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FEATURE ARTICLE

Wild Plants to the Rescue

Efforts to domesticate new, high-yield, perennial grain crops require patience and persistence—but such plants could transform agriculture

David Van Tassel, Lee DeHaan

2013-05VanTasselF1.jpgClick to Enlarge Image“You had to spend all those years in graduate school to do this?” my mother asked in disbelief. I was walking slowly backwards and dragging a heavy board, at the end of which was another heavy piece of lumber with foot-long bolts sticking through it at three-foot intervals. As the bolts scraped the soil they made parallel lines. I was trying to make those lines as straight as possible.

The reason I was dragging this medieval-looking contraption, and the reason my coauthor Lee DeHaan had built it, was to form a giant grid to help correctly place thousands of seedlings of a wild sunflower relative, Helianthus maximiliani. The seedlings needed to be at equal distances from each other and in an arrangement that allowed us to map their location. Each seedling was genetically unique, with a known family history, and each had an empty row in my spreadsheet waiting to be filled with data: height at flowering, number of seed heads, stalk diameter, leaf length and width, number of seeds per head, weight of 100 seeds. Most of these traits are fairly objective and would be measured by pairs of student field assistants, one with a ruler or measuring pole, the other with a notebook or handheld computer. For consistency, I would need to score other, more subjective traits: foliar disease severity on a scale from 1 to 9, percent of heads at a certain stage of maturation on a certain day, severity of lodging (the tendency of stalks to lean, droop or even collapse).

Because these plants are long-lived, we would be collecting data for two seasons. We would get to know the plants intimately. But of the 1,000 in this experiment, only the top-ranked 50 would be kept and mated together, their offspring used to create the next breeding population. The remaining 950 would be ruthlessly plowed in. I was molding a hardy but agriculturally useless wild plant into an oilseed grain crop, something natural selection could never have accomplished. Like a god—but a sweaty, exhausted one.

Of course, all Sylvia Van Tassel could see was her tired son dragging a board through an empty field for hours. I don’t think she ever visited me in September, when my research plots are a vast golden bouquet of thousands of wild sunflowers. She might not have been impressed even then: I had told her for years that my work would help feed people some day. Unfortunately, the sunflowers didn’t look much like a crop. My colleague Sheila Cox and I usually have at least one plot each year that we refer to as “the jungle,” and most of the others are nearly as tall and tangled.

Mom certainly would have raised her eyebrows at the tiny seeds the plants produce, if I had dared to show her. But plenty of people have been drawn to investigate the idea of grain crops that are perennial rather than annual. The Soviets were trying to breed a perennial wheat as far back as the 1930s. J. Russell Smith’s 1953 book Tree Crops, A Permanent Agriculture influenced a generation of ecologists and agronomists, including Wes Jackson, the founder of the Land Institute, where DeHaan and I work. In a 2010 article in Science, scientists from 21 institutions on 5 continents called for serious investment in perennial grain crops, and this call has been echoed in more recent publications. More generally, scientists concerned about the combined impact of climate change, continued human population growth and resource depletion on global food security have warned against complacency with our existing crops and cropping systems, and have urged innovative agricultural research.

Our domestication efforts take place at the Land Institute, founded in 1976. We begin with wild relatives of crops—Van Tassel’s breeding program focuses on sunflowers and DeHaan’s on wheat. We have chosen for practical reasons to use relatively low-tech methodologies. Still, our mothers might be forgiven for wondering if something doesn’t quite add up. Their highly educated sons are supposedly working on long-term food security—surely the most pressing and basic challenge for science and policy—on a bold project that many respected scientists have agreed could lead to a breakthrough. Yet here they are scrabbling in the dirt at a small organization privately funded by citizens’ donations. If this work is so important, where are the powerful institutions, the high-tech equipment, the labs full of students? On her first visit to the institute, DeHaan’s mother marveled that an organization with such a lofty mission was housed in what looked like a modest family farm.

Appearances aside, small nonprofit research organizations like the Land Institute occupy a unique niche in the crop-improvement ecosystem. Although progress requires time and patience on a scale that family members, friends and fellow scientists may find surprising, our plants improve year by year, and the prospects for expanding and accelerating this work are promising.

