Wheat Streak Mosaic Virus Alters the Transcriptome of Its Vector, Wheat Curl Mite (Aceria Tosichella Keifer), to Enhance Mite Development and Population Expansion
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University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 4-24-2019 Wheat streak mosaic virus alters the transcriptome of its vector, wheat curl mite (Aceria tosichella Keifer), to enhance mite development and population expansion Adarsh K. Gupta University of Nebraska-Lincoln, [email protected] Erin D. Scully Center for Grain and Animal Health Research, Stored Product Insect and Entomology Research Unit, [email protected] Nathan A. Palmer Wheat, Sorghum, and Forage Research Unit, USDA-ARS, [email protected] Scott M. Geib Daniel K. Inouye US Pacific Basin Agricultural Research Center, USDA-ARS, [email protected] Gautam Sarath Wheat, Sorghum, and Forage Research Unit, USDA-ARS & University of Nebraska-Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/plantpathpapers See P nextart of page the forOther additional Plant Sciences authors Commons , Plant Biology Commons, and the Plant Pathology Commons Gupta, Adarsh K.; Scully, Erin D.; Palmer, Nathan A.; Geib, Scott M.; Sarath, Gautam; Hein, Gary L.; and Tatineni, Satyanarayana, "Wheat streak mosaic virus alters the transcriptome of its vector, wheat curl mite (Aceria tosichella Keifer), to enhance mite development and population expansion" (2019). Papers in Plant Pathology. 626. https://digitalcommons.unl.edu/plantpathpapers/626 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Adarsh K. Gupta, Erin D. Scully, Nathan A. Palmer, Scott M. Geib, Gautam Sarath, Gary L. Hein, and Satyanarayana Tatineni This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ plantpathpapers/626 RESEARCH ARTICLE Gupta et al., Journal of General Virology 2019;100:889–910 DOI 10.1099/jgv.0.001256 Wheat streak mosaic virus alters the transcriptome of its vector, wheat curl mite (Aceria tosichella Keifer), to enhance mite development and population expansion Adarsh K. Gupta,1 Erin D. Scully,2 Nathan A. Palmer,3 Scott M. Geib,4 Gautam Sarath,3,5 Gary L. Hein6 and Satyanarayana Tatineni1,3,* Abstract Wheat streak mosaic virus (WSMV; genus Tritimovirus; family Potyviridae) is an economically important wheat virus that is transmitted by the wheat curl mite (WCM; Aceria tosichella Keifer) in a persistent manner. Virus–vector coevolution may potentially influence vector gene expression to prolong viral association and thus increase virus transmission efficiency and spread. To understand the transcriptomic responses of WCM to WSMV, RNA sequencing was performed to assemble and analyse transcriptomes of WSMV viruliferous and aviruliferous mites. Among 7291 de novo-assembled unigenes, 1020 were differentially expressed between viruliferous and aviruliferous WCMs using edgeR at a false discovery rate 0.05. Differentially expressed unigenes were enriched for 108 gene ontology terms, with the majority of the unigenes showing downregulation in viruliferous mites in comparison to only a few unigenes that were upregulated. Protein family and metabolic pathway enrichment analyses revealed that most downregulated unigenes encoded enzymes and proteins linked to stress response, immunity and development. Mechanistically, these predicted changes in mite physiology induced by viral association could be suggestive of pathways needed for promoting virus–vector interactions. Overall, our data suggest that transcriptional changes in viruliferous mites facilitate prolonged viral association and alter WCM development to expedite population expansion, both of which could enhance viral transmission. INTRODUCTION however, these genotypes vary in their ability to transmit wheat viruses [6–8]. The wheat curl mite (WCM; Aceria tosichella Keifer; family Eriophyidae) causes damage to wheat plants by feeding on Among WCM-transmitted viruses, WSMV is the most eco- leaf sap, which ultimately results in dehydration and the for- nomically important virus in the Great Plains of the USA mation of characteristic leaf curling. Cumulatively, the loss [9, 10]. Although WSMV on average causes 3–5 % annual of sap and leaf surface area due to curling hamper the pho- yield loss in wheat [11], yield losses of as high as 100 % have tosynthetic ability of the plant. However, the most detri- been observed in infected winter wheat [12]. WSMV is the type species of the genus Tritimovirus in the family Potyviri- mental effect of WCM infestation is its ability to transmit dae [13]. The 9384-nucleotide single-stranded, positive- several wheat viruses, including Wheat streak mosaic triti- sense