7. Genetic Resources and Genetic Diversity
Centers of Origin
by Lisa Baxter, Department of Crop and Soil Sciences, University of Georgia
There are many adjectives used throughout the literature describing the accomplishments and expeditions of Nikolai Vavilov. However, words cannot describe the legacy that Vavilov left or how instrumental his work has been to modern plant breeding. Vavilov dedicated most of his life to the collection of plant germplasm resources (Figure 1). He organized more than one hundred expeditions to economically important plant regions around the world in an effort to resolve famine in Russia (N.I. Vavilov Research Institute of Plant Industry, 2013; John Innes Centre, 2013). Through these missions he collected 250,000 samples that not only served as the foundation for his research but also saved his country from starvation after the collectivization which brought famine to Russia (Markova, 2013). Even today plant breeders rely on the unexploited genetic resources found in plant germplasm banks to improve efficiency and yield of crop production. Five Continents shares the details of Vavilov’s explorations but a summary is provided in Table 1 (Vavilov, 1997; N.I. Vavilov Research Institute of Plant Industry, 2013).
By 1934 a network of more than 400 research institutes and experiment stations had been established across Russia to sow the collections over the widest possible geographical range and continue Vavilov’s revolutionary research (John Innes Centre, 2013; Cohen, 1991). While Vavilov was a very prolific writer, composing over 300 articles and ten books, his most notable works include Plant Immunity to Infectious Diseases (1917), Law of Homologous Series in Variation (1920), and Centers of Origin of Cultivated Plants (1926) (N.I. Vavilov Research Institute of Plant Industry, 2013; John Innes Centre, 2013; Markova, 2013).
However, Vavilov’s work was not approved by all. Russia was in a Totalitarian state and Vavilov’s innovative theories on genetics conflicted with the traditional selection theories of Trofim Lysenko (N.I. Vavilov Research Institute of Plant Industry, 2013; Markova, 2013). Consequently, Vavilov’s research programs were deprived of support from the government thus restricting his travels (N.I. Vavilov Research Institute of Plant Industry, 2013). This disagreement also made travel outside of the country’s borders for genetic symposiums and academic endeavors more difficult (Cohen, 1991; Markova, 2013). The unrelenting controversy resulted in Vavilov’s arrest on August 6th, 1940 on the charge of “wrecking Soviet agriculture” (N.I. Vavilov Research Institute of Plant Industry, 2013; John Innes Centre, 2013; Markova, 2013). Despite his imprisonment where he was interrogated and tortured, Vavilov continued his work (Markova, 2013). He completed a book and multiple essays while in prison before his untimely death due to starvation in January 1943 (N.I. Vavilov Research Institute of Plant Industry, 2013; Markova, 2013).
Fortunately, Vavilov’s legacy did not end with his life. The germplasm collection created from Vavilov’s expeditions again saved Russia from starvation after the Great Patriotic War (June 1941 to May 1945; Markova, 2013). His colleagues recognized the significance of the collection to the rehabilitation of Russian agriculture and unselfishly gave their lives protecting this invaluable resource (Markova, 2013). Vavilov’s work also paved the way for modern biology and provided groundwork upon which the Green Revolution could emerge. His students and followers continued research to strengthen his theories and concepts (N.I. Vavilov Research Institute of Plant Industry, 2013). For instance, P.M. Zhukovsky continued to define centers of origin by adding microcenters to the map (Zhukovsky, 1975). Vavilov’s collection is estimated to be valued at 8 trillion dollars (Markova, 2013), yet many would likely debate that Vavilov’s work is priceless since his work is still very relevant and important to science today (Kulikov, 2012).
Centers for Origin
As the world population continues to increase plant breeders are looking to wild germplasm as new genetic resources. Identifying centers of origin will hopefully expand growing zones for economically important crops, overcome factors currently limiting yield, and better utilize wild germplasm sources as a solution for crop adaptation to global climate change (Abbo et al., 2010). Gepts (2001) acknowledged the significant untapped genetic potential in wild germplasm yet warned that these resources are in jeopardy due to “genetic bottlenecks” caused by domestication, movement out of the center of origin, and modern plant breeding objectives.
Since the early 1900’s many researchers have made efforts to identify and more recently, refine centers of origin for various plant species. A center of origin represents a geographical region where the early progenitors of a domesticated species may be found. Each approached the matter with different objectives and with surprisingly unique, and occasionally, opposing views. The works of Alphonse de Candolle and Nikolai Vavilov are most commonly associated with this topic but several others have contributed to the identification of centers of origin.
Alphonse de Candolle first published his findings in Origin of Cultivated Plants in 1892. It was primarily botanical evidence that led de Candolle to establish three primary domestication regions (Figure 2): China, Southwest Asia and Egypt, and tropical America (de Candolle, 1959; Smith, 1968). Although areas of diverse and unrefined plant growth suggested the center of origin for the species, de Candolle warned that abundance of plant material did not confirm the plant’s natural habitat (de Candolle, 1959; Smith, 1968). Even though de Candolle’s results have since been referenced in many articles concerning searches for new germplasm sources, Smith (1969) considered his work to be a “mental exercise” as opposed to a search for genetic resources. Nevertheless, it is argued that de Candolle’s work more accurately defined centers of origin than the work of other researchers (Harlan, 1971).
