The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Abstract

Whole-genome sequencing of the seagrass Zostera, representing the first marine angiosperm genome to be fully sequenced, provides insight into the evolutionary changes associated with a transition to a marine environment in this angiosperm lineage. The seagrass Zostera marina, or eelgrass, is widely distributed throughout the Northern Hemisphere. It is therefore of considerable ecological importance but — as with other seagrasses — its coastal habitats are among the world's most threatened ecosystems. Jeanine Olsen and colleagues report the whole-genome sequence of Zostera. Their analyses provide insights into the evolutionary changes associated with the 'back to the sea' reverse evolutionary trajectory that has occurred in this angiosperm lineage, including the loss of the entire repertoire of stomatal genes, and the presence of sulfated cell-wall polysaccharides that are more macro-algal-like than plant-like. Seagrasses colonized the sea1 on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet2. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes3, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae4 and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming5,6, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants7.