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Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment

Nature Plants volume 10, pages 240–255 (2024)Cite this article

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Abstract

We present chromosome-level genome assemblies from representative species of three independently evolved seagrass lineages: Posidonia oceanica, Cymodocea nodosa, Thalassia testudinum and Zostera marina. We also include a draft genome of Potamogeton acutifolius, belonging to a freshwater sister lineage to Zosteraceae. All seagrass species share an ancient whole-genome triplication, while additional whole-genome duplications were uncovered for C. nodosa, Z. marina and P. acutifolius. Comparative analysis of selected gene families suggests that the transition from submerged-freshwater to submerged-marine environments mainly involved fine-tuning of multiple processes (such as osmoregulation, salinity, light capture, carbon acquisition and temperature) that all had to happen in parallel, probably explaining why adaptation to a marine lifestyle has been exceedingly rare. Major gene losses related to stomata, volatiles, defence and lignification are probably a consequence of the return to the sea rather than the cause of it. These new genomes will accelerate functional studies and solutions, as continuing losses of the ‘savannahs of the sea’ are of major concern in times of climate change and loss of biodiversity.

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Fig. 1: Distribution of the genomic features for the seagrass species T. testudinum, P. oceanica, Z. marina and C. nodosa.
Fig. 2: Time-calibrated phylogeny and WGT/WGD events across flowering plants that have chromosome-level genome assemblies.
Fig. 3: The loss, contraction and expansion of gene families involved in adaptation to a marine environment.
Fig. 4: Flower development (MADS-box genes) and pollen toolkit genes.

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Data availability

The DNA sequencing data for the C. nodosa genome assembly have been deposited in the NCBI database under BioProject PRJNA1041560 via the link https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA1041560. All assemblies and annotations for all seagrass species discussed in the current paper can be found at https://bioinformatics.psb.ugent.be/gdb/seagrasses/. The transcriptome data (including raw data and clean data) and sequencing QC reports for C. nodosa can be found at https://genome.jgi.doe.gov/portal/pages/dynamicOrganismDownload.jsf?organism=Cymnodnscriptome_2, the transcriptome data and sequencing QC reports for P. oceanica can be found at https://genome.jgi.doe.gov/portal/pages/dynamicOrganismDownload.jsf?organism=Posocenscriptome_2, the transcriptome data and sequencing QC reports for T. testudinum can be found at https://genome.jgi.doe.gov/portal/pages/dynamicOrganismDownload.jsf?organism=Thatesnscriptome_4 and the transcriptome data for Z. marina are from ref. 15. For the public databases, the RFAM database v.14.7 can be downloaded at https://ftp.ebi.ac.uk/pub/databases/Rfam/14.7/, the UniProt database can be accessed from the web at http://www.uniprot.org and downloaded from http://www.uniprot.org/downloads and the NCBI nucleotide database can be accessed via https://www.ncbi.nlm.nih.gov/.

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Acknowledgements

Y.V.d.P., J.L.O., T.B.H.R. and G.P. acknowledge funding from the DOE, JGI, Berkeley, California, USA, under the Community Sequencing Program 2018, project no. 504341 (Marine Angiosperm Genomes Initiative). The work (proposal no. 10.46936/10.25585/60001196) conducted by the DOE JGI (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the DOE operated under contract no. DE-AC02-05CH11231. The Community Sequencing Program award also included support for sequencing and plant bioinformatics from HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, and DNA/RNA extraction and processing from the Arizona Genomics Institute, Tucson, Arizona. Y.V.d.P. acknowledges funding from the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant no. 833522) and from Ghent University (Methusalem funding, grant no. BOF.MET.2021.0005.01). P.N. acknowledges funding by the Deutsche Forschungsgemeinschaft (German Research Foundation)—project no. 497665889, 1606/3-1 for research on Potamogeton. M.K. acknowledges funding through the Helmholtz School for Marine Data Science, grant no. HIDSS-0005. The work of G.P., E.D., J.P. and M.R. was partially supported by the project Marine Hazard, PON03PE_00203_1 (MUR, Italian Ministry of University and Research) and by the National Biodiversity Future Centre Program, Italian Ministry of University and Research, PNRR, Missione 4 Componente 2 Investimento 1.4 (project no. CN00000033). D.-D.M., L.L.W., M.P.T. and Y.Y.S. acknowledge funding from Universiti Malaysia Terengganu (SRG Vot55317). The work of A.A.B. was performed within the Papanin Institute for Biology of Inland Waters RAS state assignment (theme no. 121051100099-5).

