Abstract
Beet curly top virus (BCTV) mediated yield loss in sugar beets is a major problem worldwide. The circular single-stranded DNA virus is transmitted by the beet leafhopper. Genetic sources of BCTV resistance in sugar beet are limited and commercial cultivars rely on chemical treatments versus durable genetic resistance. Phenotypic selection and double haploid production have resulted in sugar beet germplasm (KDH13; 13 and KDH4-9; 4) that are highly resistant to BCTV. The molecular mechanism of resistance to the virus is unknown, especially the role of small non-coding RNAs (sncRNAs) during early plant–viral interaction. Using the resistant lines along with a susceptible line (KDH19-17; 19), we demonstrate the role of sugar beet microRNAs (miRNAs) in BCTV resistance during early infection stages when symptoms are not yet visible. The differentially expressed miRNAs altered the expression of their corresponding target genes such as pyruvate dehydrogenase (EL10Ac1g02046), carboxylesterase (EL10Ac1g01087), serine/threonine protein phosphatase (EL10Ac1g01374), and leucine-rich repeats (LRR) receptor-like (EL10Ac7g17778), that were highly expressed in the resistant lines versus susceptible lines. Pathway enrichment analysis of the miRNA target genes showed an enrichment of genes involved in glycolysis/gluconeogenesis, galactose metabolism, starch, and sucrose metabolism to name a few. Carbohydrate analysis revealed altered glucose, galactose, fructose, and sucrose concentrations in the infected leaves of resistant versus susceptible lines. We also demonstrate differential regulation of BCTV derived sncRNAs in the resistant versus susceptible lines that target sugar beet genes such as LRR (EL10Ac1g01206), 7-deoxyloganetic acid glucosyltransferase (EL10Ac5g12605), and transmembrane emp24 domain containing (EL10Ac6g14074) and altered their expression. In response to viral infection, we found that plant derived miRNAs targeted BCTV capsid protein/replication related genes and showed differences in expression among resistant and susceptible lines. The data presented here demonstrate the contribution of miRNA mediated regulation of metabolic pathways and cross-kingdom RNA interference (RNAi) in sugar beet BCTV resistance.
Highlights
Sugar beet (Beta vulgaris L.) is a highly valuable crop that contributes to 55–60% of total sugar produced in the United States and Europe
Using a Beet curly top virus (BCTV) susceptible (S) sugar beet line (KDH19-17; 19) and two resistant (R) lines, KDH13 (13) and KDH4-9 (4), we demonstrate the role of small non-coding RNAs (sncRNAs) in BCTV resistance/susceptibility
We took a comprehensive approach by using sRNAseq, mRNAseq, analysis of target metabolites, and evaluation of symptoms to demonstrate the regulatory roles of sncRNAs and their potential contribution toward host resistance and/or susceptibility in the R and S lines respectively (Figure 8)
Summary
Sugar beet (Beta vulgaris L.) is a highly valuable crop that contributes to 55–60% of total sugar produced in the United States and Europe. Sugar beet production was highly impacted by BCTV in the 1920s and early 1930s until resistant varieties were introduced (Bennett, 1971; Panella et al, 2014; Strausbaugh et al, 2017). As BCTV resistance is quantitatively inherited, the trait is challenging to maintain in the parental lines used for commercial hybrid production (Strausbaugh et al, 2007; Panella et al, 2014) Additional approaches such as seed and foliar treatments with synthetic insecticides have been successful in reducing sugar beet BCTV symptoms (Strausbaugh et al, 2010, 2012, 2014), additional sources of strong genetic resistance are highly desirable to develop eco-friendly management. Implementation of alternative cutting-edge molecular biology tools such as RNA interference (RNAi) mediated Host-InducedGene-Silencing (reviewed in Majumdar et al, 2017) will largely depend upon the identification of appropriate pathogen/host target genes and/or regulatory mechanisms that are highly critical during early stages of infection
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