The potential for underutilized crops to improve security of food production

Abstract

Staple crops face major challenges in the near future and a diversification away from over-reliance on staples will be important as part of the progress towards the goal of achieving security of food production. Underutilized or neglected crops species are often indigenous ancient crop species which are still used at some level within the local, national or even international communities, but have the potential to contribute further to the mix of food sources than they currently do. The most cost-effective and easily disseminated changes that can be made to a crop are changes to the genetics, as these are contained within the seed itself and, for many species, the seed is a pure breeding, self-replicating, resource. This article focuses on the potential of underutilized crops to contribute to food security and, in particular, whether genetics and breeding can overcome some of the constraints to the enhanced uptake of these species in the future. The focus here is on overview rather than detail and subsequent articles will examine the current evidence base.

Food security: a complex issue

Attempts to increase global food security face a number of complex and interlinking challenges. The need to provide food for (and also actually to feed) nine billion people will require an intensification of farming at one end of the scale, but local issues, such as nutritional and dietary diversity and the loss of traditional diets, will increasingly demand attention if any long-term form of food security is to be achieved. In addition, simply producing enough food is not in itself enough, but that food must be harvested, processed, and distributed and the poor must be in a position to have the purchasing power in order to access that food resource. The effects of the urban poor being priced out of access to available food were seen in the world-wide food riots of 2008.

Neglected or underutilized crops have the potential to play a number of roles in the improvement of food security that include being: (i) part of a focused effort to help the poor for subsistence and income, the majority of whom live in the South; (ii) a way to reduce the risk of over-reliance on very limited numbers of major crops; (iii) a way to increase sustainability of agriculture through a reduction in inputs, such as fossil fuel-derived nitrogen fertilizers and fuel for agriculture, given the risks of the carbon footprint of agriculture on climate change and the transition to a post peak-oil world; (iv) a contribution to food quality; and (v) a way to preserve and celebrate cultural and dietary diversity. All of these aspects cannot be given the coverage that they deserve in a single article. In this article, the focus is on food production and, specifically, the potential of breeding and genetic research to overcome some of the concerns and constraints that arise when dealing with ‘unimproved’ crop species. Other aspects will be addressed in later articles.

Diversification for food security: the role of underutilized crops

The world depends for its basic diet of carbohydrates, fats, and proteins on a very limited number of crop species. For carbohydrates, three related species (wheat, rice, and maize) dominate human consumption (Collins and Hawtin, 1999). Any short-term improvement in food security will need to include modification (either transgenic or through conventional breeding) of these and other staple crops. However, a focus purely on the productivity of current major crops, often selected and developed under high intensity agriculture, cannot meet the challenge of food insecurity and potentially makes agriculture even more vulnerable to future biotic and abiotic stresses.

Underutilized, minor, orphan or neglected crops are labels often applied to plant species that are indigenous, rather than non-native or adapted introductions, and which often form a complex part of the culture and diets of the people who grow them (see Padulosi et al. (2006) for a more detailed discussion about the labels given to such species). The ‘underutilized crops’ label will be used here. There are an estimated 7000 plants which have at some point in human history been used as crop plants (FAO, 1998). Many of these crops still exist as minor or niche crops and, if still cultivated at all, are seen as of ‘low status’ so that, often, it is women who cultivate them for subsistence purposes, while men prefer to cultivate the major cash crops.

So can underutilized crops be part of the solution to providing food security?

Identifying the underutilized crops with potential: a trait-based approach?

Given the vast repository of neglected or underutilized crop species, how can those with enough potential to justify investing the very limited resources available for their improvement best be identified?

One possible strategy is to look for crops with trait values that currently exceed the equivalent trait in major crops, especially where these are evident in hostile environments such as where drought and/or heat stress restrict productivity. While this is not a new idea, it becomes more important under the twin challenges of cultivating crops in uncertain future climates and the need to increase food production with fewer inputs. However, there is also clearly no point in cultivating crop species simply because they can withstand environmental stresses; they also need to have the potential to achieve high value markets due to the characteristics of their products; perhaps the functional starch quality is unique or perhaps the levels or combination of micronutrients makes them a highly valuable addition to human nutrition. However ‘trait’ is defined, whether genetic, agroecological, nutritional or cultural, identifying that limited dozen or so crops which really stand out as having the trait (and associated market) potential to be used at a higher level for improving food security is the first task.

