Transcriptomics Reveals Fast Changes in Salicylate and Jasmonate Signaling Pathways in Shoots of Carbonate-Tolerant Arabidopsis thaliana under Bicarbonate Exposure

High bicarbonate concentrations of calcareous soils with high pH can affect crop performance due to different constraints. Among these, Fe deficiency has mostly been studied. The ability to mobilize sparingly soluble Fe is a key factor for tolerance. Here, a comparative transcriptomic analysis was performed with two naturally selected Arabidopsis thaliana demes, the carbonate-tolerant A1((c+)) and the sensitive T6((c-)). Analyses of plants exposed to either pH stress alone (pH 5.9 vs. pH 8.3) or to alkalinity caused by 10 mM NaHCO3 (pH 8.3) confirmed better growth and nutrient homeostasis of A1((c+)) under alkaline conditions. RNA-sequencing (RNA-seq) revealed that bicarbonate quickly (3 h) induced Fe deficiency-related genes in T6((c-)) leaves. Contrastingly, in A1((c+)), initial changes concerned receptor-like proteins (RLP), jasmonate (JA) and salicylate (SA) pathways, methionine-derived glucosinolates (GS), sulfur starvation, starch degradation, and cell cycle. Our results suggest that leaves of carbonate-tolerant plants do not sense iron deficiency as fast as sensitive ones. This is in line with a more efficient Fe translocation to aerial parts. In A1((c+)) leaves, the activation of other genes related to stress perception, signal transduction, GS, sulfur acquisition, and cell cycle precedes the induction of iron homeostasis mechanisms yielding an efficient response to bicarbonate stress.

Automated summary

High bicarbonate concentrations in calcareous soils with high pH can impact crop performance, with iron deficiency being a key concern. In this study, comparative transcriptomic analysis of Arabidopsis thaliana demes revealed that carbonate-tolerant plants exhibit better growth and nutrient homeostasis under alkaline conditions, with different gene expression patterns in response to bicarbonate stress compared to sensitive plants. This suggests that carbonate-tolerant plants have a more efficient response to bicarbonate stress, with a focus on stress perception, signal transduction, sulfur acquisition, and cell cycle regulation before iron homeostasis mechanisms are induced.