A Garden of Marvels

by Ruth Kassinger

  In 1885, the Prussian government became interested in truffles, the delicately flavored, highly valuable fungi so cherished by gastronomes. Truffles, round or oblong, grow on the underground roots of certain trees. Specially trained pigs and dogs sniff them out so their owners can carefully excavate them. France had long been a major source of truffles, and by the mid-1800s, some farmers in the southeastern part of the country had even figured out, if not exactly how to cultivate them, then at least how to encourage them to grow. (The trick was to have alkaline limestone soil, the exact combination of hot and dry weather, and to plant acorns taken from the soil near truffle-producing oak trees.) Only one species of truffle grew in Prussian soil, and it had never been the source of revenue that French species were. So, the Prussian government commissioned a well-regarded botanist and professor at the University of Leipzig, Albert Bernhard Frank, to see how Prussia could remedy this exasperating state of affairs. Frank’s task was to identify which Prussian trees and soils were best for growing truffles.

  Regrettably for the Prussian economy, Frank made no headway in uncovering edible truffles. However, as he investigated the subject, he was surprised to discover that certain thready fungi grew on the roots of almost all the tree species he dug up. He became fascinated with the mycorrhizae (a word he coined meaning “fungus of roots”) and realized that they are not only not harmful, but exceedingly helpful—in fact, essential—to their hosts. Not killers or even freeloaders, they are industrious miners that exude enzymes that pry apart organic and inorganic compounds and liberate chemical elements in the soil, especially phosphorous. Phosphorous is an ingredient in DNA. It is also a part of adenosine triphosphate, or ATP, the organic molecule that is the universal store of quick energy that plants (and animals) use to fuel almost every cellular process. After mycorrhizae emancipate elements from the soil, they pass them through their bodies and into a root hair. The threads also act like delicate straws, allowing root hairs to sip from reservoirs of water too minute for even root hairs to access.

  Recently, scientists in the United Kingdom have demonstrated that the mycelia also protect plants from predators. When a plant is assaulted by aphids, it produces chemicals that repel them, as well as attract parasitic wasps that attack its attackers. (The wasps lay their eggs in living aphids, which are then consumed from the inside out by emerging larvae.) If the plant is connected via mycelia to other plants, those plants receive a chemical signal from their besieged comrade, and mount their own chemical defense before the first aphid arrives. Nearby plants that are not “networked” do not gear up for an attack. (The aphids, by the way, may counter by producing winged rather than crawling young that can fly off to an unsuspecting target.)

  Mycorrhizae don’t do all this work for free. Plants compensate their partners by releasing sugars stored in roots. In some cases, they dole out as much as 30 percent of their reserve sugars to their underground partners. The mycorrhizae, nurtured by their hosts, are permanently relieved of the necessity of competing with all those other rhizospheric creatures for organic matter to eat. It is a remarkably productive symbiosis—another term that Frank coined—that can increase roots’ ability to absorb water and nutrients by as much as several thousand times. Ninety percent of plants have mycorrhizae, and many can’t survive without them.

  Paleobotanists now believe that land-based plants owe their very existence to their thready fungal partners. The first members of the plant kingdom to gain a toehold on land more than 450 million years ago were thalloid liverworts. These early liverworts had a flat, nonleafy photosynthetic surface. Instead of roots, they had rhizoids—hairlike filaments—that tentatively anchored them to river banks and shorelines. On these wet land surfaces, the rhizoids encountered fungi that had already colonized land some 250 million years earlier. (The fungi literally scraped out a living by exuding a mild acid that dissolves carbon and other elements from rocks.) A little sugar made by photosynthesis inadvertently leaked out of some liverworts’ rhizoids; some fungi didn’t gather up every bit of the nutrients they wrested from the land’s rocky surface; and a marriage of convenience was made. Over millions of years the liverworts’ simple rhizoids with their companion fungi grew longer, stronger, and more complex, and evolved into roots. Roots cracked rocks, thereby releasing more mineral nutrients. (Roots wear down rocks five times faster, it is estimated, than weather does alone.) Richer and richer soil supported ever more rooted plants, and the once-barren continents turned green.

