Seagrass genomes reveal a hexaploid ancestry facilitating adaptation to the marine environment

Abstract

Seagrasses comprise the only submerged marine angiosperms, a feat of adaptation from three independent freshwater lineages within the Alismatales. These three parallel lineages offer the unique opportunity to study convergent versus lineage-specific adaptation to a fully marine lifestyle. Here, we present chromosome-level genome assemblies from a representative species of each of the seagrass lineages -Posidonia oceanica(Posidoniaceae),Cymodocea nodosa(Cymodoceaceae), andThalassia testudinum(Hydrocharitaceae)-along with an improved assembly forZostera marina(Zosteraceae). We also include a draft genome ofPotamogeton acutifolius, a representative of Potamogetonaceae, the freshwater sister lineage to the Zosteraceae. Genome analysis reveals that all seagrasses share an ancient whole genome triplication (WGT) event, dating to the early evolution of the Alismatales. An additional whole genome duplication (WGD) event was uncovered forC. nodosaandP. acutifolius. Dating of ancient WGDs and more recent bursts of transposable elements correlate well with major geological and recent climatic events, supporting their role as rapid generators of genetic variation. Comparative analysis of selected gene families suggests that the transition from the submerged-freshwater to submerged-marine environment did not require revolutionary changes. Major gene losses related to, e.g., stomata, volatiles, defense, and lignification, are likely a consequence of the submerged lifestyle rather than the cause (‘use it or lose it’). Likewise, genes, often retained from the WGD and WGT, were co-opted for functions requiring the alignment of many small adaptations (‘tweaking’), e.g., osmoregulation, salinity, light capture, carbon acquisition, and temperature. Our ability to manage and conserve seagrass ecosystems depends on our understanding of the fundamental processes underpinning their resilience. These new genomes will accelerate functional studies and are expected to contribute to transformative solutions — as continuing worldwide losses of the ‘savannas of the sea’ are of major concern in times of climate change and loss of biodiversity.

Genome evolution in plants and the origins of innovation

“…(2020) and (right) aquatic angiosperm species following Ma et al . (2023). In each case, the arrows indicate the branch along which a gene was lost.…”

“…Duckweeds show both absent and vestigial roots (Ware et al ., 2023), with a progression towards complete loss of roots accompanied by shifts in gene expression and the ultimate loss of the key developmental gene, WOX5, through a transposon insertion (Michael et al ., 2021). Many aquatic plants also lack stomata, and the loss of multiple components of the stomatal developmental pathway has been found among aquatic Alismatales (Ma et al ., 2023). The convergent losses across these lineages occur in the same gene families as those which have been lost in liverworts (Fig.…”