Coordinated transcriptional reprogramming mediates drought tolerance in potato, revealed by temporally integrated network analysis

Drought stress (DS) significantly limits yield and quality in many crops worldwide. Understanding how subcellular processes respond to DS is critical for crop improvement. In this study, we evaluated temporal transcriptomic responses of two potato (Solanum tuberosum) accessions, namely Olalla (DS-susceptible) and Atlantic (DS-tolerant), at 7, 14, and 21 days of DS. Drought tolerance was associated with coordinated transcriptional reprogramming, with minimal early responses at 7 (21–160 differentially expressed genes; DEGs), followed by extensive transcriptional reprogramming at 14 (2770–4150 DEGs) and 21 (5229–6404 DEGs) days of DS, which correlated with the progressive severity of stress phenotypes. DEGs across accessions under DS showed increasing transcriptional dynamics at 7 (2218), 14 (3030), and 21 (4146) days of DS, and enrichment for amino acid biosynthesis pathways among DEGs suggests osmolyte accumulation as a key tolerance strategy. Gene regulatory network (GRN) analysis identified regulatory modules whose eigengene expression strongly distinguished tolerant and susceptible potato accessions, implicating coordinated network-level control rather than isolated gene effects. Furthermore, the integrative analysis of DEGs and GRN revealed co-regulated genes involved in DS response, including transcription factors (TFs), hub genes (10 genes per coexpressed module with the highest regulatory confidence), and those located within DS-associated quantitative trait loci (QTLs). Notably, the upstream regions of co-regulated genes harbored cis-regulatory elements (CREs) of ABRE and DRE, which indicated involvement of both ABA-dependent and independent signaling pathways. These findings reveal a temporally structured regulatory framework underlying drought tolerance in potato and highlight candidate network genes/hubs linking hormonal signaling to physiological resilience.