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The Hcpro from the Potyviridae Family: an Enviable Multitasking Helper Component That Every Virus Would Like to Have

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The Hcpro from the Potyviridae Family: an Enviable Multitasking Helper Component That Every Virus Would Like to Have bs_bs_banner MOLECULAR PLANT PATHOLOGY (2018) 19(3), 744–763 DOI: 10.1111/mpp.12553 Review The HCPro from the Potyviridae family: an enviable multitasking Helper Component that every virus would like to have ADRIAN A. VALLI1,*, ARAIZ GALLO1 , BERNARDO RODAMILANS1 ,JUANJOSELOPEZ-MOYA 2 AND JUAN ANTONIO GARCIA 1,* 1Centro Nacional de Biotecnologıa (CNB-CSIC), Madrid 28049, Spain 2Center for Research in Agricultural Genomics (CRAG-CSIC-IRTA-UAB-UB), Campus UAB, Bellaterra, Barcelona 08193, Spain structure, RNA sequence and transmission vectors (Revers and SUMMARY Garcıa, 2015). Most potyvirids (i.e. viruses belonging to the RNA viruses have very compact genomes and so provide a Potyviridae family) have monopartite, single-stranded and unique opportunity to study how evolution works to optimize the positive-sense genomes of around 10 000 nucleotides that are use of very limited genomic information. A widespread viral encapsidated by multiple units of a single coat protein (CP) in flex- strategy to solve this issue concerning the coding space relies on uous and filamentous virus particles of 680–900 nm in length and the expression of proteins with multiple functions. Members of 11–14 nm in diameter (Kendall et al., 2008). Exceptionally, bymo- the family Potyviridae, the most abundant group of RNA viruses viruses are peculiar in this regard, as they have a bipartite genome in plants, offer several attractive examples of viral factors which that is encapsidated separately. Inside the infected cells, the viral play roles in diverse infection-related pathways. The Helper Com- RNA of potyvirids is uncoated and translated into polyproteins ponent Proteinase (HCPro) is an essential and well-characterized which are proteolytically processed by viral-encoded proteinases multitasking protein for which at least three independent func- producing, in most cases, the following mature viral gene prod- tions have been described: (i) viral plant-to-plant transmission; ucts: P1, the helper component proteinase (HCPro), P3, 6K1, CI, (ii) polyprotein maturation; and (iii) RNA silencing suppression. 6K2, NIa (VPg 1 Pro), NIb and CP. As mentioned above, bymovi- Moreover, multitudes of host factors have been found to interact ruses have two genomic RNA segments that are independently with HCPro. Intriguingly, most of these partners have not been translated. In addition to the large polyproteins, transframe prod- ascribed to any of the HCPro roles during the infectious cycle, ucts, named P3N-PIPO and P3N-ALT, which share the N-terminal supporting the idea that this protein might play even more roles region of P3, are produced from RNA variants generated via tran- than those already established. In this comprehensive review, we scriptional slippage during viral replication (Hagiwara-Komoda attempt to summarize our current knowledge about HCPro and et al., 2016; Olspert et al., 2015; Rodamilans et al., 2015). its already attributed and putative novel roles, and to discuss the Furthermore, the same mechanism is also used during the replica- similarities and differences regarding this factor in members of tion of some sweet potato potyviruses to produce an additional this important viral family. transframe product, termed P1N-PISPO, which overlaps with the P1 cistron (Mingot et al., 2016; Untiveros et al., 2016). Keywords: multifunctional proteins, proteinase, RNA silencing RNA viruses in general are known to have small and con- suppressor, transmission. densed genomes which, at least in part, might be a result of: (i) intrinsic structural restrictions (e.g. topology and stability) of the RNA molecule (Gorbalenya et al., 2006); (ii) the need to minimize the negative impact of the error-prone viral replication (Holmes, INTRODUCTION 2003); or (iii) the need to protect themselves from the action of antiviral host defence mechanisms (Eusebio-Cope and Suzuki, Members of the family Potyviridae are the most abundant and 2015). As a consequence, RNA viruses are under intense selective socio-economically relevant RNA viruses infecting plants pressure to optimize the use of their genomic information. To (Scholthof et al., 2011; Valli et al., 2015); therefore, they have cope with this restriction, they exploit diverse strategies in order been the subject of intense studies worldwide. This family is to produce/recruit all the required components to ensure infection formed by eight genera (Brambyvirus, Bymovirus, Ipomovirus, success (Ahlquist et al., 2003; Atkins et al., 2016; Firth and Brier- Macluravirus, Poacevirus, Potyvirus, Rymovirus and Tritimovirus) ley, 2012; Sztuba-Solinska et al., 2011). One of these