Multi-omics analysis reveals distinct features of an ethyl methanesulfonate (EMS)-derived rhizomania-resistant mutant sugar beet breeding line

Background Rhizomania in sugar beet caused by Beet necrotic yellow vein virus (BNYVV) and vectored by Polymyxa betae greatly reduces sugar yield. Resistance in commercial cultivars is primarily dependent upon the use of Rz1 and Rz2 resistant genes. Considering existence of Rz1 resistance breaking BNYVV strains and limited availability of rhizomania resistance in sugar beet, new sources of resistance to this disease are desirable. Results Using an earlier developed rhizomania resistant (R) sugar beet ethylmethane sulfonate (EMS) breeding line, KEMS12, other susceptible (S) lines, natural infections in the field, and multi-omics tools, putative mechanisms of resistance were investigated. Analysis of previously deposited Illumina whole genome sequencing (WGS) data revealed a higher number of genotype-specific genomic variants including single nucleotide polymorphisms (SNPs) and indels in chromosomes five and six of KEMS12 vs. S lines. Transcriptome data generated in this study identified highly up-regulated (> 5-fold) genes such as Bevul.4G018600.1 (protein GOS9), Bevul.4G190100.1 (histone-lysine N-methyltransferase SUVR2), Bevul.2G017800.14 (U-box domain-containing protein 4), and Bevul.1G070100.1 (MLP-like protein) in the leaves and roots of R line (vs. S lines) at pre-symptomatic and symptomatic stages. Pathway analysis showed differentially expressed genes predominantly enriched for secondary metabolite biosynthesis. Metabolome analysis revealed higher abundance of metabolites such as glutamine, L-pyroglutamic acid, asparagine, and betaine in the roots of R line both at pre-symptomatic and symptomatic stages. Overlaps between EMS induced mutations in genes and corresponding changes in their expressions identified candidate genes that exhibited significant correlations with changes in specific metabolites in the R line. Conclusions This work has identified genes and metabolites associated with rhizomania resistance in a sugar beet mutant breeding line, which is potentially a new source of resistance. These findings may have future implications in improving rhizomania resistance in existing cultivars.