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

Nature volume 446, pages 312–315 (2007)Cite this article

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.

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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.

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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

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Author notes

  1. Jeffery M. Saarela

    Present address: Present address: Research Division, Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, Ontario K1P 6P4, Canada.,

Authors and Affiliations

  1. and Department of Botany, UBC Botanical Garden and Centre for Plant Research (Faculty of Land and Food Systems), Centre for Biodiversity Research, 2357 Main Mall, The University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada,

    Jeffery M. Saarela, Hardeep S. Rai & Sean W. Graham

  2. Section of Evolution and Ecology, University of California, Davis, California 95616, USA,

    James A. Doyle

  3. Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland,

    Peter K. Endress

  4. The Arnold Arboretum, 22 Divinity Avenue, Harvard University, Cambridge, Massachusetts 02138, USA,

    Sarah Mathews

  5. Royal Botanic Gardens, Mrs Macquaries Road, Sydney, New South Wales 2000, Australia,

    Adam D. Marchant & Barbara G. Briggs

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Correspondence to Sean W. Graham.

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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)

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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

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