It’s worth noting that our definition of grains is broad. Botanically speaking, many grains are actually fruits (for example, wheat or sunflower “seeds”). For our purposes, a grain is any hard, dry seed or fruit that can be harvested like a grain—including oilseed crops such as sunflower. Many kinds of plants may offer candidates for breeding perennial grains, from desert shrubs to plants capable of growing in seawater. We hope that our work toward perennial oilseeds and cereals will inform and inspire researchers and funding organizations—those who are already at work domesticating other kinds of plants and those who might wish to begin. New staple crops with enhanced functionality will help efforts to stabilize the world’s food supply and reduce the soil degradation that comes with large-scale annual grain production.

The Art and Science of Domestication

2013-05VanTasselF2.jpgClick to Enlarge ImageSince 2000, when our current perennial-grain breeding programs began, the Land Institute has expanded, built new facilities and invested in new research technologies. Although we occasionally use DeHaan’s wooden contraption to lay out small plots, more often we use a mechanical transplanter, capable of planting in hours the number of plants we used to set in days spent on hands and knees. Although we can’t get a perfect grid with this technique, we use a GPS unit with centimeter-level precision to map the location of each plant in the field. These modest technological improvements, along with others, such as bar-code readers and handheld computers, allow us to study many more plants each season. In 2012, between our two domestication programs, we evaluated over 40,000 recently transplanted, individually spaced genotypes.

Plant breeding is always a numbers game. In our case it is even more so. The wild species we use are rich in genetic variation, and individual plants are highly heterozygous and do not breed true. In addition, we are looking for rare alleles, so the more plants we try, the better. These rarities may be new mutations, or they can be existing ones that are neutral—or are even selected against—in a wild population. A good example is mutations that disrupt seed dispersal, leaving the seeds on the heads long after they are ripe. An individual expressing this trait, known as shatter resistance, would have reduced fitness in the wild, but it is precisely the kind of plant we are looking for. Shatter resistance is an absolute requirement for a grain crop, because once grain falls to the ground it is virtually impossible for the farmer to recover it.

2013-05VanTasselFA.jpgClick to Enlarge ImageSidebar: Perennially Productive. Plant domestication has resulted in small, short-lived, high-yield annual crops and longer-lived, larger perennial crops. But smaller plants with the yield of annuals and the lifespan of perennials have not developed. The authors hope to fill this gap. For more, click the image at left.

Although we use each plant’s pedigree, along with sophisticated genetics software, to make predictions about the breeding value of each plant, our overall approach could be considered rather old fashioned, even “brute force.” It certainly feels like brute force, physically weeding, harvesting and threshing thousands of plants. Another downside of this strategy is that we produce tens of thousands of data points, but relatively little in the way of publishable results. Our work might be compared to that of a natural-products chemist who screens millions of microbes for novel antibiotics. But unlike the pharmaceutical industry, we do not have standard assays or product-pipeline benchmarks. Chemists know that antibiotics exist and that novel ones are periodically discovered. We have satisfied ourselves, through deductive reasoning and careful reading of the literature, that wild perennial herbs and shrubs can be domesticated to offer dramatically higher grain yield than their wild ancestors, but this has never actually been done.

In our efforts to produce at least one breakthrough on the scale of Alexander Fleming’s discovery of penicillin, we have reasoned that it is most important to push evolutionary change as fast as possible. When we have made more progress, perhaps we will find more opportunities for funding and collaboration, allowing us to analyze more carefully what exactly happened during the domestication process and describe how it could be repeated and, if possible, accelerated. That first breakthrough may come from a wild wheat relative.

The Kernza Story

2013-05VanTasselF3.jpgClick to Enlarge ImageWhen we embarked on our breeding program, our primary approach was to develop perennial grain crops by hybridizing current annual crops with perennial relatives. We saw this method as a shortcut that would allow us to begin with domestication genes that had accumulated over thousands of years. All that was needed, we figured, was to introduce the key lifestyle trait of perenniality from a related species. The approach has promise, and for some crops, we are continuing along this path.

But back in 2001 we were also intrigued by the possibility of improving the wild perennial species themselves in order to develop entirely new perennial grain crops. With this strategy we could avoid the genetic complications that arise when two species are crossed (sterility, for instance), and we would be assured of having a strongly perennial plant to work with.

We started side projects to investigate the potential of numerous wild perennial species. One of these was intermediate wheatgrass (Thinopyrum intermedium), a species that had been studied by another nonprofit organization, the Rodale Institute, since 1987. The species is, as the name suggests, a grass; but it is no more closely related to wheat than barley or rye. After about six years of giving the wheatgrass part-time attention, we began to see signs that we could make good progress through breeding. Although our best estimates showed that it would take about 30 years to match the yield of wheat, we also saw that it would be possible to obtain a crop that farmers could successfully grow and market in much less time.