Nikolai Vavilov is considered to be a pioneer in his field and defining centers of origin (Leppik, 1969). Vavilov is known for his extensive travels and expeditions to collect germplasm resources from around the globe. Using the materials he collected, eight geographical centers of origin for economically important crop species were defined (Figure 3) (Heiser, 1975; Smith, 1968; Smith, 1969). Unlike many others, Vavilov drew centers of origin around areas where the largest number of species had been discovered. A concise summary of the criteria Vavilov used to determine a center may be found in Smith (1968) but essentially diversity of species was the leading determinant in where lines were drawn. Smith (1969) concluded that Vavilov’s centers of origin coincide with those of the wild progenitors rather than the center of the cultivated crop. Heiser (1975) did acknowledge that Vavilov revised the centers as new knowledge emerged. Vavilov’s work was continued by his student, P.M. Zhukovsky, after his untimely death (Leppik, 1969; Harlan, 1971). Zhukovsky (1975) amended the centers determined by Vavilov and added microcenters. Evolution of plant species can create variation to drive the emergence of microcenters (Harlan, 1971).
E.D. Merrill (1938) looked briefly into identifying crop origins in the 1930’s. He wrote that several crops including tomatoes and peppers are of American origin while many species now common in the United States such as cereals are Eurasian in origin. However, his work was more focused on disputing long-standing theories instead of characterizing crop origins (Smith, 1969). While the results have not been conclusively demonstrated, Sauer’s (1952) research led him to place the center for root crops in the northwestern part of South America and the origin of seed planting in Mexico (Smith, 1969). Leppik (1959) considered a new approach by incorporating resistance to fungal diseases. He demonstrated that most resistance in a species is found at its center (Leppik, 1959). Smith (1968) recognized Anderson’s (1952) work to be influential in the development of techniques used for classifying plant materials. Anderson’s findings were similar to those of de Candolle (Smith, 1968).
Jack Harlan’s (1971) review shows that plant species generally have a center of origin which differs from the center of diversity. Dvorak (2011) has discovered that as centers of diversity emerge they appear to parallel the evolution of the progenitor rather than the center of origin for the cultivated crop. For instance, the domestication of emmer and barley have been influenced by gene flow which has thus changed the diversity patterns that were recognized at domestication (Dvorak, 2011). Changes modifying the centers of diversity are likely when a crop, such as emmer or barley, evolved from a smaller, more definite population of the progenitor (Dvorak, 2011). Even though two centers appear to exist, they are both still important to plant breeders (Heiser, 1975). It could be argued that two centers are better than one as the plant breeders would have two sources of untapped genetic potential compared to only one. While the idea of a “center” of origin is a more attractive delineation to many researchers, not all plant species may have originated from an area that could realistically be defined as a center (Halran, 1971; Smith, 1968). Consequently, Harlan (1971) generated the idea of a non-center. The non-centers are not necessarily independent of the center as interactions have been documented between the two (Harlan, 1971). For example, Harlan (1971) named a center in the Near East which corresponds to a non-center in Africa, a center in China with a non-center in Southeast Asia and the South Pacific, and a Mesoamerican center paralleled by a South American non-center. General conclusions from Harlan’s (1971) research were that centers tend to be linked to temperate regions of the globe while non-centers correlate to tropical areas. These differences may be due to the fact that agriculture in temperate regions is predominantly seed agriculture while tropical regions have agriculture driven roots and trees (Harlan, 1971). It may also be a consequence of the technologies available to the researchers because until recent years archeological data has been of little use (Smith, 1969).
Archeological plant remains can help isolate sites of origin (Smith, 1965). Smith (1969) pointed out that crops may have been brought under domestication in several areas thus making the process of identifying an exact point of origin more difficult. Weiss et al. (2006) have added that early pre-domestication efforts may have been abandoned. This would likely contribute to the difficulty of narrowing down the center. Plant remains recovered during archeological excavations could help researchers answer many lingering questions. Unfortunately plant remains are not always preserved in ideal conditions because of precipitation patterns (Smith, 1969). With that said, archeological remains will be very beneficial to research in more arid climates, such as the Southwestern United States, but will provide little relevant information to research conducted in tropical Central America (Smith, 1965). Another obstacle is that entire plants are rarely uncovered (Smith, 1965). Differences in harvest, preparation, and cooking methods can make analysis of the remains more challenging (Smith, 1968). Fortunately, many of the foods sold in native markets are “surprisingly local” and can be used to check and compare the results generated in the analysis of archeological data (Smith, 1965).
Advances in microscopic techniques and molecular genetics are very promising to this field of research and will help refine the large centers (Smith, 1965; 1969). Abbo et al. (2010) discussed developments of computer simulations, archeobotany, and allozyme DNA polymorphism that are being used to confirm or contradict previously proposed centers of origin. A considerable amount of research has been conducted in the Near East for the determination of einkorn wheat, emmer wheat, and barley origin. Therefore, this will be used as an example for modern determination of a center of origin. It has been proposed that agriculture began in the “cradle of agriculture”, more commonly known as the Fertile Crescent, because the wild progenitors of the seven founder crops (lentil, chickpea, pea, barely, einkorn wheat, emmer wheat, and bitter vetch) are found to overlap in this region (Lev-Yaden et al., 2000). Archeological and archeobotanical evidence has enabled researchers to reconstruct temporal and spatial aspects of plant domestication (Abbo et al., 2010). Carbon-14 dating of the archeobotanical evidence in addition to cultural markers has isolated the areas of domestication to the Fertile Crescent (Abbo et al., 2010).