genomic RNA of WSMV is encapsidated in flexuous movirus (WSMV) [1], High Plains wheat mosaic emaravirus filamentous virions of 690–700Â11–15 nm. WSMV geno- [2], Brome streak mosaic rymovirus [3] and Triticum mosaic mic RNA contains a single large open reading frame (ORF) poacevirus [4]. Two distinct genotypes of WCM, type 1 and encoding a polyprotein of ~350 kDa that is processed into at type 2, have been identified in the USA [5]. Both mite geno- least 10 mature proteins by 3 virus-encoded proteinases: P1, types often occur as mixed populations within wheat fields; HC-Pro and NIa-Pro [13]. WCMs efficiently transmit Received 12 December 2018; Accepted 14 March 2019; Published 24 April 2019 Author affiliations: 1Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln, NE 68583, USA; 2Center for Grain and Animal Health Research, Stored Product Insect and Entomology Research Unit, United States Department of Agriculture-Agricultural Research Services (USDA- ARS), Manhattan, KS 66502, USA; 3Wheat, Sorghum, and Forage Research Unit, USDA-ARS, Lincoln, NE 68583, USA; 4Daniel K. Inouye US Pacific Basin Agricultural Research Center, USDA-ARS, Hilo, HI 96720, USA; 5Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE 68583, USA; 6Department of Entomology, University of Nebraska-Lincoln, Lincoln, NE 68583, USA. *Correspondence: Satyanarayana Tatineni, [email protected] Keywords: Wheat curl mites; Wheat streak mosaic virus; transcriptome; differential gene expression; population expansion; behavioral changes. The NCBI BioProject PRJNA489675 contains all raw reads of wheat curl mite transcriptome data. SRR7796148, SRR7796152 and SRR7796153 contain reads derived from viruliferous mites, and SRR7796149, SRR7796150 and SRR7796151 contain reads derived from aviruliferous control mite samples. Four supplementary tables and one supplementary figure are available with the online version of this article. 001256 889 Gupta et al., Journal of General Virology 2019;100:889–910 WSMV at transmission rates of approximately 50 and higher stress responses in vectors as compared to avirulifer- 100 % with single and 5 to 10 viruliferous mites per test ous insects [32], whereas the acquisition of Pea enation plant, respectively [1, 8]. HC-Pro and coat protein (CP) are mosaic luteovirus was associated with the upregulation of required for WCM transmission of WSMV [14–16]. The genes involved in transcytosis in the vector, Acyrthosiphon mode of WCM transmission of WSMV appears to be persis- pisum (pea aphid) [33]. Additionally, acquisition of Tomato tent and circulative, as virus-like particles and inclusion yellow leaf curl China begamovirus was associated with the bodies have been found in the digestive tracts of viruliferous downregulation of genes linked to immune responses and mites [17, 18]. Juveniles acquire the virus while feeding on autophagy in whiteflies [34]. infected wheat and mites remain viruliferous through The microscopic nature (~200 µm) of WCMs and the lack moulting [17, 19, 20]. of adequate genomic and transcriptomic resources for this The plant cell wall and cuticle offer primary lines of defence important vector have hampered research to discern the against biotic and abiotic factors, including viruses. To cir- impact of virus acquisition on vector physiology and delin- cumvent these physical barriers, many plant viruses have eate the virus–vector dynamics in this economically evolved precise vector-specific interactions with herbivorous important pathosystem. In this study, high-throughput insects [21]. In some cases, viruses are capable of manipu- RNA sequencing and complementary bioinformatic analy- lating vector behaviour and physiology to enable more effi- ses were used to assemble the de novo transcriptome of the cient viral transmission and spread, a phenomenon termed WCM and evaluate the transcriptomic signatures of WCMs ‘adaptive manipulation’ [22]. These behavioural changes upon acquisition of WSMV. can be quite dramatic and include enhanced feeding and increased preference of viruliferous vectors for noninfected METHODS host [22–25]. In addition to behavioural modifications, Preparation of WSMV viruliferous and aviruliferous viruses have evolved mechanisms to facilitate acquisition, control WCMs retention and, occasionally, replication in vectors, often gov- Type 2 mites reared on the WCM-susceptible wheat cultivar erned by signature motifs in the viral proteome. Often, these Settler CL (NH03614 CL) grown in caged pots maintained molecular determinants facilitate specific interactions with at the University of Nebraska-Lincoln [5] were used for this receptors of the vector