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PLANT GENETIC RESOURCES

Structure of Genetic Diversity among Common Bean Landraces of Middle American Origin Based on Correspondence Analysis of RAPD

^a Centro Internacional de Agricultura Tropical (CIAT), A.A. 6713, Cali, Colombia
^b Univ. of Wisconsin-Madison, Dep. of Horticulture, 1575 Linden Drive, Madison, WI 53706-1590 USA

s.beebe{at}cgiar.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

 
More than 60% of common bean production worldwide is derived from cultivars of Middle American origin. Understanding the diversity of these will facilitate their use in genetic improvement. The objective of this study was to analyze a collection of 269 landraces of common bean (Phaseolus vulgaris L.) by correspondence analysis of random amplified polymorphic DNA (RAPD) data to determine the genetic structure of the Middle American gene pool of cultivated bean. One hundred eighty landraces originating in Mexico, the remainder in Central America and secondary centers of diversity within the Americas, and two checks were studied. DNA was extracted, RAPD reactions carried out, and polymorphic bands were scored as present or absent on the basis of 39 primers. Groups were formed which in part corresponded to races defined previously by morphological and agroecological criteria. However, tropical small-seeded Race M was composed of two groups: one largely Mexican that included most small-seeded black beans of upright plant habit; and one Central American with landraces of various seed colors. Most non-black small-seeded germplasm of Race M phenotype from secondary centers grouped with the Central American landraces, except for cream-seeded and purple-seeded accessions from Brazil. Races D and J could be distinguished and within races D and J further divisions could be recognized which were related to geographic origin. The more commercial Race D landraces formed a genetic group that was predominant in the western part of the Mexican highland plateau. Another Race D group was concentrated at the eastern extreme of the neovolcanic axis and was differentiated morphologically as well. Guatemalan germplasm contained accessions of climbing bean that did not group with any of the previously defined races and should be considered a separate race. Thus, Middle American germplasm of common bean is more complex than previously thought, and contains diversity that remains to be explored for its practical value.

Abbreviations: CIAT, Centro Internacional de Agricultura Tropical • D, Durango • J, Jalisco • M, Mesoamerica • G, Guatemala • MCA, multiple correspondence analysis • RAPD, random amplified polymorphic DNA • RFLP, restriction fragment length polymorphism • AFLP, amplified fragment length polymorphism

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

 
THE COMMON BEAN is the most important food legume in the world. About 7 Tg are grown in Latin America and Africa, all for human consumption (CIAT, 1993a). Evidence based on allozymes (Singh et al., 1991c), seed proteins (Gepts and Bliss, 1986), morphological traits (Singh et al., 1991b), and DNA markers (Nodari et al., 1992; Becerra Velasquez and Gepts, 1994) indicates that two major gene pools exist in cultivated common bean, one Middle American and one Andean. These gene pools reflect multiple domestication events within distinct wild populations (Gepts and Bliss, 1986). Genotypes of the Middle American gene pool predominate in Mexico, Central America, and Brazil, which jointly account for about 84% of production in Latin America (CIAT, 1993a). For purposes of this paper, "Central America" refers to Guatemala, El Salvador, Honduras, Nicaragua, and Costa Rica, a convention that is accepted within this region. "Middle America" refers to the combined regions of Central America and Mexico.

Singh et al. (1991a) proposed that within each gene pool three races could be distinguished on the basis of differences in plant and seed morphology and adaptation regimes. Growth habit is an important distinguishing criterion, and is classed as Type 1 (determinate bush), Type 2 (indeterminate upright bush), Type 3 (indeterminate semi-viney prostrate), and Type 4 (indeterminate climbing) (CIAT, 1987). Within the Middle American gene pool race Mesoamerica (M) is common to both Mexico and Central America, and is characterized by relatively small seed and warm lowland adaptation. Most Race M landraces have habits of Type 2 or 3, although some have Type 4 habit. Commercial classes within Race M include small black, small Central American red and navy beans. Race Durango (D) is composed principally of growth habit Type 3 genotypes with small leaves, medium size seed, and adaptation to dry highland areas of Mexico. Commercial Race D classes include pinto, great northern, and small red Mexican beans. Race Jalisco (J) is found in the more humid highland areas of Mexico and is composed of mostly climbing Type 4 genotypes with medium size seed, such as the Garbancillo Zarco cultivar. An understanding of the race structure of bean germplasm has contributed to the more efficient utilization of genetic resources of bean. For example, Race M has been found to be complementary to races D and J in yield improvement (Singh et al., 1989).

