlorosis in transgenic tobacco through a host response to virulence function of Tav

Cauliflower mosaic virus Tav protein induces leaf chlorosis in transgenic tobacco through a host response to virulence function of Tav

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

Association of the P6 Protein of Cauliflower mosaic virus with Plasmodesmata and Plasmodesmal Proteins

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