DNA methylation is associated with transcriptional variability and transposon-driven trans-regulation under drought in wheat landraces

Abstract

Abstract Background Bread wheat (Triticum aestivum) is essential for food security, but increasingly frequent droughts threaten yields. While wheat’s transcriptional responses to drought are well characterised, DNA methylation’s role remains poorly understood. Wheat landrace panels possess extensive genomic diversity shaped by long-term environmental adaptation, making them a powerful tool for dissecting drought response mechanisms. Results We profiled single-base methylomes and transcriptomes from wheat seedlings before and after drought exposure; by pooling DNA from a small landrace panel, we captured population-level methylation patterns reflecting environmental adaptation. Gene body methylation was significantly positively associated with high, stable gene expression under stress conditions, and genic differentially methylated regions targeted stress-associated genes. Many genes associated with differential methylation maintained stable transcription across drought exposure, suggesting a potential stabilising role for DNA methylation. Differential methylation heavily localised to intergenic and transposon regions; the ancient retrotransposon family RLX_famc9 emerged as a prominent methylation target under drought. RLX_famc9 shared sequence similarity with drought-responsive genes, was enriched for differential methylation, and was downregulated under drought, supporting a speculative model in which drought-induced hypermethylation suppresses TE-derived trans-regulatory activity, ultimately moderating the expression of target genes. We also implicate ROS1a glycosylases in demethylation under drought. Conclusions DNA methylation likely has an intricate regulatory role under drought, with ROS1a-mediated demethylation, genic methylation potentially promoting high and stable expression, and methylation-controlled transposons potentially modulating gene expression in trans . These shared epigenomic signatures highlight regulatory mechanisms and offer potential epimarkers that could be leveraged to enhance drought resilience in elite cultivars.