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

Journal name:
Nature
Volume:
530,
Pages:
331–335
Date published:
DOI:
doi:10.1038/nature16548
Received
Accepted
Published online

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.

At a glance

Figures

  1. Zostera marina and phylogenetic tree showing gene family expansion/contraction analysis compared with 13 representatives of the Viridiplantae.
    Figure 1: Zostera marina and phylogenetic tree showing gene family expansion/contraction analysis compared with 13 representatives of the Viridiplantae.

    a, Gains and losses are indicated along branches and nodes. The number of gene families, orphans (single-copy gene families) and number of predicted genes is indicated next to each species. Background colours (top to bottom) are Alismatales, other monocots, dicots, mosses/algae b, Typical Zostera marina meadow, Archipelago Sea, southwest Finland (photo by C.B.).

  2. Ancient whole-genome duplication (WGD).
    Figure 2: Ancient whole-genome duplication (WGD).

    a, KS-based age distribution of the whole Z. marina paranome. The x axis shows the synonymous distance until a KS cut-off of 2, in bins of 0.04, containing the KS values that were used for mixture modelling (excluding those with a KS ≤ 0.1). The component of the Gaussian mixture model plotted in red (as identified by EMMIX) corresponds to a WGD feature based on the SiZer analysis (other components are shown in black). The transition from the blue to the red at a KS of ~0.8 in the SiZer panel (below) indicates a change in the distribution and therefore provides evidence for an ancient WGD (Supplementary Table 4.1, Supplementary Fig. 4.1). b, Absolute age distribution obtained by phylogenomic dating of Z. marina paralogues. The solid black line represents the kernel density estimate (KDE) of the dated paralogues and the vertical dashed black line represents its peak, used as the consensus WGD age estimate, at 67 Mya. Grey lines represent the density estimates from 2,500 bootstrap replicates and the vertical black dotted lines represent the corresponding 90% confidence interval for the WGD age estimate, 64–72 Mya. The original raw distribution of dated paralogues is indicated by the circles. The y axis represents the percentage of gene pairs. c, Pruned phylogenetic tree with indication of WGD events (boxes)29. The Cretaceous–Palaeogene (K–Pg) boundary is indicated by an arrow.

  3. Reconstruction of metabolic (or gene) pathways involved in the production of stomata, ethylene, terpene and pollen in Z. marina.
    Figure 3: Reconstruction of metabolic (or gene) pathways involved in the production of stomata, ethylene, terpene and pollen in Z. marina.

    a, Stomata differentiation from meristemoid mother cells (MMC) to guard mother cell (GMC) to guard cells. b, Ethylene synthesis and signalling up to EIN2 have disappeared; EIN3 and its downstream targets remain. c, Terpenoid biosynthesis in which the pathways producing volatiles are absent but those essential for primary metabolism remain. MVA, mevalonate; MEP, plastidic methylerythritol phosphate; IPP, isopentenyl pyrophosphate; DMAPP, dimethylallyl pyrophosphate; FPP, farnesyl pyrophosphate; GPP, geranyl diphosphate; GGPP, geranylgeranyl pyrophosphate; CPP, copalyl pyrophosphate; GA, gibberellic acid; PP, diphosphate; ABA, abscisic acid. d, Sporopollenin biosynthesis genes; regulatory genes in the nucleus control downstream processes (arrows) in response to signalling coming from external stimuli through receptors on the plasma membrane. All panels: genes in red are absent; blue are present; the grey line represents the plasma membrane. See Extended Data Tables 1, 2, 3.

  4. Number of genes expressed in five tissues of Z. marina.
    Extended Data Fig. 1: Number of genes expressed in five tissues of Z. marina.

    a, Venn diagram of genes with expression values (FPKM) higher than 1 are considered as expressed in the tissue. b, Pairwise differential gene expression analysis between tissues. The male flower shows the highest number of differentially expressed genes.