  One of those species that evolved, hundreds of million of years after mycorrhizae and liverworts first made their bargain, was the Citrus medica or citron, one of the oldest extant citrus species, of which my Buddha’s Hand is one variety. When the nursery bare-rooted my tree, most if not all the delicate root hairs died, and with them their even more fragile mycorrhizae. New root hairs developed after I transplanted my tree, but because I used a sterile potting mix, there were no mycorrhizae to recolonize the root hairs. Eventually, when I moved the tree outdoors in the spring, fungal spores would likely have landed on the soil, and the symbiosis would have revived. But at Edie’s suggestion, I bought a mycorrhizal mix—available in garden stores and via the Internet—and watered it in. Thanks to its fine fungal friends, my Buddha’s Hand revived and now regularly produces fruit and its attendant pleasures—zest and pith for cooking and marmalade—throughout the year.

  eleven

  Arsenic and Young Fronds

  About three miles from my home in Maryland is a Washington, D.C., neighborhood known as Spring Valley. Here, multimillion-dollar homes nestle in banks of azaleas and boxwood, shaded by oaks, tulip poplars, and other stately shade trees. Adjacent to the neighborhood is American University, an institution with some twelve thousand undergraduate and graduate students. The manicured tranquility of the neighborhood belies its past. In 1917, while American troops were rushing to the battlefields of Europe, the newly established and financially precarious university contracted its scientists and its undeveloped land to the U.S. Army’s Chemical Warfare Service. In order to simulate the western front, the army dug trenches, staked dogs and goats in them, and exploded shells filled with forty-eight poison gases over and in the trenches. The idea was to test the toxicity of the chemicals and to figure out how to defend against them. When the war ended the next year, the army abruptly shut down its operations. It burned seven structures—which, according to newspaper reports at the time, produced a “suffocating” cloud of smoke—and buried leftover shells, drums of chemicals, and contaminated laboratory equipment in pits dug at the outer reaches of the university’s acreage. Then, everyone forgot about AU’s year of living dangerously.

  Decades later, the university sold much of that acreage to real estate developers, and the Spring Valley neighborhood sprang up. In January 1993, a backhoe operator digging a trench for a new sewer line in one of the last undeveloped parcels uncovered four unexploded 75mm artillery shells. The Army Corps of Engineers investigated and discovered a total of 141 buried munitions. The Corps removed tons of soil from eleven sites, and two years later pronounced the area clean. In June 1996, however, workers planting a tree on the grounds of the university president’s home were overcome by odors and suffered severe eye irritation. Soil testing at the site revealed hazardous levels of arsenic, a poison that causes cancer and birth defects. The arsenic was undoubtedly a by-product of buried chemical weapons. Testing on the nearby property of the South Korean ambassador’s residence revealed arsenic levels that were as much as fifty times the twenty parts per million (ppm) that the U.S. Environmental Protection Agency considers acceptable. After excavation at another residence unearthed 380 shells and several fifty-five gallon drums, most containing mustard and blister gas, the Corps agreed to test every property in Spring Valley. One hundred and thirty-nine lots, as well as AU’s Child Development Center playground, were found to have excessive arsenic levels. Much of the ensuing cleanup involved digging up and carting away the contaminated soil, a process that des
troyed well-established plantings, damaged the root systems of cherished trees, and left mud wallows in front yards.

  In 2004, a Virginia-based company called Edenspace won a contract with the Corps to try a new, experimental approach. It planted the contaminated areas with Pteris vittata, commonly known as brake fern. This quite ordinary-looking fern has one extraordinary quality: Its roots pull arsenic out of soil. The arsenic then travels up the xylem to be concentrated in the fronds at levels up to a hundred times greater than in the soil. (The fronds are then harvested and disposed of safely.) Edenspace planted 2,800 brake ferns the first year and more than 20,000 in subsequent years. In 2006, the EPA determined that thirty-five sites at fourteen residences planted in ferns had been cleaned. Phytoremediation, the power of plants to decontaminate soil and water, had worked, and the cleanup cost was a small fraction of removing the soil. As a bonus, instead of wallows, the residents had fern gardens.

