HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (3) Citing Articles via Google Scholar Google Scholar Articles by Muñoz, L. C. Articles by Roca, W. Search for Related Content PubMed Articles by Muñoz, L. C. Articles by Roca, W. Agricola Articles by Muñoz, L. C. Articles by Roca, W. Related Collections Other Legumes Cell Biology & Molecular Genetics Crop Genetics

GENOMICS, MOLECULAR GENETICS & BIOTECHNOLOGY

Introgression in Common Bean x Tepary Bean Interspecific Congruity-Backcross Lines as Measured by AFLP Markers

^a International Center for Tropical Agriculture, Biotechnology Research Unit, CIAT, A.A. 6713 Cali, Colombia
^b International Potato Center, CIP, A.A. 1558 Lima 12, Peru

^* Corresponding author: (m.blair{at}cgiar.org).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Congruity and recurrent backcross interspecific hybrids between common bean (Phaseolus vulgaris L.) and tepary bean (P. acutifolius A. Gray) were compared for the amount of introgression occurring between genomes by amplified fragment length polymorphism (AFLP) markers. A total of 60 genotypes were analyzed of which 34 were obtained by congruity backcrossing, four by single backcrossing and 14 by recurrent backcrossing, with parental and representative tepary and common bean genotypes used as controls. The level of introgression of tepary bean marker bands into the common bean genome background was higher in the congruity backcross lines than in the recurrent backcross derived genotypes. Congruity backcross lines derived from five cycles of interspecific hybridization showed an average introgression of 8.8% of AFLP bands while lines derived from a single backcross with the same parents showed an average introgression of only 5.2% of the bands. For both types of backcrossing, these levels of introgression were significantly below those expected. A multiple correspondence analysis showed three major clusters consisting of the common bean accessions and interspecifics with low rates of introgression, an intermediate group of interspecific congruity backcross lines with higher rates of introgression and a more distant group that included all the tepary bean accessions. These results suggest that congruity backcrossing can be used to increase introgression rates between the species and to transfer favorable oligogenic traits from tepary bean to common bean but that levels of introgression between the species remains low.

Abbreviations: AFLP, amplified fragment length polymorphism • BC, backcross • CBC, congruity backcross • CIAT, Centro Internacional de Agricultura Tropical • MCA, multiple correspondence analysis • UPGMA, unweighted pair group method with arithmetic mean

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
COMMON BEAN and tepary bean are two of the five cultivated species of the Phaseolus genus (Debouck, 1991). Although, tepary and common bean have the same number of chromosomes (n = 11) and similar karyotypes (Maréchal, 1970), they are distinguished by agroecological adaptation, mitochondrial genome characteristics (Khairallah et al., 1991), and morphological traits (Le Marchand and Maréchal, 1977; Debouck, 1991), indicating that they are fairly divergent species. Indeed, tepary bean is considered to be in the tertiary genepool of common bean because of the difficulties in crossing the two species and the need for embryo rescue to obtain successful interspecific hybrids (Maréchal et al., 1978; Smart, 1981a, 1981b; Mejía-Jiménez et al., 1994). While common bean is a major dry edible grain legume crop grown worldwide, tepary bean is a minor, traditional crop grown in the dry regions of Northwest Mexico, southwestern USA, and Central America (Singh, 1992). Despite its reduced importance as a modern crop, tepary bean has a number of favorable characteristics that makes it a potentially useful donor parent in crosses with common bean. First, tepary bean has a number of resistances to diseases and pests that are not found in common bean (Pratt and Nabhan, 1988; Honma, 1956; Singh and Muñoz, 1999; Urrea et al., 1999). Second, tepary bean has a higher regeneration capacity in tissue culture than common bean (Dillen et al., 1996, 1997), and third it has elevated levels of tolerance to high temperatures, drought, and salinity (Miklas et al., 1994; Lin and Markhart, 1996). Of the positive traits found in tepary bean, only resistance to the common bacterial blight pathogen [Xanthomonas axonopodis pv. phaseoli (Smith) Dye] has been transferred successfully from tepary bean to cultivars and advanced breeding lines of common bean (Parker and Michaels, 1986, Singh and Muñoz, 1999).

