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Analysis of Potyvirus Terminal Protein Vpg-Transgenic Arabidopsis

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Analysis of Potyvirus Terminal Protein Vpg-Transgenic Arabidopsis Vol. 58, No 3/2011 349–353 on-line at: www.actabp.pl Regular paper Analysis of potyvirus terminal protein VPg-transgenic Arabidopsis thaliana plants Izabela Wojtal1, Paulina Piontek2, Renata Grzela1, Artur Jarmołowski2, Włodzimierz Zagórski1, and Jadwiga Chroboczek1,3* 1Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland; 2Department of Gene Expression, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland; 3Institute of Structural Biology, Grenoble, France Virus-coded VPg protein of Potato virus Y (PVY) does VPg protein interacts with potyviral RNA polymerase not have homologs apart from other VPgs. Since VPg NIb and is involved in genome replication (Schaad et al., is indispensable for the potyvirus life cycle, it appeared 1996; Fellers et al., 1998; Puustinen & Mäkinen, 2004). a good candidate for eliciting pathogen-derived resist- Furthermore, it has been found that PVA VPg can be ance to PVY. Following agroinfection used to obtain phosphorylated by plant kinases (Ivanov et al., 2001); it PVY VPg-transgenic Arabidopsis thaliana plants, only few was hypothesized that this could trigger the disassembly transgenic seeds were recovered giving rise to six trans- of infecting virions and the subsequent initiation of po- genic plants that contained the VPg gene with the cor- tyvirus protein synthesis in the infected cell (Puustinen rect sequence. They generated VPg mRNA, but VPg pro- et al., 2002). The PPV VPg has been shown to interact tein was not detected. Some plants were immune to PVY with two DEAD-box helicase-like proteins from peach infection suggesting post-transcriptional gene silencing. and Arabidopsis, which interaction is necessary for the However, the likely PVY VPg toxicity exerted at an early infection with PPV and also with TuMV (Huang et al., stage of transformed seeds development precludes its 2010). Finally, the PVA VPg interacts with fibrillarin, a use for engineering pathogen-derived resistance. nucleolar protein, whose depletion reduces accumula- tion of infectious virons (Rajamäki & Valkonen, 2009). Keywords: Potyvirus, VPg protein, transgenic plant, pathogen-de- Several studies have reported on an interaction between rived resistance the potyvirus VPg protein and the eukaryotic translation Received: 20 January, 2011; revised: 01 July, 2011; accepted: 31 initiation factor eIF4E, which is an mRNA 5 cap-bind- August, 2011; available on-line: 13 September, 2011 ing protein (Wittmann et al., 1997; Leonard et al., 2000; Duprat et al., 2002; Kang et al., 2005; Grzela et al., 2006; Khan et al., 2008). The key role of this interaction in the INTRoducTIoN virus life cycle is supported by observations that muta- tions in either VPg or in eIF4E that abolish this inter- action prevent viral infection in planta (Leonard et al., Potyviruses (genus Potyvirus) represent the largest ge- 2000; Duprat et al., 2002; Ruffel et al., 2002; Hwang et al., nus of aphid-transmitted plant-infecting viruses that in- 2009). All these data underscore the crucial role of VPg duce harmful diseases in dicot and monocot crop plants. in the virus life cycle. They have a single-stranded messenger-polarity RNA ge- nome of about 10 000 nucleotides, a poly(A) tail at the 3′ Pathogen-derived resistance (PDR) is a powerful strat- end, and the a VPg protein covalently attached to the 5′ egy to engineer plant resistance to RNA viruses (Ming terminus. The viral RNA contains a single open reading et al., 2008, and references therein). It is based on pro- frame encoding a polyprotein that is cleaved into func- tein-mediated resistance (Powell-Abel et al., 1986; Bend- tional proteins by virus-encoded proteinases (Rajamäki ahmane et al., 2007) or, more often, on RNA silencing- et al., 2004). One of the viral proteins, VPg, is a well- mediated resistance, known as posttranscriptional gene known virulence factor. Indeed, the covalent tyrosine silencing (PTGS) (Van den Boogaart et al., 2004; Lindbo residue-mediated linkage between VPg and viral RNA & Dougherty, 2005; Voinnet, 2005; Savenkov & Valko- is required for potyvirus infectivity; mutation of the ty- nen, 2002). In plants, PTGS is a gene-regulatory mecha- rosine residue abolishes viral replication (Murphy et al., nism involved in several control processes, including de- 1996). In addition, treatment of virus RNA with protei- velopment, maintenance of genome stability, and defence nase K that digests VPg significantly reduces infectivity against invasive pathogens (Matthew, 2004). This process (Redinbaugh et al., 2001). At the beginning of polypro- is initiated by double-stranded (dsRNA) or hairpin RNA tein processing VPg exists as a fusion protein NIa, also molecules (Vargas et al., 2008) and results in degradation called VPg-Pro, and is liberated in a free form after au- of cognate cytoplasmic or viral mRNA (Sijen & Kooter tocatalytic cleavage by the Pro protease. 