Research was also conducted to determine if domestication was localized or more diffuse (Abbo et al., 2010; Zohary, 1999). There are two phylogenic pathways in which a crop may evolve: monophyletic and polyphyletic (Abbo et al., 2010). Monophyletic crops were generated from a single domestication event whereas polyphyletic are the product of multiple genetically-independent events (Abbo et al., 2010). Zohary (1999) concluded that Near Eastern crops were of monophyletic origin because of their uniformity. The uniformity indicates that traits are controlled by the same major gene, as opposed to non-allelic mutations, which suggests a single genetic event was responsible for domestication (Zohary, 1999). Research has confirmed that einkorn wheat, emmer wheat, and barley are all of monophyletic origin (Heun et al., 1997; Luo et al., 2007; Badr et al., 2000). Amplified Fragment Length Polymorphism (AFLP) fingerprinting was used to place the site of einkorn wheat domestication in the Karacadag Mountains in Southeastern Turkey and barley domestication in Israel and Jordan (Heun et al., 1997; Badr et al, 2000). Emmer wheat was determined to originate from the Diyarbakir region in Southeastern Turkey based on Restricted Length Fragment Polymorphism (RFLP) results (Luo et al., 2007). It has been argued that AFLP genotyping cannot accurately distinguish between wild and sister populations of wheat and barley (Allaby and Brown 2003). However, more recent research has shown the research was valid since the domesticated forms were proven to be a product of monophyletic events and there are still wild types growing in the sites of origin determined by the AFLP and RFLP results (Salamini, 2004).
Gene Pool Concept
While taxonomy is useful for the classification of organisms, the arrangement is not always useful to those actually working with the plants. The over-classification by taxonomists and generation of unique systems by individual researchers created confusion when trying to conceptualize plant gene pools (Harlan and de Wet, 1971). It was evident that a more flexible and dynamic method was necessary.
The first widely accepted gene pool model was described by Harlan and de Wet in the early 1970’s. The goal of their model was to obtain genetic perspective in plant species to understand how genes could flow between them (Harlan and de Wet, 1971). Each crop possessed its own unique model and its dynamic nature allowed for flexibility to accommodate changes as new specimens were identified and new technologies were created to generate new species that would not have otherwise been possible. Harlan and de Wet’s proposed model consisted of a series of three gene pools (Figure 4). At the time of publication three gene pools were not recognized for all crops such as soybeans (Glycine max) (Harlan and de Wet, 1971).
Species placed in the primary gene pool (GP-1) may be easily crossed and produce hybrids that are fertile since chromosomes should pair properly and genes segregate normally (Harlan and de Wet, 1971). Genes flow easily within the primary gene pool but since selection of cultivated plant species has led to unique variation they also suggested that GP-1 be subdivided into two subspecies (Harlan and de Wet, 1971). Cultivated races belong to subspecies A while wild types growing spontaneously fall into subspecies B (Harlan and de Wet, 1971). Table 2 outlines further classification within the subspecies but it should be highlighted that both subspecies contain race and subrace distinctions. Race and subrace should be comprehensive so that they allow for variation yet refined to discouraged over-classification (Harlan and de Wet, 1971). Whereas distinctions in species are generally quite clear, race may be more difficult. Harlan and de Wet (1971) define races to have a “distinct cohesion of morphology, geographical distribution, ecological adaptation and frequently of breeding behavior” while subrace is simply a “convenient division of race” to be used when drastic variation is documented.
The secondary gene pool (GP-2) includes those that have potential to cross but the progeny will likely result in hybrids that are weak since chromosomes may pair poorly if at all (Harlan and de Wet, 1971). Success of gene transfer depends on barriers respective to each crop species (Harland and de Wet, 1971). Even though crossing between species in GP-2 is somewhat of a challenge, it is an option for plant breeders to consider when increasing variation in a population (Harlan and de Wet, 1971). Harlan and de Wet (1971) also warned that it may be difficult to recover a specific genotype in later generations. Plants assigned to the tertiary gene pool (GP-3) may be crossed using novel gene transfer techniques (Harlan and de Wet, 1971). Unfortunately the hybrids are usually sterile, lethal, and/or anomalous (Harlan and de Wet, 1971). The research conducted at this level has tested the boundaries of conceptualized gene pools. The Harlan and de Wet model was first described in a time where few worked at this level so GP-3 was somewhat nebulous (Harlan and de Wet, 1971).
There have been a few arguments for modifications to the gene pool model since it was first described. Smartt (1984) argued that the tertiary gene pool should be subdivided in two sections: A and B (Figure 5). Section A would include taxa which can cross fertilize the cultigen and produce a viable, although sterile, hybrid (Smartt, 1984). Conversely, section B would include those which do not produce a viable hybrid (Smartt, 1984). Another modification that has been suggested is the addition of a fourth gene pool (GP-4) to accommodate genetically engineered plants. It was first recommended by Hammer (1998), but Gladis and Hammer (2002) later concluded that GE crops should fall into GP-3 and that GP-4 should be reserved for synthetic crops with nucleic acids that are not normally found in nature. The most recent gene pool model seen in literature today was adapted from Gepts and Papa (2003) where GE crops belong to GP-4 (Figure 6).
With the advancement in genetic and molecular technologies, changes in gene pools are becoming more apparent. To exemplify this, let’s look to soybeans. Harlan and de Wet (1971) only assigned a primary gene pool to soybeans (Figure 7). Recent evidence suggests the addition of a secondary and tertiary gene pool (Newell and Hymowitz, 1982; Hadley and Hymowitz, 1973) (Figure 8). While not explicitly found in literature, there are GE soybeans available today which would fall under GP-4, which is the Gepts and Papa (2003) model used.
The Genetic Vulnerability of Food Crops
by Eric Elsner; Institution of Plant Breeding, Genetics and Genomics, University of Georgia
The genetic vulnerability of food crops can be defined as the susceptibility of food crops to catastrophic losses from pests or pathogens due to the narrowing of their genetic base. One of the most frequently accused culprits responsible for the genetic vulnerability of the world’s food crops is the science of modern plant breeding. Other possible causes of genetic vulnerability include the loss of traditional agricultural lands caused by development, political instability, etc… This review will focus primarily on the genetic vulnerability of food crops as viewed from a plant breeding standpoint. According to Poehlman and Sleper (1995), “Plant Breeding is the art and science of improving the heredity of plants for the benefit of mankind.” As we examine the genetic vulnerability of the world’s food crops, we will discuss what is currently being done to address the issue and assess the status of the world’s plant genetic resources.