Interspecific hybrids between common and tepary bean were first obtained with a great deal of effort by Honma (1956) for a few genotypes, including a Great Northern line and four tepary bean accessions. Haghighi et al. (1984) later used three genotypes from each species to obtain simple cross hybrids. Waines et al. (1988) were the first to use recurrent backcrosses between common and tepary bean genotypes finding that the recurrent backcross hybrids retained very little of the tepary parent phenotype. An alternative to recurrent backcrossing known as congruity backcrossing that uses multiple backcrosses alternating between the tepary and common bean parents to overcome the interspecific hybridization barrier of hybrid sterility, genotype incompatibility, and embryo abortion found in simple interspecific crosses, was proposed by Haghighi and Ascher (1988). In their congruity backcrossing program, they found that the fertility of the interspecific hybrids and the first backcross generation plants was low but increased with subsequent congruity backcross hybrids demonstrating the utility of the method. Mejía-Jiménez et al. (1994) added to the technique by using embryo rescue in an effort to obtain a greater number of mature backcross hybrid plants even in early generation F₁ hybrids. Congruity backcrossing was suggested as a way to transfer desirable quantitative traits from one species to the other as the method was postulated to encourage recombination between two species (Haghighi and Ascher, 1988; Anderson et al., 1996).

In this study, a set of congruity backcross lines were analyzed to determine the levels of introgression from the tepary bean to the common bean genome by AFLP markers. The number of tepary bean AFLP bands introgressed into the congruity backcross lines was compared with the number of tepary bean AFLP bands found in a group of cultivars and lines developed from recurrent backcrossing. The relative advantage of recurrent versus congruity backcrossing is discussed in terms of the relative investment in effort for these two methods, the level of introgression obtained, and the possibility of transferring complex traits such as drought tolerance from tepary bean to common bean.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
Plant Material
A total of 60 genotypes were used in the experiments, including five tepary beans, three common beans and 52 interspecific common bean x tepary bean genotypes. The interspecific genotypes included 34 lines from congruity backcrosses between ICA Pijao (common bean) and G40001 (tepary bean), four lines from single backcrosses with the same parents and 14 interspecific cultivars and advanced lines from recurrent backcrossing involving other parents. ICA Pijao is a commercial black-seeded cultivar with erect type II plant growth habit and resistance to Bean golden yellow mosaic virus, angular leaf spot [caused by Phaeoisariopsis griseola (Sacc.) Ferr], anthracnose [caused by Colletotrichum lindemuthianum (Sacc. & Magnus) Lambs.-Scrib], and low soil fertility, that was developed in Colombia and that was thought to be a good hybridization bridge for crosses between gene pools (Mejía-Jiménez et al., 1994). G40001 is a white-seeded accession originally from Mexico that has resistance to common bacterial blight [caused by Xanthomonas campestris pv. phaseoli (Smith) Dye] and bruchids as well as heat and drought tolerance, which was obtained from the germplasm bank held in trust at the International Center for Tropical Agriculture (CIAT). The congruity backcross lines were selected from a larger set of 420 introgression lines that were developed by Mejía-Jiménez et al. (1994). The lines were selected on the basis of phenotypic variability in the field, when grown in single row plots in a field experiment at Palmira, Colombia, (soil type: fine-silty, mixed, isohyperthermic aquic hapludoll) during the dry season in July 1999 (average daily precipitation of 2.3 mm).

All the congruity backcross lines were derived from five alternating congruity backcrosses between ICA Pijao and G40001 (Table 1) followed by nine generations of inbreeding during which individual plant or mass selections were made on the basis of agronomic characteristics. The lines will heretofore be referred to as CBC₅F₁₀ lines. Among these lines seven pairs of sister lines, were included in the study, all of which were related by selection in the CBC₅F₄ generation. Meanwhile, the simple backcross lines were derived from backcrossing the interspecific F₁ hybrid of the cross ICA Pijao x G40001 to the common bean parent ICA Pijao and selfing the resulting BC₁F₁ hybrid for five generations. The resulting lines are heretofore referred to as BC₁F₅ lines.

AFLP Analysis
Total genomic DNA was extracted from 2 g of finely ground fresh leaf tissue according to the method of Vallejos et al. (1992). Amplicon-template preparation, preamplification and selective amplification were as described for the protocol of the Gibco BRL AFLP analysis system I kit for small genomes, using a total of 250 ng of genomic DNA in EcoRI (E)–MseI (M) digestion. All of the amplification primers used three selective nucleotides each. Amplification products were electrophoresed in 6% (w/v) denaturing polyacrylamide sequencing gels for 2 h at 100 W, and DNA bands were visualized by silver staining according to methods of Cho et al. (1996). All the polymorphic AFLP bands between 100 and 350 bp were scored and fragments were sized by comparison to a 25-bp ladder molecular weight size standard.

