Genotypes of Eruca vesicaria subsp. sativa grown in contrasting field environments differ on transcriptomic and metabolomic levels, significantly impacting nutritional quality

Rocket (<i>Eruca vesicaria</i> subsp. <i>sativa</i>) is a source of sulfur-containing glucosinolates (GSLs). GSLs and their breakdown hydrolysis products (GHPs) are responsible for health-related benefits, such as anti-cancer and anti-neurodegenerative properties. Understanding how phytochemical composition changes between cultivation environments is key to developing cultivars with improved nutritional quality. Two consecutive harvests (first and second regrowth) of crops, grown in both Italy and the UK, were used to determine the phytochemical and transcriptomic differences between six lines of <i>Eruca</i>. Samples were taken upon delivery from field sites (D0) and after five days of cold storage (D5) for each location. Leaves were analysed for sulfur content, volatile organic compounds (VOCs), GSLs, GHPs, and sugars. Transcriptome data were associated with metabolite profiles to identify differentially expressed genes between plants grown in the two environments. VOC compounds (carbon disulfide, methyl thiocyanate) were associated with growth environment and with differences in sulfur metabolism gene expression (<i>APR2, LSU2, LSU3, SDI1, SiR</i>), GSL biosynthesis (<i>MYB28, FMOGS-OX2</i>) and GHP formation (<i>ESM1, TGG1, TGG2</i>). The concentrations of sugars were an order of magnitude greater in UK grown samples (up to 29.9 mg g^-1 dry weight; dw). Sulfur content was significantly higher in the Italy plant samples (11.4 - 20.1 mg g^-1 dw), which was in turn associated with higher concentrations of GSLs (pentyl GSL, up to 15.8 μmol g^-1 dw; sinigrin, up to 0.005 μmol g^-1 dw; glucoraphanin, up to 5.1 μmol g^-1 dw; glucorucolamine, up to 23.6 μmol g^-1 dw; neoglucobrassicin, up to 5.3 μmol g^-1 dw) and hydrolysis products (sativin, up to 13.5 μmol g^-1 dw; erucin, up to 1 μmol g^-1 dw; sulforaphane, up to 34.7 μmol g^-1 dw). VOC profiles of plants cultivated in the UK were distinct from Italy grown plants, with higher relative abundances of alkanes and esters in second cut and shelf-life (D5) samples. The data indicate a significant interaction of cultivar response with environment, highlighting the difficulty of producing <i>Eruca</i> crops with consistent phytochemical and postharvest traits. Genes with differential expression between plants grown in Italy and the UK could be used as markers of phytochemical quality and composition.