Enhancing wheat resilience to combined drought and heat stress through genetic mapping of transgenerational stress memory

Abstract

Combined drought–heat episodes are rising in frequency and severity. Beyond short-term acclimation, it remains unclear how plants archive these experiences across generations to influence offspring phenotype, a gap we address by interrogating transgenerational stress memory. These concurrent stresses trigger complex physiological and molecular responses and may establish a heritable stress memory in plants, potentially priming progeny for improved tolerance. To investigate this phenomenon, we explored the genetic architecture of transgenerational drought and heat stress memory in wheat through genome-wide association studies (GWAS) and candidate gene analysis. Our goal was to identify genetic loci and mechanisms that underlie adaptive responses to recurring abiotic stress. A diverse panel of wheat genotypes was evaluated under well-watered control conditions and recurring combined drought–heat stress treatments across three successive generations. We measured key physiological parameters (e.g., chlorophyll content, osmolyte and protein levels) and agronomic traits (plant height, spike characteristics, grain number, kernel weight) to assess stress tolerance and memory retention. Genome-wide association mapping linked this phenotypic variation under stress to specific genomic regions, and candidate genes within these regions were identified based on known roles in abiotic stress responses. Expression profiling of selected candidate genes was also performed to validate their stress-responsive behavior. Recurrent drought and heat stress caused a progressive decline in chlorophyll content, accompanied by marked accumulation of stress-related metabolites such as proline and soluble proteins, reflecting adaptive physiological adjustment. In contrast, key yield components, including plant height, spike length, spikelet number, grains per spike, and thousand-kernel weight, were significantly reduced, underscoring the detrimental impact on productivity. These effects varied across generations and genotypes, indicating differences in stress memory and highlighting the need to select resilient lines. GWAS identified significant single-nucleotide polymorphisms (SNPs) in four genomic regions on chromosomes 1A, 1B, and 2A that are associated with chlorophyll content, osmolyte accumulation, and yield-related traits under repeated stress. Candidate genes in these loci include factors involved in RNA splicing (arginine/serine-rich splicing factors), carbohydrate metabolism (trehalose-6-phosphate phosphatase), cytoskeletal organization (actin bundling proteins), and cell wall modification (xyloglucan endotransglucosylase). Expression analyses showed that these genes are rapidly induced under combined stress, suggesting a coordinated regulatory network for stress adaptation. Notably, some identified loci were specifically linked to traits reflecting transgenerational memory, supporting a genetic basis for intergenerational stress adaptation. By integrating phenotypic and genomic data, this study reveals key molecular mechanisms by which wheat perceives, responds to, and retains memory of drought and heat stress. The identified genetic markers and candidate genes offer valuable targets for breeding programs and biotechnological interventions aimed at enhancing wheat resilience. These insights are directly applicable to the development of stress-tolerant wheat cultivars, contributing to sustainable crop production and yield stability under the increasing abiotic stresses of climate change.

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