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

Ma, X.; Vanneste, S.; Chang, J.; Ambrosino, L.; Barry, K.; Bayer, T.; Bobrov, A. A.; Boston, L.; Campbell, J. E.; Chen, H.; Chiusano, M. L.; Dattolo, E.; Grimwood, J.; He, G.; Jenkins, J.; Khachaturyan, M.; Marin-Guirao, L.; Mesterhazy, A.; Muhd, D.-D.; Pazzaglia, J.; Plott, C.; Rajasekar, S.; Rombauts, S.; Ruocco, M.; Scott, A.; Tan, M. P.; Van de Velde, J.; Vanholme, B.; Webber, J.; Wong, L. L.; Yan, M.; Sung, Y. Y.; Novikova, P.; Schmutz, J.; Reusch, T.; Procaccini, G.; Olsen, J.; Van de Peer, Y.

doi:10.1101/2023.03.05.531170

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bioRxiv · 10.1101/2023.03.05.531170

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

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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), and Thalassia testudinum (Hydrocharitaceae) - along with an improved assembly for Zostera marina (Zosteraceae). We also include a draft genome of Potamogeton 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 for C. nodosa and P. 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.

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Ma, X., Vanneste, S., Chang, J., Ambrosino, L., Barry, K., Bayer, T., Bobrov, A. A., Boston, L., Campbell, J. E., Chen, H., Chiusano, M. L., Dattolo, E., Grimwood, J., He, G., Jenkins, J., Khachaturyan, M., Marin-Guirao, L., Mesterhazy, A., Muhd, D.-D., Pazzaglia, J., Plott, C., Rajasekar, S., Rombauts, S., Ruocco, M., Scott, A., Tan, M. P., Van de Velde, J., Vanholme, B., Webber, J., Wong, L. L., Yan, M., Sung, Y. Y., Novikova, P., Schmutz, J., Reusch, T., Procaccini, G., Olsen, J., Van de Peer, Y.. 2023-03-06. Seagrass genomes reveal a hexaploid ancestry facilitating adaptation to the marine environment. https://doi.org/10.1101/2023.03.05.531170

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