Land plants first evolved from freshwater algae, and flowering plants returned to water as early as the Cretaceous and multiple times subsequently. Alismatales is the largest clade of aquatic angiosperms including all marine angiosperms, as well as terrestrial plants. We used Alismatales to explore plant adaptations to aquatic environments by analyzing a data set that included 95 samples (89 Alismatales species) covering four genomes and 91 transcriptomes (59 generated in this study). To provide a basis for investigating adaptations, we assessed phylogenetic conflict and whole-genome duplication (WGD) events in Alismatales. We recovered a relationship for the three main clades in Alismatales as (Tofieldiaceae, Araceae) + core Alismatids. We also found phylogenetic conflict among the three main clades that was best explained by incomplete lineage sorting and introgression. Overall, we identified 18 putative WGD events across Alismatales. One of them occurred at the most recent common ancestor of core Alismatids, and three occurred at seagrass lineages. We also found that lineage and life-form were both important for different evolutionary patterns for the genes related to freshwater and marine adaptation. For example, several light or ethylene-related genes were lost in the seagrass Zosteraceae, but are present in other seagrasses and freshwater species. Stomata-related genes were lost in both submersed freshwater species and seagrasses. Nicotianamine synthase genes, which are important in iron intake, expanded in both submersed freshwater species and seagrasses. Our results advance the understanding of the adaptation to aquatic environments and whole-genome duplications using phylogenomics.

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Monocots are one of the most diverse groups of flowering plants, and tracing the evolution of their ancestral genome into modern species is essential for understanding their evolutionary success. Here, we report a high-quality assembly of the Acorus tatarinowii genome, a species that diverged early from all the other monocots. Genome-wide comparisons with a range of representative monocots characterized Acorus as a slowly evolved genome with one whole-genome duplication. Our inference of the ancestral monocot karyotypes provides new insights into the chromosomal evolutionary history assigned to modern species and reveals the probable molecular functions and processes related to the early adaptation of monocots to wetland or aquatic habitats (that is, low levels of inorganic phosphate, parallel leaf venation and ephemeral primary roots). The evolution of ancestral gene order in monocots is constrained by gene structural and functional features. The newly obtained Acorus genome offers crucial evidence for delineating the origin and diversification of monocots, including grasses.