Author information

Author notes

  1. These authors contributed equally: Xiao Ma, Steffen Vanneste, Jiyang Chang.

Authors and Affiliations

  1. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

    Xiao Ma, Jiyang Chang, Hengchi Chen, Stephane Rombauts, Bartel Vanholme & Yves Van de Peer

  2. Center for Plant Systems Biology, VIB, Ghent, Belgium

    Xiao Ma, Jiyang Chang, Hengchi Chen, Stephane Rombauts, Bartel Vanholme & Yves Van de Peer

  3. Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

    Steffen Vanneste

  4. Department of Research Infrastructure for Marine Biological Resources, Stazione Zoologica Anton Dohrn, Naples, Italy

    Luca Ambrosino & Maria Luisa Chiusano

  5. DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Kerrie Barry, Guifen He, Mi Yan & Jeremy Schmutz

  6. Marine Evolutionary Ecology, GEOMAR Helmholtz-Zentrum für Ozeanforschung Kiel, Kiel, Germany

    Till Bayer, Marina Khachaturyan & Thorsten B. H. Reusch

  7. Papanin Institute for Biology of Inland Waters RAS, Borok, Russia

    Alexander A. Bobrov

  8. Genome Sequencing Center, HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA

    LoriBeth Boston, Jane Grimwood, Jerry Jenkins, Chris Plott, Jenell Webber & Jeremy Schmutz

  9. Coastlines and Oceans Division, Institute of Environment, Florida International University—Biscayne Bay Campus, Miami, FL, USA

    Justin E. Campbell

  10. Department of Agricultural Sciences, University Federico II of Naples, Naples, Italy

    Maria Luisa Chiusano

  11. Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Naples, Italy

    Emanuela Dattolo, Lázaro Marín-Guirao, Jessica Pazzaglia, Miriam Ruocco & Gabriele Procaccini

  12. National Biodiversity Future Centre, Palermo, Italy

    Emanuela Dattolo, Jessica Pazzaglia & Gabriele Procaccini

  13. Institute of General Microbiology, University of Kiel, Kiel, Germany

    Marina Khachaturyan

  14. Seagrass Ecology Group, Oceanographic Center of Murcia, Spanish Institute of Oceanography (IEO-CSIC), Murcia, Spain

    Lázaro Marín-Guirao

  15. Centre for Ecological Research, Wetland Ecology Research Group, Debrecen, Hungary

    Attila Mesterházy

  16. Institute of Climate Adaptation and Marine Biotechnology, Universiti Malaysia Terengganu, Terengganu, Malaysia

    Danish-Daniel Muhd, Min Pau Tan, Li Lian Wong & Yeong Yik Sung

  17. Arizona Genomics Institute, University of Arizona, Tucson, AZ, USA

    Shanmugam Rajasekar

  18. Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy

    Miriam Ruocco

  19. Fano Marine Center, Fano, Italy

    Miriam Ruocco

  20. Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Köln, Germany

    Alison Scott, Jozefien Van de Velde & Polina Novikova

  21. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands

    Jeanine L. Olsen

  22. Centre for Microbial Ecology and Genomics, Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria, South Africa

    Yves Van de Peer

  23. College of Horticulture, Academy for Advanced Interdisciplinary Studies, Nanjing Agricultural University, Nanjing, China

    Yves Van de Peer

Authors
  1. Xiao Ma
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  2. Steffen Vanneste
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Contributions

