Published online 26 August 2005
Published in Crop Sci 45:1951-1957 (2005)
© 2005 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
PLANT GENETIC RESOURCES
Genetic Relationships and Diversity Revealed by AFLP Markers in Mexican Common Bean Bred Cultivars
R. Rosales-Sernaa,
S. Hernández-Delgadob,
M. González-Pazb,
J. A. Acosta-Gallegosc and
N. Mayek-Pérezb,*
a Programa de Frijol, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias (INIFAP), Campo Experimental Valle de México, Apartado Postal 307, 56101, Texcoco, Mexico
b Centro de Biotecnología Genómica-Instituto Politécnico Nacional, Blvd. del Maestro esq. Elías Piña s/n, Col. Narciso Mendoza, 88710, Reynosa, Tamaulipas, Mexico
c INIFAP-Campo Experimental Bajío, Apartado Postal 112, 38000, Celaya, Mexico
* Corresponding Author (nmayek{at}ipn.mx)
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ABSTRACT
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Landraces and bean (Phaseolus vulgaris L.) cultivars grown in Mexico are diverse, as are consumer preferences and agroecological production environments. Mexican common bean cultivars were analyzed using amplified fragment length polymorphism (AFLP) fingerprinting to examine the genetic relationships within and among races, based on the genotyping of 112 bred cultivars developed in Mexico. Molecular analysis of dry bean germplasm will be useful to corroborate previous cultivar characterizations and establish the genetic basis of improved germplasm, to facilitate the use of that diversity, and to implement the use of markers in selection. Germplasm included 111 cultivars belonging to Mesoamerica (25), Jalisco (39), Durango (28), and Nueva Granada (19) races, which are commonly cultivated throughout the bean-producing areas of Mexico. A Mexican P. coccineus species cultivar (Blanco Tlaxcala) was also included for comparison. Broad genetic diversity was found within bean races, and diversity values between races were similar. Most of the Nueva Granada germplasm was clearly different from that of all other races, whereas the P. coccineus cultivar was distinct from all P. vulgaris cultivars. A dendrogram based on the AFLP analysis did not clearly match with that made on the basis of racial classification. This mismatch was probably due to genetic recombination between Andean (Nueva Granada) and Mesoamerican (Jalisco, Durango, and Mesoamerica) gene pools. Utilization of contrasting parents for specific crosses has also contributed to broadening the genetic basis of common bean.
Abbreviations: AFLP, amplified fragment length polymorphism • EDTA, ethylenediaminetetraacetic acid • ICAMEX, Instituto de Investigación y Capacitación Agropecuaria, Acuícola y Forestal del Estado de México, Mexico • INIFAP, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias-México • ISSR, inter-simple sequence repeats • PCR, polymerase chain reaction • RAPD, random amplified polymorphic DNA • RFLP, restriction fragment length polymorphism • UPGMA, unweighted paired-grouping method with arithmetic averages
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INTRODUCTION
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COMMON BEAN is a globally important crop that originated in the Americas. In Mexico, common bean breeding started in 1943, when native germplasm was first collected. The first bred cultivars were directly developed from outstanding landraces (Voysest, 2000). Recombination between native outstanding cultivars and exotic germplasm was then performed (Cárdenas, 2000). From 1943 to 2000 the Bean Breeding Program of INIFAP (Instituto Nacional de Investigaciones Forestales, Agricolas y Pecuarias) from Mexico released more than 120 bred cultivars for all the producing areas in the country (Rosales-Serna et al., 2004) to match agroecological differences and consumer demands. The developed cultivars are diverse in their growth habit, maturity, and seed type. In Mexico, the genetic base of common bean has been broadened using genetically contrasting parents in crossing nurseries (Acosta-Gallegos et al., 2000).
Common bean diversity has been classified into two major gene pools, Middle American and Andean. Each pool can be further subdivided into three races (Singh et al., 1991b). The main races grown in Mexico are the Middle American: Mesoamerica, Jalisco, and Durango, as well as the Nueva Granada race from the Andean pool. This last race was probably introduced into Mexico in pre-Columbian times.
The knowledge of genetic diversity patterns can increase the efficiency for conservation, utilization, and genetic improvement of common bean (Beebe et al., 2000; Rosales-Serna et al., 2003). Different methodologies and traits, such as morphological (Cárdenas, 1984; Singh et al., 1991a; Rosales-Serna et al., 2003), biochemical (Singh et al., 1991a, 1991c), and molecular (Beebe et al., 2000; Metais et al., 2000; Rosales-Serna et al., 2003) have been suggested for the evaluation of genetic diversity in common bean. Bean cultivars have also been classified by seed type, growth habit, morphology, phenology, and reaction to photoperiod (Voysest, 2000; Rosales-Serna et al., 2003). Molecular markers are useful for cultivar identification, due to the fact that they are not influenced by variable environmental conditions or plant phenology, and are a basis for discriminating among cultivars with similar morphological characteristics (Beebe et al., 2000). Detection of polymorphisms among and within germplasm collections could provide insight into genome evolution, origin of cultivated species, and the current level of diversity in agricultural crops (Freyre et al., 1996).