At this point we encountered one of the less scientific problems with domesticating a new species: the name. “Intermediate wheatgrass” just doesn’t have the ring of any of our current grains’ names—corn, rice, or wheat. So we came up with a name that we hoped would be unique and catchy, and remind people of Kansas. We called this crop-in-the-making kernza.

The Land Institute also decided to give domestication full standing as an approach for obtaining perennial grain crops. DeHaan and a technician were assigned to work on the project, which allowed us the time and attention to develop larger programs and collaborations. This step was critical: We knew that the introduction of a new crop would require a lot more than just breeding and genetics.

2013-05VanTasselF4.jpgClick to Enlarge ImageThe University of Minnesota now has an interdisciplinary project to develop kernza as a perennial grain and to use the residue for biofuels or animal feed. The research team, of which DeHaan is a member, includes researchers from the fields of agronomy, food science, plant breeding, soil science, plant pathology and economics. Plots are established at six sites around the state of Minnesota. Additional plantings in other states and in Canada are helping us evaluate the crop’s performance in diverse environments.

Because kernza is a relative of wheat and other grains, genomic approaches may allow us to transfer the knowledge gained from the study of these crops to the development of this new grain. Rather than transferring genes from wheat to kernza, we are studying the genomes in an effort to identify useful genes from wheat that are already present in kernza, but need only be discovered. We are also hopeful that marker-assisted selection will be helpful in sorting out some of the complexities involved in breeding a species that is both outcrossing—it can’t pollinate itself and thereby doesn’t breed true—and polyploid—having multiple genomes, which can result in complex gene segregation patterns. To these ends, sequencing work is now beginning at several institutions.

2013-05VanTasselF5.jpgClick to Enlarge ImageAll of this work is valuable, but we still believe that domestication comes down to evaluating very large numbers of plants in the field and selecting the best to intermate. This activity requires sustained, long-term commitment. In a conventional plant breeding program, 10 to 15 years may be required from the time a first cross is made to when a variety resulting from that cross is offered to farmers. But when the breeding pipeline is full—when new crosses are made every year—varieties can be released on a regular basis. Everyone from farmers to administrators to plant breeders can be satisfied that there is good evidence of progress. The case for breeding programs that are more experimental and that are not connected to a commercial program is more tenuous: Even if a new domestication program is sustained for a decade, the plants it is developing may not yet have economic value, and any value they have accumulated will be quickly lost if the program is discontinued.

In the case of kernza, we measured 14,000 individuals in the field last year. We intermated the best plants and, based on past experience, we expect that the yield will increase by about another 20 percent. This is a truly amazing rate of progress—but varieties that are usable by farmers remain a goal for the future.

The Nonprofit Niche

2013-05VanTasselF6.jpgClick to Enlarge ImageKernza has now had over two decades of sustained breeding work. This effort would not have been possible without the dedication of two nonprofit organizations and their funders, who were willing to see this work through without a short-term return on their investment. The crop is now being investigated at several universities, a step that occurred only after substantial investment by nonprofits.

To be fair, the process is not completely one-directional, with nonprofits and nongovernmental organizations (NGOs) working on wild material and passing more refined plant material up the line to large research organizations and companies. Some government and intergovernmental agencies have been deliberately set up to facilitate high-risk, long-term work. The best example is the system of national and international germplasm collections. At the Land Institute, we made our own direct collections of native sunflower germplasm, but the Rodale Institute took advantage of the U.S. Department of Agriculture Germplasm Resources Information Network’s excellent collection of Thinopyrum intermedium seeds from central Asia. The National Resource Conservation Service’s Big Flats Plant Materials Center helped preserve and improve the breeding population when the Rodale Institute’s breeding program closed. The Land Institute took on the project from there. The result of all this work was kernza.

Moreover, all the work we do is built upon the body of basic botanical and genetic research produced by the world’s universities since the time of Charles Darwin and Gregor Mendel. New molecular tools developed by universities and life science companies could help us accelerate our work.

