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The appearance of water stress episodes triggers leaf abscission and decreases Ilex paraguariensis yield. To explore the mechanisms that allow it to overcome dehydration, we investigated how the root gene expression varied between water-stressed and non-stressed plants and how the modulation of gene expression was linked to metabolite composition and physiological status. After water deprivation, 5160 differentially expressed transcripts were obtained through RNA-seq. The functional enrichment of induced transcripts revealed significant transcriptional remodelling of stress-related perception, signalling, transcription, and metabolism. Simultaneously, the induction of the enzyme 9-cis-expoxycarotenoid dioxygenase (NCED) transcripts reflected the central role of the hormone abscisic acid in this response. Consequently, the total content of amino acids and soluble sugars increased, and that of starch decreased. Likewise, osmotic adjustment and radical growth were significantly promoted to preserve cell membranes and water uptake. This study provides a valuable resource for future research to understand the molecular adaptation of I. paraguariensis plants under drought conditions and facilitates the exploration of drought-tolerant candidate genes.

Main Conclusion: Abscisic acid is involved in the drought response of Ilex paraguariensis. Acclimation includes root growth stimulation, stomatal closure, osmotic adjustment, photoprotection, and regulation of nonstructural carbohydrates and amino acid metabolisms. Ilex paraguariensis (yerba mate) is cultivated in the subtropical region of South America, where the occurrence of drought episodes limit yield. To explore the mechanisms that allow I. paraguariensis to overcome dehydration, we investigated (1) how gene expression varied between water-stressed and non-stressed plants and (2) in what way the modulation of gene expression was linked to physiological status and metabolite composition. A total of 4920 differentially expressed transcripts were obtained through RNA-Seq after water deprivation. Drought induced the expression of several transcripts involved in the ABA-signalling pathway. Stomatal closure and leaf osmotic adjustments were promoted to minimize water loss, and these responses were accompanied by a high transcriptional remodeling of stress perception, signalling and transcriptional regulation, the photoprotective and antioxidant systems, and other stress-responsive genes. Simultaneously, significant changes in metabolite contents were detected. Glutamine, phenylalanine, isomaltose, fucose, and malate levels were shown to be positively correlated with dehydration. Principal component analysis showed differences in the metabolic profiles of control and stressed leaves. These results provide a comprehensive overview of how I. paraguariensis responds to dehydration at transcriptional and metabolomic levels and provide further characterization of the molecular mechanisms associated with drought response in perennial subtropical species.