For the definition of genetic relationships, DNA markers have advantages over morphological traits, such as distinguishing among accessions with similar morphology and discriminating polymorphism over far more loci than isozymes and seed proteins. DNA analysis with amplified fragment length polymorphisms (AFLPs) permits visualization of the genetic structure of a core collection of wild P. vulgaris (Tohme et al., 1996). Genetic differences among defined races of the Middle American pool were revealed by RFLP analysis (Becerra Velasquez and Gepts, 1994). However, some segments of the Middle American gene pool have not been explored for their genetic relationship to recognized races. The objective of the present study was to determine the genetic structure of a large sample of cultivated beans of Middle American origin through RAPD analysis.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

 
A total of 269 landraces of Middle American origin plus two standard checks were chosen for analysis (Table 1) . In this context, a landrace is considered to be a traditional inbred farmer variety, unimproved by modern methods of plant breeding. This sample was drawn in large part from the bean core collection developed at CIAT (Tohme et al., 1994) and therefore was a more systematic sample than used previously. Of these, 180 originated in Mexico and were drawn at random, 90 from the CIAT core collection and 90 from the CIAT reserve collection. These materials formed part of a separate study to compare the genetic composition of the core and reserve collections, and results of that study have been reported elsewhere (Skroch et al., 1998). An additional 89 core accessions from other countries and regions with small seed type typical of Middle American landraces were included in the present study to complement the Mexican accessions. Most were Central American in origin while others came from Andean or Caribbean countries. These latter accessions were assumed to have been introduced to the respective regions from Middle America. An agro-ecological classification of the site of origin based on soil type, rainfall, photoperiod, and expected growth cycle as a function of altitude (Tohme et al., 1994) was available for about 50% of the 269 entries. One Mesoamerican check (Race M cv ICA Pijao, with small black seed and Type 2 growth habit) and one Andean check (Race N cv Calima, with large red and white mottled seed and Type 1 growth habit) were included for comparison.

Phaseolin type had previously been characterized on the entire core collection (CIAT, 1993b) by the method described by Lareo et al. (1993). Groups formed by MCA of RAPD data were examined for their constitution as to phaseolin types and plant and seed morphology.

	Results

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

 
Thirty-nine primers produced 261 polymorphic bands, for an average of 6.7 bands per primer. In a preliminary analysis of the data, the first dimension of the MCA revealed a wide separation between one small group of 12 accessions, mostly from Mexico, and the great majority of the other accessions. The smaller group included the Andean check cultivar Calima, and inspection of phenotypic data demonstrated that the other accessions in this group were also large-seeded Andean types (Table 1). Although these are considered to be Mexican landraces, they are assumed to have been introduced many years ago from the Andes (Gepts, 1988). Another nine accessions graphed as outliers, and inspection of their band constitution revealed that they possessed several bands typical of the Andean beans. The outliers were therefore assumed to be products of introgression from Andean beans. Since the present study was focused on Middle American germplasm, the 12 Andean types and the nine outliers were eliminated from the data set and the correspondence analysis was repeated for those accessions that were truly Middle American in origin (Fig. 1) . Elimination of the Andean types and the outliers resulted in a total of 205 polymorphic bands. The first, second, and third dimensions of the subsequent analysis explained 14.48, 4.95, and 2.96% of the variation, respectively. In MCA, these percentages describe the relative importance of each dimension but their absolute values are not relevant. The first dimension discriminated principally between groups that corresponded morphologically to the lowland Race M and the highland Races D and J. The second dimension discriminated among highland races, and the third dimension revealed details of the structure within lowland and highland races. Patterns within major groups were sought by observing the structure of the dendrogram created by the correspondence analysis (Fig. 2) and relating this structure to geographic or phenotypic data. Individual accessions were classified into races and groups (Table 1).

