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Plant Molecular Responses to Potato Virus Y: a Continuum of Outcomes from Sensitivity and Tolerance to Resistance

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Plant Molecular Responses to Potato Virus Y: a Continuum of Outcomes from Sensitivity and Tolerance to Resistance viruses Review Plant Molecular Responses to Potato Virus Y: A Continuum of Outcomes from Sensitivity and Tolerance to Resistance , Špela Baebler * y , Anna Coll y and Kristina Gruden National Institute of Biology, Veˇcnapot 111, 1000 Ljubljana, Slovenia; [email protected] (A.C.); [email protected] (K.G.) * Correspondence: [email protected] These authors contributed equally to this work. y Received: 31 January 2020; Accepted: 13 February 2020; Published: 15 February 2020 Abstract: Potato virus Y (PVY) is the most economically important virus affecting potato production. PVY manipulates the plant cell machinery in order to successfully complete the infecting cycle. On the other side, the plant activates a sophisticated multilayer immune defense response to combat viral infection. The balance between these mechanisms, depending on the plant genotype and environment, results in a specific outcome that can be resistance, sensitivity, or tolerance. In this review, we summarize and compare the current knowledge on molecular events, leading to different phenotypic outcomes in response to PVY and try to link them with the known molecular mechanisms. Keywords: Potato virus Y; Potyviridae; potato; Solanum tuberosum; Solanaceae; plant immune signaling; plant hormones; tolerance; susceptibility; resistance 1. Introduction Potato virus Y (PVY) is the most economically important virus affecting potato production worldwide [1]. It severely affects potato production in terms of crop yield and quality, which, in the case of secondary infections, can reach yield reductions up to 85% [2,3]. The virus is also infecting other agronomically important crops from the Solanaceae family such as tobacco, pepper, and tomato. The fact that PVY is transmitted by 65 different aphid species in a nonpersistent manner makes the control and prevention an ongoing challenge [4]. PVY, a member of the genus Potyvirus, family Potyviridae is a flexuous rod-shaped virus with a 9.7 kb positive-sense single-stranded RNA (ssRNA) genome which contains two open reading frames (ORF) encoding 11 functional proteins. One large ORF encodes a polyprotein that is cleaved by virus-specific proteases into 10 functional proteins. In addition, the protein P3N-PIPO is produced by a short overlapping coding sequence [5]. The virions have the RNA genome encapsidated by multiple copies of the coat protein (CP) and covalently linked at the 50 end to the viral protein genome-linked (VPg). The high-resolution cryoelectron microscopy structure of the PVY virions was recently determined and it showed a left-handed helical arrangement of CPs assembled around viral ssRNA. The structure of CP revealed its intrinsic plasticity, which is most pronounced within extended terminal regions [6]. This plasticity might explain the multifunctional nature of the CP. In fact, this viral structural protein is involved in several steps of virus infection, including assembly, replication and translation, cell-to-cell movement, and long-distance transport [7–9]. Similarly, other viral proteins are multifunctional and involved in several stages of the viral cycle by establishing dynamic interactions with viral proteins, RNA and host proteins [10,11]. The complex interaction between plants and viruses includes the interplay of several mechanisms: (1) Viral hijacking of host factors required for efficient infection, (2) mechanisms of plant defense, Viruses 2020, 12, 217; doi:10.3390/v12020217 www.mdpi.com/journal/viruses Viruses 2020, 12, 217 2 of 17 Viruses 2020, 12, x FOR PEER REVIEW 2 of 17 plantand (3) defense, mechanisms and (3) of mechanisms viral counterdefense, of viral counterdefens to circumvente, plantto circumvent defense. plant The balance defense. between The balance these betweenmechanisms these defines mechanisms a specific define outcomes a specific that outcome can be beneficial that can be for beneficial the virus fo (compatibler the virus (compatible interaction) interaction)or for the plant or for(incompatible the plant (incompatible interaction). interaction). In thecase In the of case compatible of compatible interaction, interaction, thevirus the virus can canmultiply multiply and spreadand spread within within the plant; the plant; in susceptible in susceptible plants, plants, local and local systemic and systemic symptoms symptoms appear, appear,while tolerant while tolerant genotypes genotypes develop develop no or very no mildor very symptoms mild symptoms (i.e., earlier (i.e., senescence earlier senescence of infected of infectedleaves [12 leaves]). In an [12] incompatible). In an incompatible interaction, the interaction, defense response