The AFLP analysis provides a higher level of polymorphism than random amplified polymorphism DNA (RAPD) or restriction fragment length polymorphism (RFLP) (Pejic et al., 1998). Amplified fragment length polymorphisms are based on selective and semiquantitative PCR amplification of restriction fragments digested from total genomic DNA. Fragments generated by digestion of DNA with a combination of two restriction endonucleases are linked to suitable adapters and, thereafter, linked DNA fragments are amplified selectively with different primer combinations (Vos et al., 1995). The RFLPs (Becerra-Velásquez and Gepts, 1994; Duarte et al., 1999; Metais et al., 2000; Maciel et al., 2001), RAPDs (Haley et al., 1994; Nienhuis et al., 1995; Moura-Duarte et al., 1999; Beebe et al. 2000; Metais et al., 2000), inter-simple sequence repeats (ISSRs) (Rosales-Serna et al., 2003), and more recently, AFLPs (Tohme et al., 1996; Caicedo et al., 1999; Maciel et al., 2003; Pallottini et al., 2004) have been successfully used for the description of diversity in common bean. In Mexico, the characterization of dry bean germplasm by AFLP is necessary to corroborate previous findings in cultivar characterization to establish the genetic basis of improved germplasm, to facilitate the use of that diversity, and to implement in the near future the use of markers in selection. A previous report showed close association between inter-simple sequence repeats (ISSR) analysis and morphological characterization in the field (Rosales-Serna et al., 2003). The objective of this research was to examine the genetic relationships within and among races based on the genotyping of 112 bean bred cultivars developed in Mexico.
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MATERIALS AND METHODS
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Plant Materials
One-hundred and twelve common bean improved cultivars developed in Mexico from 1943 to 2000 were included in this study. One-hundred and six cultivars were developed by INIFAP, whereas the other six were released by other institutions (Rosales-Serna et al., 2004) (Table 1). The germplasm included 111 P. vulgaris cultivars and one cultivar, "Blanco Tlaxcala," of P. coccineus. The P. vulgaris germplasm was previously classified into four genetic races following the description of Singh et al. (1991b): Mesoamerica (25 cultivars), Durango (28), Jalisco (39), and Nueva Granada (19). Bred cultivars have been developed for most producing areas of Mexico, and the higher number of cultivars in the Jalisco race suggests that the breeding effort started in Central Mexico (Cárdenas, 2000), part of the natural area of distribution for this race (Singh et al., 1991b).
AFLP Analysis
Total genomic DNA was extracted from 2.5 g of a bulk of young leaves collected from 10 15-d-old plants per cultivar using the method of Dellaporta et al. (1983). The DNA concentrations were visually estimated on agarose gels by comparison with standard 
phage digested by HindIII, and AFLP protocol was performed following Vos et al. (1995). Approximately 250 ng of genomic DNA were digested with 10 U of each EcoRI and Tru91 enzymes at 37°C for 4 h and incubated at 70°C for 15 min. The DNA fragments were linked to EcoRI and MseI adapters at 15°C overnight. After preselective amplification by PCR using the nucleotide A, a second selective amplification by PCR was performed with four combinations of EcoRI and MseI primers. The AFLP reactions were denatured by boiling with formamide buffer [98% formamide, 10 mM EDTA (ethylenediamine tetra-acetic acid), bromophenol blue (3',3'',5',5''-tetrabromophenolsulfonephthalein), xylene-cyanol]. All samples were electrophoresed on 6% denaturing polyacrylamide gels (35 x 45 cm) for 3 h at 2000 V and then revealed by using the manufacturer's instructions in the Silver Sequence Staining Reagents kit (Promega, Madison, WI) manual.
Data Analysis
A binary matrix reflecting the presence (1) or absence (0) of each AFLP band was generated for each cultivar. Genetic distance among cultivars was estimated using the simple matching coefficient (Skroch et al., 1992). The distance matrix generated was used to obtain a dendrogram by the unweighted paired-grouping method with arithmetic averages (UPGMA) method using STATISTICA 5.0 (StatSoft, Inc., Tulsa, OK). Diversity values based on phenotype frequency were calculated for each bean race using Nei's unbiased distances (Nei, 1978):
where pi is the frequency of the presence or absence of a band in the population, and n is the number of individuals analyzed. Diversity values were calculated as
where r is the number of markers revealed by each primer or primer combination. Diversity values for each single bean race were calculated as the mean hi value over all markers. The similarity matrix was also used to perform a hierarchical analysis of molecular variance (Excoffier et al., 1992) using ARLEQUIN 1.0 (Schneider et al., 1997). The number of permutations for significance testing was set at 1000 for all analyses.