Data Analysis
The AFLP bands were read as present or absent and scored in binary code (0/1). Only heavy, reproducible bands were evaluated, while light bands that were difficult to score as present or absent were not considered. Each AFLP band was assumed to be an individual locus. Genetic similarities among genotypes were calculated with the statistical software SAS (SAS Institute, 1989) and the similarity coefficient from Nei and Li (1979). This coefficient is based on the formula S = 2a/(2a + b + c), were a = bands shared by both individuals, b = bands presented by individual (1) but not by (2), c = bands presented by individual (2) but not by (1). Means of genetic similarity indices were estimated between and within related sister lines. Additional means of similarity indices were estimated between the following groups: (i) simple backcross lines, (ii) congruity backcross lines, (iii) VAX lines, (iv) cultivars or lines with tepary introgression, (v) cultivars or lines without tepary introgression, and (vi) tepary accessions. Dendrograms were constructed with NTSYS-PC, version 2.0 (Rohlf, 1993), using the SAHN clustering subprograms and the UPGMA (unweighted paired grouped mean arithmetic average) method. Confidence intervals at 95% for selected nodes of the dendrograms were calculated by bootstrap analysis using a locally developed macro in SAS that calculated confidence intervals based on 1000 fold resampling of the identified groups. Multiple correspondence analyses were also performed using SAS. Chi-square tests were used to assess goodness-of-fit to the appropriate expected ratios of introgression. For the BC₁F₅ lines the expected proportion of alleles introgressed from P. acutifolius was 25.0% and from P. vulgaris was 75.0%. For the CBC₅F₁₀ lines the expected proportion of alleles introgressed from P. acutifolius was 32.8% and the expected genomic contribution from P. vulgaris was 67.2%. One degree of freedom (df) was used for the chi-square tests based on the df = n – 1, where n is the number of genotypic classes.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
An initial screening was conducted with the parental genotypes G40001 and ICA Pijao and a total of 24 AFLP primer combinations to evaluate the polymorphism level between these two genotypes. In this survey, from 73 to 95% of the bands found for each of the different AFLP combinations were polymorphic between the two parents representing the two species. The full set of introgression lines were analyzed with the four most polymorphic AFLP combinations from these initial experiments, namely (i) E-ACC/M-CTA; (ii) E-ACA/M-CAT; (iii) E-AAG/M-CTC; (iv) E-AAG/M-CTT. These primer combinations were also selected because they gave clear amplification profiles and a well-distributed range in band sizes. Together, all four primer combinations generated a total of 207 bands across the congruent backcross individuals and their two parents, for an average of 51.8 (SD = 11.8) bands per primer combination (Table 2). The average number of polymorphic bands between the parents was 40, which was equivalent to 77.2% of the total number of bands.

View larger version (94K): [in this window] [in a new window]   Fig. 1. Amplified fragment length polymorphism (AFLP) analysis of 38 interspecific congruity backcross lines derived from the cross between common bean (Phaseolus vulgaris) cultivar ‘ICA Pijao’ (P.v.) and tepary bean (P. acutifolius) accession G40001 (P.a.) using the AFLP primer combination E-ACC/M-CTA. Arrows indicate polymorphic bands associated with introgression of tepary bean allele in a common bean background. A 25-bp ladder was used as a MW size standard.

Although introgression in the interspecific advanced lines and cultivars could not measured per se because some of their common bean parents were not included, the transmission of tepary bean alleles to these lines was easy to follow given the high level of AFLP polymorphism between the two species. Tepary bean allele transmission was estimated as the percentage of all the bands (Fig. 2) found in the interspecific genotype, which were in common with the tepary bean parents used in their pedigree (Table 4). Given this, transmission of tepary bean alleles to the interspecific lines varied from 14.2% for XAN159 to 3.9% for SEL1309, Tara, and XAN87 and averaged 6.3%. Lines with no tepary bean ancestry had no bands from the subset tepary parents used in this study; and significant correlation (r = 0.631) was observed between the tepary bean allele transmission in the line and the coefficient of parentage of the line with its tepary bean ancestor.