the defen restrictsse therespo viralnse multiplication restricts the and viral/or multiplicationspread. There areand/or three spread. forms ofThere resistance are three against forms PVY: of Extremeresistance resistance against PVY: (ER), susceptibilityExtreme resistance genes (ER),(S-genes)-conferred susceptibility genes resistance, (S-genes) with- noconferred visible symptomsresistance, orwith very no limited visible necrosis, symptoms and or hypersensitive very limited necrosis,response (HR)-conferredand hypersensitive resistance, respo whichnse (HR) is manifested-conferred by resistance, the formation which of local is manifested necrotic lesions by [the13]. formationIn potato, ER,of local HR, necrotic tolerant, lesions and susceptibility [13]. In potato responses, ER, HR, are tolerant described, and (Figure susceptibility1) but no responses example are of describednatural S-gene (Figure mediated 1) but no resistance example is of currently natural S known.-gene mediated resistance is currently known. Figure 1. Outcomes of potato-potato virus Y (PVY) interaction. Outcomes depend on the host genotype, Figureviral strain, 1. Outcomes and environmental of potato-potato conditions, virus andY (PVY) are manifested interaction. as Outcomes different responsesdepend on in the terms host of genotype,virus multiplication viral strain, and and disease environmental symptoms’ conditions, development. and are Photos manifested present as symptoms different appearingresponses onin termsthe inoculated of virus leavesmultiplication 6 days after and inoculation disease symptoms’ in selected potatodevelopment cultivars. Photos in optimal present environmental symptoms appearingconditions. on Examples the inoculated of viral leaves strains 6 that days give after the inoculation same outcome in selected are shown potato for eachcultivars cultivar. in opti Scalemal= environmental1 cm. conditions. Examples of viral strains that give the same outcome are shown for each cultivar. Scale = 1 cm. The outcome of the interaction depends on the potato genotype, the environment, and the viral strain.The Potato outcome cultivars of the have interaction different depends genetic backgrounds,on the potato resultinggenotype, in the diff environmenterent responses, and to thethe virus.viral strain.It was shownPotato cultivars that a single have mutation different can genetic shift thebackgrounds, outcome [ 14resulting]. On the in other different hand, responses studies ofto PVY the virus.strains It showed was shown an exceptional that a single diversification mutation can viashift nucleotide the outcome mutation [14]. On and the genome other hand, recombination studies of PVYresulting strains in new showed strains andan isolatesexceptional with didiversificationfferent degrees ofvia pathogenicity nucleotide [1mutation,15–17]. Often, and outcomesgenome recomof thebination interaction resulting in the samein new potato strains genotype and isolates are di withfferent, different depending degrees on of PVY pathogenicity strain, as was [1,15 shown–17]. Often,for PVY outcomesN and PVY ofNTN thein interaction cvs. Igor andin the Nadine same [18 potato] and PVYgenotypeN-Wilga areand different, PVYNTN dependingin cv. Etola on [19 ].PVY On N605 NTN strain,the other as was hand, shown the appearance for PVYN and of symptoms PVYNTN in didcvs. not Igor di andffer inNadin HR responsee [18] and to PVY PVYN-Wilga -GFP,and PVY PVYNTN in, cv.and Etola PVY N-Wilga[19]. Onin cv.the Rywal other [hand,20]. There the appearance are also many of examplessymptoms that did the not outcome differ in of theHR interactionresponse to is PVaffectedYN605-GFP, by abiotic PVY environmentalNTN, and PVYN- factorsWilga in [21cv.] andRywal in mixed[20]. There infections are withalso othermany virusesexamples ([22 –that24], the see outcomealso review of the [25]). interaction is affected by abiotic environmental factors [21] and in mixed infections with Understandingother viruses ([22 of– molecular24], see also mechanisms review [25] underlying). those outcomes is of utmost importance for resistanceUnderstandin breedingg without of molecular growth mechanisms trade-offs and underlying adaptation those of agronomical outcomes is practices. of utmost The importance studies in for resistance breeding without growth trade-offs and adaptation of agronomical practices. The studies in the model plants uncovered several aspects of molecular mechanisms in plant immunity Viruses 2020, 12, 217 3 of 17 Viruses 2020, 12, x FOR PEER REVIEW 3 of 17 the model plants uncovered several aspects of molecular mechanisms in plant immunity [26]. Although [26]. Although some findings can be transferred to crop species using orthology [27,28], this is not some findings can be transferred to crop species using orthology [27,28], this is not always the case as, always the case as, for example, in recently reported redundancy of Phytoalexin-deficient
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