FREELOADERS

Dan Nickrent's "garden" boasts some of the most bizarre plants in the world. Like the enigmatic Rafflesia, whose enormous red-and-white-freckled flower smells like road kill. And Hydnora, which begins flowering underground, eventually producing flowers so powerful they can push up through concrete.

Nickrent, a professor of plant biology, works at the molecular level to unravel the mysteries of plant evolution. He delights in many kinds of flowers, but it's the "weirdest of the weird"--parasitic flowering plants--that stoke his scientific curiosity. He has trekked to Borneo, New Guinea, South Africa, Central America, and other places to gather and photograph these fascinating plants, and his lab contains the world's largest and most diverse collection of parasitic plant tissue and DNA samples.

He also tends the Parasitic Plant Connection, a fertile, award-winning web site with more than 1,700 images, representing 224 genera or 82 percent of all parasitic flowering plants--plus links to scientific articles, DNA data, and more. It is now the most comprehensive online collection of its kind, a valuable resource for botanists.

Parasitic flowering plants have a peculiar lifestyle. When their seeds make contact with a suitable host, they germinate and produce a modified root that drills its way into the tissue of the host plant, siphoning out nutrient-rich water. Some parasitic plants, called holoparasites, don't carry out photosynthesis and must load up on sugars from the host as well.

A few of the 4,000 species of these freeloaders are pathogenic, such as witchweed, the main cause of corn crop failure in Africa. But most are relatively innocuous. Take the sandalwood tree, for example. Or Indian paintbrush, common on Midwestern prairies. Or Rafflesia arnoldii, which boasts the world's largest flowers: three-foot-wide, waxy-looking reddish blooms that mimic the stench of rotting meat, hug the forest floor, and tip the scales at 25 pounds.

Sandalwood, Indian paintbrush, and Rafflesia are parasites that attach to the roots of host plants. Other parasites, such as dodder and mistletoe, are called stem parasites; they tap above-ground portions of plants. Mistletoe, for example, usually grows in the branches of trees.

Parasitic plants "represent unique evolutionary experiments," says Nickrent, who focuses on understanding their evolutionary history and the molecular mechanisms driving that evolution. Although parasitism has evolved several times among flowering plants, scientists "don't have a good handle" on why most of these species developed parasitism as an evolutionary strategy, he says.

Nickrent was one of the first scientists to begin using gene sequencing to understand the evolutionary relationships, or phylogeny, of parasitic plants. Comparing specific gene sequences across various species allows scientists to tease out how those species are related and which groups are ancestral to other groups. The more differences, the farther back in time the groups shared a common ancestor. The findings are often depicted in graphic form as a sort of "family tree."

Plants have genes in three places in the cell: in the nucleus, in energy-producing structures called mitochondria, and in chlorophyll-producing structures called chloroplasts. Early on, most plant biologists using genetic information to determine evolutionary relationships were focusing on a particular gene found in plants' chloroplasts. But there's a hitch with parasitic plants: some of them, over millions of years, have lost the ability to produce chlorophyll. As a result, they have only a remnant of chloroplast genetic material.

Nickrent, then at the University of Illinois, was among the first scientists to show that genetic material from the nucleus could be used instead. In his case, he was extracting a particular sequence of RNA and seeing how it varied in certain parasitic species. (RNA is DNA's "companion" molecule, various types of which translate DNA's instructions and assemble proteins.)

In collaboration with other scientists, Nickrent and his students proved the validity of this RNA sequence for analyzing evolutionary relationships not just among parasitic flowering plants, but among flowering plants in general. Many plant scientists have since adopted the use of nuclear genes, not just chloroplast genes, for such research.

Nickrent has worked for many years on determining the "family tree" for Santalales, the sandalwood order. This huge group of plants comprises more than 2,200 species, most of them parasitic, including the more than 1,500 species of mistletoes. His lab also has published extensively on holoparasites and how they are related to other groups of plants.

"We're fascinated with some of the processes going on in these plants at the genetic level," he says. "They're challenging a lot of 'set' biological ideas."

Nickrent and his students discovered, for example, that some genes mutate at an accelerated rate in these plants--up to three times as fast as in most other plants. The rate of genetic change, and the degree of genetic diversity, in holoparasites are so great that it is devilishly difficult to trace their evolutionary relationships. To check the reliability of their data from nuclear genes, Nickrent's team compared certain gene sequences from the mitochondria as well, since these plants have no chloroplasts. They succeeded in constructing family trees for three holoparasite families, including the one to which Rafflesia belongs.

"For 150 years we haven't known where they fit among angiosperms [flowering plants]," Nickrent says. Now botanists do.

Several labs, including Nickrent's, also recently discovered that gene swapping--technically called "horizontal gene transfer"--goes on between Rafflesia and its host. "Parasitic plants are getting genes from their hosts, and hosts are getting genes from their parasites," says Nickrent. Given such gene exchanges, scientists need to be especially cautious about the genetic methods they're using to determine the relatedness of organisms, he warns.

Plants' evolutionary history can be related to their physical features and to the fossil record to determine where certain plant groups grew many millions of years ago. Historical biogeography--the study of how plants and animals have been geographically distributed through the ages--began when 19th-century scientists noticed that very similar plants grew in widely separated parts of the Southern Hemisphere. These plant studies helped scientists understand that present-day Africa, India, South America, Australia, and Antarctica were once part of a supercontinent, Gondwanaland, back in the days of the dinosaurs.

In a recent project funded by the National Science Foundation, Nickrent proposed to study whether continental drift had affected the evolutionary history of a large family of Southern Hemisphere mistletoes (Loranthaceae). What his team found was that all the main groups of these mistletoes were already represented on Gondwanaland, rather than developing after the breakup of the supercontinent.

That means their lineages go back farther in time than many scientists had thought.

The finding "fits well with some previous hypotheses" based on chromosome data, Nickrent says, adding, "Our estimate of the age of angiosperms keeps going farther back in time--at least to the Jurassic."

It's a strange and wonderful botanic world out there, with much left to discover.

"There is still so much to learn about plants," Nickrent says.

--by Marilyn Davis, ed., and Paula Davenport, Media & Communication Resources

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