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Microbes Helping To Improve Crop Productivity

Plant-associated microbes not only provide several agronomic benefits but also furnish promising antimicrobial mixtures

Ann Reid

Ann Reid is the Director of the American Academy of Microbiology.

Fungi associated with plant roots can increase the efficiency of phosphate uptake in crops such as potatoes and rice.
Plant-associated bacteria that produce a particular deaminase can protect host plants against a variety of stresses.
Plants carrying trehalose-producing bacteria prove resistant to drought and produce more foliage and deeper roots.
A double-stranded RNA virus, paired with a fungal endophyte, enables some plants to grow in high-temperature soils.
Some endophytic fungi produce mixtures of volatile chemicals with potent antimicrobial activity.

Nearly 1 billion people go hungry every day, and providing food for them is one of the great challenges facing humanity, a challenge that continues to grow. Arable land and water for irrigation are limited resources, while the productivity gains from the Green Revolution are now mostly part of the status quo. Moreover, the financial and environmental costs of using fossil fuels to ship foods and fertilizers around the world are becoming prohibitive. Plant breeding and engineering crop plants with newer genetic technologies continue to improve yields or other traits, but are expensive, slow, and applicable mainly to the most widely planted crop species. Further, genetically modifying each and every agriculturally valuable plant species to grow optimally in many different environments does not appear practical. Thus, we need less costly, more sustainable approaches to improving productivity of a wide variety of plant crops.

One promising but largely untapped approach to improving crop plant productivity involves harnessing fungi and other plant-associated microorganisms, according to experts who spoke during a plenary session, "How Microbes Can Help Feed the World," convened during the 2011 ASM General Meeting in New Orleans last May. Those five scientists bring a different perspective to this challenge, one that considers how, over evolutionary time, plants and microbes developed mutually beneficial, cooperative relationships. Importantly, such microbe-plant partnerships can improve the resistance of host plants to a wide variety of stresses, including disease, drought, salinity, nutrient shortages, and extreme temperature. Further, understanding these natural relationships between host plants and their associated microorganisms could be put to better use and might lead to ways of increasing crop productivity while holding costs down and without harming the environment. Indeed, this approach could spark a new Green Revolution.

Several Critical Food-Crop Challenges

Although humans need to produce more food, simply adding more and more fertilizers to current crops will do little to improve yields. Part of the global challenge of producing more food entails increasing the productivity of regionally important crops instead of merely boosting productivity of commodity crops being grown in already highly efficient settings. By relying more on locally produced foodstuffs, we can begin to move away from transporting commodities such as wheat flour and rice from one place to another while consuming more and more fossil fuels in the process. Another goal is to reduce the dependence of farmers, particularly those in developing countries, on imported seeds that, typically, are selected for their high productivity where they were bred.

Greater agricultural productivity is unlikely to come from farmers expanding their efforts into new territories--the global supply of highquality arable land is more or less fixed, and unlikely to expand significantly without sacrifices, for example, in biodiversity. If anything, the goal is to grow crops on reduced acreage or on land that is considered marginally useful for agricultural purposes. Not all such land is marginal in the same way; some of it may be too dry, too salty, or have limited nutrients. Each situation calls for crop plants with different adaptations. Thus, we need to develop crop plants that continue to be productive even when growth conditions are poor.

Rising global temperatures are yet another important factor complicating efforts to improve global crop productivity. One goal is to ensure that staple crops continue to thrive within the climate zones where they now grow. Another goal is to adjust or take advantage of zones in which they cannot grow but soon might. Collectively, these challenges constitute a huge and perhaps overwhelming task for plant breeders.

Plants routinely establish relationships with microorganisms, some of which may be familiar while others are little recognized or appreciated. noduleFor instance, nitrogen-fixing bacteria typically live in nodules along the roots of leguminous plants, forming a mutually beneficial relationship. Bacteria are not the only members of the microbial world to form close partnerships with plants. Many fungi and viruses also form such partnerships. Some of these relationships between plants and microbes, which developed over millions of years, are close to being harnessed on a commercial scale to support crop growth, according to several experts who spoke at the ASM General Meeting session.

