Integrating multiple omics to dissect the common and specific molecular changes occurring in Arabidopsis thaliana (L.) under nitrate and sulfate chronic limitations.

Plants, which have fundamental dependence on nitrogen and sulfur, have to cope with chronic limitations when fertilizers are not provided. Our study aimed at characterizing the metabolomic, proteomic and transcriptomic changes occurring in Arabidopsis leaves under chronic nitrate (Low-N) and chronic sulfate (Low-S) limitations in order to compare Low-S and Low-N effects and enlighten interconnections and strategies of plant adaptation. Metabolite profiling globally revealed an opposite effect of Low-S and Low-N on carbohydrate and amino acid accumulations. Proteomic data showed by contrast that both Low-N and Low-S resulted in the exacerbation of catabolic processes, stimulation of mitochondrial and cytosolic metabolisms and decrease of chloroplast metabolism. The lower abundances of ribosomal proteins and translation factors under Low-N and Low-S attested from growth limitation. At transcript level, the major and specific effect of Low-N was the enhancement of plant defence and immunity genes. The main effect of chronic Low-S was the decrease of transcripts involved in cell division, DNA replication and cytoskeleton and the increase of autophagy gene expressions. This was consistent with a role of the Target-of-Rapamycin kinase in the control of plant metabolism and cell growth and division under chronic Low-S. In addition, Low-S decreased the expression of several NLP transcription factors, which are master actors of nitrate sensing. Finally, both transcriptome and proteome revealed the effect of Low-S on the repression of glucosinolate synthesis, and the effect of Low-N on the exacerbation of glucosinolate degradation. This showed the importance of glucosinolate as buffering molecules for N and S management.