Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree

Abstract

Although the relationship of angiosperms to other seed plants remains controversial1, great progress has been made in identifying the earliest extant splits in flowering-plant phylogeny, with the discovery that the New Caledonian shrub Amborella trichopoda, the water lilies (Nymphaeales), and the woody Austrobaileyales constitute a basal grade of lines that diverged before the main radiation in the clade2,3,4,5,6,7,8. By focusing attention on these ancient lines, this finding has re-written our understanding of angiosperm structural and reproductive biology, physiology, ecology and taxonomy9,10,11,12. The discovery of a new basal lineage would lead to further re-evaluation of the initial angiosperm radiation, but would also be unexpected, as nearly all of the 460 flowering-plant families have been surveyed in molecular studies10. Here we show that Hydatellaceae, a small family of dwarf aquatics that were formerly interpreted as monocots, are instead a highly modified and previously unrecognized ancient lineage of angiosperms. Molecular phylogenetic analyses of multiple plastid genes and associated noncoding regions from the two genera of Hydatellaceae identify this overlooked family as the sister group of Nymphaeales. This surprising result is further corroborated by evidence from the nuclear gene phytochrome C (PHYC), and by numerous morphological characters. This indicates that water lilies are part of a larger lineage that evolved more extreme and diverse modifications for life in an aquatic habitat than previously recognized.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Hydatellaceae.
Figure 2: Phylogenetic placement of Trithuria submersa (Hydatellaceae) in angiosperms according to 17 plastid protein-coding loci and six associated noncoding regions.
Figure 3: Local placement of Hydatellaceae according to additional molecular data for Hydatella and Trithuria , and morphological data for the family as a whole.
Figure 4: Most parsimonious position of Hydatellaceae on the basis of morphology.

References

  1. Burleigh, J. G. & Mathews, S. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. Am. J. Bot. 91, 1599–1613 (2004)

    CAS  Article  Google Scholar 

  2. Soltis, P. S., Soltis, D. E. & Chase, M. W. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402–404 (1999)

    ADS  CAS  Article  Google Scholar 

  3. Graham, S. W. & Olmstead, R. G. Utility of 17 chloroplast genes for inferring the phylogeny of the basal angiosperms. Am. J. Bot. 87, 1712–1730 (2000)

    CAS  Article  Google Scholar 

  4. Mathews, S. & Donoghue, M. J. Basal angiosperm phylogeny inferred from duplicate phytochromes A and C. Int. J. Plant Sci. 161, (6 Suppl.)S41–S55 (2000)

    Article  Google Scholar 

  5. Zanis, M. J., Soltis, D. E., Soltis, P. S., Mathews, S. & Donoghue, M. J. The root of angiosperms revisited. Proc. Natl Acad. Sci. USA 99, 6848–6853 (2002)

    ADS  CAS  Article  Google Scholar 

  6. Borsch, T. et al. Noncoding plastid trnTtrnF sequences reveal a well resolved phylogeny of basal angiosperms. J. Evol. Biol. 16, 558–576 (2003)

    CAS  Article  Google Scholar 

  7. Qiu, Y.-L. et al. Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. Int. J. Plant Sci. 166, 815–842 (2005)

    CAS  Article  Google Scholar 

  8. Leebens-Mack, J. et al. Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one’s way out of the Felsenstein zone. Mol. Biol. Evol. 22, 1948–1963 (2005)

    CAS  Article  Google Scholar 

  9. Doyle, J. A. & Endress, P. K. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int. J. Plant Sci. 161, (6 Suppl.)S121–S153 (2000)

    CAS  Article  Google Scholar 

  10. Angiosperm Phylogeny Group (APG II). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. Bot. J. Linn. Soc. 141, 399–436 (2003)

  11. Williams, J. H. & Friedman, W. E. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. Am. J. Bot. 91, 332–351 (2004)

