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April 21, 2009

Another Ancient Angiosperm Comes Out of the Closet

As I pointed out in my essay on the origin of flowering plants, a key breakthrough came in the late 1990s when molecular studies showed water lilies and the New Caledonia plant Amborella to be toward the bottom of the angiosperm tree. With these basal lineages in place, botanists could begin to tease out the more primitive angiosperm traits. More recently, another plant, this one masquerading as a monocot, a major group of flowering plants that includes grasses, orchids, and palms, has been reassigned to the primitive part of the tree, near the water lilies. Found in Australia and New Zealand, with one species in India, these tiny plants, which make up the Hydatellaceae family, like to be submerged, sometimes more than a meter deep, sending up flower stems 1 to 3.5 centimeters high with flowers 1 or 2 millimeters in size. From afar, they can look like a lawn of underwater moss.

stevenson_trithuria_submersa_02Though very odd in appearance and lifestyle, the Hydatellaceae had seemed to fit best with grasses: Both have reduced flowers, for example, and their seeds seemed similar in having what looks like one seedling leaf and not two as in the majority of angiosperms. At least one gene study has placed one of this group, Trithuria submersa (left), squarely among the grasses—although later this turned out to be a contaminant sequence.

Fascinated by this oddball, Sean Graham of the University of British Columbia Botanical Garden and his colleagues did a more thorough gene analysis. They isolated chloroplast genes from Trithuria and compared them to the same genes in a variety of other species. To their surprise, Trithuria proved to be quite a distant relative to grasses. Instead, this plant branched off the angiosperm family tree at about the same place as water lilies. This arrangement held fast even after Graham and his colleagues analyzed the data several different ways. Analyzing sequences from a nuclear gene and chloroplast genes from another Hydatellaceae, Hydatella inconspicua, supported this new classification as well, which they reported on in 2007.

From this new perspective, botanists have begun to realize that Hydatella and Trithuria really do fit nicely down at the base of the angiosperm tree, not high up among the later-evolving monocots. Their seeds have a cap called an operculum just like water lilies. Their embryo sacs, specialized sexual tissue of seeds, have fewer cells compared to those of more later-evolving species. And their carpels, protective sheaths surrounding the seeds, start out as cup-shaped, with margins that do not completely fuse as in carpels of most other plants. These traits in Hydatella “fit with an emerging picture in which the earliest angiosperms likely had many of these features,” says Graham. It also raises the question about whether the first flowering plants were aquatic, but many botanists don't think that was the case.

Now firmly ensconced among the water lilies, the Hydatellaceae are attracting quite a bit of interest. “We are trying to develop Hydatellaceae as a model organism for early-divergent angiosperms and are successfully growing and flowering it at Kew, though so far we have not managed to set seed,” says Paula Rudall, a botanist at the Royal Botanic Gardens, Kew. Her team has even isolated many of its genes.

Rudall, Dimitry Sokoloff of Moscow State University in Russia, and their colleagues have been going over these species micrometer by micrometer as well as second by second, probing both the structure and the development for clues about the most ancient angiosperms. The Trithuria flower seems to be inside-out, with stamens at the center instead of rimming centrally located carpels, they reported earlier this year, illustrating their paper with stunning pictures of the flower’s development.

Graham is refining the relationships among these and other basal angiosperms. Others, including his student Will Iles, are taking a close look at the species within this group. Already, these botanists have concluded that there’s just one genus, not two as had been thought, and at least 12 species, not 10. "We found that previously, males and females of the same species (some species are sexually dimorphic) had been included in different genera,” notes Rudall.

Graham hopes that one day botanical gardens will exhibit Hydatellaceae. “It’s not going to be a spectacular [display],” he admits, but for the study of angiosperm evolution, these plants’ contribution could be enormous.

—Elizabeth Pennisi

Credit: Dennis Wm. Stevenson, New York Botanical Garden

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