Phytophthora man

Recent Ph.D. graduate Tyler Bourret is a phytophthorologist to watch out for. In his nascent career Dr. Bourret has pushed the boundaries of knowledge about that peculiar group of organisms known as Phytophthora.

Once believed to be a type of fungus, Phytophthora is actually a fungal-like organism descended from algae, a member of a group of organisms known in the vernacular as the water molds. It forms a network of tiny threads like a fungus, but its cell wall is made of cellulose, the same material that makes up plant cell walls, where a true fungus would have a cell wall made of a different material known as chitin. From its waterborne ancestors Phytophtora has inherited a type of spore that propels itself through water using flagella. Furthermore, it is not susceptible to many of the usual fungicides.

The name Phytophthora comes from the Greek, meaning “plant destroyer”. Phytophthora blazed a path of destruction across Europe starting in 1845, when late blight disease, caused by the species dubbed Phytophthora infestans, destroyed potato crops in several northern countries, notably Ireland. P. infestans’ uncharacteristically airborne spores allowed it to spread widely to infect whole fields of potatoes. Nevertheless, while many plant pathologists consider P. infestans as the cause of the so-called Irish Potato Famine, such a reductionist disciplinary view ignores the role of the English overlords, who exported great quantities of food from Ireland while the common people starved.

Since that time scores of other Phytophthora species have been discovered. The pathogenic forms normally cause root rot in annual and perennial crops and in wild plants, unlike the whole-plant-infecting P. infestans. The swimming spores take advantage of water-saturated soil, which can be a result of overwatering, to find a banquet of roots. The non-pathogenic forms live in ponds and streams, where they colonize dead plant matter and are probably what you smell when you get a whiff of stagnant water. The most recent species to grab headlines is Phytophthora ramorum, “Phytopthora of the branches”, cause of sudden oak death. P. ramorum can live in streams, colonize California bay trees without causing symptoms except for burned leaf tips, and then from those leaf tips produce spores that get splashed or blown onto the trunks of susceptible trees, most notably tan oaks, where they produce massive deadly cankers.

Sudden oak death burst onto the scene seemingly out of nowhere. At the same time that it was found devastating California woodlands, it was ravaging the European nursery trade. Only years later was a diversity hotspot of P. ramorum was found in southeast Asia, indicating that region as its native range. Unfortunately this kind of knowledge gap is common regarding Phytophthora. Dr. Bourret and colleagues discovered new species of Phytophthora while monitoring streams for P. ramorum and also while screening native plants from a nursery that were used in a restoration planting. It is not known whether these new species are native or introduced because no coordinated effort has been made to survey Phytophthora in different habitats around the world.

The other gap in knowledge is the virulence of these species in introduced habitats. Phytophthora pluvialis, a North American stream dweller, is now causing epidemics on Monterey pine in New Zealand. Plants or soil coming into the US could carry a strain with the virulence capable of causing the next epidemic of forests or crops, and in an era of rollbacks of government spending and regulations, they may not be discovered before mass plant destruction. In another questionable endeavor, Dr. Soum Sanogo’s lab in New Mexico is experimenting with inoculating the non-pathogenic water-dweller Phytophthora riparia onto chili pepper plants to essentially vaccinate them against Phytophthora root rot. Dr. Bourret points out that every Phytophthora species has all the machinery in its genetic makeup for causing disease in plants, but that the water-dwellers are generally overburdened with this machinery, making them easy targets for the plant innate immune system. The risk is that a water-dweller could lose some of its burdening genes and become a pathogen, as seems to have happened with Phytophthora megasperma.

One of Dr. Bourret’s areas of special fascination is the complex family tree of Phytophthora and its relationship with another set of algae descendants, the downy mildews. Downy mildews are not plant destroyers, but rather parasites that can only survive while their host is living, a condition known as obligate biotrophy. Their spores, still encased in their spore-bearing structures, travel through air and land on leaves to infect. The name comes from the fluff that appears on the underside of leaves when their threadlike growths exit through the leaf stomate pores to send off more spores. Because they are intimately dependent on their host’s cellular processes, they are confined to the single host species that they have co-evolved with. They are divided into twenty different genera based on characteristics such as host type, spore color, and leaf-penetration organ.

Since the turn of the current century, advances in molecular genetics have led to the unexpected finding that downy mildews are actually descendants of Phytophthora. The question then became where the downy mildews fit within the family tree if obligate biotrophy is all but absent in Phytophthora. Dr. Bourret analyzed the sequences of six common genes in over 100 species, including all of the downy mildew genera. His big innovation was to include an unusual species of Phytophthora from nutsedge that exhibits obligate biotrophy and an unnamed New Zealand Phytophthora species that was found infecting leaves of the totara tree, a conifer. He was able to show that the those downy mildews that infect sunflower-family plants are descended from a common ancestor they share with the nutsedge-infecting Phytophthora, and that the downy mildews that infect grasses, mustard-family plants, and others such as spinach descended from a common ancestor they share with the New Zealand leaf-infecting Phytophthora. Of course, with all the evolutionary changes required for a family tree branch to lead to true obligate biotrophy, the branches that lead to powdery mildews stick way out from the main tree.

Another result that popped out of the data is that of the six genes studied, those genes contained within the nucleus indicated some different family relationships among the different species than did the genes maintained outside of the nucleus. This disagreement suggests that sometime in the past there were hybridizations between species, or perhaps some species picked up DNA from the environment. Good science leads to the next set of questions, and Dr. Bourret is on his way to a lifetime of discoveries.