Transcriptomic and metabolic reprogramming of durum wheat under nanoplastic exposure

Polystyrene nanoplastics (PSNPs) in agricultural soils are emerging contaminants, yet their effects on staple crops and the extent to which plants genetic background modulates these responses remain poorly understood. Using molecular and biochemical analyses, we investigated the uptake and translocation of 50 and 100 nm PSNPs in durum wheat seedlings and their short-term effects on physiology, metabolism, and transcriptomic profiles. We compared the wild-type Kronos with MRP3, a TILLING-derived mutant in the TdMRP3 genes encoding the multidrug resistance–associated protein 3, a vacuolar phytic acid transporter, also known to sequester xenobiotics from the cytosol to direct them in the vacuoles. PSNPs penetrated roots and were translocated to shoots in both genotypes. In Kronos, exposure to PSNPs stimulated growth, photosynthetic performance, and carbohydrate mobilization, indicating adaptive metabolic reprogramming. Transcriptomic profiling revealed enrichment of osmotic stress related pathways, including upregulation of aquaporin genes and glycolytic routes, supporting water balance and energy homeostasis. Conversely, MRP3 showed growth reduction, increased lipid peroxidation, proline accumulation, and transcriptional repression of photosynthesis-related genes, reflecting a reduced capacity to cope with stress induced by PSNPs. These results demonstrate a key role for TdMRP3 in mitigating the effects of PSNPs in durum wheat, likely by enhancing sequestration of PSNPs into vacuoles. By contrast, mutations in this transporter may favor accumulation of PSNPs in the cytosol, exacerbating stress and impairing cellular functions. Although Kronos adapts to PSNPs in the short term, reduced transpiration and gas exchange suggest that this response may be unsustainable over longer exposures. This study provides the first genotype-dependent, multi-omics analysis of durum wheat responses to PSNPs exposure, identifying early signatures associated with short-term tolerance or susceptibility that are directly relevant for the environmental risks assessment of PSNPs contamination in agroecosystems. • PSNPs induce osmotic stress in durum wheat • PSNPs induce a metabolic switch favouring simple sugars increase in durum wheat • PSNPs deeply alter the photosynthetic activity in the TdMRP3 mutant • 21 days exposure to PSNPs already reduced transpiration and gas exchange in both genpotypes