2000; Aravin et al., 2002; Hammond et al., 2001). Dur- VPg is responsible for numerous important virus- host interactions during the viral infection cycle. It *email: [email protected]; [email protected] seems to be involved in protein synthesis and cell-to- Abbreviations: A. t., Arabidopsis thaliana (A. thaliana); dpi, days cell and long-distance movement in plant and is a de- post inoculation; eIF4E, eukaryotic initiation factor 4E; NIa, nuclear terminant of potyvirus systemic infection in certain host inclusion protein a; PPV, Plum pox potyvirus; PVA, Potato virus A; plants (Schaad et al., 1997; Lellis et al., 2002; Rajamaki PVY, Potato virus Y; TuMV, Turnip mosaic virus; VPg, genome linked & Valkonen, 2002; Dunoyer et al., 2004). Additionally, viral protein; wt, wild type 350 I. Wojtal and others 2011 ing silencing, the dsRNA is processed to short interfer- contains GFP under the control of the At2S3 seed-spe- ing RNAs (siRNA) of 21–25 nucleotides by an RNase cific promoter (Bensmihen et al., 2004). GFP expression III-like enzyme called Dicer (Ramachandran & Chen, allows selection of transgenic Arabidopsis seeds on the 2008). These siRNAs confer specificity on the endonu- basis of their fluorescence, without using any antibiotic clease-contning, RNA-induced silencing complex (RISC), or herbicide. Agrobacterium tumefaciens (ASE strain) was which targets homologous RNAs for degradation. It has transformed with pFP101VPg plasmid in the following been well established that PTGS is a major plant defense way. Competent cells were prepared from A. tumifaciens response against viruses (Ding & Voinnet, 2007) and vi- grown at 30 °C in LB medium with rifampicin (50 μg/ ruses have been described as activators as well as targets ml) and gentamycin (20 μg/ml), by a standard CaCl2 of this mechanism (Ding et al., 2004; Wang & Metzlaff, method. Competent A. tumifaciens were transformed with 2005). pFPVPg (1 μg) and plated on LB agar containing rifam- picin, gentamycin and spectinomycin (70 μg/ml). The Many examples of virus resistance and posttranscrip- presence of the VPg gene was demonstrated by cleavage tional gene silencing of endogenous or reporter genes with PstI restriction endonuclease of plasmids purified by have been described in transgenic plants containing a standard method. Recombinant A. tumefaciens was used transgenes. The PTGS mechanism is typified by the to transform wild-type A. thaliana (ecotype Columbia) by highly specific degradation of both the transgene mRNA the floral dip method (Fraley et al., 1985). and the target RNA, which contains either the same or complementary nucleotide sequences. The endogenous The first experiment generated only one transformed RNA-dependent RNA polymerase (RdRp) may synthe- seed. For the second inoculation developmentally young- size dsRNA using the transgene mRNA as a template, er plants were used, which resulted in nine transformed resulting in the activation of transgene silencing. If the seeds (F1 progeny). Since in a parallel experiment with transgene contains viral sequences, then the viral genom- the same plant and vector but with a different gene ic RNA containing these sequences cannot accumulate in about 100 seeds were obtained, the low number of VPg- the plant (Waterhouse et al., 1998). Alternatively, trans- transgenic seeds recovered suggested VPg toxicity exert- gene mRNA may hybridize to the viral (−)RNA strand ed at an early stage of transformed seed formation. (replicative form) to induce silencing, but this situation Transformed F1 seeds were planted and grown for requires infection and accumulation of a threshold level greenhouse experiments under natural daylight supple- of the viral RNA. Consequently, transgenic plants ex- mented with illumination by sodium halide lamps (pho- pressing virus-derived transgenes may by initially suscep- toperiod 16 h, temperature 20/25 °C at night/day). Only tible to homologous viruses and show typical infection six plants were recovered (designated F1_At_VPg1–6 symptoms, but new leaves developed later are symptom- lines), all morphologically similar to wt A. thaliana. How- and virus-free and resistant to subsequent infections with ever, in comparison with wild type plants, the trans- the same virus (Ratcliff et al., 1997; Hamilton et al., 2002; genic seedlings grew rather slowly. Seeds (F2 progeny) Savenkov & Valkonen, 2002; Yoo et al., 2004). from each of the F1_At_VPg lines were collected and We have shown that the VPg protein of PVY is an planted. The F2 progeny, designated F2_At_VPg lines, intrinsically unfolded protein (Grzela et al., 2008), which were screened by RT-PCR and Western
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