Transgenerational plasticity (TGP) refers to the influence of ancestral environmental signals on offspring’s traits across generations. While evidence of TGP in plants is growing, its role in plant adaptation over successive generations remains unclear, particularly in floating plants facing fluctuating environments. Duckweed (Lemna minor), a common ecological remediation material, often coexists with the harmful bloom-forming cyanobacterium Microcystis aeruginosa, which releases a highly toxic exudate mixture (MaE) during its growth. In this study, we investigate the TGP of duckweed and its adaptive role under stress from MaE during the bloom-forming process. We found that exposure to MaE induces significant phenotypic plasticity in duckweed, manifested by alterations in morphological, physiological, and transcriptomic profiles. Specifically, MaE exposure significantly affected duckweed, promoting growth at low concentrations but inhibiting it at high concentrations, affecting traits like biomass, frond number, total frond area, and photosynthetic efficiency. Additionally, the activities of antioxidant enzymes, together with the levels of proline, soluble sugars, and proteins, are elevated with increasing MaE concentrations. These plastic changes are largely retained through asexual reproductive cycles, persisting for several generations even under MaE-free conditions. We identified 619 genes that maintain a ‘transcriptional memory’, some of which correlate with the TGP-linked alterations in morphological and physiological traits in response to MaE stress. Notably, progeny from MaE-exposed lineages demonstrate enhanced fitness when re-exposed to MaE. These results enhance our comprehension of the adaptive significance of TGP in plants and suggest feasible approaches for utilizing duckweed’s TGP in the bioremediation of detrimental algal blooms.