It is nevertheless remarkable that young nonprofit organizations should undertake projects that older, much better funded institutions and corporations won’t touch or have abandoned. One explanation for this phenomenon is the tendency for institutions to mature along with the technologies they were founded to develop. The land-grant colleges and state experiment stations of 100 years ago, and the international crop-improvement centers of 50 years ago, probably looked and operated more like today’s agricultural NGOs than modern research universities. The crops they worked with would appear only partially domesticated to our eyes, and their breeders tackled some of the same kinds of challenges faced by those of us doing domestication today.

Some plant breeders express concern that fewer students are being trained in breeding techniques at university and government experiment stations, and that existing programs have increasingly invested in gene- and genome-level research. But perhaps the era of domestication of our traditional crops is over. We may have gotten almost as much yield as possible through reshaping plant form and allocation patterns, and new gains may require precision targeting genes for plant health and grain chemistry. The adjustments that remain possible to make are fine scale; they require techniques capable of identifying more subtle and smaller phenotypes. The institutions devoted to the wheat, rice, maize and soybean economy have changed in parallel with the needs of their client species. The trade-off is that these programs are probably less adapted for working with large, primitive, diverse populations than they were a century ago.

A second difference between mainstream research and nonprofits is that funding for universities and experiment stations increasingly comes from competitive grants. Allocation of funds at this scale becomes dependent on an average of the opinions of numerous bureaucrats, lawmakers, administrators and committees. This is a far cry from the privately wealthy gentlemen of science of the 17th to 19th centuries, some of whom (including Darwin) were able to spend decades developing their theories without having to convince grant reviewers of their ideas’ merit or utility.

Jackson, whose ideas reviewers might have considered heretical or impractical, chose to find the nonprofit equivalent of venture capital to fund the Land Institute’s research, rather than try to meet the expectations of those grant review panels. But individual philanthropists and visionary CEOs present other challenges for research programs: They may have more freedom to support high-risk, high-impact projects than established bureaucracies, but they are also free to change their priorities at any time. Only unceasing education of the donor community and unwavering administrative priorities have allowed Land Institute researchers to maintain such long-term programs.

Even if many of our colleagues in the scientific mainstream who are interested in new crop domestication find themselves constrained by institutional culture and funding issues, we have found that a relatively small amount of domestication can make a species much more amenable to academic research and funding. Simply providing food chemists with quantities of kernza grain and flour made it possible for them to plan experiments. Likewise, making available genetically improved breeding populations reduces the risk and time required for starting a regional breeding program—as is happening in the research program on kernza in Minnesota.

Amber Waves of Sunflowers

Early-stage plant domestication is truly a process of trial and error. We make observations on many candidate species and carry a number of them through several generations of selection. At some point, entire species may have to be culled so we can invest intensely in more promising candidates. Another species that at first seemed less promising may respond to a few cycles of selection in a dramatic way. We have learned that a wild species’ average traits, particularly if measured on plants growing in a natural ecosystem, tells us little about what potential it will have when growing under agricultural conditions—and even less about the potential of rare individuals.

Maximilian sunflower (H. maximiliani) has been our top perennial oilseed candidate for domestication since 2000. Fast growing and widely adapted, this species produces many tiny seeds. But recently a close relative and another subject of our research, Silphium integrifolium, has emerged as another promising plant. In its wild state, Silphium appears to be a poor crop candidate. Its traits are almost the opposite of maximilian sunflower: It establishes slowly, flowering only in its second year. Its seeds are very large for a wild plant, but it produces only 15 to 20 per head in the wild. The flower heads have hundreds of florets, but the vast majority are staminate, producing only pollen rather than developing into seeds. In this genus, the seed-bearing florets are found on the rim of the head, where they produce one very long petal and several tiny ones. Collectively, these inconspicuous florets create the large ring of showy sunflower petals that attracts the attention of bees and painters—and plant breeders. It was those large seeds that kept us from completely disregarding this species.

Was there genetic variation for the number of pistillate florets in Silphium, we wondered? In 2004 we grew thousands of plants and spent days walking through the field counting the number of long petals. That number indicates the maximum number of seeds the head can produce. We found and flagged a few dozen plants with heads bearing more than 25 petals, and we covered the next unopened head on each plant with a cloth bag to keep out pollen carried by butterflies and other insects. We checked these bags every day or two. If a bagged head was shedding pollen, we brushed it off into a small jar. Then we went back through the bagged plants, checking for heads with receptive stigmas and pollinating them with this mixed pollen. (Silphium is self-incompatible, so a plant’s own pollen will not fertilize its ovules.) We collected the resulting seeds and planted them the next year. A year later we repeated the process, this time raising the bar: Only plants with 35 long petals were flagged and bagged. Again and again we repeated this cycle of selection and intermating. In 2012 several plants had heads with more than 100 long petals, and one plant had more than 150.

