A transcriptomic study with RNAseq where a cultivated and a wild lettuce species were compared under different irrigation regimes

Lettuce (Lactuca sativa L.) is highly susceptible to drought. To understand the molecular mechanisms causing the anthocyanin increase observed before in several Lactuca spp. in response to drought, we conducted a transcriptomic study in the red commercial variety 'Romired' and the wild relative Lactuca homblei De Wild under control and deficit irrigation (DI) conditions applied 3 weeks before harvesting. RNA-seq analyses revealed 5,329 differentially expressed genes (DEGs) in 'Romired' and 6,179 in L. homblei, with 2,272 DEGs common to both. The number of exclusive upregulated genes was more than twice in L. homblei than in 'Romired', whereas the amount of exclusive downregulated genes was 1.3 times higher in 'Romired'. Within the upregulated DEGs, the most abundant and significant GO terms were those involved in regulation processes (including response to water) and cellular components in L. homblei and 'Romired', respectively, which could indicate that the wild species is triggering more mechanisms of response to drought. The downregulated DEGs were mainly related to growth and basal processes in both accessions (deceleration of basal metabolism to redirect resources to drought tolerance). Anthocyanin contents were always higher under DI within each accession, with both upregulated genes and anthocyanin content being clearly higher in L. homblei than in 'Romired' under DI. A total of 36 DEGs in at least one of the two species were mapped in the phenylpropanoid and flavonoid pathways, being more commonly activated in L. homblei (17 versus 7). Nineteen candidate DEGs with the strongest change of expression and correlation with anthocyanin content and drought were validated by qPCR, being all differentially expressed only in the wild species, in which the expression profiles obtained with the two techniques (RNA-seq and qPCR) coincided. Their functions were related to anthocyanins and/or stress response and harboured numerous polymorphisms, 412 and 11 in the wild and the cultivated species, respectively, four with high or moderate predicted impacts in the protein function, which could explain the differences between both species. Transcriptomic changes in the anthocyanin-related response to drought stress were more drastic in the wild species, which points to a potential source of drought tolerance for lettuce.