Small RNAs and their targets are associated with the transgenerational effects of water-deficit stress in durum wheat.

Water-deficit stress negatively affects wheat yield and quality. Abiotic stress on parental plants during reproduction may have transgenerational effects on progeny. Here we investigated the transgenerational influence of pre-anthesis water-deficit stress by detailed analysis of the yield components, grain quality traits, and physiological traits in durum wheat. Next-generation sequencing analysis profiled the small RNA-omics, mRNA transcriptomics, and mRNA degradomics in first generation progeny. Parental water-deficit stress had positive impacts on the progeny for traits including harvest index and protein content in the less stress-tolerant variety. Small RNA-seq identified 1739 conserved and 774 novel microRNAs (miRNAs). Transcriptome-seq characterised the expression of 66,559 genes while degradome-seq profiled the miRNA-guided mRNA cleavage dynamics. Differentially expressed miRNAs and genes were identified, with significant regulatory patterns subject to trans- and inter-generational stress. Integrated analysis using three omics platforms revealed significant biological interactions between stress-responsive miRNA and targets, with transgenerational stress tolerance potentially contributed via pathways such as hormone signalling and nutrient metabolism. Our study provides the first confirmation of the transgenerational effects of water-deficit stress in durum wheat. New insights gained at the molecular level indicate that key miRNA-mRNA modules are candidates for transgenerational stress improvement.