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RESULTS
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The four AFLP primer combinations produced a total of 464 bands. The number of bands amplified by primer combination varied from 100 to 130. A total of 344 bands were polymorphic across the entire sample. The percentage of polymorphic markers varied from 71.0 to 76.2% (Table 2). Analysis of molecular variance was performed among and within races of common bean (Table 3). A small but significant proportion of the total variation detected (7%) was attributed to differences between bean races, although the greatest differences were found within genetic races. Nueva Granada race showed the lowest variation (19.3%) in comparison with other races. All four primer combinations produced similar estimates of intrarace population diversity. Genetic diversity levels fluctuated from 0.28 (Mesoamerica race) to 0.33 (Durango race), whereas the average level of diversity was 0.31 (Table 4).
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Table 4. Partitioning of diversity (H) between common bean races of Phaseolus vulgaris for four AFLP primer combinations.
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Dendrograms produced by the UPGMA method showed similar relationships among the 112 bean cultivars, since AFLP analysis readily separates P. vulgaris cultivars from P. coccineus. However, unclear separation between cultivars on the basis of their genetic race was found, since cultivars from Mesoamerica, Jalisco, and Durango races were included in a single cluster throughout the dendrogram, although most of the Nueva Granada cultivars were grouped separately from all other cultivars (Fig. 1). Genetic dissimilarity between the two Phaseolus species was >12%, while within P. vulgaris, genetic dissimilarities varied from 4 to 11%. The UPGMA dendrogram (Fig. 1) showed seven different clusters that included variable numbers of cultivars and the P. coccineus as outlier. Clusters 1 and 5 included cultivars from the four genetic races; Cluster 2 grouped only cultivars from Nueva Granada race; Cluster 3 included genotypes from Mesoamerica, Durango, and Nueva Granada races; Cluster 4 grouped Mesoamerica and Jalisco cultivars; and Cluster 6 grouped germoplasm from the three Mesoamerica races. Finally, Cluster 7 included the P. coccineus cultivar Blanco Tlaxcala (Table 5; Fig. 1).
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Fig. 1. Unweighted pair-group method with arithmetic averages cluster analysis for 112 bean cultivars based on 464 AFLP markers (PC = P. coccineus, M = Mesoamerica, J = Jalisco, D = Durango, NG = Nueva Granada).
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When subgroups of cultivars were analyzed on the basis of racial adscription, a clear separation of cultivars was found, with separation corresponding to pedigrees (Table 1; Fig. 2). The AFLP analysis separated race Jalisco germplasm on yellow and flor de mayo seed types (Group A) from recombinant cultivars (black, garbancillo, pinto, and ojo de cabra seed types) (Group B) (Fig. 2a). Mesoamerica cultivars (Fig. 2b) were separated on former landrace cultivars (Group A) from bred cultivars (Group B), most of them opaque black-seeded cultivars. Durango germplasm was subdivided into two clear groups of cultivars: former landraces such as Siechi 73, Bayo 159, and other Bayo cultivars (Group A), and pinto and black-seeded cultivars (Group B) (Fig. 2c). Finally, the Nueva Granada cultivars were separated mainly on the basis of their genetic status: bred cultivars such as azufrado and cacahuate seed types (Group A), and former landraces such as canaries (Group B) (Fig. 2d).
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Fig. 2. Unweighted pair-group method with arithmetic averages cluster analyses for 112 bean cultivars based on AFLP markers and genetic race of origin (PC = P. coccineus).
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DISCUSSION
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The AFLP fingerprinting produced an unclear separation among bean cultivars as compared with racial classification. Only germplasm belonging to the Nueva Granada race was grouped together after UPGMA cluster analysis. Results suggest that recombination among cultivars in the three Middle American races (Mesoamerica, Jalisco, and Durango) has occurred to incorporate resistances to biotic and abiotic stresses and, as a consequence, the genetic base of bred cultivars was broadened. Results are similar to previous reports, which assumed that outliers in Mesoamerican common bean diversity characterizations are produced by introgression from Andean bean (Beebe et al., 2000). Influence of artificial selection, natural out-crossing, and deliberate or unconscious errors in pedigree and line records was also possible. In the case of cultivars of the race Nueva Granada, improvement has focused on the recombination of outstanding elite germplasm within the race and seed class. Our results confirmed the fact that the Andean and Mesoamerican Phaseolus genotypes are distinct from one another, although the distinctions between gene pools were not as clear as previously reported (Becerra-Velásquez and Gepts, 1994; Maciel et al., 2001). It is worth mentioning that at least 20 cultivars ascribed to the Durango and Jalisco races have Nueva Granada germplasm in their pedigree, mainly the local canaries used as sources of rust resistance and earliness.