View larger version (116K): [in this window] [in a new window]   Fig. 2. Amplified fragment length polymorphism (AFLP) analysis of common bean lines (Phaseolus vulgaris/P.v.); tepary bean accessions (P. acutifolius/P.a.) and interspecific hybrid advanced lines (series SEL, VAX, and XAN) or cultivars (Tara and Jules), as indicated by asterisk, using the primer combination E-ACC/M-CTA. A 25-bp ladder was used as a MW size standard.

View larger version (20K): [in this window] [in a new window]   Fig. 3. Dendrogram showing the association between 58 Phaseolus genotypes: 4 tepary bean (P. acutifolius), 2 common bean (P. vulgaris), 14 recurrent backcross interspecific lines (SEL, VAX, and XAN) or cultivars (Tara, Jules) and 38 congruity backcross (CBC) interspecific hybrids. UPGMA analysis was based on genetic similarities calculated with the Dice coefficient (Nei and Li, 1979). The values above key nodes denote 95% confidence intervals for those nodes, as revealed by a bootstrap analysis.

The second group was closely related to the first group and to the common bean genotypes but consisted completely of CBC₅F₁₀ lines. Within this second group, a total of six pairs of CBC₅F₆ sister lines were analyzed and genetic similarity between them was found to be greater than for non-sister lines as shown be their proximity on the dendrogram (Fig. 3), their similar levels of introgression (Table 1) and the similarity coefficients between them which was higher between sister lines than among pairs of sister lines or with the full set of congruent backcross individuals (data not shown).

Separate from either group and alone in the dendrogram, the interspecific line XAN159, with the highest amount of introgression was separated by a similarity level of 0.82 to 0.89 from the other interspecific genotypes and was intermediate between them and the tepary beans. It was notable that XAN159 was more similar to the CBC₅F₁₀ lines than to the other XAN lines.

To clarify these results further, we undertook a principal cluster analysis for the full dataset (Fig. 4) . In this multiple correspondence analysis, two dimensions were sufficient to explain the majority of the observed variation. This analysis showed three major clusters that agreed with the groupings observed in the dendrogram. The positions of the interspecific congruity backcross lines in each cluster were associated with the amount of introgression from tepary bean found in the lines. Within each one of these three clusters, the average similarity indices were high (0.92, 0.96, and 0.93, respectively) while between the three clusters the average similarity indices were variable. Variability around these mean similarity values were low and standard deviations did not exceed 0.03 in any of the between or within group comparisons.

View larger version (20K): [in this window] [in a new window]   Fig. 4. Multiple correspondence analysis showing the association between 58 Phaseolus genotypes: 4 tepary beans (P. acutifolius), 2 common bean (P. vulgaris), 14 recurrent backcross interspecific lines (SEL, VAX, and XAN) or cultivars (Tara, Jules) and 38 congruity backcross (CBC) interspecific hybrids. Three clusters indicated with circles corresponding to I: genotypes of common beans and interspecific with low rates of introgression. II interspecific congruity backcross lines with higher rates of introgression and III genotypes of P. acutifolius. Arrows indicate the position of genotypes; ICA Pijao (P. vulgaris), XAN 159 (recurrent backcross interspecific line) and G40001 (P. acutifolius).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

Given the genetic distance between tepary and common bean, it was not surprising that evidence of introgression between the two species has been rare. The first studies of interspecific hybrids between the species used morphological and biochemical markers to demonstrate introgression of new genes and traits from tepary bean into a common bean background (Prendota et al., 1982; Haghighi et al., 1984; Mejía-Jiménez et al., 1994; Alvarez et al., 1981). Some genetic studies of interspecific crosses have reported the presence of morphological characteristics (inflorescence structure, flower color, bracteoles, plant height, and growth habit) from tepary bean in lines resulting from interspecific hybrids with common bean. The incorporation of these new traits into common bean background was often used to measure the success of these crosses. For example, Mejía-Jiménez et al. (1994) used the seed protein phaseolin to verify introgression among the congruity backcross lines generated by the same cross described here. Garvin et al. (1997) used a wider range of isozyme markers to compare the introgression of tepary bean genes in backcross F₁ and F₂ generations from the same cross.

