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| U N I V E R S E M A G A Z I N E - F A L L 1 9 9 7 | THE SMELL OF FRESHLY PLOWED SOIL: A Natural History of the Underground SELF-DEFENSE Try though he has for the past 30 years, Jim Cook cannot find resistance genes for root disease in wheat. So how do wild plants manage soilborne pathogens? A big difference between plants in natural habitats and plants in agriculture is genetic diversity, says plant pathologist Jim Cook, warming up to his narrative on root disease. This difference is a given and the subject of much study. But Cook is concerned with an interesting twist on the theme. Because of their diversity, wild plants are a priceless stockpile for genetic material to strengthen agricultural plants. A particularly crucial trait that they offer is resistance, whether it be to disease or insect pests. (See Universe, Fall 1995, p. 5.) But try though he has for the past 30 years, Cook cannot find resistance genes for root disease in wheat. So how, he asks, do wild plants manage soilborne pathogens, if the only way we can manage them in agriculture is through crop rotation or fumigation? The lack of resistance genes for root diseases means there's simply no selection pressure underground. But why? A plant that seeds itself in the same soil every year ought to have root disease, says Cook. That's what happens in agriculture. "I can't help but think that something else is going on out there that relieves the plant of selection pressure, so there's no need over evolutionary time to come up with a genetic strategy within plant populations. Something else is keeping these pathogens in a state of suppression, so they're there, but not raising havoc." Some further comparison is in order here. Natural plant communities grow year after year. Crop rotation, though considered good farming, is a peculiarity of agriculture. One purpose of rotation is to combat soil pathogens. So how do plants in natural communities combat these pathogens? Somehow, writes Cook, in a paper presented at a National Academy of Sciences colloquium, "natural selection has produced abundant examples of useful genetic resistance to above-ground but not to below-ground pathogens." So as Kennedy's work also shows, underground communities must follow a different logic than do above-ground communities. Plants may not develop genetic resistance, but Cook hypothesizes that they do have a strategy. This strategy includes a symbiosis between the root and the community of organisms associated with and supported by that root to provide a defense system. Rather than a genetically conferred resistance, it is a kind of elevation in general plant response to microorganisms that helps the plant be less vulnerable. This strategy lets the root-associated microorganisms compete for nutrients, leaving pathogens and parasites uninvited. In turn, certain bacteria make antibiotics, a form of inhibition of pathogens. Cook and his colleagues call this strategy "induced suppression." The players in this suppression were all once thought to be simply hangers-on, excess baggage on the plant roots. But now they are known to be there for a reason. And, says Cook, it is a general phenomenon. "We're finding that roots do support a select group of organisms adapted to physical habitat provided by those roots." A major focus of Cook's research lab has been the wheat disease take-all, which is caused by the fungus Gaeumannomyces graminis var. tritici. We'll just call it the take-all fungus. Roots turn black as they're eaten by the take-all fungus. Yields in crops hit by take-all generally drop from 10 to 50 percent, though the fungus can "take all" the crop. Take-all can be controlled through rotation, by planting at least one other crop between crops of wheat. When the residue from the old wheat roots rots away from microbial activity, the fungus loses its food base. But farmers have longed to plant wheat continuously, as it's more profitable. They and scientists have long known that continuous cropping of wheat is possibleafter a fairly disastrous first couple of years or so. Gradually, the crop improves, and finally the take-all is gone. In 1988, plant pathologist David Weller and geneticist Linda Thomashow proved that take-all in these fields was being controlled by antibiotics produced by the bacteria Pseudomonas fluorescens. Over time, populations of these bacteria build up in the soil until the take-all is under control. The lab has since developed a seed treatment that coats seed with the Pseudomonas, sending the antibiotic-producing bacteria straight to the battle front. Scientists at the National Center for Agricultural Utilization Research in Peoria, Illinois, are working to develop a commercial process for the treatment. Meanwhile, the search continues for other antibiotic-producing bacteria, both for take-all and other root diseases. Jos Raaijmakers, a post doc, has identified a strain of bacteria that is so good as a colonist of wheat roots that he can put just 10 cells on the seed of wheat and it will grow up to a hundred thousand cells per gram of root in the rhizosphere. Interestingly, he can start with 100 cells and still get only 100,000. Apparently, says Cook, there is a certain size to that strain's niche, a certain carrying capacity. But, he says, "That bug is so good it will achieve the limits of that niche below ground no matter what he starts with on the seed." What Cook and his colleagues are observing is similar to what Kennedy is finding in her work. Different genotypes of rhizobacteria seem to align themselves with certain genotypes of plants. "Presumably we could find different varieties of wheat that could support different varieties of bacteria below ground," says Cook. That approach would admittedly get very complicated. What they're also observing is that there seems to be a natural balance that keeps pathogens in check. Of course, the pathogens do exist in natural ecosystems. For example, says Cook, when previously undisturbed sagebrush country of the Columbia Basin is cultivated, the wheat pathogens are already there, waiting. They just don't seem to cause much trouble in the natural system. It's not as if every wild plant is healthy, says Cook. Disease exists in the wild. But it's generally chronic and rarely reaches epidemic levels. The same is true for above-ground diseases. Again, there's a difference, though maybe it's only one of perception or degree. "We've always explained the lack of epidemics above-ground as a product of diversity in stands of plants there, plus the availability of genes for resistance," says Cook. If the pathogen evolves a virulent trait, the host plant evolves a resistant trait, and things stay in balance. When a field is moved to no-till, at first take-all becomes more severe. But gradually it ebbs. Cook draws his hypothesis of what is happening from natural systems. There is a conversion in the soil from a conducive state to a suppressive state. "As we understand what's going on, the plant-microbe association little-by-little changes toward strains that not only really like those roots, but can make antibiotics that can protect those roots." Organic farmers say that conversion to organic methods takes about three or four years. No-till farmers say the same thing about their fields. First they have a lot of problems, then a conversion. But no one knew for sure what exactly was happening until Cook and his colleagues explained one part of this conversion phenomenon. It is the first case of conversion that has a scientific explanation. But it also shows the complexity of explaining the phenomenon. One of the biggest questions remaining about take-all, as well as other root pathogens, is whether there is one mechanism for take-all decline, or will another part of the world reveal a different one? To answer that question, this summer Dave Weller took off in a van full of buckets, sampling fields across the U.S. to test what he and his colleagues observed so far in the lab. Although several are made by rhizosphere bacteria, molecular analysis shows only one important antibiotic2,4-diacetylphloroglucinol. "It shows up every time the soil is converted from conducive to suppressive," says Cook. "Knock out the phloroglucinol producers, and the soil is again conducive. Add them back, the soil begins suppressing." Close as Cook's team seems to be to controlling take-all, plenty of challenges remain. Inoculating wheat for take-all does nothing against other pathogens. And without that strong competitor, the other pathogens can thrive. So the challenge is to broaden the spectrum of activity of the antibiotic strain. Cook's team has identified traits that will control Rhizoctonia. Now the question is whether they can add those traits to one of their good genotypes, or do they need to find another strain and add it as a mixture? Or will they need to find another method altogether? "It took 30 years to get where we are with take-all," says Cook. "We can't afford another 30 to clear up the others." | U N I V E R S E M A G A Z I N E H O M E | |