View larger version (23K): [in this window] [in a new window]   Fig. 1 Plot of 250 Middle American bean genotypes in Dimensions 1 and 2 of the correspondence analysis of RAPD data

View larger version (16K): [in this window] [in a new window]   Fig. 2 Dendrogram based on Multiple Correspondence Analysis of RAPD data, illustrating the relationship among races and subraces of Middle American common bean landraces. Letters refer to classification of accessions into races

View larger version (26K): [in this window] [in a new window]   Fig. 3 Plot of 206 Middle American bean genotypes of Races M and D in Dimensions 1 and 3 of the correspondence analysis of RAPD data

Groups within Races D and J could be defined by the correspondence analysis dendrogram (Fig. 2) and were also discriminated by other traits. Race D divided into two groups which separated principally on Dimension 3 (Fig. 3). These groups could also be discriminated by growth habit, geographic distribution, and seed type. Group D1 was the larger and was composed of the genotypes which most closely fit the morphological description of Race D proposed by Singh et al. (1991a). Of 60 genotypes of this group, 66% were of Type 3 and only 28% of Type 4. Group D1 predominated in the important bean-producing states of Durango, Zacatecas, and Aguascalientes, and 66% of this group originated to the west of 100° W latitude in the dry central plateau (Fig. 4) . A full range of colors and seed types were represented in this group, including pinto, Jacob's cattle, Mexican bayo, and the flor de mayo type. In contrast, Group D2 presented a more limited range in seed types, with typically less attractive seed colors including many black-seeded accessions and several of small seed size. Some of these could easily be confused with Race M landraces. Group D2 also presented a higher proportion (52%) of Type 4 habits that are atypical of Race Durango. Geographically, 70% of this group was found to the east of 100° W latitude and was concentrated at the eastern extreme of the neovolcanic axis in the states of Puebla, Hidalgo, and Veracruz, and extending down into Oaxaca (Fig. 4). Compared with Group D1, accessions of D2 occurred with greater frequency on volcanic soils, reflecting the origins of the latter in the mountainous areas of eastern Mexico. An examination of phaseolin types present in the two Race D groups revealed differences in constitution. While S, Sb, and/or Sd types were found in both groups, an unusual phaseolin designated "M9" was present mostly in group D1, in about 25% of the accessions for which data were available.

View larger version (31K): [in this window] [in a new window]   Fig. 4 Geographic distribution within Mexico of Race Durango subraces. Sites of 93 accessions for which coordinates were available were mapped. Areas enclosed by dark lines represent mountain ranges

View larger version (30K): [in this window] [in a new window]   Fig. 5 Geographic distribution within Mexico of Race Jalisco accessions. Sites of 29 accessions for which coordinates were available were mapped. Areas enclosed by dark lines represent mountain ranges

Relative Degrees of Diversity
For purposes of comparing diversity, major races as well as groups within races were considered, with the exception of J2 which were few in number (Table 2) . Races J and M were similarly diverse and significantly more so that Races D or G, the latter of which was the least diverse of all. Groups M1, M2, D1, and D2 were all similarly diverse.

	Discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

Does the variability within Race M reflect other relevant genetic diversity that can be exploited, especially for yield potential? Many crosses have been made in the past between Type 2 black beans and Central American beans of other colors, but little or no genetic gain was reported in crosses among Race M genotypes (Singh et al., 1989). In Central America, some modest genetic gain in yield potential has been registered in small reds and small blacks, but this was obtained with great difficulty, probably due to problems of genetic linkages between seed color genes and genes for desirable traits (Beebe et al., 1995). Many Central American genotypes do not yield well outside of that region, and this might also confound attempts to recognize superior progeny in populations selected in other regions. On the other hand, Subrace M1 already presents some of the highest yield potential in bush beans. Experience suggests that if additional gain in yield potential is to be made in crosses between these two subraces of Race M, it will be with some difficulty. However, given the discrimination among these two groups, other data related to race structure such as disease resistance patterns (Beebe and Pastor-Corrales, 1991) should be reviewed in this light.

In the formation of the bean core collection (Tohme et al., 1994), accessions which were known to be recent introductions to a region were eliminated from consideration so as to focus on diversity of true landraces. This practice eliminated many of the Type 2 black genotypes which are popular for commercial production in Brazil, Chile, Cuba, Argentina, the USA, and other countries outside of Mexico. Most small-seeded landraces from the Andean zone and the Caribbean clustered with the Central American Subrace M2. This suggests that communication of Central America with the Caribbean and/or the Andean zone is more ancient than interchange of these latter regions with Mexico. For example, Gepts and Bliss (1986) have reported on the movement of bean germplasm between Central America and northern Colombia. Archaeological evidence suggests that the introduction of Middle American beans into the Andean zone occurred in pre-Columbian times (Kaplan and Kaplan, 1988; Towle, 1961). On the basis of the present evidence, this probably occurred from Central America. However, no small-seeded accessions from Cuba were included. In Cuba, small-seeded germplasm was traditionally planted in the western part of the island. This should be compared with Subraces M1 and M2 to determine its origin.

