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Defense-Related Gene Expression Following an Orthotospovirus Infection Is Influenced by Host Resistance in Arachis Hypogaea

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Defense-Related Gene Expression Following an Orthotospovirus Infection Is Influenced by Host Resistance in Arachis Hypogaea viruses Article Defense-Related Gene Expression Following an Orthotospovirus Infection Is Influenced by Host Resistance in Arachis hypogaea Michael A. Catto 1,† , Anita Shrestha 2,†, Mark R. Abney 2, Donald E. Champagne 1, Albert K. Culbreath 3, Soraya C. M. Leal-Bertioli 4, Brendan G. Hunt 5 and Rajagopalbabu Srinivasan 5,* 1 Department of Entomology, University of Georgia, Athens, GA 30606, USA; [email protected] (M.A.C.); [email protected] (D.E.C.) 2 Department of Entomology, University of Georgia, Tifton, GA 31793, USA; [email protected] (A.S.); [email protected] (M.R.A.) 3 Department of Plant Pathology, University of Georgia, Tifton, GA 31793, USA; [email protected] 4 Department of Plant Pathology, University of Georgia, Athens, GA 30602, USA; [email protected] 5 Department of Entomology, University of Georgia, Griffin, GA 30223, USA; [email protected] * Correspondence: [email protected]; Tel.: +1-770-229-3099 † These authors contributed equally to this manuscript. Abstract: Planting resistant cultivars is the most effective tactic to manage the thrips-transmitted tomato spotted wilt orthotospovirus (TSWV) in peanut plants. However, molecular mechanisms conferring resistance to TSWV in resistant cultivars are unknown. In this study, transcriptomes of TSWV-susceptible (SunOleic 97R) and field-resistant (Tifguard) peanut cultivars with and without TSWV infection were assembled and differentially expressed genes (DEGs) were compared. There Citation: Catto, M.A.; Shrestha, A.; were 4605 and 2579 significant DEGs in SunOleic 97R and Tifguard, respectively. Despite the lower Abney, M.R.; Champagne, D.E.; number of DEGs in Tifguard, an increased proportion of defense-related genes were upregulated in Culbreath, A.K.; Leal-Bertioli, S.C.M.; Tifguard than in the susceptible cultivar. Examples included disease resistance (R) proteins, leucine- Hunt, B.G.; Srinivasan, R. rich repeats, stilbene synthase, dicer, and calmodulin. Pathway analysis revealed the increased Defense-Related Gene Expression downregulation of genes associated with defense and photosynthesis in the susceptible cultivar Following an Orthotospovirus rather than in the resistant cultivar. These results suggest that essential physiological functions were Infection Is Influenced by Host less perturbed in the resistant cultivar than in the susceptible cultivar and that the defense response Resistance in Arachis hypogaea. Viruses 2021, 13, 1303. https://doi.org/ following TSWV infection was more robust in the resistant cultivar than in the susceptible cultivar. 10.3390/v13071303 Keywords: tomato spotted wilt orthotospovirus; field-resistant peanut cultivars; Sunoleic 97R; Academic Editor: Feng Qu Tifguard; differential gene expression Received: 1 June 2021 Accepted: 3 July 2021 Published: 5 July 2021 1. Introduction Peanut (Arachis hypogaea L.) is an important crop for oil and protein production [1]. Publisher’s Note: MDPI stays neutral Spotted wilt disease caused by thrips-transmitted tomato spotted wilt orthotospovirus with regard to jurisdictional claims in (TSWV) severely affects peanut production in southeastern United States [2,3]. In Georgia published maps and institutional affil- alone, spotted wilt disease causes an annual loss of over USD 10 million [4–6]. Tomato spotted iations. wilt orthotospovirus is the species type of the genus Orthotospovirus in the family Tospoviridae. TSWV is an ambisense RNA virus that is exclusively transmitted in a persistent and propagative fashion by the peanut-colonizing thrips species in the family Thripidae [7–9]. Tobacco thrips, Frankliniella fusca [Hinds], and western flower thrips, Frankliniella occidentalis Copyright: © 2021 by the authors. [Pergande], are the predominant vectors of TSWV in southeastern United States [5,10]. Licensee MDPI, Basel, Switzerland. The use of resistant cultivars is one of the most effective tactics used for managing This article is an open access article the incidence of TSWV and reducing the impact of spotted wilt in peanut production [2,3]. distributed under the terms and Intensive breeding programs since the 1990s in Georgia and Florida have led to the de- conditions of the Creative Commons velopment of three generations of resistant cultivars with incremental field resistance to Attribution (CC BY) license (https:// TSWV in each generation [3,11,12]. Under TSWV pressure, field-resistant cultivars display creativecommons.org/licenses/by/ less severe symptoms and produce higher yields when compared with TSWV-susceptible 4.0/). Viruses 2021, 13, 1303. https://doi.org/10.3390/v13071303 https://www.mdpi.com/journal/viruses Viruses 2021, 13, x FOR