This is the kind of low-tech, protracted genetic work that could never have been funded through competitive grants. It was a back-burner project even at the Land Institute, and we did not keep careful records of average petal number or calculate heritabilities. We simply tried to find the most extreme plants in the population and intermate them. Recently, we began to feel confident that this trait responded well enough to selection that the number of seeds per head was not likely to impose serious limitations.

This year we estimated yields more carefully. In our unfertilized breeding nursery, the average seed yield in 2012 was 278 pounds per acre, although some plant families did much better. That’s not very impressive compared with the typical yields of 1,500 to 2,000 pounds per acre obtained from commercial annual hybrid cultivars in a nearby experiment at Kansas State University’s South Central Kansas Experiment Field. However, this was not a typical couple of years. Our 2012 Silphium yield compares quite favorably with that of the commercial sunflowers in 2011, 263 pounds per acre, and 2012—0 pounds per acre. During these drought years, Silphium grew normally while native grasses, annual sunflower cultivars and even some perennial grain species showed severe stress and stunting.

Prairie ecologist John Weaver noted in 1935 that S. integrifolium flowered normally in the great drought of 1934, when many other prairie plants turned brown and dormant. He attributed this success to Silphium’s deep roots. Perhaps it will be the next slightly domesticated perennial grain to move up through the crop-development pipeline. Years of somewhat informal breeding seem to have greatly increased the species’ yield potential, although a few cycles of selection for actual yield, not just petal number, are needed to increase the average yields. We have also seen great variation in the amount of seed shattering, although we have not done much selection for that. The oil content of the grains is similar to cultivated sunflower, and Silphium has more protein than its domesticated cousin. Suddenly we find that this candidate, with its large seeds and upright growth form, is more promising than the interspecific perennial–annual hybrids and the maximilian sunflower on which we have spent much more effort.

Once we have a population with reduced shattering and have demonstrated that Silphium can be harvested mechanically at the 5- to 10-acre scale, this candidate should be much more attractive to potential university collaborators around the world. We still need to learn much more about its soil fertility requirements, pathology, ecology and oil chemistry. But its surprise potential illustrates the need for careful research over a broad range of species—even those that may not initially seem that promising.

The Next Grains

2013-05VanTasselF7.jpgClick to Enlarge ImageGrains form the basis of the global food system, and they can relatively easily be processed into liquid fuels. Many new possibilities for crop development can be found in these plants. Perennial grains developed from tropical plants are the most obvious area for further research. We do not know how well the temperate-grassland–adapted species we are working on might perform in the humid or arid tropics, but even if they can be bred for adaptation to those climates, there is a wealth of indigenous vegetation likely to produce better candidates.

Saline environments are even more challenging. More than 4 million square kilometers of cropland are already salinized, and additional land is at risk, mostly as a result of years of irrigation. Although plant breeders are having some success in increasing the salt tolerance of standard crops, others have predicted that strong salt tolerance is genetically complex and that domestication of wild halophytes (salt-loving plants) might be more successful in the long term. At least one halophyte has traditionally been harvested for grain by the Native Americans of the Colorado River delta: Distichlis palmeri.

Woody crops have been traditionally placed in a separate category from grains, but some, like chestnuts and hazelnuts, have food value similar to plants more usually recognized as grains. Breeding for reduced height and threshability might make it possible to harvest these nuts nearly as easily as corn. Any plant with starch-, oil- or protein-rich reproductive structures that can be harvested, transported and processed like a grain is a candidate for investigation.

Most humans will be seed-eaters for the foreseeable future, it seems. Alternatives to seed-based food systems, such as algae or enzymatic conversion of cellulose, have been proposed, but they have received almost no funding. Fortunately, we live on a planet with more than 220,000 species of seed-bearing plants. These species occupy almost every global habitat across a wide span of plant forms and sizes. The crop base of the world’s food system could be dramatically broadened in the next several decades—if other organizations can replicate the conditions Wes Jackson created at the Land Institute, in which projects are given, in his words, “the freedom to fail,” along with sufficient time to prove their potential.

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