Before modern plant breeding is vilified as an evil that is quickly destroying plant genetic resources, it is important that two very important points are made. First, one must realize that the world’s population cannot be fed effectively using landrace or wild type plants alone. The science of modern plant breeding, including genetically modified organisms (GMOs) has allowed farmers to feed the world’s population except in cases of extreme climatic occurrences or political strife. Second, it is unclear how much responsibility modern plant breeding should shoulder for a reduction in the genetic variability of food crops. A review of the available literature on the subject will not lead to a clear answer. For example, Fu et al., (2005) reported that obvious genetic shift and allelic reduction was observed in cultivars of Canadian hard red spring wheat released over a span of 59 years from 1845 to 2004 and that these shifts coincided with six distinct breeding efforts that were undertaken. Christiansen et al., (2002) reported an increase in the genetic diversity of 75 Nordic spring wheat cultivars during the period ranging from 1900 – 1940. However, they further identify a loss of diversity in the same 75 cultivars occurring from 1940-1960 and another increase in diversity from 1960-2000. Lastly, Donini et al., (2000) investigated the genetic diversity of the dominant winter wheat varieties utilized in the UK from 1934-1994 and found little evidence pointing towards a significant narrowing of genetic diversity in the cultivars studied. They indicated that breeding resulted in a qualitative rather than quantitative shift in diversity (Donini et al., 2000). From these examples it is clear that when viewed from the perspective of the plant breeder, the issue of declining crop genetic diversity is by no means clear cut but must be an important consideration in order to protect the world’s food supply.
A Hint of A Problem
For at least the last 10,000 years humans have been selecting plants that performed better for them across a wide range of criteria including fruit size, number of fruit per plant, adaptation to specific environments, resistance to certain pests, and many other characteristics. It is reasonable to assume that thousands of plants were utilized and therefore a tremendous range of genetic diversity existed. Even as late as the middle of the 20th century, approximately 30,000 different cultivars of rice were grown in India (Kotschi, 2010). Mankind has shifted from relying on many species rich in genetic diversity to the place where we find ourselves today; with approximately 150 species in cultivation and 60% of the world’s food production coming from three species: rice, maize, and wheat (Kotschi, 2010). Simply put, fewer and fewer species are being used to feed an ever expanding population and the cultivars are becoming more genetically uniform (Harlan, 1975).
One may speculate that the current interest in the genetic diversity and vulnerability of crop plants was brought about by the United States’ experience with corn leaf blight in 1969 – 1970 (Brown, 1983). During 1970, a previously unknown race of Helminthosporium maydis destroyed approximately 15% of the U.S. corn crop. This widespread destruction was due to the disease susceptibility of the T cytoplasm used by a majority of the hybrid corn seed companies during this time (Brown, 1983). Following this outbreak, the National Academy of Sciences commissioned a survey that resulted in a statement of the genetic vulnerability of food crops. From the survey, it became evident that the genetic base of every major crop grown in the United States was very narrow. For example, in 1975, the U.S. soybean industry could trace its heritage to 6 introductions from the same region in China (Harlan, 1975).
How and Why Breeding Can Cause Vulnerability
Plant breeding by definition is the selection of superior genotypes and/or phenotypes over a period of time. This selection naturally results in a narrowing of the genetic base of the plant in question. Even if the breeder has introduced alleles from wild types or landraces to his target crop, he/she must then begin the process of “weeding out” the alleles that are undesirable. This weeding out of undesirable alleles is once again narrowing the genetic base of the line. If a breeder is working with a species that has previously been a target of breeding research, the breeding materials will likely be elite varieties that are currently in use (Brown, 1983). A breeder typically intermates the best varieties available and selects superior progeny from the mating. The continual use of the best varieties as parents naturally narrows the gene pool to only those alleles that are available from the elite parents and therefore tends to decrease the genetic variation of the population (Brown, 1983). It is not hard to understand the breeder’s reasons for following this path. Farming is a business and a farmer needs to produce maximum yield for the least amount of input in order to run a profitable business. In order to attain this goal and be able to farm for multiple years, farmers must have access to crops that have favorable qualitative traits such as disease or pest resistance and favorable quantitative traits such as high yield, resistance to environmental stresses, favorable grain moisture at harvest, favorable test weight, and a crop that matures uniformly in order to allow for mechanical harvest (Khoury et al., 2010). In response to this need, plant breeders work to produce high yielding, elite cultivars that are tailored to the farmer’s needs.
Modern plant breeding is a business as well and Gepts and Hancock (2006), report that approximately 75% of plant breeders are employed by private industry. Multi-national seed companies employ thousands of breeders who are tasked with creating new and improved varieties on an almost yearly basis in order for their parent companies to compete for market share and to please company shareholders. In the private sector, each company is in a race of sorts with its competitors to introduce improved varieties to the marketplace in order to compete for market share. Essentially the same is true in the public sector where funding for many plant breeding projects is received from outside sources and progress towards improved cultivars via genetic gain is expected in order for continued funding to occur.
Given the time constraints often placed on breeders, and when we take into account that a typical breeding cycle for many agronomic crops may take up to seven to ten years from cross to cultivar, it is not hard to understand why breeders rely on elite lines for their parental stock. For instance, if a corn breeder in the mid-western United States would like to develop a cultivar with resistance to a certain pathogen, the logical step would be for the breeder to take an existing elite line that already contains a suite of traits that are adapted to the mid-west and introgress resistance for the pathogen of interest into the elite line. This method would be much more efficient and streamlined as opposed to starting with a wild-type or landrace with a broader genetic base and breeding for the suite of traits that already exist in the elite line. In most instances, the elite lines will already contain most of the desired alleles and it is only necessary for the breeder to introgress a few specific alleles into the elite line or to further the breeding program of the elite line and make further phenotypic selections. Elite lines are the product of extensive research from both private and public funds. To expect a breeder to ignore these lines is to expect that breeder to not use all of the tools at his/her disposal.
