This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American
Can you guess which are the mummy berries? Caleb Slemmons, University of Wisconsin, Stevens Point, Bugwood.org
Author’s note: This is the latest post in the Wonderful Things series. You can read more about this series here.
There is a fungus on our planet which is capable of not one, but two audacious and duplicitous acts: it pretends, on separate occasions, to be a flower and a pollen grain, and its performances are so successful that it manages to fool both the bumblebee and the blueberry bush.
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That fungus goes by the tongue-twisting name Monilinia vaccinii-corymbosi, but the common name for the disease it causes is mummy berry (which sounds like it should have its own breakfast cereal). That's because it has a third act too: turning blueberries into time bombs.
Plant pathogenic fungi are everywhere, as I can attest from the two years I spent studying them in graduate school. They are fascinating specialists evolved to finagle their way into plant bodies and sneak past or exploit plant defense systems with practiced polish.
Some, like the gloriously named rusts, smuts, and bunts, are so specialized that they shuttle between two often wildly unrelated host plant species and can produce up to five types of spores. But M. vacciniii-corymbosi (hereafter M. v-c.) takes this artful and deadly dance to a new level of sophistication and guile with its successful imitation of entire plant organs.
The story begins with the resting stage of the fungus, called a sclerotium. Many fungi make these, and odds are good that if you dig up a random patch of forest soil and sift through it you will find the hard, knobby, black, yellow, or white sclerotium of some unnammed and unsung fungus or other. M. v-c. makes sclerotia too, and in spring, when a young fungus's thoughts turn to love (or at least reproduction), the sclerotium comes to life and produces a cup-like structure called an apothecium from which it launches its sexual spores (the sex having already happened; these are its products).
Apothecia of Monilinia vaccinii-corymbosi growing out of buried mummy berries. Caleb Slemmons, University of Wisconsin, Stevens Point, Bugwood.org
If these windborne spores are lucky, they will land on an errant bud-bearing branch of a blueberry or huckleberry bush, preferably right on that tender, tasty young shoot. These leaves, stricken by the fungus growing within, begin to wilt and grow a furry fungus coat the way you have observed many a time on fruit, bread or cheese.
Leaf damage caused by Monilinia vaccinii-corymbosi. Notice the white, urn shaped blueberry flowers nearby. Edward Beasley, University of Georgia, Bugwood.org
But then they do something bizarre. The gray-brown, deep brown, or dark brown leaf lesions often seem strangely tinged with violet. The leaf begins to emit the odor of "fermented tea" (I can only assume somewhat similar to a pu-erh, for you fellow tea enthusiasts out there). It has also described as "sweet".
And, oddly, pollinating insects begin to land on these withered leaves -- and lick them. That is probably because the leaf has now begun to ooze the sugars sucrose, glucose and fructose.
A wild bee licking the blueberry leaf lesions of Monilinia vaccinii-corymbosi. Fig.1 B and C from Batra and Batra 1985. Click image for source.
The blueberry leaf lesions of Monilinia vaccinii-corymbosi photographed under UV light. In constrast to surrounding foliate, they reflect the light and appear white (arrows). Fig. 1F from Batra and Batra 1985. Click image for source.
If you take these odd leaves and photograph them under UV light, you will see that they reflect UV on the lesions, but not elsewhere on the leaf. Many flowers are colored ultraviolet for bee benefit, as bees can see UV but not red.
In effect, the fungus has turned itself and its host into a fake blueberry flower, complete with fake UV-reflective landing guides, fake perfume, and fake nectar. Blueberry sepals -- the little green leafy objects that surround blueberries' white urn-like flowers -- are indeed UV reflective, and the flowers secrete nectar and their petals emit an odor that attracts bees and other pollinators.
Although real blueberry flowers are white, yellow, or pink and bear little resemblance to our eyes to M. v-c.'s lesions, pollinators behave like they're landing on any other flower. When pollinating insects approach these leaves, they use many of the same flying, landing, and feeding behaviors they would toward a blushing young flower. But what happens next is not a happy bout of pollination. Instead, the unsuspecting insect bathes in the gray spores of M. v-c., and when it next lands on a real blueberry flower, these spores stick to the stigma and perform their next trick.
Once safely ensconced on the stigma -- the sticky receptive tip of the female flower parts -- the fungal spore germinates and now pretends to be a blueberry pollen grain. It helps itself to the food secreted there for the benefit of germinating pollen grains. Then it starts growing down into the five-lobed chamber through which pollen germ tubes are meant to travel.
It restrains itself from running amok through the tissues of the stigma as any common fungus would do -- and indeed, as M. v-c.'s close relative Monilinia fructicola did in control experiments, and as M. v-c. will do itself when it attacks leaves or grows on lab food. Instead, it sends slender, rarely-branching filaments down the surface of the hollow, 1-cm long stylar canal toward the ovary of the flower in groups resembling the bundling of pollen tubes.
In A and B below you see blueberry pollen germ tube bundles travelling down the chamber after being launched from sprouted pollen grains. In C, you see the fungal filaments of M. v-c. travelling very purposely in similar one-track bundles. In D, you see Monilinia fructicola going haywire through the same tissues, branching this way and that in typical fungal fashion.
Further, M. v-c.'s filaments travel by carefully adhering to the surface of the chamber, just as pollen grains do. In A below, you see the five-lobed chamber in the center of a cross section of the stigma. In B, the red arrows point toward dark pollen germ tubes adhered to the edge of the chamber. In C, the red arrows point not to pollen but to the dark filaments of M. v-c. growing in identical fashion. In D, you see the control Monolinia fructicola inside the red circles going nuts growing all over, including in the space right in the center of the chamber, and not taking any particular care to adhere to the walls.
M. v-c. also adheres to the chamber's surface only by its tip, just as pollen tubes do, and appears to use similar chemical cues and bonding. It carefully avoids any ill-thought-out penetration of any of the cells in the chamber's wall. By quietly mimicking pollen both physically and chemically, the fungus thus avoids triggering a destructive host defense that would prevent it from ever reaching the fruit of its desires.
Once it reaches that goal, in the flower's egg or embryo, the plant has itself a new STD and the fungus goes wild. The infected ovary -- which was probably also fertilized by a pollen grain -- matures into a blueberry, but the blueberry is blighted. It shrivels, mummifies and falls to the ground. Inside, as the chill of winter comes, the fungus forms its sclerotium. And there these fungal time bombs tick until next spring, whence they will launch their next blueberry-bound volley.
Both of these acts of mimicry are extraordinary. It is rare for fungi to infect plants through what amounts to their reproductive tract -- only the aforementioned smut fungi and another group called ergot fungi also infect their hosts through the flower's lady bits. At the time the studies on the leaf-based fake flowers were done in 1985, no other example of fungal leaf-based floral mimicry was known. Finding both behaviors in *one* fungus is nothing short of spectacular.
References
Ngugi H.K. & Scherm H. (2004). Pollen mimicry during infection of blueberry flowers by conidia of Monilinia vaccinii-corymbosi, Physiological and Molecular Plant Pathology, 64 (3) 113-123. DOI: 10.1016/j.pmpp.2004.08.004
BATRA L.R. & BATRA S.W.T. (1985). Floral Mimicry Induced by Mummy-Berry Fungus Exploits Host's Pollinators as Vectors, Science, 228 (4702) 1011-1013. DOI: 10.1126/science.228.4702.1011