  5. Circos plot of the ten largest scaffolds of Z. marina.
    Extended Data Fig. 2: Circos plot of the ten largest scaffolds of Z. marina.

    Tracks from outside to inside. GC percentage, gene density, and transposable element (TE) density (density measured in 20-Kb sliding windows and gene expression profiles from five tissues (root, leaf, male flower, female flower early and female flower late) presented as log2 FPKM values.

  6. Potential impact of transposable elements (TEs) on Z. marina evolution.
    Extended Data Fig. 3: Potential impact of transposable elements (TEs) on Z. marina evolution.

    a, Frequency distribution of pairwise sequence identity values between copies of Copia- and Gypsy-type LTR retrotransposons and DNA transposons, and their cognate consensus sequences (younger repeats share higher sequence similarity). Two peaks are detectable for Copia-type elements. b, Distance to the closest TE for the set of Z. marina single-copy genes and the set of Z. marina accessory genes. TE-proximal accessory genes are more frequent than TE-proximal single-copy genes. c, Frequency of pairwise sequence identity between accessory gene-proximal Ty3-Gypsy elements and their cognate consensus sequences. A number of high-identity copies (that is, putatively young duplicate genes) is observed.

  7. Unrooted maximum likelihood tree of genes encoding light-harvesting complex A (LHCA) and LHCB proteins of Z.marina, Spirodela polyrhiza and Arabidopsis thaliana.
    Extended Data Fig. 4: Unrooted maximum likelihood tree of genes encoding light-harvesting complex A (LHCA) and LHCB proteins of Z.marina, Spirodela polyrhiza and Arabidopsis thaliana.

    The analysis was carried out on protein sequences using PhyML 3 with LG substitution model and 100 bootstrap replicates. Supplementary Note 7.1, Supplementary Table 7.3.

  8. Alignment of metallothionein (MT) and half-metallothionein (HMT) genes in Z. marina as compared with other plants.
    Extended Data Fig. 5: Alignment of metallothionein (MT) and half-metallothionein (HMT) genes in Z. marina as compared with other plants.

    Alignments were performed in ClustalW on the Lyon PBIL web server and edited manually. The upper alignments are for type 1–3 MTs and HMTs; the lower alignment is for type 4 EcMTs where there is no Zostera homologue. Conserved residues are shown in red and residues in the same amino acid group in blue. Cys and His residues, putatively involved in binding metals, are highlighted in green and yellow, respectively. Aromatic amino acids absent in canonical animal MTs are highlighted in grey. MTs and MT-like proteins were obtained from: Arabidopsis thaliana (ARATH), Japanese rice (ORYSJ), Cicer arietinum (CICAR), banana (MUSAC), wheat (WHEAT), potato (SOLTU), Setaria Italica (SETIT), Vitis vinifera (VITVI) and the alismatids: Posidonia oceanica (POSOC) highlighted in grey, Spirodela polyrhiza (SPIPO) highlighted in blue, and Zostera marina (ZOSMA) highlighted in yellow. See Supplementary Note 8.2.

  9. Conceptual summary of physiological and structural adaptations made by Z. marina in its return to the sea.
    Extended Data Fig. 6: Conceptual summary of physiological and structural adaptations made by Z. marina in its return to the sea.

    Ecosystem services shown in blue. Physical processes related to salinity, light and CO2 availability shown in white within light-green boxes. Gene losses and gains associated with morphological and physiological processes shown in white within the dark-green box on the right.