Towards Decreasing Vulnerability
If it is logical to assume that the plant breeder can increase genetic vulnerability by decreasing genetic variability then that same breeder can also reverse the trend and decrease genetic vulnerability by increasing genetic variability. One method used by breeders to increase the genetic variability of crop plants is to use crop wild relatives (CWR). Crop wild relatives have been enormously useful to plant breeders and to modern agriculture by allowing breeders to tap into a broad pool of genetic diversity (Hajjar and Hodgkin, 2007). Generally speaking, wild relatives have poor agronomic performance and are not typically used as the foundation for any breeding program (Hajjar and Hodgkin, 2007). However, plant breeders have had significant success using the CWR of modern crops to introgress favorable alleles into elite lines with the most common use being using CWR as a source of disease and pest resistance (Hajjar and Hodgkin, 2007). Hajjar and Hodgkin (2007) conducted a survey of the introduction of genes from CWR into cultivars of crops of major importance to the world food supply. The crops surveyed were: rice, wheat, maize, barley, sorghum, millet, cassava, potato, chickpea, cowpea, lentil, soybean, bean, pigeon pea, banana, tomato, sunflower, lettuce, and peanut (Hajjar and Hodgkin, 2007). Examples of wild genes being included in a released cultivar were found in every crop surveyed with the exception of soybean, pigeon pea, sorghum, and lentil with over 60 wild species identified as having been used to derive over 100 beneficial traits (Hajjar and Hodgkin, 2007). Current examples of CWR genes being used in cultivars include genes that convey resistance to leaf and stem rust, powdery mildew, and wheat streak mosaic virus in wheat, and resistance in sunflower to imidazolinone and sulfonylurea chemicals resulting in cultivated hybrids sold under the “Clearfield” trade name (Hajjar and Hodgkin, 2007). In 2010, three soybean plant introductions were found to have unique resistance to peanut root-knot nematode and it is hoped that these plant introductions can be used to improve the current resistance levels in elite lines (Yates et al., 2010).
Typically, a breeder identifies a trait that he/she would like to introgress into an elite line and then screens available germplasm for the trait of interest and selects potential parents based on the phenotype of the CWR. This type of system works well for traits controlled by one or a few genes with disease resistance being an important example. For traits controlled by multiple alleles, the situation is more complex. Breeders who are using CWRs as donors of favorable alleles contributing to quantitative traits such as yield or stress tolerance are almost certainly leaving behind some desirable alleles if they select parents based purely on phenotype. Recent advances in genomics and genome mapping are allowing breeders to shift from selection based solely on phenotype to selection based on the presence of useful genes (genotypic selection) (Tanksley and McCouch, 1997). One would assume that a high yielding parent would contain most of the genes for high yield and that a low yielding parent would not make a substantial contribution to the yield of the progeny of a cross. However, when molecular markers are used to identify loci controlling yield for a population derived from this type of cross, the results are contrary to what is expected. DeVicente and Tanksley (1993) found that while most of the “high yield contribution” comes from the high yielding parent, there are almost always some loci with alleles contributed by the inferior parent. One implication of this discovery is that assessing the breeding value of an accession based solely on its phenotype is likely to be misleading when one is dealing with quantitative traits and that potential parents should be evaluated using molecular markers and quantitative trait loci (QTL) analysis to identify useful genes/loci (Tanksley and McCouch, 1997). Tanksley and McCouch (1997) further report that using this technique and a breeding technique referred to as the advanced backcross QTL method in tomato led to the creation of lines that contain specific loci from the wild species Lycopersicon hirsutum and that these lines outperform the original elite cultivar by 48% when grown in different environments around the world. It is clear that the technology exists to confer alleles from CWR into modern elite lines either through phenotypic or genotypic selection. The obvious conclusion is that genetic diversity is important and plant breeders must have access to CWR in order to introduce new genes and characteristics into new cultivars. Therefore it is important to briefly review the state of the world’s plant genetic resources.
Conservation of Plant Genetic Resources
More than 70 years ago, Vavilov noted the important role that crop relatives play as a source of genes (Vavilov, 1940). The two means of plant genetic resource conservation are in gene banks (ex situ) and in nature (in situ) with ex situ being vitally important for breeders who need ready access to germplasm (Cohen et al., 1991). In situ conservation of genetic resources on a global scale seems to be increasing with the number of protected areas in the world increasing from 56,000 in 1996 to 70,000 in 2007 with an increase in total area from 13 million to 17.5 million km2 (FAO, 2009). In 2009, there were more than 1,750 gene banks around the world with at least 130 of these holding more than 10,000 accessions each (FAO, 2009). Approximately 1.4 million accessions have been added worldwide since 1996 bringing the total number of accessions held to approximately 7.4 million with roughly 30% of these holdings being unique (FAO, 2009). One of the largest ex situ collections is the United States National Plant Germplasm System (US NPGS) which currently holds approximately 450,000 accessions of 10,000 species of the 85 most commonly grown crops (Smale and Day-Rubenstein, 2002). In 1997, the United States dedicated approximately $20 million to germplasm acquisition and preservation (Tanksley and McCouch, 1997). These data are encouraging for the long term as they speak to the world’s growing commitment to conserve plant genetic resources in both in situ and ex situ situations. The plant breeding community is moving in the right direction with respect to plant genetic resource conservation but more work remains. As always, regional and world politics continue to play a role in how resources are collected and shared and, as reported by the Global Crop Diversity Trust, a major constraint affecting resource conservation is the availability of the resources needed for the collection, storage, and regeneration of germplasm (Khoury et al., 2010).