This study presents the first use of DNA markers to measure introgression in Phaseolus interspecific hybrids. Recent studies in other crops have used AFLP markers to quantify the number of introgressions in interspecific crosses of cotton and coffee (Vroh Bi et al., 1999; Lashermes et al., 2000). Introgression analysis using molecular markers has also been conducted in several legumes, such as peanuts, Arachis hypogaea L., and soybean, Glycine max (L.) Merr., (García et al., 1995; Maughan et al., 1996; Van Toai et al., 1997). In bean species, AFLP markers have been applied previously to study diversity in wild species of Phaseolus (Tohme et al., 1996) and to study lima bean (P. lunatus) diversity (Caicedo et al., 1999). The advantages of using AFLPs for our study was that the markers generated were phenotypically neutral and detected multiple loci thus providing widespread genome coverage.

Our comparison of the introgression rates in CBC₅F₁₀ and BC₁F₅ generations suggested that congruity backcrossing increased the introgression between tepary and common bean genomes more than a single backcross. While the overall amount of introgression was significantly different from the expected level for all of the simple and congruity backcross lines, the CBC₅F₁₀ lines had a significantly higher average introgression rate (8.9%) compared to the BC₁F₅ lines (5.2%). Therefore, it appears that genetic incompatibilities in the interspecific crosses may have been better resolved by congruity backcrossing between parent species than by simple backcrossing. Additionally, the selection for common bean phenotype imposed by breeders may have eliminated much of the tepary bean introgressions in the simple backcrosses, whereas a breeding method that encourages recombination such as congruity backcrossing, might have reduced the elimination of the tepary bean genome by reducing linkage drag and the propensity of phenotypic selection to remove large introgressions.

Predominance of the common bean alleles was also observed in genotypes developed by previous simple backcrosses between common and tepary bean. Garvin et al. (1997) found that the ratio of tepary to common bean alleles fit the expected ratio in the BC₁F₁ generations, but dropped significantly in the BC₁F₂ generation and that selfing of the interspecific hybrid caused a general elimination of the tepary genome. Waines et al. (1988) were unable to detect tepary alleles for three isozymes in the BC₁F₁ generation suggesting even more loss of the tepary genome. Anderson et al. (1996) observed that seeds of early generations of congruity backcross pedigrees exhibited a preponderance of traits (size, shape, color, and pattern) of the common bean parent when it was used as the cytoplasmic donor, while after a second cycle of congruity backcrossing the progeny became more alike and had intermediate expression of parental traits.

In our study, the transmission of tepary bean alleles was also low in the interspecific genotypes and cultivars not derived from congruity backcrossing (6.3% on average). In these genotypes, many of the initial introgressions of tepary genes have now been used in multiple generations of crosses, backcrosses, and recurrent selection with common bean and the resulting genotypes present very few phenotypic characteristics of tepary beans. A recent study by Miklas et al. (2002) suggested that GN #1 Sel #27, a genotype that was used to develop the cultivars Jules and Tara, probably contains genes from tepary bean but owes its common bacterial blight resistance to its common bean parent Montana #5 and not to the tepary bean, as previously was thought. The present results showed that Tara and Jules still demonstrate a small amount of tepary bean introgression and thus provide evidence that Honma (1956) did indeed achieve interspecific crosses that transferred tepary bean alleles, albeit at a low percentage, to these cultivars.

One exception to the low transmission of tepary bean alleles in the interspecific lines was found in the genotype XAN159, which had higher number of tepary bean alleles than even the congruity backcross lines. The unique nature of XAN159 was recognized by Jung et al. (1997), when they suggested that the amount of tepary bean introgression in this line influenced the genome coverage in their genetic mapping study. The higher transmission of tepary bean alleles in XAN159 may be a reflection of greater cross compatibility of the tepary bean genotype G40020 that was used in its pedigree. The use of possible bridging genotypes such as this one has been suggested for tepary by common bean crosses before (Parker and Michaels, 1986).

