Transcriptome and metabolite profiles reveal differential molecular responses of wild and cultivated amaranth species to water deficit and salt stress

MAIN CONCLUSION: A. hybridus tolerance to salinity depends on constitutively active mechanisms, whereas A. hypochondriacus tolerance to salt and water deficit depends on a constitutive protection and a robust transcriptional response. Drought and soil salinity are two environmental factors that significantly affect crop production. To gain a better understanding of how amaranth responds to these abiotic stresses, we analyzed the transcriptomic and metabolomic changes in the leaves of Amaranthus hybridus, a wild species, and A. hypochondriacus, a cultivated species used for seed production. We identified differentially expressed genes (DEGs) between the two species and under different stress conditions. Control plants of A. hypochondriacus exhibited higher expression levels of genes associated with photosynthesis, amino acid metabolism, fatty acid metabolism, sulfur metabolism, thiamine metabolism, and secondary metabolism. Notably, A. hybridus under salt stress showed an up-regulation of genes related to phosphonate and phosphinate metabolism and steroid biosynthesis. In contrast, the response of A. hypochondriacus to salt stress was characterized by increased expression of ABC transporters and genes involved in fructose, mannose, trehalose, porphyrin, thiamine, and monoterpenoid metabolism. When subjected to both types of stresses, A. hypochondriacus showed up-regulation of MAPK signaling pathways, ABC transporters, galactose, branched-chain amino acid (BCAA) degradation, and the production of defense compounds. Both amaranth species modulated their metabolic processes in response to drought and salinity stress towards cell wall modification, as well as the metabolism of pectin and lignin, while also producing antimicrobial and antifungal metabolites. Additionally, we detected differential accumulation of compounds, including methylphosphonate, 2-hydroxyethylphosphonate, and several metabolites related to fatty acid metabolism in the leaves of both amaranth species.