Cadmium (Cd) contamination poses a persistent threat to plant fitness and ecosystem stability, yet the molecular basis of sex-dependent Cd tolerance in dioecious plants remains unclear. In this study, the dioecious early land plant Marchantia polymorpha was employed to investigate the transcriptomic and metabolomic responses, physiological and morphological variations, and the remedial effects of exogenous glutathione (GSH). Physiological analyses revealed pronounced sexual dimorphism: females accumulated significantly more Cd (82.97 ± 0.75 mg kg⁻1) than males (61.80 ± 0.10 mg·kg⁻1) and suffered more severe chlorosis and oxidative damage, whereas males maintained lower Cd burdens and exhibited stronger antioxidant enzyme activities, including superoxide dismutase (SOD) and catalase (CAT). Transcriptomic analysis identified 4,547 differentially expressed genes (DEGs) in females and 4,102 in males under Cd stress, with GO and KEGG enrichment revealing that females preferentially reprogrammed photosynthesis and defense-related pathways, while males activated carbohydrate metabolism and cell wall remodeling. Metabolomic profiling further uncovered sex-divergent metabolic flux, with females accumulating naringenin chalcone (log₂FC = 3.88) and males specifically upregulating quercetin biosynthesis via F3’H. Integrated transcriptomic and metabolomic analysis highlighted three core pathways—flavonoid biosynthesis, tyrosine metabolism, and GSH metabolism—as central hubs of sex-specific Cd responses. Exogenous GSH application alleviated Cd-induced toxicity in a sex-dependent manner: males showed greater reduction in Cd accumulation (32.58%) compared to females (8.36%) and more efficient restoration of redox homeostasis, while females exhibited stronger recovery of photosynthetic pigments and flavonoid accumulation. This study provides a molecular-level perspective for understanding sex-dependent heavy metal adaptation in early land plants and offers a rationale for sex-aware phytoremediation strategies.
Yang et al. (Wed,) studied this question.