Rosales-Serna et al. (2003) performed an ISSR analysis on most of the germplasm analyzed in this work. They found a close association between morphological classification and genetic analysis, and suggested that the loci that control molecular and morphological characteristics are closely associated (Moura-Duarte et al., 1999). We suggest that the tendency toward a genetic continuity among Mexican bean cultivars resulted from the recombination among few specific and distinct parents from the three major bean races cultivated in Mexico (Mesoamerica, Jalisco, and Durango) and the Nueva Granada race. If so, the genetic continuity among bred cultivars and landraces may be the result of repeated use of landraces in the breeding process and from the exchange of cultivars among geographical regions.
Despite the high number of bred cultivars released in Mexico, many cultivars were not adopted by farmers, either due to lack of seed or because commonly grown landraces that are well adapted to poor soils, restrictive environmental conditions, and low inputs, which are common to remote rainfed areas of Mexico, are locally preferred. Those landraces represent a low portion of the total bean consumption. Preferences of Mexican urban consumers can very well contribute to the reduction of the genetic diversity in landraces, since bred cultivars are preferred for their uniformity in seed characteristics (mainly type and color of seed) and those bred cultivars that included appropriate marketing characteristics and great agronomic adaptation are preferred and commonly cultivated in Mexico and, thus, well-adapted landraces and bred cultivars are being displaced. For those reasons, the conservation, characterization, and use of Mexican bean genetic resources must be improved and studied for the optimal knowledge and exploitation.
In this work, the studied germplasm included four common bean races that are commonly cultivated in Mexico: Mesoamerica, Jalisco, Durango, and Nueva Granada. Each race included different seed types, which is one of the main marketing criteria used to meet the demand of consumers in Mexico (Castellanos et al., 1997). For example, Mesoamerica race mainly included opaque black-seeded cultivars, while the Durango race included bayo and pinto types; Nueva Granada included canarios, azufrado-peruanos, and red stripped (cacahuate) seed types, whereas the Jalisco race was the most variable on seed-type basis (Rosales-Serna et al., 2003). It was evident that Mexican bean breeders have focused on the development of specific cultivars according to the requirements that are demanded by Mexican consumers and by the environment where they are grown. The variation observed within Nueva Granda race was lower than that of the other races, but still significant, as was also pointed out by Pallottini et al. (2004), who found the azufrado-peruano to be distinct from other types in this race. The first Nueva Granada landraces, the canarios, were introduced into Mexico in pre-Columbian times. Actually, the first cultivar developed through hybridization in central Mexico was Bayomex, a type I Nueva Granada race cultivar.
The limitations imposed by bean marketing in Mexico resulted in the narrowing of the genetic base on opaque black (Mesoamerica) and azufrado (Nueva Granada) bean types, mainly because of the recurrent use of parents in each grain type, parents of similar morphology and agronomic traits, and the strong artificial selection based on grain type. Bean cultivars produced for the highlands (central and northern regions) have exploited the native genetic diversity and Nueva Granada germplasm to enhance earliness and disease resistance in the new bred cultivars (Acosta-Gallegos et al., 2000). No dwarf lethals have been observed in those intergenepool crosses in the highlands (Singh and Gutiérrez, 1984). It might be that the DL1DL2 system is not complemented or that it needs higher temperature for full expression.
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CONCLUSIONS
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Trends in the Mexican market, consumer preferences and the recombination among genetic races contributed to maintenance and, in some cases, to broadening the common bean genetic base. Our results demonstrated that diversity of Mexican common bean cultivars has been increased by recombination between Andean and Mesoamerican gene pools. The utilization of contrasting parents for specific crosses has contributed to broadening the genetic basis of common bean. Finally, the knowledge of genetic diversity in Mexican bean germplasm will provide bean breeders with a starting point in designing crosses using contrasted and complementary parents to broaden the genetic basis within the different commercial classes of bean grown in Mexico.
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ACKNOWLEDGMENTS
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The authors are grateful to the Instituto Politécnico Nacional (Project 20040311) and FOMIX-Tamaulipas (Project TAMPS-2003-C03-06) for partial funding to this work, and to Dr. Mireille M. Khairallah for critical reading of the manuscript and helpful discussions.
Received for publication October 2, 2004.
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ABSTRACT
INTRODUCTION