In this review, we have discussed the genetic vulnerability of food crops through the lenses of the plant breeder. The plant breeder plays an important role in determining the level of genetic variability that is contained in our food crops. It is clear that by using traditional techniques and cutting edge genomics, plant breeders have the ability to and are currently introgressing wild-type genes and loci into today’s elite cultivars thereby potentially decreasing the vulnerability of some of our food crops. It seems equally clear from the available literature that efforts have been and are continuing to be made to protect the world’s crop plant diversity both in ex situ and in situ settings. As with every other topic of any importance, there are those who would have the reader believe that the situation is dire and possibly hopeless along with those who would say that there is nothing at all to worry about. As is usually the case, the answer lies somewhere in the middle and the case of the genetic vulnerability of food crops is no different. The genetic vulnerability of our food crops is an issue that we must continue to take seriously. We must take steps to minimize the potential impact of a narrow genetic base for our crops and this author believes that we are currently taking those steps.
Germplasm Utilization in Plant Breeding
Ownership of Plant Genetic Resources and The Effects of Ownership Rights on Plant Breeding
by Emily C. Pierce, Institution of Plant Breeding, Genetics and Genomics, University of Georgia
As the demand for agricultural productivity continues to rise, there is an increasing pressure on plant breeders to develop new varieties that are higher yielding and able to produce in more challenging environments. The world is not only facing rapid population growth, but also a dwindling supply of water and arable land. It is the responsibility of plant breeders to develop cultivars that are capable of higher yields with limited resources. In order to do this, breeders rely on plant genetic resources to introduce desirable traits (Smale and Day-Rubenstein, 2002). Plant genetic resources are the functional units of heredity found in plants that are actually or potentially valuable (Fowler, 2001). These resources include wild relatives and landraces as well as commercial varieties that can serve as the platform for further improvement (Le Buanec, 2005). Without these plant genetic resources, breeders would struggle to find sources of new traits. Because environmental and biological challenges are constantly evolving, breeders cannot predict what resources they might require in order to meet the needs of the future. Therefore, it is important that a diverse collection of plant genetic resources is well preserved, and that these resources remain accessible to breeders (Smale and Day-Rubenstein, 2002).
Although plant genetic resources were traditionally regarded as being the common heritage of mankind, there has been a shift towards awarding property rights to these resources and restricting their availability. There is a possibility that such restriction could hinder the efforts of plant breeders. However, property rights can help to stimulate interest and innovation in plant breeding due to monetary incentives. How society decides to deal with the complex issues surrounding ownership of plant genetic resources will strongly influence how plant breeding is carried out in the future.
The Need For Exchange of Plant Genetic Resources
The open use of agricultural genetic resources has historically played an important role in breeding to create plants with a diverse range of desirable characteristics (Roa-Rodríguez and Van Dooren, 2008). The genetic variation that breeders need to introduce these characteristics is often available only through the exchange of plant genetic resources. This exchange is necessary because some areas of the world, especially the centers of origin for crop species, have richer resources of genetic diversity. These resources have thus frequently moved between countries (Falcon and Fowler, 2002).
Crop genetic resources are a combination of the efforts of many people over many years, and thus in the past these resources have been exchanged as part of a common heritage that belongs to the public rather than to any single person or group. The concept of common heritage is a logical consequence of the inherent nature of plant genetic resources, which are easily transported and reproduced (Brush, 2007). This relatively unrestricted transfer of diverse genetic materials has allowed crops that are major food sources worldwide to travel far from their origins. The majority of crops that some countries now rely on are not indigenous crops, but have been introduced by this free exchange (Falcon and Fowler, 2002). Free exchange of plant genetic resources has therefore played an important role in supplying food for the world in the past, and this need is only increasing. Research has also shown that crop breeding programs in developing countries, where much of the increased food need is concentrated, are especially dependent on international germplasm exchange programs (Brush, 2007). Not only do plant breeders need a wide base of genetic resources to meet the world’s needs, but individual farmers also rely on these resources to ensure their own food security (Cooper, 2002).
Plant genetic resources have also become increasingly important as informational goods rather than as tangible goods. Although tangible plant genetic resources such as seeds have been important in the past, the genetic information that codes for the inheritance of certain traits is now of greater importance to plant breeders. These informational resources are becoming increasingly valuable, and their exchange is necessary to facilitate future innovation (Roa-Rodríguez and Van Dooren, 2008).
Reasons for Increased Restriction of Plant Genetic Resources Exchange
Although plant genetic resources were previously regarded as the common heritage of mankind, this is no longer the case. The recent trend has been a shift towards ownership claims that lead to a restriction of open access (Le Buanec, 2005). This restriction is not necessarily negative. One of the reasons for awarding property rights is to provide incentives to individuals or groups to participate in plant breeding, which should lead to more investment in breeding overall (Thiele-Wittig and Claus, 2003). Some other factors causing this shift in thought are related to the development of biotechnology and the ability to transfer genes; these advances have led to legislation that grants patents for many types of biological materials. The awarding of these patents is in stark contrast to the traditional free access to wild relatives and landraces. In the 1970s, the Plant Variety Protection (PVP) Act in the United States gave breeders of new varieties a protection similar to that that a patent would provide, given that the variety was somehow different from current varieties and was reproducible. However, PVP protection does not prevent the use of the protected variety in breeding programs. Following a court case that made a genetically modified microorganism patentable, there was a rush of patent applications for biotechnological “inventions.” Intellectual Property Rights were granted for genes, molecular constructs, and traits. These events led to increasing concern that plant genetic resources currently available for use by the public might become patented and inaccessible. Countries have responded to this concern by trying to claim materials that have traditionally belonged to the public and by limiting international agreements that allow access to these materials. This could put public germplasm collections at risk if fewer resources are part of the public domain. The increase in Intellectual Property Rights involving plant “inventions” has also led to a large increase in the merging of small companies into a few large applied biological science firms. These firms have a significant number of patents on plant genetic resources and control seed distribution, making it difficult for new genetic resource development companies to survive. These patents also make it difficult for research institutions to access these resources (Falcon and Fowler, 2002).