Y.V.d.P., J.L.O., T.B.H.R. and G.P. conceived the project, provided the overall evolutionary context and wrote the proposal. Y.V.d.P., J.L.O., T.B.H.R., G.P. and S.V. wrote and edited the main paper and organized and further edited the individual contributions for the Supplementary Notes (as listed in the Supplementary Information). All authors then provided specific feedback in forming the final version. J.L.O., J.E.C., G.P., L.M.-G., T.B.H.R., A.A.B., A.M. and P.N. contributed to sample tissue collection, preparation and shipping for DNA extraction. S. Rajasekar, L.B., G.H., J.W. and M.Y. performed the HMW DNA extractions and quality control (QC), as well as RNA extractions and QC for annotation assistance. J.S. and J.G. coordinated the genome sequencing management steps for the seagrasses. A.M. and P.N. coordinated the genome sequencing management steps for Potamogeton. K.B. was responsible for overall JGI technical coordination and was the liaison with the principal investigators and project manager. J.J., C.P., J.S., Y.V.d.P., S. Rajasekar, A.S., J.V.d.V. and T.B. performed the analysis activities surrounding genome assembly (PacBio and HiC), supporting transcriptomics for annotation. J.J., Y.V.d.P., S. Rombauts and X.M. were responsible for the deposition and maintenance of the species on the ORCAE site and the deposition of the new genomes to NCBI and Phytozome. J.C., X.M. and S. Rombauts were responsible for the paper graphics. The authors responsible for the analysis of the architectural features of genome evolution and annotation of specific gene families, including the written contributions to the main paper and Supplementary Information sections, were as follows: M.L.C. and L.A. for the orthogroups master extended data; M.L.C., A.S., X.M. and J.C. for the overview of gene families; H.C., X.M., J.C. and Y.V.d.P. for WGDs/WGTs and dating; M.L.C. and X.M. for TEs and repeat elements; M.K. and T.B.H.R. for organellar genomes; M.L.C. and L.A. for non-protein-coding RNA families; S.V. and X.M. for stomata; S.V. and X.M. for volatile metabolites, signalling and ethylene; X.M. and S.V. for plant body development, lignification and vascular tissue; T.B. for plant defence and R-genes; L.M.-G. for heat shock factors; S.V. and X.M. for flavonoids and phenolics; S.V. for cellular salt tolerance; S.V. and B.V. for cell wall plasticity; S.V. and X.M. for hypoxia; G.P. for light perception, photosynthesis, light harvesting and transcription factors; G.P. and M.R. for carbon acquisition and CCMs; G.P. for UVB tolerance; G.P. and E.D. for clock genes; J.P. for No Apical Meristem genes; and D.-D.M., L.L.W., M.P.T. and Y.Y.S. for nitrogen metabolism.

Corresponding authors

Correspondence to Thorsten B. H. Reusch, Gabriele Procaccini, Jeanine L. Olsen or Yves Van de Peer.

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Peer review information

Nature Plants thanks Sean Graham and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Table 1 The copy number of guard cell toolkit genes
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Extended Data Table 2 The copy number of genes involved in triterpenes, JA, MeJA/MeSA and ethylene biosynthesis and signaling pathways
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Extended Data Table 3 The copy number of genes involved in vascular development
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Extended Data Table 4 The copy number of genes involved in lignin biosynthesis
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Extended Data Table 5 The copy number of resistance (NRL) genes and heat shock factors (HSF)
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Extended Data Table 6 The copy number of genes involved in flavonoid biosynthesis
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Extended Data Table 7 The copy number of genes involved in salt stress
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Extended Data Table 8 The copy number of genes involved in hypoxia tolerance
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Extended Data Table 9 The copy number of CO2-concentrating mechanisms (CCM)-related genes (Carbonic anhydrases, Boron transporters and proton pumps, C4-metabolism, Rubisco activase)
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Extended Data Table 10 The copy number of gene families involved in nitrogen metabolism
Full size table

Supplementary information

Supplementary Information

Five sections including Supplementary Figs. 1.1–5.9, Tables 1.1–5.9 and Notes.

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Ma, X., Vanneste, S., Chang, J. et al. Seagrass genomes reveal ancient polyploidy and adaptations to the marine environment. Nat. Plants 10, 240–255 (2024). https://doi.org/10.1038/s41477-023-01608-5

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