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Crop Science 42:2128-2136 (2002)
© 2002 Crop Science Society of America

CELL BIOLOGY & MOLECULAR GENETICS

Microsatellite Repeats in Common Bean (Phaseolus vulgaris)

Isolation, Characterization, and Cross-Species Amplification in Phaseolus ssp.

E. Gaitán-Solísa, M. C. Duquea, K. J. Edwardsb and J. Tohme*,a

a Biotechnology Research Unit, Centro Internacional de Agricultura Tropical (CIAT), A.A. 6713, Cali, Colombia
b Long Ashton Research Station of the Institute of Arable Crops Research (IACR), Bristol, UK

* Corresponding author (j.tohme{at}cgiar.org)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Phaseolus beans are distributed worldwide and are cultivated in the tropics, subtropics, and temperate zones. The common bean is the most important grain legume for direct human consumption in the world. The objectives of this study were to isolate microsatellite repeats and to establish their discriminatory power (DL) to be used in bean diversity characterization and mapping. We isolated, cloned, and sequenced genomic DNA fragments that contained microsatellite loci from three genomic libraries of Phaseolus vulgaris L. The polymorphism of the microsatellites was evaluated in a panel of 21 P. vulgaris genotypes made up of cultivated and wild beans from the Mesoamerican and Andean pools, and nine genotypes from four Phaseolus species. The number of alleles per microsatellite locus ranged from 1 to 14, with an average of 6 alleles per primer pair. Almost all the microsatellite loci showed high levels of discriminatory power, with the highest value being 0.94. These results indicate that microsatellites can be valuable genetic markers for assessing genetic diversity in the P. vulgaris. The high levels of polymorphism of these new bean microsatellites and their wide cross-species transportability make these new markers useful for mapping and molecular characterization of Phaseolus species.

Abbreviations: SSR, simple sequence repeats • bp, base pairs • PCR, polymerase chain reaction • DL, Discriminatory power


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
PHASEOLUS BEANS are distributed worldwide. They are cultivated in the tropics, subtropics, and temperate zones. Of the 50 Phaseolus species that have been described (http://www.ncbi.nlm.nih.gov/Taxonomy/taxonomyhome.html; verified May 7, 2002), only five are cultivated for human consumption. Of these, the common bean, P. vulgaris, is the most widely grown throughout the world. The remaining four species are the runner bean (P. coccineus L.), year-bean (P. polyanthus Greenm), lima bean (P. lunatus L.), and tepary bean (P. acutifolius A. Gray) (Debouck, 1991).

Microsatellites (also known as simple sequence repeats, SSRs, or hypervariable sequences) are arrays of short tandem repeat motifs of 1 to 5 base pairs in length. These single-locus markers are characterized by their hypervariability, abundance, reproducibility, Mendelian mode of inheritance, and codominant nature (Scott et al., 2000). In addition, microsatellites occur frequently and randomly in eukaryotic genomes (Tautz and Renz, 1984) and are highly informative markers (Weber, 1990). Simple sequence repeats (without interruption) are reported to be more variable than restriction fragment length polymorphisms (RFLPs) or random amplified polymorphic DNA (RAPDs) and have been widely adopted for genetic studies in humans (Dib et al., 1996) and other mammals (Sun and Kirkpatrick, 1996), as well as in plants such as soybean [Glycine max (L.) Merr.] (Rongwen et al., 1995), Avicennia marina Forsk (Maguire et al., 2000), tea tree (Melaleuca alternifolia Maiden) (Rossetto et al., 1999), and cassava (Manihot esculenta Crantz) (Chavarriaga-Aguirre et al., 1998; Mba et al., 2001).