Another cause in the decline of the use of common heritage is that some countries associate this concept with imperialism. This perception is a result of the imbalance between the free flow of genetic diversity from developing countries where it naturally occurs and the subsequent sale of products derived from these resources by developed countries back to the developing countries for a profit (Le Buanec, 2005). This imbalance between the free flow of genetic resources from some countries and the high price of improved cultivars under patents/plant variety protections from others has led to an increase in political tensions. The controversy has arisen because although plant genetic resources that have been worked with and made distinct are eligible for PVP, the raw materials are not. This led to a situation in which countries whose inhabitants had developed germplasm over many years were giving this germplasm away under the common heritage rule, but were then having to buy the protected varieties created from this germplasm (Roa-Rodríguez and Van Dooren, 2008). There is a strong perception that developed countries have taken advantage of developing countries. The increase in Intellectual Property Rights for biological materials exacerbated this situation. Developed countries claimed ownership over genetic resources provided by developing countries, and developing countries lacked the appropriate means to acquire any reward for their contributions (Falcon and Fowler, 2002). As developing countries became aware of the economic value of their genetic resources, they began fighting to restrict access to these resources. Conflict has therefore arisen because although there is a trend towards patenting biological materials and improved cultivars, the groups holding these patents still want to have free access to the genetic resources that can be used to create or improve these cultivars (Rodríguez and Van Dooren, 2008). The common heritage idea has therefore declined to some degree due to the unidirectional nature of the flow of unimproved plant genetic resources from areas naturally rich in biodiversity (Falcon and Fowler, 2002).
Political Developments in the Struggle for Ownership of Plant Genetic Resources
In order to fully understand the debate over ownership of plant genetic resources, it is important to have some knowledge of the legislative attempts that have been made to settle these issues. Legislation regarding ownership of plant genetic resources can be traced back to 1930, when the United States passed the Plant Patent Act, which gave protection to vegetatively propagated crops. As the breeding industry became more commercialized, there arose a need for some form of regulation of plant genetic resources on an international level. This led to the International Convention for the Protection of New Plant Varieties (UPOV) in 1961. One important outcome of this convention was the establishment of Plant Breeders’ Rights, which gives ownership of sale and marketing rights of new commercial plant varieties to the breeder. Another significant effect of this convention was that it provided a way to remove plant genetic resources from common use. In 1970, the United States provided protection equivalent to that of the UPOV with the Plant Variety Protection Act. Plant Variety Protection systems do provide exemptions to breeders for further research and to farmers so that they can save seed if they are using it on their own land (Roa-Rodríguez and Van Dooren, 2008). This is in contrast to utility patents. Following a Supreme Court decision in 1980, living organisms are eligible for these patents, which do not include a “Breeder’s exception” to allow use of patented material in breeding programs (Le Buanec, 2005). The main difference between utility patents and plant patents or plant variety protection is the scope of the protection. Plant patents and plant variety protections are narrower and are variety specific. On the other hand, utility patents, which are much more difficult to obtain, protect the use of inventive concepts and are thus able to protect more than one variety containing these concepts. Utility patents are much broader in scope, but also require a lot of time and money to acquire (Williams, 1986). This could put public research entities at a disadvantage if they do not possess the legal or financial resources that a large corporation would to obtain this kind of patent. The differences between plant patents, utility patents, and plant variety protection are summarized in Table 1 (Williams, 1986).
In 1983, the Food and Agriculture Organization of the United Nations organized the International Undertaking on Plant Genetic Resources agreement, which attempted to negate some of the consequences of the ability to obtain patents on living organisms. The undertaking tried to return to the idea of common heritage and hoped to promote cooperation among nations in the use of plant genetic resources (Cooper, 2002). It also spelled out the concept of Farmer’s Rights (Roa-Rodríguez and Van Dooren, 2008), which aim to minimize individual ownership of plant genetic resources (Van Overwalle, 2005). Farmer’s Rights also include the idea that farmers should receive compensation from a general conservation fund for their role in developing plant resources. Unfortunately, participation in this agreement was voluntary and little progress was made (Aoki and Luvai, 2007). In 1992, the Convention on Biological Diversity met in a political climate of tension regarding the unequal exchange of plant genetic resources and biodiversity. Developing countries felt a need to protect their resources from exploitation, and thus the convention replaced common heritage with a philosophy of national sovereignty. Since this convention, countries have been racing to make laws positioning themselves as the suppliers of genetic resources and restricting access to these resources. Under this system, negotiations for the transfer of genetic resources must go through the country of origin (Falcon and Fowler, 2002).
In 1994, the Food and Agriculture Organization began negotiations to implement a legal agreement regarding ownership of plant genetic resources. In 2001, the International Treaty on Plant Genetic Resources for Food and Agriculture was created (Falcon and Fowler, 2002). The treaty took over seven years to complete, because of the challenge of respecting the rights of national sovereignty over resources while also ensuring that these genetic resources are accessible (Cooper, 2002). This treaty aims to create a multilateral system in which countries cooperate to allow access to resources to other countries in exchange for a portion of the profits made from anything incorporating these genetic resources. This money will be put into an international fund that will be used in projects such as germplasm conservation, etc. (Falcon and Fowler, 2002). The access to resources is based on terms agreed upon by both parties and the country must provide informed consent (Cooper, 2002).
This treaty may help to facilitate transfer of resources, but it still has some drawbacks. Although it covers most major crops, a few important crops, especially those important in developing countries, are not included because countries thought they might profit more from not including these crops and selling the resources through another avenue. For example, China withheld soybean, which is an important crop worldwide (Falcon and Fowler, 2002). Developing countries suffer the most as a result because they are more likely to lack the resources to obtain plant genetic resources that are not included in this system. Excluded crops will likely be transferred based on national sovereignty, which could make access more restricted. On the other hand, this treaty does back up the international status of the valuable collections held by the Consultative Group for International Agricultural Research (CGIAR). The CGIAR centers have some of the best collections of genetic resources, including resources of regionally important crops, and the materials are freely available upon request (Falcon and Fowler, 2002). The Convention on Biological Diversity did not specifically address the ownership of these collections, and there was a legitimate concern that countries might demand the return of germplasm or restrict its distribution on the basis of national sovereignty. This would have meant fewer plant genetic resources available for plant breeding. However, the Food and Agriculture Organization signed agreements in 1994 to establish these collections as “in-trust.” Under these agreements, the CGIAR centers do not own the collections, but are responsible for their upkeep and distribution. These agreements prevent anyone from seeking Intellectual Property Rights over the germplasm in the CGIAR centers. This was an important step in ensuring that these vital collections remain accessible (Gotor et al., 2010). The treaty also includes measures to work towards the sustainable use and conservation of plant genetic resources (Cooper, 2002). Despite its flaws, the International Treaty on Plant Genetic Resources for Food and Agriculture does attempt to provide some regulation to germplasm transfer and could prevent the creation of unnecessarily restrictive national legislation (Falcon and Fowler, 2002). Lastly, in the Trade-Related Aspects of Intellectual Property Rights agreement, which came into force in 1995, developing countries agreed to try to create an Intellectual Property Rights system but also maintained the right to not allow patents on plants, animals, and biological materials (Gepts, 2004).
Possible Consequences of the Restriction of Plant Genetic Resource Exchange
The restriction of plant genetic resource flow has the potential to prevent the movement of germplasm between nations. As mentioned previously, most countries depend on genetic resources from other countries. Legal measures restricting the continued exchange of this material will thus be detrimental to all countries.
One consequence of the struggle for ownership rights is that national sovereignty over plant genetic resources has led to the creation of overly restrictive laws in some countries. Benefit-sharing can also lead to an increased emphasis on monetary benefits. On the whole, this can lead to a decrease in access and a decrease in collections of plant genetic resources (Roa-Rodríguez and Van Dooren, 2008).
The ability to obtain patents on biological materials also has consequences on plant breeding. Patent law helps to provide motivation to invent and commercialize new products by protecting the inventor from competition for a period of time (Van Overwalle, 2005). It also encourages investment in plant genetic resources and the creation of companies participating in this area of research. Because the budgets of public research institutions are increasingly tight, it is important to have plant breeding research in the private sector. Intellectual Property Rights are needed to encourage private investment (Srinivasan, 2003). In addition, the high-cost and high-risk nature of plant biotechnology research makes this financial incentive even more important (Figg, 1995). However, patenting of biological materials also inhibits the freedom of others to use the most improved germplasm. Because most patents occur in developed countries, this could put developing countries at greater disadvantage (Falcon and Fowler, 2002). In addition, farmers need plant genetic resources in order to adapt to changing conditions, and removing their access to these resources through patents might limit the role of farmers in developing diversity in the future (Eyzaguirre and Dennis, 2007). Additionally, because patents are valid only in the nation that issues them and many countries lack patent laws for biological materials, trade might be further restricted if patent holders do not want to release their materials into an area where they will not be protected (Falcon and Fowler, 2002). Patents might also lead to less breeding research involving traits for which there are many patents for fear that the outcomes of the research would fall under patent claims. There might also be a decrease in funding for breeding research that will not be patentable (Correa, 1995).
Another important consequence of removing the common heritage philosophy is increased cost in obtaining resources. Increased transaction costs due to ownership rights could put poor countries even further behind because of their inability to access the protected materials and technologies (Falcon and Fowler, 2002). The developing countries of the world, despite the fact that most of them are located in genetically diverse regions, are now the largest borrowers of plant germplasm. These countries are dependent on seed banks in developed countries, but access is increasingly difficult now that the common heritage system is disappearing (Aoki and Luvai, 2007). Less informed rural populations are also less likely to have the resources to claim ownership, and thus might lose access to germplasm (Eyzaguirre and Dennis, 2007).
Lastly, it is important to note another aspect of the issue of plant genetic resource exchange: the role of traditional communities and their knowledge. These communities protect the biodiversity of wild relatives of crop plants because they recognize the communal good that comes from possessing many varieties (Eyzaguirre and Dennis, 2007). The common heritage philosophy is common in these communities and seed is frequently exchanged (Brush, 2007). An increase in private ownership of germplasm could be harmful to this system, because if plant genetic resources are not freely traded, it makes less sense to maintain these wild relatives for the public good. Improvements in plant genetic resources are also the result of community efforts, which makes it impossible to assign property rights. Private property rights are not in sync with the traditional structures that have maintained plant genetic resources in the past, and thus traditional knowledge may not receive the compensation that it deserves (Eyzaguirre and Dennis, 2007).
The access to plant genetic resources has been a vital part of plant breeding and the development of modern agriculture. Although property rights on plant genetic resources can serve a purpose, the trend towards increasing legal restriction on this access could be detrimental if breeders are unable to use the best germplasm available in their breeding programs. This restriction could be especially threatening to breeding programs in developing countries that are now net importers of plant germplasm. This conflict is complex, and negotiations over ownership rights are ongoing. It will no doubt be challenging to find a solution that meets the needs of all groups involved.
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