At the core of salinity: Divergent transcriptomic responses to neutral and alkaline salinity in Arabidopsis thaliana

In the context of current climate change, alkaline salinity is increasingly challenging crop yields, especially in arid and semiarid regions. Alkaline salinity is more detrimental to plant performance than neutral salinity and tolerance to neutral salinity may not confer tolerance to alkaline salinity. The mechanisms behind are still poorly understood. This study aims to identify physiological and genetic traits underlying this differential tolerance to neutral and alkaline salinity by exploiting the variation present in natural populations (demes) of Arabidopsis thaliana . Growth, photosynthesis, phytohormone and mineral nutrient profiles, plant water status and transcriptomic changes were analyzed in four demes with contrasting tolerance to neutral and alkaline salinity. Results of this novel holistic approach suggest low internal Fe use efficiency caused by bicarbonate as a driver of enhanced sensitivity to alkaline salinity in plants adapted to neutral salinity prompting photosynthesis inhibition and alteration of the plant’s carbon budget for primary and secondary metabolism. Moreover, alkaline salinity specifically altered the auxin and jasmonic acid signaling pathways, while sustained ABA biosynthesis was an adaptive trait under neutral salinity. Exploring the genes with non-shared expression trends between salinity types, we identified sequence variation at the BGAL4 locus associated with advantageous responses to each type of salinity. Weighted correlation network analysis (WGCNA) validated the significant involvement of gene co-expression modules targeted by the enrichment analyses, highlighting the hubs correlated with favorable responses to both salinity types. Overall, the present study points out the complex physiological and genetic mechanisms responsible for plant tolerance to alkaline salinity and proposes target genes for breeding strategies under alkaline saline soils. • Demes adapted to neutral salinity (NS demes) exhibit significant growth reduction under alkaline salinity (alkSAL) compared to non-adapted demes. • Under alkSAL, photosynthetic efficiency and K+ retention is better maintained in demes adapted to alkaline salinity (AS demes). • Bicarbonate-induced alterations in NS demes lead to a decreased internal use efficiency, contributing to their sensitivity to alkSAL. • Alkaline salinity triggers more extensive transcriptomic changes than neutral salinity, with NS demes showing greater alteration in gene expression. • Alkaline salinity induces a specific hormonal response, with higher inhibition of auxin and jasmonic acid (JA) signaling pathways, whereas neutral salinity leads to sustained ABA biosynthesis in NS demes, correlating with improved water use efficiency. • The study proposes target genes associated to advantageous responses to each type of salinity.