In the past, SSRs have been expensive to develop and thus often limited to applications to the major commercial crops (Scott et al., 2000). The first report (Condit and Hubbell, 1991) on the isolation and cloning of plant microsatellites was for tropical tree species. Microsatellites can be isolated directly from total genomic DNA libraries, cDNA libraries, libraries enriched for specific microsatellites (Maguire et al., 2000), or from sequences deposited at the GenBank as previously reported in Phaseolus vulgaris and Vigna (Yu et al.,1999). Several methods have been used for isolating plant microsatellites, and these usually involve the construction of small-insert libraries, screening by hybridization, sequencing, primer design, and loci amplification. The low efficiency obtained with such libraries has led to the development of more efficient strategies. Precloning enrichment methods, such as that used by Edwards et al. (1996), involve the endonuclease digestion of the genomic DNA, followed by ligation of adapters to create DNA fragments with defined sequences at both ends. Microsatellite-containing fragments are then enriched by hybridizing to membranes with bound oligonucleotides. These fragments are then isolated and cloned. Another major advantage in the use of SSRs as molecular genetic markers is that the sequences flanking the repeat regions are highly conserved and therefore suitable for the design of polymerase chain reaction (PCR) oligonucleotide primers for amplification of the repeat loci (Maguire et al., 2000). They are therefore very useful in germplasm characterization and molecular genetic mapping. The objectives of the study reported here were: (i) to obtain microsatellite sequences in Phaseolus vulgaris by means of enrichment techniques to produce efficiently a larger number of SSR markers for this economically important species; (ii) determine the level of polymorphism of microsatellite on a set of wild and cultivated P. vulgaris accessions; and (iii) to examine the ability of the SSR primer pairs to amplify PCR products from a range of Phaseolus species.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Plant Materials and DNA Isolation
Three enriched, small-insert libraries were constructed from P. vulgaris: Library 1 from the Andean accession G 4494 (Diacol-Calima) at the Long Ashton Research Station of the Institute of Arable Crops Research (IACR, Bristol, UK); Library 2 (dinucleotide SSRs) and Library 3 (trinucleotide SSR) from the Andean accession G19833 at CIAT (Cali, Colombia). Total genomic DNA was isolated from leaf tissues by means of the protocol for bean DNA extraction followed by Tohme et al. (1996).

Construction of an Enriched Microsatellite Library of Phaseolus vulgaris
We followed the procedure described by Edwards et al. (1996) to construct all three enriched-microsatellite libraries. Two hundred nanograms of genomic DNA was digested with RsaI. A MluI adaptor (consisting of a 21- and 25-mer primer) was ligated to the digested fragments. Filter-immobilized oligonucleotides, representing CT20 and GT20 for both Library 1 and 2 and ATT14, CAG14, CAA14, and ACG14 SSR marker classes for Library 3, were used to select genomic fragments containing SSRs. Enriched fragments for microsatellite sequences were amplified by PCR, using the 21-mer adaptor primer. The enriched DNA was then digested with MluI and ligated into a modified pUC19 vector, pJV1 that contains a BssHI site. Plasmids were introduced into DH5{alpha}, and transformed cells plated onto L-agar plates containing 100 µg mL-1 of ampicillin and 50 µg mL-1 of X-galactosidase. Following incubation overnight at 37°C, single colonies were transferred into microplates for long-term storage at 80°C.

Hybridization Screening of Enriched Libraries
The genomic libraries were screened by transferring clones onto nylon membranes and probing with a mixture of radio-labeled oligonucleotides (CT20 and GT20) and (ATT14, CAG14, CAA14 and ACG14). Membranes were prewashed with hybridization buffer [6 x SSC—1 x SSC is 0.15 M NaCl plus 0.015 M sodium citrate pH7, 0.25% (w/v) dried milk powder, 0.01% (w/v) sodium dodecyl sulfate (SDS), and 25 mM Na-phosphate] at 50°C for 4 h. Following this, 100 ng of the labeled oligonucleotides were added and hybridization proceeded at 50°C overnight for dinucleotides SSR and 65°C for trinucleotides SSR. Membranes were washed at 60°C (dinucleotide SSR) and 65°C (trinucleotide SSR), five times for 5 min each time, with 150 mL of a mixture of 2 x SSC and 0.1% SDS, and exposed to X-ray film for 2 h. Putative positive colonies were cultured in Luria-Bertani Broth with 100 µg mL-1 of ampicillin. Plasmid DNA was isolated from the culture with the plasmid purification kit (QIAGEN Inc., Valencia, CA). Sequencing of the purified plasmid DNA fragments was done by means of M13 primer sites and the BigDye Terminator Cycle Sequencing Kit (PE Applied Biosystems, Foster City, CA), and the product was run with an Applied Biosystem ABI 377 sequencer.

