smaller fleas

It was during smalltalk over a shared breakfast table on Amtrak that the man across from me began excoriating powdery mildew. He was a Colorado pot grower. His greenhouse operation held hundreds of plants, and the air circulating between his and the adjoining pot greenhouses was spreading the spores of the leaf parasitic fungus that had somehow gained a foothold inside. The greenhouse conditions provided an ideal environment for germination and growth of powdery mildew, and the high density of plants insured an endless supply of favorable landing spots for the dust-like particles that can each start a new colony. Despite the lore, pot plants are not indestructible, but rather serve as hosts to many pests and diseases, with powdery mildew being a leading factor threatening pot growers’ investment. Powdery mildew doesn’t kill a plant outright, but it weakens the plant and lowers the harvest quality.

There are about a hundred species of powdery mildew that make up this family of fungi. A powdery mildew’s thread-like growths cover the surface of a leaf and send root-like structures into the cells to feed. Its upright chains of spores give the impression of powder on the leaf. Powdery mildew is known as an “obligate biotroph”, meaning it can only survive on living host tissue. A key requirement of this infection type is that the fungus must come pre-programmed to neither kill the parasitized plant cell nor awaken the cell’s defense mechanisms, a balancing act accomplished through a tightly choreographed sequence of interactions with the cell’s machinery.

A reality of the plant world, though, is that distantly related plant species have distinct cellular machinery, meaning that a powdery mildew species that is not correctly pre-programmed, that is to say, coevolved with the plant it arrives on, will trip up and not be able to infect. Thus the powdery mildew on the sowthistle next door will not spread to your pumpkins, and the powdery mildew that emerges on the rosebush at the end of the row of grapevines and signals the grower to spray sulfur on the vines is not the species that actually infects the vines.

What the powdery mildew species have in common is similar germination requirements. The reason for this is that the spores carry their own moisture, allowing them to germinate without the liquid water that most fungal spores require. In fact, liquid water inhibits powdery mildew spore germination and can even cause the spores to burst. The spores do need a certain amount of humidity to germinate, but it can be as low as 50% relative humidity, and germination works better within a mild temperature range and at lower light levels. Outdoors there are certain times of year when powdery mildew blooms, but greenhouses are always ideal incubators waiting for spores to arrive.

For control of powdery mildew on grapevines, great quantities of sulfur and fungicides are sprayed, the most for any pathogen. However, since weed is newly legalized and gets smoked, growers don’t have an arsenal of chemicals registered for use on it. Cannabis pathologist Zamir Punja from British Columbia has found a few treatments to be effective, including Regalia, which is an extract of giant knotweed, Milstop, which is similar to baking soda but without the sodium, and germicidal ultraviolet light for a few seconds a day. There are some biocontrols that show promise as well. These mostly produce inhibitory chemicals or destructive enzymes against the fungus, or prime the plant to fight off infection, but a recent study from Hungary led by Márk Németh working in the lab of Levente Kiss shows the potential of a biocontrol agent that acts like a creature from science fiction.

In John Carpenter’s 1982 re-visioning of the sci fi classic The Thing, there is not monster played by a man in a suit as in the original, but instead a shape-shifting menace that lives inside its victims, compelling them to act in ways that benefit this alien life form while they retain their own personality. The most riveting scene is where the Kurt Russell character uses a flamethrower to kill a crew member carrying the parasite, which had revealed itself when it had burst out of his chest to engulf the arms of a comrade. The carrier is lying on a table as the flames sear his body, but his head hanging over the edge is out of direct exposure. To the horror of the crew and the audience alike, the head grows a stalk to lower itself to the ground then sprouts legs and tries to slink away. The film proceeds with an air of paranoia as crew members try to figure out who else may be harboring the monster.

The Thing was inspired by the atmosphere of fear and suspicion associated with the cold war, as were many if not all classic sci fi movies, but it could have been inspired by Ampelomyces. This fungus lives inside the tiny threads that make up the powdery mildew. It doesn’t kill the host fungus at first, but grows inside it, finally hijacking its reproductive structures to make more Ampelomyces. The tiny powdery mildew spores become filled with the even tinier spores of the hyperparasite, so-called because it is a parasite of a parasite.

The basic life history of Ampelomyces has been known since the nineteenth century, but Németh et al. have done the definitive study by engineering this fungus to glow green under blue light, allowing them to see its diminutive threads inside its host. They accomplished this using a gene from a jellyfish and a bacterium from a plant gall. The jellyfish is the bioluminescent crystal jelly of Puget Sound, which has a gene for producing green fluorescent protein. The bacterium is the pathogen responsible crown gall in plants, and it alters the growth of its host by inserting a plant tumor gene into the host’s DNA. The scientists replaced the bacterium’s tumor gene with the green fluorescent protein gene, added the bacterium to the fungus culture, and created the green-glowing fungus they were seeking.

One of the key questions that could be answered with an easily seen fungus was, what happens to it outside its host? It turns out that it can survive on a leaf surface for weeks after germination before any host comes along. Considering how utterly tiny the hyperparasite is, and the fact that it is not eating during that time, this is quite a feat. This feature is advantageous for harnessing it as a biocontrol agent, as a grower would not have to wait until a plant is suffering from a powdery mildew infestation to apply Ampelomyces spores. With some appropriate greenhouse trials this might become an additional tool in the pot grower’s toolbox.

Németh et al. also confirmed previous work showing that, unlike powdery mildew, Ampelomyces is not specific to a single host species, but is able grow within many different species of powdery mildew. This feature might make it amenable to conservation biocontrol, where the biocontrol agent is not raised commercially and sprayed onto the crop, but rather the agroecosystem is managed in such a way that hosts are always available for the biocontrol agent to survive on site. Perhaps a grower could leave sowthistles growing around the perimeter of the system to protect the pumpkins. Perhaps the rosebushes at the ends of the grapevine rows could serve not as early warnings for spray timing, but as reservoirs of biocontrol fungus. Further study is required.

And so Jonathan Swift’s observation rings true: “…a Flea/ Hath smaller Fleas that on him prey,/ And these have smaller yet to bite ’em,/ And so proceed ad infinitum…”. Powdery mildew will always be around, but for Ampelomyces that’s a good thing.