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Out of one, many. The fungus C. neoformans produces genetic diversity from scratch.

Edmond Byrnes and Joseph Heitman/Duke University

Fungus, Get Off My Lawn!

Life demands tradeoffs, and plants are no exception. Virginia wildrye, common on U.S. prairies and rangelands, often plays host to a fungus that helps this grass grow. But the plant pays a price. Researchers have discovered that infected plants produce less pollen than their noninfected counterparts. Instead, the fungus causes the rye grass to make extra seeds, which transmit the fungus to the next generation and new locations. This is the first time a fungus has proven capable of manipulating plant reproduction. The finding highlights the complexity of the relationship between hosts and their guests.

Relationships abound in which a plant or animal partners with another organism. That organism, called a symbiont, gets protection from the environment and, in return, sometimes offers some benefit. In the case of Virginia wildrye, the microscopic fungus thrives between the cells of the stem and leaves. It makes a toxin that deters insects and other animals from eating the plant and also protects its host against disease and drought.

But Jennifer Rudgers, a botanist at the University of New Mexico, Albuquerque, who led the new study, began to wonder if there was more to the relationship. Even though Virginia wildrye is hermaphroditic, producing seeds (the female contribution) and pollen (male contribution), the fungus gets passed on to the next generation only in seeds. Pollen is too small to carry the fungus, she notes. "Basic theory predicts that whenever a symbiont is preferentially transmitted through one sex, it will evolve [ways] to overproduce that sex," explains John Werren, an evolutionary geneticist at the University of Rochester in New York who was not involved with the work. The same thing might hold true for an organism's sex cells, such as pollen and eggs. Many insects, for example, host microbes that are "inherited" through the eggs but not through sperm. The microbes often cause more female insects to be produced. They may convert genetic males into females, allow females to produce only daughters without the need for mating, or kill male offspring of infected females so that the daughters have more food. "These 'strategies' enhance transmission of the microbe," Werren says.

Rudgers decided to test whether the fungus was skewing the grass's reproductive efforts in a similar way. She compared pollen and seed production in plants that were infected with the fungus and plants that were not.

Infected plants produced one-quarter more seeds than noninfected plants, she and her colleagues have reported in the April issue of The American Naturalist. But the tradeoff was that they produced only about half the usual amount of pollen. Because Virginia wildrye is wind-pollinated, much of the pollen fails to reach its target and thus quite a lot is needed to assure adequate pollination occurs, Rudgers says. "They are not able to reproduce as they usually would," she notes. It is not clear whether the increase in seed number can make up for there being less pollen.

"There is a fairly dramatic effect on that tradeoff," says Christopher Schardl, a biologist at the University of Kentucky, Lexington, who was not involved with the work. "There's clearly an advantage to the fungus."

"To my knowledge, it is the first clear demonstration that symbionts can alter the seed to pollen ratio in plants," Werren says.

Schardl has some evidence to support this finding. He has been studying differences in gene expression in infected and uninfected plants and finds that the fungus seems to increase the activity of genes involved in seed production. Given that fungal symbionts are quite common in some plants, "it would be interesting to know how general this conclusion is," he notes.