In an extreme example of botanical body-snatching, a rust fungus invades a host plant and forces it to play a mating game for the fungus that often kills the host and may have repercussions for the surrounding natural community, according to a University of California, Davis, researcher.
In the cover article of the March 4 issue of Nature, UC Davis postdoctoral fellow Barbara "Bitty" Roy describes for the first time how a rust fungus commandeers two species of native plants commonly known as rock cress, forcing the host plant to create counterfeit flowers that the fungus uses for its flower-like reproductive process.
Taking over the host's cell-making machinery, the fungus radically redirects the plant's energy to send up a stem with petal-like leaves completely unlike the plant's natural flower. The fungus infuses the false flower with a bright yellow color, a sweet odor and a sugary nectar. To many insects, including bees, butterflies and flies, the fake flower apparently looks, smells and tastes like a flower.
"This is not the only rust fungus that uses insects for reproduction, but it is the only one I know of that changes the host so drastically and in such a flower-like way," Roy said. "These changes are probably more common than we think, but people haven't been looking for it."
The floral mimicry fooled students at the Rocky Mountain Biological Laboratory in Colorado, where Roy observed them picking the fake flowers. Professional botanists also frequently mistake the bright yellow infected leaves as flowers from a distance, she said.
Up close, the infected leaves display tiny pockets of fluid that contain slender stationary "female" sex cells and free-floating "male" sex cells. Like many plants, this rust fungus cannot mate with itself. Like all rusts with similar life cycles, the fungus relies on insects to carry the male sex cells to compatible female parts on other infected plants for the right match or simply around the leaf if the host plant has multiple infections, a process called out-crossing.
Once the mating is completed, the sexually produced spores are carried away by the wind to a different host. Later in the summer, a different spore stage causes infection in rock cress. Over the winter, the rust invades the region of the host where new cells are made, called the meristem, causing a systemic infection that induces pseudoflowers in early spring.
Shortly after snowmelt at Roy's study sites in the subalpine meadows near Crested Butte, Colorado, the fungus caused infected rock cress to create its counterfeit flower. These pseudoflowers formed weeks before the plant was ready to send up its own wispier, less visible, pale-blue flower. Once the pseudoflowers had been cross-fertilized by insects, the infected faux flower turned from yellow to green and stopped producing nectar.
The flowering stage of the rust infection almost always prevents the plant from producing its own flower and is usually lethal, Roy said.
In addition to its frequently fatal impact upon the host plant, the fungus may impact the entire plant community by altering pollinator movement. Insects seem to prefer the rust pseudoflower to other similar blooms, visiting at least as often and staying longer on infected leaves than on similar looking flowers of buttercups, yellow violets and wild yellow parsley. Flies, for example, lingered an average of five times longer on the sweeter rust pseudoflowers than on pasque flowers, members of the buttercup family, according to Roy's study.
"Pseudoflowers could compete for pollinators," Roy said. "Alternately, rust pseudoflowers could facilitate pollination of co-occurring flowers by increasing the total floral display or by providing an additional food source." A negative or positive impact is likely to depend upon the neighboring species present, Roy said.
Roy's work shows that certain rust fungi can alter the growth and character of their host plants to a degree previously unknown. From an evolutionary perspective, this indirect mimicry system is different from the more usual direct types, say, where an edible butterfly gains a survival advantage by its close resemblance to an inedible species. "In this case," Roy said, "you have one organism making another organism look like still another organism."