    Article  Google Scholar 

  12. Feild, T. S., Arens, N. C., Doyle, J. A., Dawson, T. E. & Donoghue, M. J. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82–107 (2004)

    Article  Google Scholar 

  13. Hamann, U. Hydatellaceae—a new family of Monocotyledoneae. N. Zeal. J. Bot. 14, 193–196 (1976)

    Article  Google Scholar 

  14. Bremer, K. Gondwanan evolution of the grass alliance of families (Poales). Evolution 56, 1374–1387 (2002)

    CAS  Article  Google Scholar 

  15. Dahlgren, R. M. T., Clifford, H. T. & Yeo, P. F. The Families of the Monocotyledons: Structure, Evolution, and Taxonomy (Springer, Berlin, 1985)

    Book  Google Scholar 

  16. Hamann, U. in The Families and Genera of Vascular Plants IV. Flowering Plants. Monocotyledons. Alismatanae and Commelinanae (except Gramineae) (ed. Kubitzki, K.) 231–234 (Springer, Berlin, 1998)

    Google Scholar 

  17. Stevenson, D. W. et al. in Monocots: Systematics and Evolution (eds Wilson, K. L. & Morrison, D. A.) 17–24 (CSIRO, Collingwood, Australia, 2000)

    Google Scholar 

  18. Michelangeli, F. A., Davis, J. I. & Stevenson, D. W. Phylogenetic relationships among Poaceae and related families as inferred from morphology, inversions in the plastid genome, and sequence data from the mitochondrial and plastid genomes. Am. J. Bot. 90, 93–106 (2003)

    CAS  Article  Google Scholar 

  19. Graham, S. W., Olmstead, R. G. & Barrett, S. C. H. Rooting phylogenetic trees with distant outgroups: a case study from the commelinoid monocots. Mol. Biol. Evol. 19, 1769–1781 (2002)

    CAS  Article  Google Scholar 

  20. Doyle, J. A. Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44, 227–251 (2005)

    Article  Google Scholar 

  21. Sun, G. et al. Archaefructaceae, a new basal angiosperm family. Science 296, 899–904 (2002)

    ADS  CAS  Article  Google Scholar 

  22. Graham, S. W. et al. in Monocots: Comparative Biology and Evolution (excluding Poales) (eds Columbus, J. T., Friar, E. A., Porter, J. M., Prince, L. M. & Simpson, M. G.) 3–21 (Rancho Santa Ana Botanic Garden, Claremont, California, 2006)

    Google Scholar 

  23. Chase, M. W. et al. in Monocots: Comparative Biology and Evolution (excluding Poales) (eds Columbus, J. T., Friar, E. A., Porter, J. M., Prince, L. M. & Simpson, M. G.) 63–75 (Rancho Santa Ana Botanic Garden, Claremont, California, 2006)

    Google Scholar 

  24. Swofford, D. L. Phylogenetic Analysis Using Parsimony* (PAUP*) (Sinauer Associates, Sunderland, Massachusetts, 2002)

    Google Scholar 

  25. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

    Article  Google Scholar 

  26. Hamann, U. Neue Untersuchungen zur Embryologie und Systematik der Centrolepidaceae. Bot. Jahrb. Syst. 96, 154–191 (1975)

    ADS  Google Scholar 

  27. Cooke, D. A. in The Families and Genera of Vascular Plants IV. Flowering Plants. Monocotyledons. Alismatanae and Commelinanae (except Gramineae) (ed. Kubitzki, K.) 106–109 (Springer-Verlag, Berlin, 1998)

    Google Scholar 

  28. Appel, O. & Bayer, C. in The Families and Genera of Vascular Plants IV. Flowering Plants. Monocotyledons. Alismatanae and Commelinanae (except Gramineae) (ed. Kubitzki, K.) 208–211 (Springer, Berlin, 1998)

    Google Scholar 

  29. Kim, S., Soltis, D. E., Soltis, P. S., Zanis, M. J. & Suh, Y. Phylogenetic relationships among early-diverging eudicots based on four genes: were the eudicots ancestrally woody? Mol. Phylog. Evol. 31, 16–30 (2004)