strategies which are differentiated by their genome composition and relies on the expression of viral proteins with several functions. In *Correspondence: Email: [email protected]; [email protected] particular, the well-characterized RNA viruses of the family 744 VC 2017 BSPP AND JOHN WILEY & SONS LTD The HCPro from the Potyviridae family 745 Potyviridae provide fascinating examples of multitasking proteins artificial feeding systems, based on stretched parafilm membranes, (e.g. Sorel et al., 2014; Weber and Bujarski, 2015). Here, we pres- was instrumental in the verification that insects often failed to trans- ent a comprehensive review concerning the potyvirid HCPro, with mit the disease when purified virions were used for the transmission particular emphasis on members of the genus Potyvirus,inwhich assay (Pirone and Megahed, 1966). Hence, this result indicated that at least three clearly independent functions have been described. the viral particle alone is not sufficient for efficient transmission. Tak- ing advantage of UV radiation treatments to inactivate viral RNAs, it TRANSMISSION—A HISTORICAL OVERVIEW OF was shown that a UV-resistant component (probably a protein) must HCPro DISCOVERY be acquired by aphids simultaneously (or prior) to virions in order to Potyviruses are transmitted by aphids by a mode of transmission transmit the virus (Govier and Kassanis, 1974a,b; Kassanis and Gov- that is described as non-persistent, as it occurs rapidly, with the ier, 1971a,b). Later, equipped with very simple experimental tools, duration of acquisition and inoculation phases in the range of sec- the purification of the active factor was achieved and allowed the onds to minutes without retention periods (Bradley, 1952; Day and generation of specific antisera (Govier et al., 1977; Thornbury et al., Irzykiewicz, 1954; Kassanis, 1941). This fast and usually efficient 1985), which was certainly crucial to establish its origin as part of mode of transmission was recognized as a serious caveat in the the viral polyprotein (Carrington et al., 1989a; Dougherty and adoption of control measures against pathogenic virus dissemina- Hiebert, 1980; Hiebert et al., 1984). Indeed, antibodies against tion, because it leaves virtually no time available for effective insecti- HCPro have been very useful to establish the presence of this viral cide treatment aimed to target their vectors. Therefore, intense factor in amorphous inclusions of cells infected with some potyvi- research efforts took place to better understand potyviral transmis- ruses (De Mejia et al., 1985), as well as to unravel other aspects of sion. In this context, the role of HCPro in this process was found HCPro that will be described in diverse sections of this article. even before it was known that it was a viral protein. The name Based on results from the experiments described above, a ‘Helper Component’ was coined to describe the existence of a ‘com- molecular mechanism by which HCPro participates in the trans- ponent’ of unknown source, but present in infected plants, which mission process was suggested long ago by Govier and Kassanis ‘helped’ the transmission of potyviruses mediated by aphid vectors. (1974b). The so-called ‘bridge hypothesis’ proposes that the How this function was identified is an extraordinary story that helper component acts as a reversible link between the viral parti- reveals the resources, skills and imagination of those researchers cle and the vector mouthparts (Fig. 1). Over the years, accumula- involved in its discovery (Pirone and Thornbury, 1984). Chronologi- tive evidence has provided ample support for this hypothesis, cally, the finding of certain natural virus isolates with altered trans- whereas alternative models, such as the proposition of a direct mission properties was the first indication that this function was interaction between CP and aphid receptors with HCPro acting to genetically regulated (Kamm, 1969; Simons, 1976). The use of aphid expose CP binding sites (Salomon and Bernardi, 1995), failed to Fig. 1 ‘Bridge hypothesis’ for aphid transmission of potyviruses. Left: an aphid is feeding from an infected plant. Centre: longitudinal section of the mandibular stylet (the external flanking maxillae have been omitted to simplify the figure), including the two parallel channels (the food canal that connects to the digestive system and the salivary canal that allows secretions during feeding) joining at the common duct. Right: a helper component proteinase (HCPro) complex (depicted in a dimeric form) is bound at one end of the viral particle and allows a reversible interaction with potential receptors located over the cuticle lining (internal side of the stylet tip). It should be noted that this figure is a predictive representation of the viral transmission process based on very limited available experimental data on interactions and the consequent role of HCPro during
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