For instance, arbuscular myccorhizhal fungi (AMF) live within plant roots, from which they send out filaments that collect phosphate, a critical nutrient for their host plants, according to Ian Sanders from the University of Lausanne in Switzerland, who spoke during that session. These fungi, which microbiologists first recognized about 40 years ago, are "found in all soils," where they form "symbioses with plant roots," he says. When scientists applied AMF to crops years ago, they conducted those field trials in North America and Europe where plants grow well with conventional phosphate fertilizers, he says. Thus, adding the fungi had little effect, "and hardly anyone uses them."

Farming in the tropics is another story, Sanders continues. "In the tropics, farmers need to add huge amounts of phosphates," he says. "All farmers add phosphate, but we're aiming to increase yields and reduce the amounts of phosphate being added." His research involves selecting and adapting isolates of AMF that will thrive in tropical soils, improve uptake of phosphate along the roots of plants being grown commercially in those regions, and testing whether adding such fungi will improve yields of crops such as cassava, rice and potatoes. "Those crops form natural [symbioses] with myccorhizhal fungi, and we're adding more and modifying the genetics hopefully to get better yields," he says.

There are some promising results, particularly with potatoes being grown in test plots by his collaborators at the National University of Colombia, according to Sanders. Yields of potatoes grown with AMF remain steady, but those plants require only 38% of the phosphate fertilizer that is usually added to this crop plant, he says. This savings in use of phosphate fertilizer is additionally important because intensive use of phosphate comes with an "environmental cost" and "phosphate reserves are being depleted," he points out. Meanwhile, in other experiments in Colombia in which such fungi are added to rice, there is a 20% increase in yield, according to Sanders. "We never expected this increase in yield, but it's very encouraging," he says.

The prospects are bright for using AMF in many settings involving crop plants, in part because of the inherent genetic diversity of such fungi, Sanders adds. Each fungal cell contains thousands of nuclei with a range of genetic variation distributed among those nuclei. By crossing fungi and allowing nuclei to segregate into separate spores, it is possible to develop novel fungal lines to evaluate for their growth effects on host plants. Improved lines are sent to a biotechnology company that has methods for expanding fungal lines and for packaging them in a proprietary gel that makes it easier to ship and apply the material to plants in fields.

Some Microbial Products Reduce Stress Pathways in Host Plants

Bacteria with the gene encoding the enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase can protect host plants against a variety of stresses, including drought and flooding, heavy metals, high salinity, and pathogens, according to Bernard Glick from the University of Waterloo in Ontario, Canada, another speaker during the plenary session.

ACC deaminase acts by damping a major stress response pathway in plants. When plants are stressed, they produce ethylene gas, which plays many roles in plant growth and development, including stimulating root lengthening and fruit ripening. However, when plants produce ethylene in response to stress, root growth stops, leaves fall off, and fruit production slows. While these effects may be protective in the wild, all of them reduce productivity in agricultural settings. Because ACC deaminase inactivates an ethylene precursor, plants no longer can produce the gas, even when stressed, and productivity remains high.

Another approach easing drought stress on plants involves bacteria that make the sugar trehalose, according to another plenary session speaker, Gabriel Iturriaga from the Universidad Autonoma del Estado de Morelos in Mexico. Helping crop plants withstand drought is critically important because high temperatures and salinity affect more than 30% of arable land, reducing crop yields by up to 50%.

Some naturally drought-tolerant plants produce trehalose, which stabilizes membranes and enzymes, protecting them against damage when cells are subjected to repeated cycles of drying and rehydration. Although the capacity to synthesize trehalose is rather scarce among plants, many microorganisms, including bacteria and fungi, can synthesize this simple disaccharide. "We were surprised to find several genes for the biosynthesis of trehalose in many plants that do not come from arid environments, where those genes are tuned down or silent," Iturriaga says. Inducing such plants to produce extra trehalose makes them resistant to drought.

However, it might prove more effective to use plant-associated bacteria to provide the hosts with trehalose, instead of engineering plants to make more of the disaccharide, according to Iturriaga. In pursuit of that strategy, he and his collaborators induced
Rhizobium etli,
a bacterium that grows within the roots of bean plants, to overexpress trehalose. Plants carrying the trehalose-producing bacteria prove more resistant to drought and produce more foliage and deeper roots, he says. The productivity of such plants increases by more than 50% under normal conditions, and continues to produce at least 50% of normal yields under conditions of drought. Meanwhile, the productivity of plants without the trehalose-producing bacteria drops to nearly zero.

