Heterophylly, characterized by distinct leaf morphologies, is an adaptive strategy evolved by some aquatic plants to cope with the contrasting environments in which they grow. It is shaped by environmental factors and by hormones, particularly abscisic and gibberellic acids. We conducted a comparative multi-omics analysis of submerged and floating leaves of Potamogeton nodosus, a heterophyllous species of the Alismatales order. Genome sequencing has confirmed its tetraploid status. A phylogenomic analysis has identified genes associated with aquatic adaptation, notably genes possibly involved in aurone biosynthesis, which are antioxidant flavonoids. Transcriptomic and metabolomic analyses have revealed distinct gene expression and metabolite patterns depending on the leaf position in the water column. The floating leaves exhibited upregulated genes associated with photosynthetic and metabolic activities, and with the accumulation of UV-protective metabolites reflecting light capture and photoprotection optimization. Conversely, submerged leaves showed upregulated genes associated with homeostatic processes, defense responses, and cell wall remodeling, reflecting tissue maintenance. We have also identified genes involved in the abscisic and gibberellic acids pathways. The developmental analyses highlighted active growth processes in young leaves. This multi-omic study provides an integrated understanding of the complex molecular mechanisms underlying the adaptation of P. nodosus to a dual lifestyle.
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