Primer Design
Each sequence was aligned against all the other sequences, by the SEQUENCHER program to eliminate redundant clones. Primers were then designed for the unique clones, by means of the PRIMER3.0 software program (available at http://www-genome.wi.mit.edu/cgi-bin/primer/primer3_www.cg; verified June 26, 2002). The selected parameters included the length of 18 to 22 bp and the annealing temperatures between 55°C and 65°C (optimum 60°C). This software also took care of such criteria as GC content of more than 50%, minimal repetitive DNA within a primer, no extensive palindromes within a primer, and no pairing between primers.

Sequence Homologies
The flanking sequences of 68 microsatellites were compared with GenBank entries at the amino acid level with the BLASTX and at the nucleotide level with BLASTN by means of the default settings from the National Center for Biotechnology Information (NCBI, http://www.ncbi.nlm.nih.gov; verified May 7, 2002). Matches with a score of <2 x 10-4 were considered to be significant. Accession numbers listed correspond to the respective entries in the GenBank Nucleotide Sequence database.

Microsatellite Primer Characterization
A total of 21 P. vulgaris genotypes were used for the evaluation of the primer pairs (Table 1) . These were chosen on the basis of previous AFLP (amplified fragment length polymorphism) diversity results (Tohme et al., 1996). This included 14 wild accessions from CIAT's wild core collection and seven cultivated accessions from the Mesoamerican and Andean pools. In addition, three and two accessions, respectively, P. acutifolius and P. coccineus were also evaluated. Also, two genotypes of wild and cultivated P. polyanthus Greenman (Table 1) and two wild genotypes from P. lunatus were analyzed to check cross-specific amplification, bringing the total number of Phaseolus accessions used in the study to 30.


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  		Table 1. List of Phaseolus vulgaris and other Phaseolus species used in microsatellite assays.

 
The SSRs were first amplified from the P. vulgaris genotypes G19833 and DOR364 to standardize the PCR conditions. The PCR reaction was carried out in a 20-µL final volume containing 20 ng of genomic DNA, 0.1 µM of each of the forward and reverse primers, 10 mM Tris-HCl (pH = 7.2), 50 mM KCl, 1.5 to 2.5 mM MgCl2, depending on the primer combination, 250 mM of total dNTP, and 1 unit of Taq DNA polymerase. The temperature cycling profile involved an initial denaturation step of 2 min at 94°C. This was followed by 35 cycles of 94°C for 15 s, an annealing phase of between 48°C to 65°C (depending on the annealing temperature for the given primer pair) for 15 s, and an extension at 72°C for 15 s. A volume of 6 µL of formamide, containing 0.4% (w/v) bromophenol blue and 0.25% (w/v) xylene cyanol FF, was added to each reaction and denatured. Four microliters were loaded onto 6% (w/v) denaturing polyacrylamide gels (19:1 acrylamide to bis-acrylamide) that contained 5 M urea and 0.5 x TBE. Electrophoresis was at 100-W constant power for 2 to 2.5 h. PCR amplifications were visualized by silver staining according to the manufacturer's guide (Promega Manual, 1995), with some modifications. A list of the primer sequences used for the reactions is given in Table 2 .


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  		Table 2. Properties of the microsatellite primer pairs (organized in alphabetical order) used for reactions in primer characterization.

 
Data Analysis
In this study, we used the value discriminatory power (DL) to compare the efficiency of the microsatellites to differentiate among genotypes. The DL value represents the probability that two randomly chosen individuals show different allelic patterns at the same microsatellite locus, and thus are distinguishable from one another. That is, if pi is the proportion of the population carrying the ith banding patterns at the jth primer, and if pi were calculated for each pattern generated by the primer (Tessier et al., 1999), then DL = 1 - {sum}p2i. This is an extension of the polymorphism information content (PIC) (Anderson et al., 1993), available from the frequencies of the different banding patterns (or genotypes) generated by a primer.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Isolation of SSR Clones
Library 1 (G 4494)
Of the 3936 clones screened with oligonucleotide probes CT20 and GT20, a total of 354 putative positive colonies (9%) were isolated and 267 were sequenced. Of these, 136 (51%) were suitable for designing primers (Table 2). The remainder consisted of redundant clones, those that contained no SSR loci (false positives), and clones in which the SSR loci were too close to the vector linker site to permit primer design.