The practical implications of distinct subraces of Race D germplasm should be investigated. Much of the commercial bean production in Mexico is found in the states of Durango, Zacatecas, and Aguascalientes, and much of the research with Race D genotypes has focused on germplasm of group D1 from that region. Germplasm of Subrace D2 from the eastern extreme of the volcanic axis may offer useful variability in agronomic traits that has not yet been recognized. Likewise, studies of Race J have focused on climbing beans from Jalisco and neighboring states. Climbing beans from the states of Oaxaca and Chiapas in the south of Mexico have not been properly explored for their potential value in breeding programs.

The geographic distribution of races and subraces in Mexico implies a relationship between the major topographical features of Mexico and the evolution of cultivated common bean. Most accessions of Race J are found in and around the volcanic axis, and extending into the Oaxacan highlands to the south. Subrace D1 occurs most frequently to the north of the volcanic axis in the dry highland plateau. Subrace D2, on the other hand, seems to occupy a different niche in the mountainous region at the eastern end of the volcanic axis, and in the highlands of Oaxaca. The races and groups of Mexican bean germplasm appear to converge in the state of Puebla, which is a region of particularly broad diversity.

Further to the south, the highlands of Chiapas and Guatemala represent an ecological zone that is largely isolated from other cool temperature bean growing regions. On the north, it is limited by the isthmus of Tehuantepec, with a maximum altitude of about 1000 m above sea level. To the south the altitude drops gradually to about 100 m above sea level in Nicaragua. Highland adapted beans would be unable to migrate readily into or out of the Chiapas-Guatemala region. This relative isolation could have led to the evolution of unique populations of climbing beans as observed in the present study. We have repeated this comparison with a second sample of accessions from this region and have found a consistent difference between germplasm from Guatemala and central Mexico. The geographic isolation and the genetic distinction between Race J and the climbers of Guatemala argue in favor of considering the accessions from Guatemala and southern Mexico as a separate race. Race G represents genetic variability that is little understood. We noted that it is possible that some internal variability may exist within this race but this is still uncertain. In fact, even Race G does not include all the Guatemalan climbing beans, since some of these clustered in Group M2, and others as outliers of Race J. Therefore, Guatemalan climbing beans as a whole are unusually diverse. On the basis of DNA analysis, Guatemalan wild beans have also proven to be distinct from Mexican wild beans (Tohme et al., 1996). Unfortunately, detailed passport data on the cultivated Guatemalan accessions is mostly unavailable, and therefore it is not possible to relate the groups formed to more specific environments. However, the fact that one landrace from this group has already been widely adopted as a cultivar in Rwanda suggests that this germplasm could be useful. Recent data indicate that this germplasm presents a high frequency of accessions resistant to certain races of Phaeoisariopsis griseola (Sacc.) Ferrais. PI181996, an important source of rust resistance, is also from Guatemala (Stavely, 1990) but is of unknown genetic classification. Further studies should reveal to what extent this variability is unique and useful to enrich existing breeding programs.

Diversity could be loosely related to growth habits predominant within each group. Race J, which is predominantly Type 4 habit, was the most diverse, followed by Type 3 habit (in Race D and the Subrace M2). Subrace M1, which presented the highest proportion of habit Type 2, was somewhat less diverse. Although Race G climbers were less diverse, Guatemalan climbers as a whole fell into at least three races or groups of races. The greater diversity of climbing and Type 3 beans was in fact one of the assumptions which was used to select the bean core collection (Tohme et al., 1994).