Tables

  1. Genes involved in stomata development in Z. marina compared to other angiosperms
    Extended Data Table 1: Genes involved in stomata development in Z. marina compared to other angiosperms
  2. Ethylene-responsive transcription factor genes (ERF) in Zostera marina
    Extended Data Table 2: Ethylene-responsive transcription factor genes (ERF) in Zostera marina
  3. Genes involved in pollen development of Z. marina compared to other angiosperms
    Extended Data Table 3: Genes involved in pollen development of Z. marina compared to other angiosperms

Accession codes

Primary accessions

BioProject

Gene Expression Omnibus

NCBI Reference Sequence

Sequence Read Archive

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Author information

  1. These authors contributed equally to this work.

    • Jeanine L. Olsen,
    • Gabriele Procaccini,
    • Thorsten B. H. Reusch &
    • Yves Van de Peer

Affiliations

  1. Groningen Institute of Evolutionary Life Sciences (GELIFES), University of Groningen, PO Box 11103, 9700 CC Groningen, The Netherlands

    • Jeanine L. Olsen &
    • Wytze T. Stam
  2. Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927, B-9052 Ghent, Belgium

    • Pierre Rouzé,
    • Bram Verhelst,
    • Yao-Cheng Lin,
    • Rolf Lohaus,
    • Kevin Vanneste &
    • Yves Van de Peer
  3. GEOMAR Helmholtz Centre for Ocean Research-Kiel, Evolutionary Ecology, Düsternbrooker Weg 20, D-24105 Kiel, Germany

    • Till Bayer,
    • Janina Brakel &
    • Thorsten B. H. Reusch
  4. Sorbonne Université, UPMC Univ Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688, Roscoff cedex, France

    • Jonas Collen,
    • Simon Dittami,
    • Gurvan Michel &
    • Thierry Tonon
  5. Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy

    • Emanuela Dattolo,
    • Chiara Lauritano &
    • Gabriele Procaccini
  6. Dipartimento di Scienze Agrarie e Ambientali, University of Udine, Via delle Scienze 206, 33100 Udine, Italy

    • Emanuele De Paoli
  7. INRA, UR1164 URGI—Research Unit in Genomics-Info, INRA de Versailles-Grignon, Route de Saint-Cyr, Versailles 78026, France

    • Florian Maumus
  8. Institute for Evolution and Biodiversity, Westfälische Wilhelms-University of Münster, Hüfferstrasse 1, D-48149 Münster, Germany

    • Anna Kersting &
    • Erich Bornberg-Bauer
  9. Institute for Computer Science, Heinrich Heine University, D-40255 Duesseldorf, Germany

    • Anna Kersting
  10. Department of Biological and Environmental Sciences, Bioinformatics Infrastructure for Life Sciences (BILS), University of Gothenburg, Medicinaregatan 18A, 40530 Gothenburg, Sweden

    • Mats Töpel
  11. Department of Energy Joint Genome Institute, 2800 Mitchell Dr., #100, Walnut Creek, California 94598, USA

    • Mojgan Amirebrahimi,
    • Mansi Chovatia,
    • Jane Grimwood,
    • Jerry W. Jenkins,
    • Hope Tice &
    • Jeremy Schmutz
  12. Environmental and Marine Biology, Faculty of Science and Engineering, Åbo Akademi University, Artillerigatan 6, FI-20520 Turku/Åbo, Finland

    • Christoffer Boström
  13. HudsonAlpha Institute for Biotechnology, 601 Genome Way NW, Huntsville, Alabama 35806, USA.

    • Jane Grimwood,
    • Jerry W. Jenkins &
    • Jeremy Schmutz
  14. Marine Ecology Group, Nord University, Postbox 1490, 8049 Bodø, Norway.

    • Alexander Jueterbock
  15. Amplicon Express, 2345 NE Hopkins Ct., Pullman, Washington 99163, USA.