Libraries 2 and 3 (G19833)
A total of 1007 positive clones were identified for Library 2 (dinucleotide SSR), of which 503 (50%) clones were sequenced. Of these, 13% were suitable for designing primers (Table 2), while 355 (70%) were redundant and 39 (7.7%) were false positives. Also, 224 putative positive clones were not sequenced because double bands were observed when they were amplified by means of vector primers. For the trinucleotide library (Library 3), 3321 positive clones were identified, 86 clones were sequenced which 61 (71%) of these were redundant clones, and almost 13% were false positives. For the last library, only four primer pairs were possible to design. Because of the higher number of redundant clones, false positives and the low number of clones suitable for primer design we did not continue sequencing clones from Library 3. The library enrichment procedure adopted here made searching for microsatellites substantially more efficient, since the percentage of inserts containing a microsatellite repeat was considerably higher than that usually found in non-enriched libraries (data not shown).

Microsatellite Description
Four different dinucleotide repeats were isolated from the Library 1 and three from the Library 2. Of these, the CA repeat was the most common dinucleotide detected in Library 1, representing 84% of all microsatellites. This trend was, however, reversed for Library 2, where the GA dinucleotide repeats accounted for 62.7% of the SSRs. This result would therefore vary from most published reports on SSR isolation from many plant species where the GA repeats are usually consistently more abundant than CA repeats (Powell et al., 1996). Examples include results obtained for Avicennia marina (Maguire et al., 2000) and pine trees (Echt and May-Marquardt, 1997) where the GA motif was the most abundant found. On average, dinucleotide motifs have a higher number of repeats than trinucleotide motifs, their maximum numbers of repeat units being 55 and 9, respectively. This result agrees with those reported for other plants such as tea tree (Rossetto et al., 1999). Dinucleotide AT was the more frequent SSR repeat reported in a previous paper in P. vulgaris and Vigna, followed by GA motifs (Yu et al., 1999). The screening of Library 3 for trinucleotide motifs yielded 87% of positive clones with TGC repeats as the most common perfect trinucleotide motifs founded (2.1%). 2.8% of trinucleotide compound motifs were observed. This result complements previous report on SSR isolation from P. vulgaris (Yu et al., 1999) in which the CCA was found to be the most frequent trinucleotide motif after the dinucleotides AT and GA. The combined three libraries also resulted in the isolation of additional motifs. They included nine tetra-mers (with a maximum of 17 repeat units) where almost all of them were founded as a compounded repeat, one penta-mer, and three hexa-mers. Primer design was suitable for some of them. No sequenced clone was found with the trinucleotide ATT that was used in the enrichment procedure. To date, sequence comparison of enriched clones from the various libraries has shown no evidence for the selective enrichment of specific microsatellite sequences (Maguire et al., 2000). Here, we identified clones containing microsatellites which were not bound to the Hybond N+ membrane (AT and GC), a result also shown by Maguire et al. (2000).

GenBank Sequence Comparison Analysis
The flanking sequences of 68 microsatellites reported in this work were compared with the sequences of the GenBank database. No matches to the microsatellite sequences previously reported by Yu et al. (2000) were found. Nineteen (28%) of the microsatellite flanking sequences showed significant homology at nucleotide level to four microsatellite sequences from P. vulgaris isolated as MADS clones (http//www.ncbi.nlm.nih.gov/, verified June 26, 2002, GenBank number AJ416409, AJ416389, AJ416395, and AJ416396), six cDNA clones and one stress responsive protein from G. max (generated from different stages), and to one clone from Medicago truncatula Gaertner related to a stem development sequence (Table 3) . At the protein level 10 clones (15%) showed significant homology with several clones from Arabidopsis thaliana Heynh. Two clones presented homologies to MADS box proteins from A. thaliana, Pinus radiata D. Don, and Capsicum annuum L. These MADS box genes form a large family active in a wide range of eukaryotic organisms (reviewed in Greco et al., 1997). In plants, the MADS box proteins seem to be mainly involved in the genetic control of flower development (reviewed in Greco et al., 1997). It has been strongly suggested that the regulatory network controlling flower development has been conserved during the evolution of higher plants (Ma, 1994; Theissen and Saedler, 1995)


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  		Table 3. Nucleic acid and protein homologies of P. vulgaris microsatellite clones used in this study with GenBank sequences.

 
PCR Amplification and Visualization of Microsatellites
Two hundred thirteen primer pairs were tested by PCR amplification using as a template the plasmid preparation from which they were obtained, and then they were tested on parental lines. A total of 68 of these produced strong amplification products. These 68 primer pairs were then assayed against the set of cultivated and wild P. vulgaris and other Phaseolus species to test their ability to detect polymorphic loci. The other primer pairs either had no amplifications or yielded fragments of many sizes.