  But why would brake fern roots snarf up arsenic? How could the brake ferns survive laced with so much of a metal generally as poisonous to plants as it is to animals? One of the world’s leading experts on the uptake of metals from soil and a founding father of phytoremediation is Dr. Rufus Chaney, senior research agronomist at the U.S. Department of Agriculture. I go looking for him at the redbrick campus of USDA’s Agricultural Research Center in Beltsville, Maryland.

  The scientist I find in the basement of Building 7 is a ruddy, gray-haired, crew-cut bear of a man who waves me into an office that seems two sizes too small for its occupant. It is lined floor to ceiling and wall to wall with file cabinets and shelves. The shelves are crammed with stacks of papers. Rufus, as he introduces himself, has been working at USDA for forty-three years, and his published work fills a number of those shelves. He has 428 papers and 266 abstracts to his name, and a dozen more papers in the works. In addition to his own research and writing, he lectures frequently, and has directed the theses of three dozen Ph.D. candidates. He could have retired a decade ago, but the work he loves is as yet unfinished.

  Nickel has been the leitmotif of Rufus’s life, played with variations—mournful, exciting, hopeful, frustrating—for more than half a century. His first encounter with the metal was as a teenager, growing up on a corn and soybean farm in the flatlands of northern Ohio in the 1950s. One year his father applied a liquid fertilizer to their soybean crop, and to his horror, the plants shriveled and died. It turned out that the fertilizer had been delivered in dirty drums contaminated with the waste of a nickel-plating operation.

  “At that point,” Rufus told me, “my father felt he could gain more by suing the fertilizer company than farming. Unfortunately, that was a very slow process, and he lost the farm to the banks and the lawyers before he could collect. I’d been planning to work on the farm so, of course, it had a huge effect on me: I had to find a different job. It’s ironic, but that experience gave me a career.”

  As an undergraduate, he studied chemistry and wrote his senior paper on nickel in tobacco smoke. As a graduate student at Purdue, he worked on nickel uptake in soybeans, and how it inhibits the uptake of iron, to the detriment of the crop’s health. Postdoctoral work at USDA led to a full-time position in 1971, and he was assigned to work on the problem of heavy metals in sewage. At the time, cities were growing rapidly and septic systems that had been built in the previous century were becoming overburdened. Municipalities were replacing them with sewage and wastewater treatment facilities at a rapid pace. But what were the facilities going to do with all the thick residue called sludge (and now, more scientifically but less vividly, referred to as “biosolids”) that emerged at the end of the water-cleansing process? Because biosolids are basically human manure, and manure is rich in essential fertilizers like nitrogen and phosphorous, it seemed like a good idea to plow it into farmland.

  And it was, in theory. But nitrogen and phosphorous were not the only elements that made their way into the sewers and through the treatment process. Some sludges also contained heavy metals like zinc, cadmium, cobalt, nickel, and others that could kill crops and might, if they entered the food chain, harm people. Rufus was asked to investigate the toxicity of heavy metals to particular crops, whether they entered the food chain, and if there was a way to prevent their uptake into plants.

  In 1977, Rufus read a paper on a remarkable quality of Alyssum bertolonii, a low-growing plant (unrelated to what gardeners know as sweet alyssum) with masses of small, four-petaled yellow flowers. The paper reported that roots of Alyssum took up large amounts of nickel that then accumulated in the plants’ tissues at levels that should have been toxic. The plants were found growing on “serpentine barrens,” that is, areas where it was generally assumed that the naturally occurring high levels of nickel, cobalt, and chromium (and perhaps low levels of calcium and phosphate) made the soil infertile. Somehow Alyssum not only tolerated the conditions, but thrived, never mind that its leaves contained nickel at levels a thousand times greater than average. The paper’s authors concluded that “the reason for this preferential accumulation of nickel . . . should prove to be an interesting problem.”