PEER REVIEW 2 of 18 Intensive breeding programs since the 1990s in Georgia and Florida have led to the devel- Viruses 2021, 13, 1303 2 of 17 opment of three generations of resistant cultivars with incremental field resistance to TSWV in each generation [3,11,12]. Under TSWV pressure, field-resistant cultivars display less severe symptoms and produce higher yields when compared with TSWV-susceptible cultivarscultivars (Figure (Figure 11))[ [3].3]. Despite Despite the the extensive extensive usage usage of of TSWV TSWV field-resistant field-resistant cultivars cultivars over thethe past past two decades, informationinformation onon host-virushost-virus interactions interactions at at both both macro macro and and micro micro levels lev- elsis limited,is limited, and and the the mechanism mechanis ofm resistanceof resistance is unknown. is unknown. Figure 1. TSVW-susceptibleTSVW-susceptible peanut peanut cultivar cultivar (SunOleic (SunOleic 97R) 97R) on on the the left left and and field-resistant field-resistant peanut peanut cultivar cultivar (Tifguard) (Tifguard) on the on right.the right. Both Bothcultivars cultivars were wereplanted planted at the atsame the time. same TSWV time. TSWVinfection infection established established naturally naturally in the selected in the selectedfield. As field.evident, As thereevident, was there increased was increased yellowing yellowing and stunting and stunting in the TSWV-suscept in the TSWV-susceptibleible cultivar cultivar in comparison in comparison with the with field-resistant the field-resistant culti- var. Foliar symptoms such as chlorotic and ring spots were also more severe in the TSWV-susceptible cultivar than in the cultivar. Foliar symptoms such as chlorotic and ring spots were also more severe in the TSWV-susceptible cultivar than in field-resistant cultivar. the field-resistant cultivar. InIn contrast contrast to to peanut, peanut, in in other other crops, crops, genes genes conferring conferring resistance resistance to TSWV have been identifiedidentified and and the the resistance mechanism has been characterized. For instance, dominant genesgenes Sw-5Sw-5 andand TswTsw inin tomato tomato (Solanum (Solanum lycopersicon lycopersicon L.)L.) and and pepper pepper (Capsicum (Capsicum annuum annuum L.), respectively,L.), respectively, have have been beenknown known to confer to confer resistance resistance to TSWV to TSWV [13–16]. [13 Upon–16]. TSWV Upon TSWVinocu- lation,inoculation, these genes these genesinduced induced a hypersensitive a hypersensitive reaction reaction in TSWV-resistant in TSWV-resistant tomato tomato and pep- and perpepper cultivars cultivars [16,17]. [16 ,The17]. hypersensitive The hypersensitive reaction reaction is characterized is characterized by localized by localized cell death, cell suppresseddeath, suppressed virus replication, virus replication, and a lack and of a lacksystemic of systemic movement movement of the virus of the [18]. virus [18]. Gene(s)Gene(s) conferring conferring resistance resistance to toTSWV TSWV have have notnot been been identified identified in field-resistant in field-resistant pea- nutpeanut cultivars, cultivars, but butseveral several quantitative quantitative trait trait loci loci(QTL) (QTL) believed believed to be to involved be involved in field in field re- sistanceresistance have have been been mapped mapped [19–23]. [19–23 ].Unlike Unlike in in tomato tomato and and pepper, pepper, TSWV-resistant TSWV-resistant peanut peanut cultivarscultivars do do not not produce a hypersensitive responseresponse upon inoculation. An An earlier study demonstrateddemonstrated that that thrips-mediated thrips-mediated and and mechan mechanicalical inoculation of TSWV field-resistantfield-resistant and susceptible cultivars produced typical TSWV symptoms [24,25]. Those studies also documented the reduced TSWV accumulation in some resistant cultivars when compared with the susceptible cultivar. The underlying molecular basis for reduced accumulation of TSWV in field-resistant peanut cultivars remains unknown. Earlier studies have doc- Viruses 2021, 13, 1303 3 of 17 umented molecular changes induced by bacterial and fungal infections in peanut plants at the transcript levels [26–28]. Moreover, a repertoire of genes in peanut plants that were induced by various abiotic factors was identified [29–31]. Recently, affordable short-read sequencing technology is being extensively used for elucidating interactions between plant hosts and pathogens at genomic and transcriptomic levels. Studies have widely used RNA sequencing to examine the expression levels of genes following pathogen infection and to characterize genes conferring resistance to pathogens [26,27,30]. In addition, genome assemblies of the peanut sub-genomes, derived from two diploid ancestors (Arachis dura- nensis (Karpov and W. C. Gregory) and Arachis ipaensis (Karpov and W. C. Gregory)) [32], and two allotetraploid genomes
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