Many crops, however, face bottlenecks to their increased uptake. These may be purely practical, such as limited post-harvest shelf life, or could be related to dietary intake issues, such as anti-nutritional factors, poor taste or unpleasant texture. Many suffer from poorly developed markets and a lack of value-added products which may limit their value for providing the poor with buying power to obtain their staple foods. Some of these aspects may be addressed in the laboratory and in field plots, while others may need advocacy and market development work—in practice, many will need both.

From a breeding perspective, the genetic potential of a crop is determined by the combination of genes it contains, their mutual interactions and interactions with the environment to produce the phenotype, whether that is yield or disease resistance or drought tolerance. Agronomy and management are important tools to favour the crop by generating as optimal an environment as possible. How far agronomy can contribute will be dependent upon what the crop is and where it is being grown, with more resource-intensive agriculture often applied to the major staple crops. Farmers are being asked to reduce the inputs for agriculture (particularly fossil fuel-derived nitrogen and fuel use for machinery) but to intensify farming. Even in the most developed agricultural systems this is difficult to achieve. Developments in precision agriculture for the application of pesticides, fertilizers, and growth regulators may be one way to optimize the crop agronomy further. For many underutilized crops, the agronomy/management may well not have been optimized (if it exists beyond limited irrigation and hand weeding).

The most cost-effective improvements that can be made are in the genetics of the crops. Over the last five years there has been a significant change of pace in crop genomics through the technological development of Next Generation Sequencing (NGS) (Varshney et al., 2009). These technologies have increased our ability to generate sequence data from any species by at least 100-fold, if not more. This allows us to generate significant sequence data so that molecular tools, such as DNA markers, can be produced at reasonable cost in a species where there may have been little or no information. It also allows in-depth comparisons to be made between underutilized crops and their major staple crop cousins. There has been continuous investment in staple crop research driven by both commercial and public sectors. This is often at very high levels and has generated significant data on the genetic control of traits and their interactions with the environment. NGS and other high throughput technologies potentially allow us to import some of that knowledge into underutilized species and test whether it holds true, rather than having to generate data de novo for each species. In this way, there is a shift from working on single species in isolation to working on complexes of species. Using such approaches, it should be possible to identify what the genetic issues (and potentials) of such species are.

This still leaves the question, ‘Is it possible to modify those characters of underutilized crops which are preventing further uptake of a species?’ Clearly, the answer to that will be species- and trait-specific, but one area of research where we might get a clue as to what is possible is to examine our understanding of the domestication of major crops and their subsequent farmer-selected genetic modification to match them to new and different environments.

Developing new crops and improving underutilized crops: what can we learn from achievements in staple crops?

Most staple crops were domesticated millennia ago, with the first wave of domestication taking place independently for different crops on different continents some 8 000–10 000 years before present (Harlan, 1992). In recent years, the molecular basis of domestication has begun to be understood (Doebley et al., 2006; Vaughan et al., 2007) and the term ‘Domestication Syndrome’ was coined to describe a set of common changes present in many domesticated species, compared with their wild ancestors. These often include; a reduction in seed dormancy, altered morphology, and the loss of seed dispersal mechanisms. Domestication Syndrome Factors (DSF) have also been identified which represent the actual genetic changes which have occurred and one major surprise from this work was that the number of DSF can be relatively limited. In maize, most morphological changes needed to produce maize from teosinte, the wild progenitor, are controlled by just five genes (Doebley and Stec, 1991). In wheat, closer to seven DSFs have been identified (Peng et al., 2003). This demonstrates that there are relatively few genetic changes needed to domesticate a wild species into a new potential crop. However, a number of major crops grown today can be seen as essentially undomesticated in a number of traits. The oil palm (Elaeis guineensis Jacq), for example, still naturally abscises fruit from ripe bunches which requires a significant labour cost to collect loose fruit from under palm trees. This contrasts with wheat, where the seed remain on the ear after ripening until they are physically threshed loose.

Molecular evidence also gives clues as to how frequently a species has been domesticated. For wheat, it is probably a number of times, with a complex of wheat species of different ploidy levels co-existing, from which modern hexaploid bread wheat was selected. With maize, the molecular evidence suggests that domestication only occurred in a single location (Matsuoka et al., 2002)

For the majority of the staple crop species, these domestication events are ancient and, since then, a process of adaptation and optimization has occurred. This has allowed the spread of the newly domesticated crop from its centre of origin to new environments (centres of production). For wheat, for example, the second phase of domestication has adapted the crop to certain environments through changes in photoperiod and vernalization requirements, both of which affect the timing of the switch from vegetative to reproductive development. Both requirements (and their interactions) reflect the prevailing environments of the regions where wheat is now grown, rather than from where it originated. Subsequent selection, breeding, and agronomic practices have allowed wheat to produce more stable or greater yields than when it is grown near its centre of domestication. It is noteworthy that no similar processes of adaptation, improvement, and optimization of agronomic management practices have been applied to many of the underutilized crops which, to a large extent, remain imprisoned in their centres of domestication.

