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April 27, 2009

Grain's Evolutionary Secret

popcornSome 300,000 species strong, flowering plants dominate terrestrial landscapes, prompting awe and wonder dating from the days of Charles Darwin about how this group arose. (See this month's Origins essay.) And although the blossoms themselves contributed much to the success of angiosperms—attracting and making efficient use of insects and other pollinators—they are not the only feature that gave angiosperms a leg up on earlier seed plants. The way angiosperms provide nutrients for their seeds represents an underappreciated, cost-saving innovation that arguably made human civilization possible. It’s called the endosperm, and it's what pops in popcorn (left) and forms the bulk of what's in flour, rice, oats, and other grains, providing humans with two out of every three calories worldwide. “You take endosperm off the table, and you have fern fiddleheads and not much more [to eat],” says William "Ned" Friedman, a botanist at the University of Colorado, Boulder. “Even a grain-fed cow is really processed endosperm.”

Endosperm is the nutrient-filled tissue that sustains the growth of the embryo within a seed, sometimes early in development and sometimes later, once the seed has germinated. It arises through an innovation called “double fertilization.”  Each pollen grain produces two sperm, one of which fertilizes the “egg” and one of which merges with a so-called central cell that’s colocated with the “egg” in the female embryo sac. That latter fertilization sets off the growth and development of endosperm, which becomes packed with starches, proteins, lipids, or oil, depending on the species. Endosperm can be solid, as in wheat, or liquid, as in coconut milk. This double fertilization ensures that the embryo will have the sustenance it needs to complete its development.

embryoPines, firs, ginkgoes, and other gymnosperms also have nutritive tissue, but their tissue is prepared well in advance, laid down as the egg is maturing and well before fertilization. “It’s a slow process,” says Friedman, and should subsequent fertilization fail, this effort goes to waste. By jump-starting embryo and endosperm development simultaneously, angiosperms save time and cut down on wasted effort. “My sense is this [change] opened up all kinds of opportunities,” he adds. For example, now life cycles could be completed in a season, making possible annuals and other rapidly reproducing plants. But how did this just-in-time provisioning evolve?


Photo Credits:  William "Ned" Friedman.

Friedman has been studying double fertilization in plants at the bottom of the angiosperm family tree to find out. With the help of technician Samuel Holloway and other colleagues, he has characterized the structure of embryo sacs in several ancient living angiosperms. They have shown that different plants vary in the number of cells, the number of nuclei, and sets of chromosomes in the central cell of the embryo sac. As with the egg’s nucleus, each central cell nucleus typically has a single set, or haploid number, of chromosomes. But in some species, particularly later-evolving ones, the central cell can have double, quadruple, or even more sets of chromosomes. When these central cells merge with the sperm’s nucleus, they create endosperm with high numbers of sets of chromosomes.

If the early evolving water lilies are any indication, endosperm fertilization was once as straightforward as fertilization of the egg. In most flowering plants, the endosperm is triploid, and the ratio of female to male DNA is 2:1 within the endosperm. For almost a century, researchers had assumed that the endosperm of the first flowering plants was triploid.

But in 2002, Friedman and Joseph Williams of the University of Tennessee, Knoxville, took a close look at endosperm in a water lily, Nuphar polysepalum. Water lilies sit low on the angiosperm tree, and their features could represent the ancestral conditions. The duo found that instead of consisting of cells with triploid nuclei, Nuphar endosperm was diploid, just like the embryo. Moreover, Nuphar’s embryo sac had just four cells, not seven as in most angiosperms. Those four are an egg cell, a central cell, and two sterile cells. With the typical seven seen in most angiosperms, all but the central cell have one nucleus, while the central cell has two, which merge with a sperm to make triploid endosperm.

For years, some researchers had proposed that the “missing” cells in Nuphar had died or fused prefertilization. Williams and Friedman used fluorescent microspectrophotometry to closely monitor the amount of DNA in each cell as fertilization occurred to help determine if any DNA—that is, extra cells—were involved. They observed that the second sperm fused with the central cell and that, with both the egg and the central cell, fertilization led to no more than diploid amounts of DNA, demonstrating that this species never had more than four cells or nuclei.

Williams and Friedman hypothesized that the diploid endosperm and the four-cell embryo sac was the ancestral condition. But Friedman’s 2006 study of Amborella trichopoda, a New Caledonia flower that represents the oldest lineage of angiosperms, gave him pause. Though another basal angiosperm, Amborella had a much bigger embryo sac, with eight cells and nine nuclei, making him question what the ancestral endosperm was like. However, last year he and other researchers looked at another primitive angiosperm, Hydatella, a supposed monocot that recently was moved down to the water lilies on the angiosperm family tree. It too has a four-cell embryo sac, with four nuclei, and a diploid endosperm, he reported in Nature. “The diploid endosperm is the beginning point and the four-celled [embryo sac] is the beginning point,” he says.

Hydatella had another perhaps primitive feature. Unlike other flowering plants, it, like gymnosperms, creates an embryo-nourishing tissue prior to fertilization. “Hydatella may be bridging the gap to early angiosperms,” Friedman suggests.

In a recent paper, he and Kirsten Ryerson of the University of Colorado, Boulder, synthesized these ideas. They suggest that the production of embryo sac cells in all ancient lineages of angiosperms was modular. With one module, four nuclei—distributed in the egg, two sterile cells, and the central cell—arise; with two modules, mitosis leads to eight nuclei distributed among seven cells, including a central cell with two nuclei. Amborella is unique in that an extra cell division forms the egg, resulting in the eight cells and nine nuclei. Modularity is a recurrent theme in plants and is seen in the leaves on a shoot system as well, says Friedman.

—Elizabeth Pennisi

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