    • Amy Mraz
  16. School of Marine Science and Policy, Department of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, 15-Innovation Way, Newark, Delaware 19711, USA

    • Pamela J. Green
  17. Marine Ecology and Evolution, Centre for Marine Sciences (CCMAR), University of Algarve, 8005-139 Faro, Portugal

    • Gareth A. Pearson
  18. King Abdullah University of Science and Technology (KAUST), Red Sea Research Center (RSRC), Thuwal 23955-6900, Saudi Arabia

    • Carlos M. Duarte
  19. University of Kiel, Faculty of Mathematics and Natural Sciences, Christian-Albrechts-Platz 4, 24118 Kiel, Germany

    • Thorsten B. H. Reusch
  20. Genomics Research Institute, University of Pretoria, Hatfield Campus, Pretoria 0028, South Africa

    • Yves Van de Peer
  21. Bioinformatics Institute Ghent, Ghent University, Ghent B-9000, Belgium

    • Yves Van de Peer

Contributions

J.L.O., T.B.H.R., G.P. and Y.V.d.P. are the lead investigators and contributed equally to the work. J.S., J.W.J., J.G., Y.V.d.P., B.V. and Y.-C.L. coordinated the bioinformatics activities surrounding assembly, quality control, set-up and maintenance of Z. marina on the ORCAE site and deposition of the Z. marina genome resource. T.B.H.R and T.B. generated and analysed RNA-seq libraries from flowers, rhizome, roots. J.L.O., Y.-C.L. and A.J. generated and analysed RNA-seq libraries from the genome genotype and temperature stress experiments. C.B., W.T.S. and J.L.O. contributed to biological sample collection, preparation and quality control prior to DNA extraction. A.M. performed the HMW DNA extraction and quality control from the genome genotype/clone. M.A., J.G., H.T. and M.C. contributed to WGS libraries and sequencing, (fosmid)-cloning and quality control. J.G. coordinated the sequencing of FES, quality control projects. Analysis of architectural features of the genome and annotation of specific gene families, including the written contributions to the main paper and Supplementary Information sections, were performed by the following co-authors: J.W.J., the chromosome assembly analysis; B.V. and Y.-C.L., gene family clustering and comparative phylogenomics; A.R.K. and E.B.B., Pfam domains; E.D.P. and P.J.G., miRNA; R.L., K.V. and Y.V.d.P., whole-genome duplication; F.M., Y.-C.L. and Y.V.d.P., transposable elements; B.V., co-linearity and synteny comparisons; M.T., organellar genomes; P.R., stomata gene family; G.M., cell wall polysaccharides and sulfotransferases; T.T., fatty acid metabolism and its relationship to cell walls and ion homeostasis; P.R., volatiles (ethylene, terpenes); P.R., J.B. and T.B.H.R., metallothioniens; P.R., G.A.P. and C.L., osmoregulation/ion homeostasis/stress-related genes; S.D. and E.D., photosynthetic/ light-sensing genes; G.M., CAZymes; T.B., T.B.H.R. and P.R., plant defence-related; T.B. assembly and analysis of MADS box genes (flowering); P.R.; Y.V.d.P. and Y.-C.L., pollen-related and self-incompatibility genes; F.M., SLR-1gene and core eukaryotic genes analysis (CEGMA). J.L.O., Y.V.d.P., T.B.H.R., C.M.D., Y.-C.L. and P.R. wrote and edited the main manuscript (including the Methods and Extended Data), and organized and further edited the individual contributions (as listed above) for the Supplementary Information sections. J.L.O. and Y.V.d.P. provided the overall evolutionary context and T.B.H.R., G.P. and C.M.D. provided the ecological and societal context. All authors read and commented on the manuscript.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Raw reads, the assembled genome sequence and annotation are accessible from NCBI under BioProject number PRJNA41721 with GenBank accession number LFYR00000000. The accession number for the Zostera marina Finnish Clone is BioSample SAMN00991190. Fosmid end sequence: GSS KG963492KG999999; KO000001KO144970, whole-genome shotgun data: SRA020075 and RNA-seq: GEO GSE67579. Further information on the Zostera marina project is available via the Online Resource for Community Annotation Eukaryotes (ORCA) at http://bioinformatics.psb.ugent.be/orcae/.