The conclusion that can be drawn is that the initial process of crop domestication of the major species, whilst enormously significant, is relatively simple in genetic terms. Indeed, early farmers were certainly no less intelligent than crop breeders today and they were likely to have selected for phenotypically clear traits in their fields, such as a many-branched teosinte crop having a single branched mutation within it. This phenotype is now known to be caused by molecular changes to the gene promoter of the tesointe branched 1 gene (Doebley et al., 1997; Wang et al., 1999). Indeed, until breeders began to understand the principles of genetic analysis in the early 20th century, yield improvements were quite limited. In the last century, the yield of seed from wheat and the yield of oil from oil palm have both quadrupled. Interestingly, this improvement can be attributed roughly equally to management/agronomy and genetic improvement in both crops (Calderini and Slafer, 1998; Corley and Lee, 1992). This argument, when applied to species which are partially domesticated or even undomesticated, indicates that they have the potential to be dramatically improved for yield, based on a strategic mix of improved management/agronomy and selective breeding. Given recent advances in our understanding of the genetic control of agronomic traits in staple crops and the plethora of tools and techniques available for both crop and model species (including rice as a crop and a model) modern breeders should be able to replicate the achievements of the last century on a number of promising underutilized crops in a fraction of the time that it took for the major crops. Using this knowledge and the detailed understanding of gene action which is becoming available in these systems, even developing a new crop from scratch should be feasible.

Perhaps, more importantly, addressing some of the characteristics in current underutilized crops which are acting as a constraint to their wider adoption should certainly be possible within the time-scale required to make a useful contribution to food security. At the same time, optimization of agronomy and management techniques tailored to the crop and location will make a real contribution to yields and quality of the product.

The focus in this article is on the genetics and breeding of underutilized crops, however, the targets for such work must be informed by the markets and end-user requirements if such work is to have any impact. In some species, genetic improvement may be secondary (although breeding for improved tolerance to biotic and abiotic stresses is likely to be desirable) and markets or even the politics of food (much in the same way that ‘food for fuel’ subsidies have distorted food markets) may be the driver for adoption of an underutilized crop. Our contention here is that it is possible to improve underutilized crops significantly through breeding and agronomic research for food security within the time-scales needed. However, is there a collective will and focus to achieve this?

The underutilized crop community: creative tension?

Like most research communities there is a broad range of opinion on how to develop underutilized crops for the benefit of mankind. This is probably more evident than in many other academic communities, because the increasing use of underutilized crops for food security involves overcoming many constraints and obstacles, from genetic through management, cultural acceptability, and marketing, to policy and decision-makers in government. There are good examples of the development of an indigenous crop within its local community where it provides direct benefits to that community through food and often income security, providing the local community with purchasing power. The major crops probably represent the other extreme option, with the use of germplasm from worldwide collections, with crops often grown as monocultures under high intensity agriculture and in the presence of global commodity markets. This contrast between promoting the localism and globalization of different crops is often a source of friction within the underutilized crops community. Some social champions may argue that there is little to be gained from recent developments in genetics and research for underutilized crop species and that it is not experiment and breeding that is needed, but advocacy. They may point to the model plant species that are supposed to inform research in major crops, where there has been a great deal of money spent on fundamental plant research which may never see any impact in the field. This argument has some traction and advocacy of a similar research investment in hitherto underutilized crops is both implausible and counterproductive. However, we would argue that highly focused, applied research to answer questions fundamental to a crop (such as understanding the breeding system, the population structure of germplasm, and for quality control in research and breeding work) is warranted. Work to modify specific quality traits or tackle particular disease issues may also be important, but should not be assumed. Whatever research is done, it must be done as cheaply as possible using whatever tools/information are available from other species. It should have a clear pathway to making an impact and should be means to an end, not an end in itself. The (freely available) crop seed is the most effective way to deliver improvements in both agricultural and end-user traits to farmers of the future. Genetic improvement of seed will be an important part (but only part) of the requirements for underutilized crops to reach their potential.