In the past, phaseolin has been an important evolutionary marker. It is therefore appropriate to compare the results with phaseolin and those with RAPD analysis. Nearly all cultivated Middle American beans present S phaseolin or some variant thereof (Koenig et al., 1990; Gepts, 1988). Why has the S phaseolin or its variants dominated in Middle American cultivars, considering that as many as 19 other phaseolins exist in Middle America (Romero Andreas and Bliss, 1985; Gepts, 1988; Toro et al., 1990; our unpublished data) which presumably could have been included in populations that were domesticated? Three hypotheses can be proposed. First, Gepts (1988) suggested that S phaseolin cultivars were domesticated in Jalisco and Guanajuato states of Mexico. Subsequently S type beans would have diffused to other regions where variants for plant and seed type and local adaptation were selected. In this scenario, the different races should be generally similar in their genomes, differing essentially in a few key genes for those traits that were selected. However, RAPD analysis of tropical and temperate races demonstrates quite discrete differences in genomes, suggesting independent domestication events of distinct wild populations. A second hypothesis suggests that S or S variants were domesticated several times. Although S types are widely distributed in wild beans (Toro et al., 1990), only in the region of Jalisco and Guanajuato are they a predominant type. Therefore, the probability that S types were domesticated repeatedly and to the exclusion of other phaseolin types is low. A third hypothesis is that the S type could have been domesticated in one site (possibly Jalisco) from which primitive cultivars diffused to other regions, and through intermating with local populations of wild or cultivated bean, it became the dominant type. This presupposes that some selective pressure favored S type in segregating populations, perhaps through linkage to readily visible traits that were selected consciously by early bean cultivators. Genetic studies of domestication traits have found factors for seed size linked to the phaseolin gene family (Nodari et al., 1993; Koinange et al., 1996). Similarly, Hartana (cited in Osborn, 1988) found that backcrossing M1, M2, and M5 phaseolins from Mexican wild beans into a common background resulted in smaller seed than in the recurrent parent with S phaseolin, indicating an advantage for S type among Middle American phaseolins. The phaseolin locus is also linked to the P gene which confers white seed (Bassett, 1991). A genetic association with these traits could explain the selective advantage of S phaseolin and its prevalence over other phaseolin types. In this scenario, an S type domesticate would have served as a source of certain domesticated traits for several populations of cultivated bean which derive most of their genome from independent populations of wild bean. The domestication process could then have advanced within the otherwise independent populations, creating the races as we know them. This scenario implies that outcrossing of common bean over long periods in a wild–weed–crop complex, albeit at low rates, would have played a significant role in bean domestication and evolution. In the early days of incipient agriculture, conditions favoring such intermating in wild–weed–crop complexes were probably common (Beebe et al., 1997). In light of the foregoing, the existence of M9 phaseolin in about 25% of Group D1 is of interest. Why does this group present both S and M9 phaseolins? Could the M9 phaseolin be a remnant of an earlier domestication event that has not yet been totally displaced by S type?

An important step to elucidate the evolutionary relationship among races and groups would be to compare these with populations of wild bean from Mexico and Central America. This could reveal if the genomes of these races or groups might be derived largely from different wild populations, as might be suggested by discrete molecular groups. For example, comparisons of DNA from Guatemalan climbing beans and local wild bean populations could elucidate whether or not these populations were involved in a primitive selection process.

The many polymorphisms which are the basis of the molecular analysis are the result of the accumulation of numerous mutations over time. The subsequent results revealed by the statistical analysis thus reflect the long-term, broad evolutionary trends of the species. In this context, the magnitude of molecular differences should be correlated with the evolutionary time span over which divergence occurs, which in turn should reflect on the probability that genes influencing a given trait in two genotypes are the same gene, or different genes that can be recombined. The results presented here thus should orient plant breeders in their search for distinct genes that can be recombined and result in genetic gain.

	Conclusions

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion Conclusions REFERENCES

 
Use of the bean core collection as the base from which to subsample for molecular analysis has permitted a more integral view of the Middle American gene pool. Genetic relationships among and within the three Middle American races defined previously have been further resolved by RAPD analysis. Although much of the Middle American germplasm fits the description of three races, the Middle American gene pool is in fact more complex. In particular, the regions that include Guatemala and the states of Oaxaca and Chiapas in Mexico appear to hold important genetic diversity which has yet to be properly studied. Likewise, the eastern extreme of the volcanic axis in Mexico may be a source of variability that has not been well exploited.Basset 1991; Centro Internacional de Agricultura Tropical. 1987; Centro Internacional de Agricultura Tropical. 1993; Centro Internacional de Agricultura Tropical. 1993

	ACKNOWLEDGMENTS

 
We express our gratitude to the University of Wisconsin and the International Center of Tropical Agriculture for their support of the research herein reported. We thank colleagues at CIAT for reviewing this manuscript, Patricia Zamorano and Isabel Cristina Giraldo for secretarial assistance, and Carlos Jara for help with disease screening.

Received for publication February 22, 1999.

	REFERENCES

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