This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American
A broken primrose fruit showing the remains of a fuzzy black parasitic fungus called smut (upper left). Intact fruit surrounds the broken pod. Photo by Dr. A. Martyn Ainsworth. Used with permission.
Not long ago I was perusing some old press releases when I stumbled onto an interesting tidbit buried in one from the Royal Botanic Gardens at Kew (I know I probably said that like a dumb American since I don't know what people actually call it in the UK, but let's face it: I am a dumb American). For extra Britishness, try to imagine David Attenborough reading this:
The long-lost British fungus bird’s-eye primrose smut (Urocystis primulicola), recognised as a species of “principal importance for the conservation of biological diversity” (BAP review 2007) had not been seen for 106 years until it was rediscovered by Kew and Natural England mycologist, Martyn Ainsworth (8), during a two hour ‘ovary squeezing’ session.
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Those British mycologists really know how to party. Speaking as a trained mycologist myself, of course. Ahem.
In all fairness, the ovaries in question were part of the maturing flower parts of the plant, and as they were already dried up and dead, the plant presumably did not mind the indignity. Also, according to Kew, the mycologist in question (Dr. A. Martyn Ainsworth) conducted said ovary-squeezing when he happened to be stopping at a nearby village on a trip to Scotland and remembered he had seen a bird's eye primrose in flower there several years ago. It did not constitute his Friday night plans.
Smuts are species of inconspicuous, microscopic fungi that are found inside living host plants, in this case the red-listed wild pink flowered bird’s-eye primrose (Primula farinosa) found in the North Pennines. The bird’s-eye primrose smut has co-evolved with the plant and hijacks its ovaries, replacing its seeds with a black powdery mass of smut spores. Concealed in the ovaries, it is only when the bird’s-eye primrose seed-pods are squeezed in the late summer, when the seeds are ripe, that this rare smut can be found.
The flower is apparently rare now in the UK, explaining the smut's 106-year disappearing act. Here is a picture of a bird's-eye primrose as-yet unmolested by smut:
We should now at least have a word on what smuts actually are to make up for my shameless headline and grade-school tittering1.
Smut fungi, along with the closely related rusts2, may have been some of the earliest evolving basidiomycetes, the large group of fungi that includes most mushrooms. Smuts are plant parasites and produce reproductive structures called teliospores. These beautiful fortified, textured, and usually sunscreen-darkened spores represent the sexual phase of the fungus, and are what make them so delightfully smutty, as you can see at the photo at top.
Sometimes teliospores are the overwintering stage. When they germinate, they produce the basidia that characterize basidiomycetes and the basidiospores which are the product of meiosis in these fungi (eggs and sperm are human products of meiosis). Smut basidia are not club-shaped like most mushrooms'; they're finger-like and bear basidiospores along their length or at their tips.
Unlike rusts, which can infect conifers and ferns, smuts infect only flowering plants (at least now. In the deep past? Who knows). They may do this when their spores land on plant tissue, or they may already be present in seed from infected plants. Once smuts start growing, they may live quietly without any evidence of their presence as endophytes in between the cells of the plant until it matures. Then they often grow into and replace important, high-investment structures like pollen, bulbs, or fruit with their mycelium(the filamentous body of the fungus) and teliospores.There are many, many crop diseases caused by smuts, and they have kept plant pathologists busy for a long time. But there are also many smuts that affect wild plants that have little to do with us. And, no doubt, they play an important part of their own in nature.
Some smuts also have the ability to live as saprobes on detritus for a while, and all smuts seem to have interesting yeasty tendencies. Yeast is simply a word for fungi that -- at least for part of their life cycle and sometimes permanently -- given up the filamentous lifestyle and gone back to living as single-celled organisms that reproduce by budding. Many unrelated fungi can live this way. When smuts are cultured on artificial media in petri dishes in labs, they almost all grow as yeast that reproduce by budding. I do not know why. There is also an interesting group of smuts that seem to prefer living as yeasts for long stretches in the wild (though they can also make mycelium), and they are called "basidiomycetous yeasts".
You may have heard of corn smut (aka Porn on the Cob), known as huitlacoche to the refined people of Mexico, who consider it a delicacy. In this case, the fungus takes over individual kernels of corn (each the ovary and fruit of a single corn flower) and replaces the tissue with masses of its own, severely distorting the kernels into gray, grotesque, but apparently tasty spore masses. Here's a beautiful drawing of the life cycle of this smut, to give you the general idea of how smuts operate that, as a bonus, allows you to practice your Spanish skills! Just imagine this one narrated by one of those Latin American soccer announcers and it'll be fine: ("TELIOOOOOOOOOOOOOOOOO!").
Smuts, to put it bluntly, have a smorgasbord of suggestive names. There are [clears throat] loose smuts and covered smuts (loose smuts release their spores to the wind). The covered smuts are also called bunts, or [cough] stinking smuts. Stinking smuts (bunts) do indeed stink, and grain contaminated with them is suitable for feed use only. Bunt spores have an additional quirk: they are oily. This may not seem remarkable, but it becomes remarkable when they are present in sufficient numbers, and a spark from machinery or static electricity causes a smut-dust-filled grain elevator, combine, or thresher to explode. I'm fairly certain we were shown photos of the aftermath of this in grad school, and here are photos of a grain elevator and thresher that got blowed-up by smut in a 1916 edition of Popular Science.
Finally, there are three bunt subtypes: Common Bunt, Dwarf Bunt, and [cough] Karnal Bunt. Karnal Bunt was named for the city in India, not for any indiscretions our bunt may or may not have committed.
So smuts and bunts specialize, essentially, in shang-hai-ing parts of flowering plants, be they grasses or primroses. They replace the developing plant tissue with their own. In the case of our Bird's Eye Primrose Smut, the fungus replaces the developing ovaries inside the fruit (hence the need for ovary-squeezing). In the healthy plant at right, you can see a long green ovary with a few mature seeds peeking out at the base of the capsule. On the left, you see what happens when the smut fungus takes over. The black mass is made of fungal filaments and teliospores.
It's exciting we found an organism alive that was once thought lost and it's even more remarkable someone spent two hours squeezing ovaries to find it. Hats off to you, sir. Smuts are common, important, and usually overlooked parts of the natural world. Just because they're not sexy (though certainly suggestively named!) doesn't mean they don't deserve our attention and appreciation -- and not just during Grain Elevator Explosion Awareness Week.
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1It was a bit awkward writing Kew with a subject line requesting "smut photos". I definitely did not see that one coming when I rolled out of bed in the morning.
2Informally, it is Mycology Week(s) here at The Artful Amoeba, as it was recently over at Small Things Considered. In addition to last week's post on chytrids and this post on smuts, I have two more fungal posts in the lineup, including one on rusts that turned up in a very unusual place and guise -- and were mistaken for crustaceans.