    CAS  Article  Google Scholar 

  30. Maddison, D. R. & Maddison, W. P. MacClade 4: Analysis of Phylogeny and Character Evolution, Version 4.03 (Sinauer Associates, Sunderland, Massachusetts, 2001)

    Google Scholar 

  31. Harden, G. J. (ed.) Flora of New South Wales. Vol. 4 (Univ. of New South Wales, Kensington, New South Wales, Australia, 1993)

    Google Scholar 

Download references

Acknowledgements

We are grateful to K. Bremer (Uppsala University) and the Royal Botanic Gardens, Kew, for generously providing DNAs, and to J. Conran, J. Davis, A. Doust, P. Rudall and D. Stevenson and other workers responsible for making the field collections and generating cultivated material. We acknowledge critical review of the manuscript by S. C. H. Barrett, M. W. Chase, T. S. Feild and E. M. Friis. This research was supported by an NSERC Discovery Grant to S.W.G., NSERC postgraduate scholarships to J.M.S. and H.S.R., Alberta Ingenuity and University Graduate Fellowship (University of British Columbia) funding to J.M.S, an NSF grant to S.M, and Royal Botanic Gardens Trust Sydney funding to A.D.M. and B.G.B.

Author Contributions Plastid data were generated by J.M.S., H.S.R. and A.D.M.; nuclear data were generated by S.M.; morphological data were compiled and scored by J.A.D, P.K.E. and B.G.B. Analyses were conceived and performed by S.W.G, J.A.D., J.M.S., H.S.R and S.M. All authors contributed to the writing, which was coordinated by S.W.G. and J.A.D.

Novel sequences for this study have GenBank accession numbers as follows: Aphelia brizula (EF153935, EF153937, EF153939, EF153942, EF153945, EF153948, EF153950, EF153952, EF153954); Brasenia schreberi (DQ981792); Centrolepis monogyna (EF153934, EF153936, EF153938, EF153941, EF153944, EF153947, EF153949, EF153951, EF153953); Hydatella inconspicua (DQ916291); Trithuria submersa (AJ419142, DQ915185-DQ915189, DQ981794, EF153940, EF153943, EF153946); Schisandra sphenanthera (DQ981793). Alignments used are available for download in Supplementary Information

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sean W. Graham.

Ethics declarations

Competing interests

. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-4 with Legends, Supplementary Methods and additional references. The Supplementary Figures 1-4 are four full phylogenetic tree figures from analyses of: (1) 17 plastid genes combined, for an expanded taxon sampling compared to Fig. 2 of the main text; (2) the nuclear locus PHYC; (3) the plastid region trnTLF; (4) the unconstrained morphological analysis. Supplementary Methods contain notes on DNA sources, molecular analyses and scoring of morphological characters. (PDF 718 kb)

Supplementary Data 1

This file contains Supplementary Data 1 with Nexus file which is the main multigene plastid data set used to perform analyses summarized in Fig. 2 and Suppl. Fig. 1. (TXT 2633 kb)

Supplementary Data 2

This file contains Supplementary Data 2 with Nexus file which is the PHYC data set used to perform analyses summarized in Fig. 3a and Suppl. Fig. 2. (TXT 39 kb)

Supplementary Data 3

This file contains Supplementary Data 3 with Nexus file which is the plastid trnTLF data set used to perform analyses summarized in Fig. 3b and Suppl. Fig. 3. (TXT 205 kb)

Supplementary Data 4

This file contains Supplementary Data 4 with Nexus file which is the morphology data set used to perform analyses summarized in Fig. 3c, Fig. 4 and Suppl. Fig. 4. (TXT 19 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Saarela, J., Rai, H., Doyle, J. et al. Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree. Nature 446, 312–315 (2007). https://doi.org/10.1038/nature05612

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05612

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing