Crop Science 43:409-414 (2003)
© 2003 Crop Science Society of America
PLANT GENETIC RESOURCES
Impact of Transgenic Genotypes and Subdivision on Diversity within Elite North American Soybean Germplasm
Clay H. Sneller*
The Ohio State University, OARDC, Dep. of Horticulture and Crop Science, 1680 Madison Ave., Wooster, OH 44691
* Corresponding author (sneller.5{at}osu.edu)
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ABSTRACT
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There are several recent trends in North American soybean [Glycine max (L.) Merr.] breeding that call for a new evaluation of the pedigree structure of this population. These are the introduction of Roundup Ready (RR) soybean and restricted exchange of germplasm between breeding programs. The objectives of this study were to assess the genetic structure of the current elite North American soybean population and the current and potential affect of RR soybean and crossing restrictions on this population. This study used coefficient of parentage (CP) analysis of 312 current RR and conventional lines. The RR trait was initially backcrossed into elite lines from a total of 30 different recurrent parents. Many of the intermediates of the backcrossing were also crossed to other elite lines and it is from such crosses that many of the current RR lines derive. Only 1% of the total variation in CP among lines from the northern or southern regions was accounted for by differences between conventional lines, RR lines, and the recurrent parents used to initiate RR breeding programs. The advent of RR cultivars has had little impact on diversity because of the wide use of this technology by many programs and its incorporation into many lines. In contrast, 19% of the variation in CP among northern lines, and 14% among southern lines, was due to difference between lines from different companies and institutions. Diversity was limited among elite lines from some companies. The restricted diversity within some companies coupled with limited exchange of germplasm could affect the soybean industry if marketplace shifts favor one company. Public programs can work to ensure and expand diversity.
Abbreviations: RR, Roundup Ready1 • CP, coefficient of parentage • MG, maturity group.
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INTRODUCTION
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PEDIGREE ANALYSIS of breeding populations allows breeders to examine the genetic structure of their populations. Such studies estimate the average degree of relationship among the individuals of a population, effective population size, the number of ancestors contributing to a population, the relative contribution of each ancestor to a population, and natural grouping of the individuals. This information is useful in managing diversity within a population.
The genetic structure of a population can change over time as breeders manipulate the population to attain their objectives. Changes can occur when new ancestors are introduced, some lineages are used more or less often than average on the basis of their perceived value, breeding procedures are modified, and the population is subdivided. Selection, where effective, will change gene frequencies for traits, though pedigree analysis cannot monitor such changes, as the calculations assume no selection effect on a single gene.
Pedigree analysis has been applied frequently to the elite North American soybean population (Carter et al., 1993; Delannay et al., 1983; Gizlice et al., 1993, 1996; Kisha et al., 1998; Sneller 1994a; St. Martin, 1982). There have been several recent trends in North American soybean breeding that call for a new evaluation of the pedigree structure of this population. Foremost is the introduction and rapid acceptance of Roundup Ready1 (RR) soybeans. RR soybean cultivars are resistant to the nonselective herbicide Roundup whose active ingredient is glyphosate (N-phosphonomethyl glycine), a compound that binds to and blocks the activity of 5-enol-pyruvylshikimate-3-phosphate synthase. Resistance to glyphosate is conferred by a gene from Agrobacterium sp. strain CP4 that produces a form of 5-enol-pyruvylshikimate-3-phosphate synthase that is tolerant to glyphosate (Padgette et al., 1995). This gene was engineered into the soybean cultivar A5403 to produce the line 40-3-2, which is highly tolerant of glyphosate (Padgette et al., 1995). The line 40-3-2 was then used in traditional breeding schemes to develop RR soybean cultivars currently grown in North America. Seed of 40-3-2 was distributed to different breeding programs. In addition, some public breeders received the glyphosate tolerant gene after it had been backcrossed into ‘Resnik’ with 40-3-2 used as the donor. First introduced to growers in 1996, RR soybean cultivars are now grown on an estimated 60 to 75% of the U.S. acreage. Since RR soybean cultivars now dominant many soybean breeding programs, the breeding history of RR soybean may have affected the genetic structure of the elite population.
The other trend that may affect the genetic structure of soybean is reduced exchange of germplasm among breeding programs. Until the mid 1980s, breeders were free to cross with any line regardless of its source. This is no longer possible because some companies have utility patents on released conventional and RR cultivars as well as additional use restrictions on germplasm beyond that covered by the Plant Variety Protection Act. The end result of these actions is that many lines from proprietary sources are being used only by the company that developed the line as the imposed restrictions are too severe for acceptance by other breeders. Thus, the elite soybean population is becoming subdivided by the source of elite lines. The objectives of this study were to assess the genetic structure of the current elite North American soybean population and the current and potential affect of RR soybean and crossing restrictions on this population.
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MATERIALS AND METHODS
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The pedigrees of 312 elite soybean genotypes were analyzed. The genotypes consisted of released cultivars and advanced breeding lines and ranged from maturity group (MG) 00 to VIII (Table 1). All proprietary lines were selected because they were widely sold in 1999 or they were anticipated to be released and sold in 2000 or 2001 (proprietary sources, personal communications). The public lines were selected from the 1998 USDA Uniform trial reports for their superior yield or because they were high-yielding released cultivars used by growers in 1999. The proprietary lines came from eight different companies (Table 1). The pedigree information from some companies was obtained under confidentiality agreements, which preclude explicitly revealing the pedigree of the lines. To comply fully and fairly with these requests, I have not named the source of any proprietary lines in the study. Three of the companies market soybean cultivars in the north and south, two primarily market in the north, while three market only in the south. A nearly equal number of RR and conventional soybean lines were chosen from each company and MG combination (Table 1). Nearly 34% of the 312 lines were from public programs, 55% were northern maturity (MG 00 to MG IV north), and 50% of the proprietary lines were RR.
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Table 1. Number of soybean lines summarized by source (public or proprietary), type [conventional or Roundup Ready (RR)], and maturity group (MG).
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Coefficient of parentage (CP) was calculated on the basis of the assumptions of Sneller (1994a) and Carter et al. (1993) and with SAS (SAS Institute Inc., 1998) programs written by the author (Sneller, 1994b). Several CP matrices were constructed with different subsets of lines: (i) all 312 lines, (ii) proprietary conventional and RR lines from the south and recurrent parents used in the development of the RR lines, (iii) proprietary conventional and RR lines from the north and recurrent parents used in the development of the RR lines, and (iv) all southern lines except MG VIII, and v) all northern lines except MG 00. The last two matrices were used to compare the CP between public versus proprietary sources without the confounding effect of a greater range of MG among lines from public sources than proprietary sources (Table 1).
Multidimensional scaling (Gizlice et al., 1996) was performed on matrices of genetic distances (1 - CP) constructed from matrices 4 and 5 described above to facilitate two-dimensional graphic display of the matrices. The variance within each matrix was partitioned by means of regression techniques and SAS (Gizlice et al., 1996). The variation attributable to MG, source (public, proprietary, and company), or type (conventional, RR, and RR recurrent parent) was estimated for each of the seven matrices described above.
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RESULTS AND DISCUSSION
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RR and Proprietary Conventional Soybean Lines
The transgenic line 40-3-2 (Padgette et al., 1995) was the sole source of the glyphosate tolerance in this study. Line 40-3-2 is a transgenic version of an older southern cultivar, A5403, from Asgrow Seed Company. In all cases, the glyphosate tolerance gene from 40-3-2 was backcrossed at least one time to an established high-yielding recurrent parent. Thirty recurrent parents were in the pedigree of the 102 RR lines in this study, 19 for northern lines and 11 for southern lines. In many instances, the glyphosate tolerance gene was backcrossed three or more times into an established line. These BC derivatives were often then released as the first RR cultivars in the USA. Most of these initial RR cultivars were not among the 312 lines analyzed in this study because they have been replaced by more recent RR cultivars. During the backcrossing to develop the initial RR cultivars, the backcross intermediates (BC1F1, BC2F1, BC3F1) were also crossed to conventional nonrecurrent parent lines. The more recent RR lines included in this analysis were derived from such crosses as well as crosses between the initial RR cultivars and other conventional high-yielding parents.
It is well established (Delannay et al., 1983; Gizlice et al., 1996; Sneller, 1994a) that much of the variation in CP among North American soybean lines derives from the contrast of northern (MG 00 to IV north) and southern (MG IV south to VIII) lines. Thus, separate analyses of conventional versus RR elite lines were performed for proprietary lines from the north and south.
The average CP among and between proprietary conventional lines, RR lines, and the recurrent parents used in the development of RR lines indicates little difference among these three types of lines in either region (Table 2). Variation between these three types of lines accounted for only 1% of the total CP variation among either the northern or southern proprietary lines. In contrast, variation due to classifying the lines by MG and source (different companies) combined accounted for over 45% of the variation in each region. Gizlice et al. (1996) reported that MG and source of lines (different public breeding programs) accounted for 48% of the CP variation among 258 public lines released from 1945 to 1988. It is apparent that the set of 30 recurrent parents initially crossed to 40-3-2 was large and diverse enough to capture most of the elite genetic base of the northern and southern regions. The 19 recurrent parents from the northern region were slightly more related to one another than average for elite northern lines (Table 2). This is because 12 of the 19 northern recurrent parents were MG III and IV. These MG have more ancestry from ‘Lincoln’ and ‘Richland’, and less ancestry from ‘Mandarin Ottawa’ than MG 0 to II cultivars (Gizlice et al., 1996; Kisha et al., 1998; Sneller, 1994a). Whereas the initial sample of recurrent parents in the north may have been skewed towards these MG and lineages, this initial bias has been diluted in subsequent crossing that developed the current RR elite lines. The 11 recurrent parents used in the south were all MG IV or V lines, yet this biased sampling of early southern MG did not appear to greatly restrict the diversity among these parents.
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Table 2. Average coefficient of parentage among and between proprietary conventional and Roundup Ready (RR) soybean lines and the recurrent parents used in developing RR lines. Lines are from the northern (maturity group 0–V north) and southern (maturity groups IV south–VII) regions.
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Pedigree Diversity of Current Elite Population
The average CP over all 312 lines was 0.17 (Table 3). This value appears unchanged over the last 25 yr when compared with values reported from other periods (Gizlice et al., 1993; Sneller, 1994a). There is a trend over the last 25 yr for decreasing CP within the northern and southern regions while the average CP between regions has more than doubled. This trend is particularly pronounced for MG V lines whose average CP has declined 25% in the past 10 yr (Table 3) while the CP of MG V lines with northern lines has increased. It is apparent that there is more crossing between lines from different regions than in the past and that this intercrossing has reduced the average CP in each region, especially for the MG V cultivars. This can also be seen in the analyses of the ancestral contributions to each region. The contribution of the main northern ancestor Lincoln to the southern region has increased in the past 10 yr while the contribution of the main southern ancestors CNS and S100 has increased in the north (Table 4). This is primarily due to the extensive use of the cultivar A3127 and its derivatives in the development of MG III, IV, and recently MG V cultivars (Kisha et al., 1998; Sneller, 1994a). A3127 was derived from a cross of a northern parent (‘Williams’) with considerable ancestry from Lincoln, and a southern parent (‘Essex’) with considerable ancestry from CNS and S100. Recent research indicates that northern elite lines can be a source of beneficial yield genes for southern breeders (Cornelious and Sneller, 2002).
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Table 3. Average coefficient of parentage among elite soybean lines from different maturity groups, regions, and periods.
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Table 4. Proportion of elite North American soybean ancestry in 1999–2001 and 1989 to 1992 from key ancestors. The 1989 to 1992 data is from Sneller, 1994a.
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There have been some changes in the ancestral base of North American soybean over the last 10 yr. Seventeen ancestors accounted for 90% of the elite ancestry in this study (Table 4), while Sneller (1994a) reported that only 11 ancestors accounted for 90% of the ancestry of elite North American public and proprietary lines in 1989-1990. This increase is not from the addition of new ancestors, but from a more even sampling of ancestors that have been used for the past 15 yr (Table 4). In contrast, 266 ancestors account for 90% of the ancestry of 651 elite Chinese lines (Cui and Carter, 2000), while 57 ancestors account for 90% of the ancestry of 86 elite Japanese cultivars (Zhou et al., 2000).
For lines from the northern region, 16 ancestors contributed at least 1% of the ancestry while 18 contributed at least 1% in the south. The only major change in the northern genetic base in the last 10 yr, other than that noted above, was a reduced contribution from AK (Harrow) and Mandarin (Ottawa) (Table 4). Among southern lines, PI71506 contributed nearly 2% of the current ancestry, while 10 yr ago it was not in the pedigrees of elite southern lines (Sneller, 1994a). PI71506 contributed 25% of the ancestry to the MG V cultivar Hutcheson. Hutcheson was a very successful cultivar and an extremely successful parent in many southern breeding programs. The positive impact of PI71506 and Hutcheson mirror the impact of PI257345 and its progeny S1346 15 yr ago in the north (Sneller 1994a; Kisha et al., 1998). The recent extensive use of PI71506 ancestry in the south also contributed to the reduction in CP noted over the past 10 yr. This is seen particularly among the MG V lines where PI71506 now contributes 3% of the ancestry.
The introduction of RR soybean has had little impact on the overall diversity of the elite soybean population. The changes noted above are attributed to intercrossing of lines from different regions and the use of new lineages. The broad distribution of 40-3-2 to many companies and public institutions allowed the glyphosate tolerance gene to be backcrossed into many lineages. Subsequent crossing to additional elite non-RR parents from many sources is quickly diluting the effect on diversity from sampling of the initial recurrent parents.
Subdivision of the Elite Population
Restricted exchange of germplasm among companies and public institutions could affect the diversity of the elite population and its utilization. In the north, 19% of the total CP variation was between lines from different sources (public and the five companies), while 18% was between lines from different MGs (0–IV north). A plot derived from the CP-based distance matrix indicates that lines from different companies tend to group together while the lines from public sources tend to be quite dispersed (Fig. 1). The average CP among northern lines from companies A (0.28), B (0.29), D (0.25), and E (0.42) was greater than the average CP among all northern lines in this set (0.23), while the average CP among lines from company C (0.21) and public institutions (0.22) were close to the overall average. Lines from company E were quite related to lines from companies A (0.30), B (0.32), and D (0.29). Lines from company C were fairly distinct having an average CP ranging from 0.16 to 0.19 with lines from other proprietary or public sources. The average CP of lines from any company with public lines was lower than average with the exception of lines from company E (0.26).
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Fig. 1. Plot of the first two dimensions from multidimensional scaling of the coefficient of parentage-based distance among 168 maturity group 0 to IV (north) conventional and Roundup Ready soybean lines from proprietary and public sources. The legend identifies the source of the proprietary lines by the letter code for each company.
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There was less separation of lines by source among southern lines (MG IV south to VII) than among northern lines (Fig. 2). Only 14% of CP variation in the south could be accounted for by different sources (public and the seven companies), while 20.7% was accounted for by different MGs. Still the average CP among southern lines from companies A (0.27), B (0.31), C (0.33), D (0.50), and G (0.32) was above the average CP among all southern lines (0.22). Company D only had four MG IV lines in the southern analysis and this explains the high CP among the lines from company D. With the exception of company D, the average CP among lines from different companies was close to average. The southern lines from public institutions were not as evenly dispersed through the entire genetic space, as were the northern public lines (Fig. 2). Ancestral analysis showed that the southern public lines had more ancestry from the traditional southern ancestors CNS and S100 (43%) than the southern proprietary lines (36%) and less ancestry from Lincoln (5%) than proprietary lines (11%).
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Fig. 2. Plot of the first two dimensions from multidimensional scaling of the coefficient of parentage-based distance among 126 maturity group IV (south) to VII conventional and Roundup Ready soybean lines from proprietary and public sources. The legend identifies the source of the proprietary lines by the letter code for each company.
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The analyses included only elite lines and the sample probably does not represent the diversity in the entire program of each company. Still these are the best lines from each source and will certainly form the foundation for successive cycles of breeding. The results show restricted diversity within most companies because of extensive use of their best lines as parents for the next cycle of selection. Without exchange of germplasm, or use of other lineages not present in this analysis, this scenario will not change and in fact will worsen with continued nonrandom mating in a closed and restricted gene pool.
Fortunately, continued access to elite public germplasm will allow each company to expand its diversity. Public lines originate from many independent programs and collectively tend to represent the entire scope of elite diversity. In addition, current public programs to increase diversity through the use of exotic germplasm (Cornelious and Sneller, 2002; Manjarrez-Sandoval et al., 1998; Sneller et al., 1997; Thompson and Nelson, 1998) will allow each company to access improved exotic germplasm. This is an important function for public institutions. Soybean breeders were fortunate that germplasm derived from the last two plant introductions (PI257435 through the Northrup King cultivar S1346, and PI71506 through the cultivar Hutcheson) successfully used to improve yield of commercial cultivars was available to all breeders. Without public facilitated exchange of diverse germplasm, each company may develop its own program to maintain or expand the diversity of its germplasm, thereby deepening the division of the elite diversity. Such fracturing will lead to marketplace instability as history shows that some breeding programs (companies) will periodically be quite successful at capturing value from exotic sources. This could result in a significant competitive advantage for the successful program in an era where germplasm is not freely exchanged. While this scenario is beneficial to the successful program, it could have dramatic ramifications on other companies and soybean growers.
Limited access to high-yielding proprietary germplasm will affect public efforts to expand diversity. Breeders of commercial cultivars will be reluctant to use improved exotic-based germplasm with only average yield potential. Thus, any program trying to capture yield value from exotic sources will need to develop germplasm with above average yield potential if it wants the germplasm to be used by proprietary breeders. While there has been some success in capturing value from exotic x exotic crosses (Thompson and Nelson, 1998), most studies indicate that exotic parentage needs to be mixed with elite parentage to attain high yield potential (Cornelious and Sneller, 2002; Ininda et al., 1996; Khalaf et al., 1984; Schoener and Fehr, 1979; Thompson and Nelson, 1998; Thorne and Fehr, 1970; Vello et al., 1984). Thus, public breeders working with exotic germplasm will need to access high-yielding elite lines to develop acceptable germplasm from programs aimed at expanding diversity for yield.
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CONCLUSIONS
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Deployment of transgenes in cultivars can alter genetic diversity of elite populations because of limited sampling of the elite population when selecting the transformed line(s) and the set of parents used in subsequent crossing and backcrossing schemes. Currently, few soybean cultivars can be successfully transformed; so limited sampling of lines to transform will cause an initial alteration of the genetic base of lines with the transgene. The ancestry of transgenic lines derived from subsequent crossing will depend on the number and ancestry of the parents used in the crossing.
The manner in which the glyphosate-tolerance transgene was deployed minimized the disruption of the genetic base of elite North America soybean germplasm. The transgene was made available to many companies and public institutions. As a result, a large set of recurrent and elite parents that captured the current diversity in conventional elite North American soybean was used to develop current RR cultivars. The diversity among elite lines though is not evenly distributed among all companies and some companies appear to have limited diversity among their elite lines. Thus, diversity among future cultivars with a particular transgene could be quite skewed and restricted if the transgenic cultivars derive from one company. If this occurs, the transgenic crop could be genetically vulnerable to some biotic and abiotic stresses.
The impact of limited diversity among lines from some companies and restricted germplasm exchange between companies is not limited to transgenic cultivars or traits. Soybean breeding is punctuated by extensive use of certain parents, some derived from diverse crosses, that appear to lead to significant yield increases (Sneller, 1999). Such lines have been available to all breeders in the past, but this is unlikely in the future if a private company develops the successful line. Public institutions can minimize the risk of genetic vulnerability in elite soybean lines posed by possible dominance of certain transgenic types or companies by developing diverse high-yielding lines that are available to all companies. To be useful, such germplasm must have good yield potential. Cooperative partnerships between proprietary and public institutions may optimize the value and impact of such germplasm.
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ACKNOWLEDGMENTS
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I wish to express my gratitude to Zhanglin Cui for providing the SAS programs used to perform the regression analyses and to partition the variance in the CP matrices and to the many people who kindly provided pedigree information.
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NOTES
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1 Roundup and Roundup Ready are registered trademarks of the Monsanto Company. 
Received for publication October 10, 2001.
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TOP
ABSTRACT
INTRODUCTION
