Gradual genomic streamlining and convergent adaptation during terrestrial-to-aquatic transitions in angiosperms

Aquatic angiosperms are crucial to global ecosystems. They independently transitioned from land to water multiple times, yet the overarching pattern of these transitions remains poorly understood. We analyzed over 330,000 angiosperm species, including 1,001 sequenced genomes, alongside ecoenvironmental datasets. Our results identify at least 132 transitions from terrestrial-to-aquatic habits and 86 reversals. Notably, terrestrial-to-aquatic transitions are marked by the contraction of 232 gene families, with no evidence of expansion. This contraction follows a gradient: greater aquatic adaptations, more contractions. Knowledge-enhanced machine learning associates these contractions with reduced functions in plant organ growth and development, structural support, drought responses, hormone regulation, and microbial defense. Interestingly, the contraction of microbial defense genes highlights a gradient of immune system reduction across aquatic plants. Biogeographic analysis further shows that precipitation and elevation, rather than temperature, shape the global distribution of aquatic species. However, historical temperature shifts, such as Cenozoic cooling, contributed to the decline of aquatic plants by reducing precipitation and elevation during polar ice-sheet formation. By contrast, ongoing global warming may reverse this trend by expanding aquatic habitats, though increased evaporation and drought are expected in some regions. This study provides a molecular framework for understanding aquatic plant evolution and offers insights into their potential responses to future climate change.