  Alyssum bertolonii has bright yellow flowers.

  Rufus was indeed intrigued. Why would plants have evolved a mechanism to hyperaccumulate a toxin, and how did they do so safely? Serpentine barrens are not common, but there happened to be one not far from his office, and he planted some seeds and began to experiment. In 1980, the EPA became interested in his work, but then the administration changed and the project was killed the next year. Nonetheless, he kept working on unraveling the biochemistry and agronomy of what are known as “hyperaccumulators.”

  To understand how hyperaccumulators work, we have to drill into roots. Taking up certain chemical elements from the soil is one of the prime functions of roots. Today, the consensus is that seventeen of the ninety-two naturally occurring elements on Earth are essential for all plants. Three of those elements—carbon, hydrogen, and oxygen—plants take from air and water. Of the fourteen soil-based nutrients, six—nitrogen, phosphorous, potassium, calcium, sulfur, and magnesium—are macronutrients, which simply means that they are present in plant tissues in large quantity. (Large is a relative term here: Together, the weight of all the soil-derived elements is only about 1.5 percent of a plant’s total weight.) The other eight—copper, iron, manganese, nickel, zinc, boron, chlorine, and molybdenum—are micronutrients. Some of these are integrated into the substance of a plant’s leaves, stems, roots, and flowers. Others are important to processes like photosynthesis and transporting carbohydrates in and out of cells. A trace amount of nickel, for example, is necessary to make an enzyme that breaks down urea, which would otherwise accumulate and damage leaves. An insufficiency of any essential element means the plant grows to less—in some instances, far less—than its genetic potential. (Therefore, when you shop for houseplant fertilizers, look for ones that contain all essential macro- and micro-nutrients.)

  In order for a plant to take up any element in the soil, that element has to be soluble in water. When a water-mineral solution encounters the epidermal cells of a root tip, it flows either directly through them or through spaces between them. Once past the epidermis, it continues through the loosely packed parenchyma cells toward the xylem at the interior of the root. But before it gets to the xylem, the solution encounters the endodermal tissue, a layer of tightly packed cells. Here the going gets tough, at least for the minerals. Any spaces between these cells are tightly caulked by a fatty, waterproof material called suberin that blocks fluid from entering. This means that minerals in the water must pass through the membrane of the endodermal cell. While water can pass through freely, larger molecules are stopped. They can only enter via protein-constructed membrane transporters, which are something like automated revolving doors. These are not like the revolving doors at airports, however, able to accommodate everyone, including a traveler pushing a luggage cart. Membrane transporters generally fit only one particular element, and the plant creates them or
dismantles them in accordance with its need for that particular nutrient. Because plants must spend energy to create and operate transporters, they have evolved to admit only those chemical elements that contribute to the plant’s survival.

  (The discovery of this dual system for taking up inorganic nutrients—effortless osmosis of some molecules and the selective uptake of others—answered a question that had troubled scientists since the ancient Greek era: Do roots actively choose nutrients from the soil or only passively receive them? The answer, we now know, is both.)

  So, why and how does Alyssum take up nickel in such quantities? The first thing Rufus discovered is that nickel is hyperaccumulated only when the soil is acidic, as in the case of serpentine soil. Acidic conditions alter the chemistry of the revolving door for iron so that nickel can slip inside, too. But what about toxicity? It turns out that Alyssum has evolved an ability to move the nickel out of its cells and isolate it in its leaves in fluid-filled cells called vacuoles. Better yet, once sequestered in the vacuoles, the nickel becomes a homemade pesticide. Nibbling bugs that get a mouthful of nickel-laced leaf either die or look elsewhere for dinner. High levels of nickel actually give hyperaccumulators a competitive advantage. The insecticide is so effective that some nickel hyperaccumulators (and there are nearly four hundred such species in several genera) have lost other disease-resistance mechanisms and cannot survive in soils that have only average amounts of nickel.