Rust fungus induces flower mimics in host plants

By Jeff Mitton

Early in April, I was looking for the first of the spring flowers in the mountains and had found pasque flowers and, to my surprise, mountain ball cactus in bloom at Meyers Gulch, near Walker Ranch.

But then I found a tiny plant with bright yellow flowers with prominent bumps on the petals. I had never seen it before, so I imagined that I had found a diminutive and rare wildflower.

I photographed it and sent the photo to colleagues for identification.

Professor William Weber, emeritus director of University of Colorado's Herbarium, noted that every year people would bring in Fendler's rockcress infected with rust, hopeful that they had found something unique and rare.Erin Tripp and Dina Clark conferred and agreed that I had not really photographed a wildflower at all.

I had found a small wildflower, in the mustard family, that had become infected with a rust, a type of fungus. The yellow structure was a floral mimic constructed by the plant, but designed by the rust.

Puccinia monoica is a rust that uses several species of grasses as its primary host and several species of mustards as its alternate host. In Colorado, it is known to infect three mustard species, Holboell's Rock Cress, Drummond's Rock Cress and Fendler's rockcress.

Professor William Weber, emeritus director of University of Colorado's Herbarium, noted that every year people would bring in Fendler's rockcress infected with rust, hopeful that they had found something unique and rare.

The rockcresses are close relative of the Arabidopsis thaliana, the model plant species used most commonly by geneticists and developmental biologists.

Spores blow from an infected grass to infect one of the mustards. As the infection proceeds, the rust sterilizes the plant and takes increasing control of the host's physiology and development. Note, in the photo, the flower buds at the top of the plant — they will not open.

The rust forces the plant to modify the color and surface texture of leaves, producing the floral mimic. The mimic is functional and it is the site of sexual reproduction, but it is reproduction of the rust, not the plant.

The rust also causes the plant to produce a thick, sticky fluid that serves as nectar to attract pollinators. The nectar has more than 20 times the sugar content of nearby flowers and although it has a sweet fragrance, it is distinctly different from the fragrance of the host species.

The fragrance of the floral mimic comes from aromatic alcohols and aldehydes, while the fragrance of the hosts's nectar comes from terpenoid compounds.

To complete the rusty deception, the floral mimics have evolved to resemble the common wildflowers sharing the same environment.

In a study based at Rocky Mountain Biological Laboratory in Gothic, Colo., Bitty Roy recorded the pollinators that came to floral mimics. Pollinator species included halictid bees, ants, wasps and flies.

If the pollinator was moving among floral mimics, it was carrying the fungal equivalent of pollen. The male gametes unite with receptive fungal hyphae to produce spores, which would be carried by breezes to the next host, one of the grasses.

The rust exerts an extreme degree of control over its host — it sterilizes it, steals its nutrients, forces it to turn its leaves into floral mimics and produce a rich fungal nectar. Extreme, but not unprecedented.

One of my favorite examples of control of a host is visible on the blue spruces growing in town and along the creeks in the canyons.

An adelgid insect called a wooly aphid lays eggs near needle buds on spruces. As the needles appear, the eggs hatch and larvae begin to chew. Their saliva contains a compound similar to the hormone that initiates development of spruce cones. The tree begins to form a cone, but the resulting structure is a gall, which looks similar to a cone (except for the dead needles and lack of scales), but serves as a protective shelter for larval development.

Parasitic control ranges widely among species, from the relatively harmless gall production by wooly aphids to castration and complete control by Puccinia monoica. I am somewhat humbled (galled but by no means castrated) by being fooled by a fungus, but at least I am in the good company of a horde of clever pollinators.

Jeff Mitton, mitton@colorado.edu, is a professor in the Department of Ecology and Evolutionary Biology at the University of Colorado. This column originally appeared in the Boulder Camera.

April 27, 2015