Inoculating corn with trehalose-producing
Azospirillum brasilense
also improves drought tolerance and productivity, Iturriaga continues. Curiously, the drought resistance in the corn and bean plants does not correlate with increased trehalose production. Instead, the trehalose apparently signals several stress-resistance pathways in the plants, he says.

Unexpectedly, Some Viruses Improve Plant Productivity

If the notion that bacteria or fungi can improve plant productivity takes some getting used to, what about the idea that viruses also improve plant productivity and provide help toward reducing stress? However, symbiotic viruses help to explain how some plants manage to grow in soils next to hot springs in Yellowstone National Park, according to Marilyn Roossinck from the Noble Foundation in Ardmore, Okla. Soils surrounding such hot springs sometimes reach temperatures greater than 50oC (122o
F), well above the usual limits for vascular plants. Nonetheless, panic grass thrives, growing in clumps surrounding hot springs.

Panic grass survives by growing in symbiosis with an endophytic fungus,
Curvularia protuberata. Plants with C. protuberata in their roots can survive soil held at 65o
C for 10 days, Roosinck says. However, the fungus itself is not equipped to protect the plant, she finds. In the wild, that fungus is infected with a doublestranded RNA virus, and if the fungus is "cured" of the virus, its host plant can no longer withstand hot soils. Somehow this virus, whose genome encodes only five proteins, enables the fungus and the plant to survive high temperatures. Other kinds of plants living in hot volcanic soils in Central America carry fungus-virus pairs similar to those found in the Yellowstone panic grass, she adds.

Roossinck is studying the molecular basis of these partnerships with the goals of better understanding how fungi-viral pairs can enable host plants to withstand hot soils and then using this information to apply to crop plants. In more general terms, endophytes from native plants growing in harsh environments may prove useful if they can be matched with, adapted to, and proved protective for commercially important plant crops, she says.

Some Fungi Protect Plants against Damaging Insects and Pathogens

Fungi may help increase crop productivity and, thus, the food supply in another way--by reducing waste, according to another session participant, Gary Strobel of Montana State University. "For fun and work, I go to jungles in the equatorial regions of the world to find new microorganisms," he says. "I've been to rain forests, the tropics, and temperate zones looking for low-hanging ‘fruit' to bring back to the lab." Like Roossnick, he has a particular interest in endophytes, particularly filamentous fungal species that live on and within plant tissues, forming many different kinds of relationships with their host plants.

About 12 years ago, Strobel returned from South America with plant samples that were infested with mites. After placing cuttings on agar to encourage endophyte growth, he put the materials in an airtight box for 12 days that, once opened, gave off a strange odor and contained a white fungus, which he later named
Muscodor albus
-"stinky white fungus." Indeed, this fungus produces a mix of about 30 volatile compounds, most of which are harmless in themselves, but collectively prove profoundly antimicrobial. Calling it as effective as bleach but safe enough to drink, Strobel says the mixture "is ready to go for decontaminating fruits and vegetables" and also "can be used to take care of biofilms." The fact that activity resides in a mix of chemicals is "important," he says. Many researchers "follow a mindset" of looking for single molecules with antimicrobial activity, "but nature doesn't work that way; it's a mixture."

Other endophytic fungi that Strobel collected during his travels produce a diverse array of compounds with an equally diverse array of activities. "This field [of research] is enormous, and we just don't know how these microbes interact with plants," he says. "All kinds of barriers say this research is impossible." However, he urges others to take up many of its challenges, which include traveling to exotic locales to collect specimens, braving diseases and discomfort, conducting the chemical assays and the microbiological workups, and writing the patent applications to protect intellectual property needed to commercialize it.

For the 1 billion people who face starvation, this emerging field of microbiological research "can really contribute" toward helping to "provide more food," adds Sanders from the University of Lausanne. "For those of us in microbiology, we need to use what we have and also find new things."

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