Duckweed genomes and epigenomes underlie triploid hybridization and clonal reproduction

The Lemnaceae (duckweeds) are the world's smallest but fastest-growing flowering plants. Prolific clonal propagation facilitates continuous micro-cropping for plant-based protein and starch production and holds tremendous promise for sequestration of atmospheric CO2. Here, we present chromosomal assemblies, annotations, and phylogenomic analysis of Lemna genomes that uncover candidate genes responsible for the unique metabolic and developmental traits of the family, such as anatomical reduction, adaxial stomata, lack of stomatal closure, and carbon sequestration via crystalline calcium oxalate. Lemnaceae have selectively lost genes required for RNA interference, including Argonaute genes required for reproductive isolation (the triploid block) and haploid gamete formation. Triploid hybrids arise commonly among Lemna, and we have found mutations in highly conserved meiotic crossover genes that could support polyploid meiosis. Further, mapping centromeres by chromatin immunoprecipitation suggests their epigenetic origin despite divergence of underlying tandem repeats and centromeric retrotransposons. Syntenic comparisons with Wolffia and Spirodela reveal that diversification of these genera coincided with the "Azolla event" in the mid-Eocene, during which aquatic macrophytes reduced high atmospheric CO2 levels to those of the current ice age. Facile regeneration of transgenic fronds from tissue culture, aided by reduced epigenetic silencing, makes Lemna a powerful biotechnological platform, as exemplified by recent engineering of high-oil Lemna that outperforms oil-seed crops.