In a recent article, Foley et al. (2011) argued for a pragmatic approach to increasing food security through decreasing yield gaps, increasing efficiency of resource use, changing diets, and reducing waste. We would argue (and they mention) that underutilized crops can play an essential part of this process, particularly in terms of the resilience of food production systems and matching crops to their above- and below-ground environments. Our brief overview of the process of domestication and the history of increases in yields of staple crops argues that there are underutilized crops which could becomes new minor or even major crops under the new agricultural regime of low inputs which we will have to adapt to in the future. This is not to denigrate the importance of local and niche crops, which can also improve environmental and economic resilience and provide important food and income sources. Our understanding of agricultural systems and the tools that are now available have never been greater. The focused application of these can help to diversify cropping systems, for food and nutritional security.

Making it happen: Crops for the Future

Unlike the limited numbers of major crops which each have at least one research centre with an international mandate for their genetic conservation and improvement, until recently the many underutilized crops of the world have not merited a global centre responsible for their improvement. Crops for the Future (CFF) is a global organization that works with its partners to advocate research, policies, and capacity building on underutilized crops for the diversification of agricultural systems and diets. It was formed in 2008 following a merger between the International Centre for Underutilized Crops (ICUC) and the Global Facilitation Unit for Underutilized Species (GFU). An independent institution, CFF is hosted in Malaysia jointly by Bioversity International of the Consultative Group on International Agricultural Research (CGIAR) and the University of Nottingham Malaysian Campus (UNMC). Bioversity International brings extensive research and advocacy expertise and outreach, while UNMC brings specific crop research expertise.

In addition, Crops for the Future Research Centre (CFFRC), a research arm of CFF being built adjacent to UNMC is the first-of-its-kind, with a global mandate for research and development of underutilized plants for food and non-food uses. In a unique public/private partnership, CFFRC is guaranteed by the Government of Malaysia and the University of Nottingham but has the freedom to drive innovative research on novel crops within the objectives of CFF and its stakeholders. The centre will allow the systematic evaluation of a series of crops with potential for wider use and develop those which could make a useful contribution to food security as well as non-food uses, such as fibres for textiles or construction.

The establishment of CFF and CFFRC helps focus efforts for diversification of the plant species that humans exploit. Shifting away from our over-dependence on a limited number of crop species is crucial. If climate change and other pressures on food production, such as pests and diseases, lead to the catastrophic and long-term failure of a major crop in some parts of the world, it is important to have other options.

Underutilized crops: integrating disciplines to achieve results

The potential challenge of trying to provide food security in the future should not be underestimated. While the exact effects of climate change combined with population growth are not known, it seems highly likely that agriculture in large regions of the world may need to undergo significant adjustment over the next four decades for us to have any chance of meeting needs. Nor should the uncertainty regarding the effects of climate change be used as an excuse to prevaricate—we need to prepare for the worst, while hoping for the best. Even if the worst predicted effects of climate change do not materialize, we will at least have made world-wide farming and food supply more sustainable.

The need is for an integrated effort across all levels which affect food security, from basic genetics through to the politics of aid and trade. Without such an approach, largely successful efforts may still fail to achieve practical results because of a single flaw in the chain. It is also important to see underutilized crops as part of a food mix for a particular region, rather than as ‘stand-alone’ crops and using combinations of underutilized crops as additions to the existing staples could help make nutritional and food security more of an achievable goal.

This paper has been an overview of the potential of genetics and breeding to address one aspect of the challenge that faces us if we want to diversify crops and increase the contribution that underutilized crops can make to food security. Domestication and adaptation of many major crops species has been driven by a limited number of changes at the genetic level. With the advent of high throughput genomics, particularly NGS, focused projects tackling specific issues or traits limiting further uptake of underutilized crops can make a genuine difference. Classical breeding programmes in the past have been very successful in increasing yields in staple crops, with a 4-fold-increase having occurred in at least two contrasting crops (wheat and oil palm) over the last century, so the current low yields of underutilized crops should not be assumed to be close to the maximum achievable. However, our current model of increasing yields while reducing inputs is more challenging than the paradigm used in previous breeding work.

If suitable crops with exceptional traits with market or end-user potential can be identified, genetics and breeding can help to resolve some of the current issues which are preventing the more extensive use of that species, but it must be a focused effort and is likely to be enabling, rather than transformative.

Underutilized crops have great potential to alleviate hunger directly, through increasing food production in challenging environments where major crops are severely limited, through nutritional enhancement to diets focused on staples, and through providing the poor with purchasing power, helping them buy the food that is available. Crops for the Future will complement CGIAR centres, which tackle issues relating to major crops. For the first time, underutilized crops have their own body to assist their research and development for greater food security.