Nefarious fungus mimics a grass flower to facilitate its own transmission

Some of the most fascinating observations in biology, at least to me, involve the comandeering of one species by a parasite, who take the host over, changing it in a way that facilitates the parasite’s own reproduction. “Zombie ants“, infected by a behavior-altering fungus, are one example, and some people think that the protozoan Toxoplasma gondii, which humans get from cat feces, changes the behavior of rats when it infects them, making the rats lose their evolved fear of cats. The infected rats then are more readily eaten by cats, thus facilitating the reproduction of the protozoan, which becomes infectious when it gets into the cats and exits through their feces. Any mutant protozoan with the tendency to make rats less afraid of cats will be more likely to be passed on, which of course is positive natural selection.  But in neither that case nor the case of zombie ants infected with fungus do we know exactly how the parasite commandeers the host and changes their behavior. Working that out will be a fascinating task.

Today we have another fungus that affects its host in a way detrimental to that host but good for the fungus. The system is described in a new paper in Fungal Genetics and Biology (click on screenshot below, full reference at the bottom), or find the pdf here.  There’s also a summary in Scientific American. 

Now there are a couple of cases known of fungi that actually take over a plant host’s development and produce pseudoflowers that attract insects. Those pseudoflowers, while made of plant material, are also covered with fungal hyphae. The fungus also somehow induces the plant to produce a nectarlike substance. Both the pseudoflower and nectar attract pollinating insects, who instead of getting pollen get covered with fungal spores. The spore-covered pollinators then move to a new infected plant. This is a way the fungus manages to disperse its genes and also (some fungi have “sexes” or mating types) effect matings with another fungus on another plant. It’s a form of fungal reproduction, just as pollination is a form of plant reproduction.

In today’s case we have something a bit different: the fungus, when infecting the plant, itself assumes the form of a flower that looks remarkably like the host flower. It also develops pigments that are known to attract insects, including those in the UV light spectrum. Finally, the fungus appears to emit volatile chemicals that are identical to some chemicals of the host flower that attract bees.

Did I mention that the fungus also sterilizes the host plant (a flowering grass), so that the fungus doesn’t compete with the grass flowers for pollinators?

Click to read:

The two species of grass that the fungus infects were found in western Guyana, and are “yellow-eyed grasses,” Xyris setigera and X. surinamensis. Both are infected with the fungus Fusarium xyrophlium, a new species described by these authors. When it infects the grasses, the fungus sterilizes them, so that they produce no flowers or mature fruit, and the fungus sets up a systemic infection of the grass plant. Infections are patchy in Guyana; not all grasses have them and most grasses don’t.

After a plant has been infected for a certain time, the fungal hyphae grow into a “pseudoflower” at the grass tip that is a remarkable mimic of the grasses’ own flowers. Have a look at this figure from the paper. The first three photos show the fungus “flower”, and only the last shows the grass’s own natural flower. Again, the faux flower in the three photos at the left is made of pure fungal hyphae; it’s not made of plant cells “directed” by the fungus to assume the configuration of a flower, as in other cases.

Do the faux flowers attract insects? Yes, they were observed to attract small bees, though the flowers weren’t watched very long.

Do the bees carry spores that they get from trying to extract nectar from the fungus? We don’t know. The fungus is “self-sterile”, having different mating types, so it’s likely that these false flowers have evolved to not only disperse the fungus, but to facilitating its mating, since the spore-laden bee would likely be duped again and, in so doing, bring together two spores that could effect a mating.

Do the same bees pollinate the real flowers and the fake ones? That’s essential, for the mimicry involves duping the regular pollinators. Again, we don’t know. Note, though, that the faux flower has the same general shape and color as the real flower.

It’s interesting to note that, besides sterilizing the grass, the fungus seems to have no other detrimental effect on it. That’s what the fungus “wants,” of course, for its propagation depends on not killing off the grass, which is a perennial.

Bees not only see in the visible light spectrum, but also in the UV. The authors extracted pigment compounds from the fungus and found that there were indeed pigments in them that fluoresce in the UV spectrum. Thus bees could see more than just what we do. But we don’t know how the faux fungus flowers look to the bees, or whether bee vision makes the faux flowers resemble the real grass flowers. (There are many unanswered questions raised by this study.)

Finally, the authors looked at the volatile compounds of the fungus and flowers to see if they had anything in common; that is, was the fungus mimicking the odor as well as the appearance of the flower? Because the authors couldn’t get back to Guyana because of the pandemic, they used a related flower, X. laxifolia from North Carolina, compared to the lab-cultured fungus. Gas chromatography revealed only one volatile compound in common between the fungus and the grass flower: 2-ethylhexanol. This compound, however, is known to be a fairly powerful attractant of bees.

While many questions remain hanging, they can in principle be answered, and this paper describes a unique system: another weird way evolution works.  Here are some of the questions remaining:

a.) Did the fungus independently evolve its ability to produce faux flowers on both species of grass? (I would guess not.)

b.) Do the pollinators really move spores between infected grasses? (My guess would be yes; why else would the fungus evolve such an elaborate ability to make mimetic flowers?)

c.) What it is about infecting a grass that makes the fungus suddenly able to form flower-like shapes? Does some compound or gene in the grass itself induce the fungus to do this?

d.) How similar does the grass flower appear to the fungus “flower” to the eye of a bee?

e.) What other compounds of the fungus “flower” attract insects, and are they similar to odorants from the grass flower?

As Orgel’s Second Rule of Biology states, “Evolution is cleverer than you are.” And in this case it’s been very clever!

h/t: Jean

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Laraba, I., S. P. McCormick, M. M. Vaughan, R. H. Proctor, M. Busman, M. Appell, K. O’Donnell, F. C. Felker, M. Catherine Aime, and K. J. Wurdack. 2020. Pseudoflowers produced by Fusarium xyrophilum on yellow-eyed grass (Xyris spp.) in Guyana: A novel floral mimicry system? Fungal Genetics and Biology 144:103466.