Genome evolution at the extreme of angiosperm miniaturization

Eukaryotic genomes vary by several orders of magnitude, yet this vast variation bears little relation to the complexity of the organisms they encode. Thus, how genome evolution accompanies changes in organismal complexity remains unresolved. A central obstacle is that major differences in body plan usually occur among deeply divergent lineages, entangling body plan evolution with the genomic divergence accumulated over long independent histories. Duckweeds offer a rare system in which successive body plan reductions can be traced within a single plant family. Across this trajectory, body size declined by nearly an order of magnitude and roots were progressively lost, culminating in the extreme of angiosperm miniaturization. Yet genome size increased nearly sixfold. Here, using a new chromosome-scale genome of Wolffia globosa and comparative genomics across nested evolutionary scales, we show that genome size, gene number, and functional repertoire followed distinct trajectories during miniaturization. Genome expansion was driven largely by transposable element accumulation, whereas the number of protein-coding genes remained stable. Aquatic adaptation itself promotes functional simplification, but establishes only a baseline. Duckweeds pushed this streamlining much further through additional contraction of developmental, structural, and biotic defense functions, alongside selective expansion of functions associated with growth and abiotic adaptation. This remodeling accumulated across successive evolutionary transitions through continued contraction of the same gene families and, more commonly, contraction of different families affecting the same biological processes. Organismal complexity may therefore reflect not simply the size of a genome or its functional repertoire, but how that repertoire is selectively reconfigured through evolution.