Psst….Let’s talk smut today

© Else C. Vellinga
Lab
Original publication: Mycena News, November 2004

Smut—1. A fungous disease affecting various plants, esp. cereals, which are spoiled by the grain being wholly or partly converted into a blackish powder; also, one or other of the fungi (species of Ustilagineæ) causing the disease. 2. A black mark or stain; a smudge. 3. Bad, soft, earthy coal. 4. Soot or sooty matter. 5. Indecent or obscene language. (Oxford English Dictionary, online version.)

Let’s talk infectious diseases, let’s talk huitlacoche, and blisters of black spores, and sex, sure sex is involved as well.

Ah yes, huitlachoche is a smut, by some considered a pest, by many others a delicacy; it is also a perfect lab ‘animal’ and its complete genome has been sequenced.

Common smut, Corn or Boil smut, huitlacoche and cuitlacoche, and Ustilago maydis in Latin, different names for the same thing, a fungus that grows on corn. Infected corn ears develop huge galls, part fungus, part plant, which eventually burst open and release the dark dusty spores. Less conspicuous is the presence of fungus on other parts of the plant, but it certainly is not restricted to the cobs.

Ustilago

Corn is not the only smut-infested plant valued by gourmets; tender young shoots of wild rice with the smut Yenia (Ustilago) esculenta are a much-prized delicacy in China. However, there is little good (from a human perspective) about most of the c. 1450 species of smut that parasitize around 4100 species of plants. Only a few tree and shrub species are prone to smut infections, and the same is true for ferns. Furthermore, the huge family of orchids is completely free of smut. However, where smut is at home is among sedges and grasses (corn, barley, wheat, and a whole array of non-cereals). We see it next to sidewalks here in Berkeley looking like dark powdery flower stalks in the Bermuda grass.

There is the usual variation in host specificity – the corn smut only occurs on corn (Zea mays), while others can be found on a wide array of plants. Ustilago hordei for instance infects not only barley as the name indicates, but a slew of other grasses. Water plants, like arrowleaf and water lily, have their own special fungal communities. Here it is the environment that shapes the species composition, rather than the identity of the host plants. There is even one species of smut or smut-like thing, Malassezia furfur, that is a human pathogen, and causes a skin rash.

Smuts can cause havoc in agricultural crops, especially on cereals like wheat, with losses in yield and in money. Karnal bunt is an example: when this Asian disease turned up in some counties in Texas, in 2001, within a day over 25 countries had banned the import of grains from the infected areas, with an estimated loss of $ 27 million. This disease has such potential to cause economic damage that it is mentioned as a possible bioterror agent.

But what exactly is a smut, how does it grow, what are its closest relatives? Let us zoom in on the corn smut, and see how it lives.

We’ll start with the spores that are formed in the gall. These are called teliospores and their appearance in huge amounts on the plant is in many cases the first and only signal that the plant is diseased. The dark thick spore wall indicates that these spores, which are carried by the wind, are adapted for dispersal and survival under adverse circumstances. There are other smuts, the anther smuts, in which the spores are transported from plant to plant by flower-visiting insects, but corn smut spores over-winter in the soil. When the teliospore starts to germinate, it acts like a basidium, the structure in which nuclei (the cell regulators) fuse. In this case, the binucleate teliospores produce basidiospores with a single nucleus. Mushrooms, from boletes to chanterelles, from conks to crusts, need special fruiting structures to produce spores. Smuts do it with a single cell.

These basidiospores have a saprotrophic lifestyle and can grow outside the plants; they are single cells which bud and behave like yeasts. This phase has been studied extensively in the lab, as you can grow these cells on agar plates. The spores are also the primary infection agents. When two basidiospores mate they fuse to form a new mycelium and the smut embarks on its parasitic phase. Infection takes place in different parts of the plant. It can happen via the silk of the cob, interfering with pollination, a race between pollen grain and smut spore. As the mycelium grows, within and between the plant cells, it causes these cells to divide like crazy and at the same time grow bigger; a gall is born. The teliospores are then formed as modified parts of hyphae. The plant epidermis breaks open, the spores appear, and the circle is complete.

Of course, other smuts do parts of this cycle in different ways. But, for most species the life cycle is not known in such detail as it is for the economically important Corn smut. Some species infect seeds, some grow throughout the plant and persist in it for the whole lifetime of the plant. As one example, take Microbotryum violoaceum, which is a very interesting anther smut, specializing on carnation-like plants in the family Caryophyllaceae. Species in this family are often dioecious, which means that there are plants exclusively with female flowers and plants with male flowers. The anther smut only occurs on the male flowers and subverts the flowers to produce dark purple spores instead of pollen. This strategy should mean only a 50 % infection rate (only half of the plants are male), but, the smut has found a way to do better. It attacks plants with female flowers by first performing a sex-change operation!

It took mankind quite a while to understand the real nature of the smuts. The classical Greek Theophrastus wrote: “Bunt or stinking smut of wheat is caused by the action of the burning rays of the sun falling on the heads that had been penetrated by abundant rain.” It was only in the mid 1700s that this theory was proven wrong by a Frenchman, Matthieu Tillet, who did a bunch of nice experiments. First he planted a wheat plant in a pot which he kept really wet. The plant stayed infection free, contrary to the prevailing opinion that abundant rain would cause the infection. Secondly, he planted grains with smut spores in some plots and non-infected seeds in others and recorded carefully the number of diseased plants in each plot. The infected seeds produced infected plants, and most plants of the blanks stayed disease free. This method did not work for corn smut, as the infection does not happen via the seeds, so there he concluded that it was a character of the plant and the circumstances under which it was grown. Even when it was known that the smuts were not part of the plants, it still took considerable time to realize that they were fungi. Researchers did not see any hyphae among the spore masses. Even as recently as1967, new Silene species were described based on the dark colour of the ‘pollen grains’. We know now that this was merely due to an anther smut.

Fungi with so few apparent characters, mainly spores and hidden hyphae, are difficult to classify. The big breakthrough came with electron microscopy and with the use of molecular characters for identifying major groups. It then was realized that anther smuts are more closely related to rusts, another big group of basidiomycete plant pathogens, and that other groups of plant infesting fungi are nested within the ‘proper’ smuts. Exobasidiums, for instance, the fungi which cause galls and misshapen leaves in Rhododendrons, Vacciniums and Manzanitas. In other words, different groups of fungi have come up with the same idea of forming powdery spores in great masses on plants. When we look at family relationships with molecular techniques we find that rusts and some smuts haven’t changed much since the common ancestor of all fungi with basidia. The other smuts had a somewhat more recent ancestor, but also haven’t changed much. The branch that underwent extensive evolutionary change is the one that led to the familiar gilled mushrooms and boletes.

The question ‘what exactly is a smut?’ is harder than ever to answer; the best definition right now is: basidiomycete plant parasites which produce teliospores.