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Number of genes expressed in five tissues of Z. marina. (336 KB)

    a, Venn diagram of genes with expression values (FPKM) higher than 1 are considered as expressed in the tissue. b, Pairwise differential gene expression analysis between tissues. The male flower shows the highest number of differentially expressed genes.

  2. Extended Data Figure 2: Circos plot of the ten largest scaffolds of Z. marina. (676 KB)

    Tracks from outside to inside. GC percentage, gene density, and transposable element (TE) density (density measured in 20-Kb sliding windows and gene expression profiles from five tissues (root, leaf, male flower, female flower early and female flower late) presented as log2 FPKM values.

  3. Extended Data Figure 3: Potential impact of transposable elements (TEs) on Z. marina evolution. (151 KB)

    a, Frequency distribution of pairwise sequence identity values between copies of Copia- and Gypsy-type LTR retrotransposons and DNA transposons, and their cognate consensus sequences (younger repeats share higher sequence similarity). Two peaks are detectable for Copia-type elements. b, Distance to the closest TE for the set of Z. marina single-copy genes and the set of Z. marina accessory genes. TE-proximal accessory genes are more frequent than TE-proximal single-copy genes. c, Frequency of pairwise sequence identity between accessory gene-proximal Ty3-Gypsy elements and their cognate consensus sequences. A number of high-identity copies (that is, putatively young duplicate genes) is observed.

  4. Extended Data Figure 4: Unrooted maximum likelihood tree of genes encoding light-harvesting complex A (LHCA) and LHCB proteins of Z.marina, Spirodela polyrhiza and Arabidopsis thaliana. (229 KB)

    The analysis was carried out on protein sequences using PhyML 3 with LG substitution model and 100 bootstrap replicates. Supplementary Note 7.1, Supplementary Table 7.3.

  5. Extended Data Figure 5: Alignment of metallothionein (MT) and half-metallothionein (HMT) genes in Z. marina as compared with other plants. (954 KB)

    Alignments were performed in ClustalW on the Lyon PBIL web server and edited manually. The upper alignments are for type 1–3 MTs and HMTs; the lower alignment is for type 4 EcMTs where there is no Zostera homologue. Conserved residues are shown in red and residues in the same amino acid group in blue. Cys and His residues, putatively involved in binding metals, are highlighted in green and yellow, respectively. Aromatic amino acids absent in canonical animal MTs are highlighted in grey. MTs and MT-like proteins were obtained from: Arabidopsis thaliana (ARATH), Japanese rice (ORYSJ), Cicer arietinum (CICAR), banana (MUSAC), wheat (WHEAT), potato (SOLTU), Setaria Italica (SETIT), Vitis vinifera (VITVI) and the alismatids: Posidonia oceanica (POSOC) highlighted in grey, Spirodela polyrhiza (SPIPO) highlighted in blue, and Zostera marina (ZOSMA) highlighted in yellow. See Supplementary Note 8.2.

  6. Extended Data Figure 6: Conceptual summary of physiological and structural adaptations made by Z. marina in its return to the sea. (631 KB)

    Ecosystem services shown in blue. Physical processes related to salinity, light and CO2 availability shown in white within light-green boxes. Gene losses and gains associated with morphological and physiological processes shown in white within the dark-green box on the right.

Extended Data Tables

  1. Extended Data Table 1: Genes involved in stomata development in Z. marina compared to other angiosperms (601 KB)
  2. Extended Data Table 2: Ethylene-responsive transcription factor genes (ERF) in Zostera marina (572 KB)
  3. Extended Data Table 3: Genes involved in pollen development of Z. marina compared to other angiosperms (408 KB)

Supplementary information

PDF files

  1. Supplementary information (16.3 MB)

    This file contains Supplementary Text, Supplementary Figures and Supplementary Tables – see contents page for details.

Zip files

  1. Supplementary Data (19.9 MB)

    This zipped file contains Supplementary Datasets 1-8.

Additional data