Killer Fungi and Shape Changers

© Else Vellinga
Lab
Original publication: Mycena News, September 2010

“Billions at risk from wheat super-blight” – “Red menace: Stop the Ug99 Fungus Before Its Spores Bring Starvation” – “Deadly wheat fungus Ug99 hits South Africa” – these are just some of the headlines on a new strain of Puccinia graminis, the Black or Stem rust of wheat, that originated in Uganda and spread northeast to Iran, which it reached in 2009, and to South Africa, where it arrived in 2010. Wheat is not resistant to this particular strain of rust fungus, but the race is on to develop wheat that can withstand the rust.

Puccinia

Rusts are ubiquitous plant-pathogenic fungi and affect many plants. On my daily walk to campus their orange or dark brown powdery spots are conspicuous on many garden plants. Rust fungi got their name from the rusty brown spores they produce. They belong to a group of basidiomycetes called the Pucciniomycotina, one of the three main groups in the basidium-forming fungi, along with the Ustilagomycotina (smut fungi belong here), and the Agaricomycotina where our regular mushrooms are accommodated (boletes, Russulas, chantererelles, conks, etc.) Just for the record, the next big grouping of fungi, the ascomyetes, with spores produced in tube-like cells called asci, includes molds and mushrooms like morels.

Unlike the mushroom-forming species, rusts in the class Pucciniomycetes do not form obvious fruitbodies and in fact have quite a different lifestyle than mushrooms. They only grow on plants and they form their spores in little heaps, originating from special structures in the leaves and stems. The plants suffer from this foreigner living inside them, and crop plants grown in monocultures are especially vulnerable; yields are severely reduced by rust fungi. The rust fungi form spores in huge quantities, and what kinds of spores these rusts have! They have the most complicated life cycles you can imagine. Bolete and button mushrooms produce just one type of spore (known as basidiospores as they are borne on the basidia that cover the tubes and gills, respectively), but your typical rust species is capable of forming four different types of spores. Needless to say, the number of nuclei and the number of chromosomes differ according to the type of spore. In the literature cited below you can find complete descriptions of life cycles for the various species.

Rusts grow on all kinds of plants – I see them on grasses, pines, geraniums, fava beans, Baccharis (Coyote bush and related species), juniper trees, roses and hollyhocks; I could go on and on. One of the crazy things rusts do is to spend different parts of their life cycle on different plants. So, the infamous wheat rust Puccinia graminis overwinters in the fields as spores in the wheat stubble, infects Berberis (barberry) or Mahonia bushes in the spring with one kind of spore, then jumps to the wheat with the other three types of spores to complete its cycle before it goes back to the barberry bushes. This is a classic example of a rust life cycle. Another group of rusts has simplified life by only growing on one host and skipping part of the life cycle; it forms just two types of spores. The hollyhock rust, Puccinia malvacearum, which is restricted to hollyhocks and related plants, is a good example. You can easily find it as little orange to mauve-lilac humps on the undersides of the leaves of hollyhocks (the color indicates the kind of spore that is produced).

Euphorbia

However, for the really cool stuff we need to explain a little more about the life cycle. After the basidiospores have germinated, the fungus forms structures called spermogonia, each of which derives from one or another type of genetic makeup (roughly equivalent to male and female). The spermogonia produce spores (actually the fifth kind of spores), which must find a receptive hypha of the opposite “sex” for the next phase in the rust’s life to begin.

Puccinia on Arabis

Puccinia monoica on Arabis (Photo © Michael Wood)

In the high mountains of the American west, small rosetteforming plants of the genus Arabis (a relative of cabbage and such) go berserk as their appearance changes totally when they are infected by basidiospores of Puccinia monoica. Instead of a long, leafless flower stalk, a stocky leafed stem grows out of the basal rosette, while at the top of the stem bright, yellow fragrant leaves appear. Insects are attracted by this flower-like structure, and bring the spermatia to the receptive hyphae, thereby playing an essential role in the life of the rust. The insects are lured by the colors, fragrance, and stickiness of the leaves. Although the smell emitted by the infected plants is different from that of the real flowers, and also from the flowers of the other plants around, it still does its job of attracting “pollinators”. Uromyces pisi does the same thing on the European spurge Euphorbia cyparissias. Instead of whorls of thin leaves with widely arranged flowers at the top, the plant forms short, relatively broad leaves along a long stem, with a denser set of yellow leaves at the top, luring insects to disperse the rust spores. It is hard to imagine that the two forms of the plant are really the same species, they are so different. The changes in plant morphology are much more dramatic than those in the roots caused by ectomycorrhzial fungi.

In the case of the Arabis- and the Euphorbia-rust symbioses, there is no benefit for the plants; the rust prevents them from forming flowers, and for them there will be no offspring. Conversely, the fungus’ well being is obviously enhanced, as a critical step in its life is taken care of. The “pollinators” get some sweet reward, so they are happy too.

Try sniffing other rusts, to see whether they are fragrant. If you are lucky you may find the rust that covers the underside of leaves of Cirsium arvense (a European thistle species that has invaded North America, but is named Canada thistle) – it emits a very nice sweet honey smell!

Rust fungi not only shape plants, but by their presence and importance on human food plants they affect all our lives.

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