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Hydatellaceae are water lilies with gymnospermous tendencies

Abstract

The flowering plant family Hydatellaceae was recently discovered to be allied to the ancient angiosperm lineage Nymphaeales (water lilies)1. Because of its critical phylogenetic position, members of the Hydatellaceae have the potential to provide insights into the origin and early diversification of angiosperms2. Here I report that Hydatella expresses several rare embryological features that, in combination, are found only in members of the Nymphaeales. At maturity, the female gametophyte is four-celled, four-nucleate and will produce a diploid endosperm, as is characteristic of most early divergent angiosperm lineages3,4. As with all members of the Nymphaeales, endosperm in Hydatella is minimally developed and perisperm is the major embryo-nourishing tissue within the seed5,6. Remarkably, Hydatella exhibits a maternal seed-provisioning strategy that is unique among flowering plants, but common to all gymnosperms7: pre-fertilization allocation of nutrients to the embryo-nourishing tissue. This exceptional case of pre-fertilization maternal provisioning of a seed in Hydatella may well be an apomorphic feature of Hydatellaceae alone but, given the newly discovered phylogenetic position of this family, potentially represents a plesiomorphic and transitional condition associated with the origin of flowering plants from gymnospermous ancestors.

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Figure 1: Schematic of four-celled, four-nucleate (Nuphar/Schisandra-type) female gametophyte development in Nymphaeales and Austrobaileyales and of seven-celled, eight-nucleate (Polygonum-type) development in most other angiosperms.
Figure 2: Female gametophyte development in Hydatella inconspicua.
Figure 3: Pre- and post-fertilization development of perisperm in H. inconspicua.

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Acknowledgements

I thank: P. Champion and A. Drinnan for collecting plant materials; S. Holloway for histological work; S. Renner for translation of the embryological studies of U. Hamaan; and P. Diggle, L. Hufford, J. Williams and R. Robichaux for feedback on this manuscript. This work was supported by a National Science Foundation Research Grant.

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Correspondence to William E. Friedman.

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Supplementary Figure

The file contains Supplementary Figure with Legend showing longitudinal section of recently fertilized ovule of Hydatella inconspicua. A pollen tube that entered the ovule through the micropyle formed by the two integuments can be clearly seen. The zygote contains a prominent vacuole and the primary endosperm nucleus is situated at the base of the former female gametophyte. Upper grey box contains digital superposition of pollen tube from adjacent histological section. Lower grey box contains digital superposition of primary endosperm from adjacent histological section. Bar = 10 μm. pen = primary endosperm nucleus; ps = perisperm; pt = pollen tube; z = zygote. (PDF 2617 kb)

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Friedman, W. Hydatellaceae are water lilies with gymnospermous tendencies. Nature 453, 94–97 (2008). https://doi.org/10.1038/nature06733

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