Characterization of Selected Microsatellite Sequences for Phaseolus vulgaris
Sixty-eight primers were used to investigate the polymorphism detected among 21 individuals of P. vulgaris. Of these, 59 were dinucleotide repeats, four were trinucleotide repeats, one a tetranucleotide repeat, one a pentanucleotide repeat, and three were compound repeats (Table 2). Fourteen loci were monomorphic in the materials tested. A total of 584 alleles were detected at the 68 microsatellite loci. The number of alleles per microsatellite locus ranged from 1 to 14, with an average of 6 alleles per primer pair (Table 4) . Also, 1 to 19 banding patterns (between homozygotic and heterozygotic genotypes) were generated. We used the data from the microsatellite loci and their corresponding alleles and patterns per loci to calculate the DL to examine the extent of diversity information that these markers can provide for P. vulgaris.


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  		Table 4. Results of analyses of 68 polymorphic microsatellite loci in 21 Phaseolus vulgaris individuals, ordered by discriminatory power value, DL.*

 
The DL value in the present study ranged from 0.09 to 0.94, with an average of 0.73 for loci with more than 1 banding pattern. We observed that 73% of the loci had more than a 50% probability of discriminating between two individuals. As reported by Tessier et al. (1999), we found that the analysis of DL revealed that the efficiency of a given primer does not depend only on the number of patterns it generated (Fig. 1 and Table 4). For example, primers BM170 and BM140 produced the same number of patterns and alleles, but they had different discriminatory powers. In contrast, primers BM153 and BM164, with different numbers of patterns (7 and 11, respectively), had similar discriminatory powers. Primers BM188, GATS91, and BM143 have DL values higher than 0.90, which means that they would be very useful for genotyping P. vulgaris germplasm accessions. The high discriminatory power values exhibited by the microsatellites and their ease of scoring make them suitable to saturate the bean map with new and useful PCR-based markers.



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  		Fig. 1. Value of the discriminatory power (DL) of primers as a function of their number of banding patterns.

 
Amplification of Microsatellite Loci across Phaseolus Species
The level of conservation of these 68 SSRs in the Phaseolus genus was examined by evaluating them in P. coccineus, P. polyanthus, P. acutifolius, and P. lunatus. The first two species share a lineage with P. vulgaris and are more distant to P. lunatus, which belongs to a different lineage (Fofana et al., 1999). Thirty-three microsatellite markers (48.5%) produced amplification products in all samples, with some showing length variability between species. This indicates that a considerable level of sequence conservation exists within the primer regions flanking the microsatellite loci. Primers BM16, BM138, and BM195 failed to amplify any nonsource species (Table 5) .


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  		Table 5. Cross-species amplification of 68 microsatellite loci in four Phaseolus species.{dagger}

 
Thirty-eight primer pairs (56%) were polymorphic when they were used to amplified genotypes from P. coccineus, 21 (31%) were monomorphic and 6 (9%) failed to amplify. When the primer set were used on P. acutifolius, 36 (53%) primer pairs were polymorphic, 14 (20.5%) were monomporphic and 8 (12%) failed to amplify. For the P. polyanthus and P. lunatus genotypes used to amplified with the 68 primer set, 18 and 26 were polymorphic, 37 and 17 were monomorphic, and 7 and 18 failed to amplify, respectively. Eighteen microsatellite loci (26%) produced nonspecific amplification products in P. lunatus. This occurred mainly with primers BM16, GATS11B, BM167, BM195, BM138, BM25, BM150, and BM200 that failed to amplify in 50% or less of the tested species. As has been pointed out in other studies on SSR loci conservation in plant species, amplification success and polymorphism declines with increased genetic distance (White and Powell, 1997; Roa et al., 2000). Nevertheless, the utility of the bean primers in producing PCR-amplified products across the genus has been demonstrated and can be applied for germplasm characterization and mapping.


   ACKNOWLEDGMENTS
 
The authors thank Chikelu Mba for reviewing the manuscript and Elizabeth de Páez for editorial comments. We are also grateful to Roxana Pineda and Olga Giraldo for technical support in the laboratory, and to O. Toro for technical support in the greenhouse.

Received for publication November 1, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 




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