All of these results suggest that in crosses between common and tepary bean the common bean genome is usually favored more than expected, especially when the common bean phenotype is used as a cytoplasm or recurrent parent. Guo et al. (1991)(1994) made similar observations when they analyzed interspecific populations developed from a cross between P. vulgaris x P. coccineus and the reciprocal. In statistical analysis with RFLP markers, they found gametic selection with preferential transmission of common bean alleles and segregation ratios that deviated significantly from the expected. The genetic control of tepary x common bean cross-incompatibility has not been found but will be of interest for the future and the interspecific lines used in this study could be a useful resource for discovering why introgression rates are low in these types of crosses.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 
The results showing that congruity backcrossing can increase the introgression of tepary alleles into the common bean genome, but that overall rates of introgression are low, have important implications for researchers planning to use the congruity backcrossing method in tepary bean x common bean interspecific breeding programs and on the possibility of transferring quantitative traits from one species to the other. Although congruity backcrossing can be more effort and more time-consuming than recurrent backcrossing it has the major advantage of increasing fertility during interspecific crossing (Mejía-Jiménez et al., 1994) in addition to the increases in introgression found here. Increased fertility would be advantageous for developing bridging genotypes for crosses to either species, while heightened introgression would be advantageous for the transfer of complex traits from tepary bean to common bean which to date have proven impossible to obtain. While simple traits have been transferred successfully from tepary bean to common bean advanced lines and cultivars (Coyne, 1964; Parker and Michaels, 1986), it would be very useful to be able to transfer characteristics such as drought, salinity or high temperature tolerance, which as complex traits would rely on the simultaneous introgression of the right combination of tepary genes into the common bean genome. Judicious use of congruity and recurrent backcrossing and the use of specific bridging genotypes may encourage recombination between the two species and one day allow the transfer of complex traits from tepary bean to common bean.

	ACKNOWLEDGMENTS

 
We are grateful to S.P. Singh and A. Mejía-Jimenez for development of the congruity backcross lines, to S.E. Beebe and H. Terán for field experiments and help in selecting the genotypes used in these experiments, to P. Zamorano for editorial assistance, and S.E. Beebe, D. Debouck and P. Leterme as reviewers. This work was supported with funds from AGCD Belgian assistance program and the US Agency for International Development.

Received for publication March 19, 2003.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION CONCLUSIONS REFERENCES

 

• Alvarez, M.N., P.D. Ascher, and D.W. Davis. 1981. Interspecific hybridization in Euphaseolus through embryo rescue. HortScience 16:541–543.
• Anderson, O.N., P.D. Ascher, and K. Haghighi. 1996. Congruity backcrossing as a means of creating genetic variability in self-pollinated crops: Seed morphology of Phaseolus vulgaris L. and P. acutifolius A Gray hybrids. Euphytica 87:211–224.
• Caicedo, A.L., E. Gaitán, M.C. Duque, O. Toro, D.G. Debouck, and J. Tohme. 1999. AFLP Fingerprinting of Phaseolus lunatus L. and related wild species from South America. Crop Sci. 39:1497–1507.[Abstract/Free Full Text]
• Cho, Y.G., M. Blair, O. Panaud, and S. McCouch. 1996. Cloning and mapping of variety-specific rice genomic DNA sequences: Amplified fragment polymorphisms (AFLP) from silver stained polyacrylamide gels. Genome 39:373–378.[Medline]
• Coyne, D.P. 1964. Species hybridization in Phaseolus. J. Hered. 55:5–6.[Free Full Text]
• Debouck, D.G. 1991. Systematiccs and morphology. p. 55–118. In A.V. Schoonhoven and O. Voysest (ed.). Common beans: Research for improvement. CIAT.
• Delgado Salinas, A., T. Turley, A. Richman, and M. Lavin. 1999. Phylogenetic analises of the cultivated and wild species of Phaseolus (Fabaceae). Syst. Bot. 24(3):438–460.
• Dillen, W.J., J. De Clercq, M. Van Montagu, and G. Angeon. 1996. Plant regeneration from callus in a range of Phaseolus acutifolius A. Gray genotypes. Plant Sci. 118:81–88.
• Dillen, W., J. De Clercq, A. Goossens, M. Van Montagu, and G. Angeon. 1997. Agrobacterium mediated transformation of Phaseolus acutifolius. Theor. Appl. Genet. 94:151–158.
• García, G.M., H.T. Stalker, and G. Kochert. 1995. Introgression analyses of an interspecific hybrid population in peanuts (Arachis hypogea) using RFLP and RAPD. Genome 38:166–176.[Medline]
• Garvin, D.F., C.T. Federici, E.J. Stockinger, and J.G. Waines. 1997. Genetic marker transmission in early generation common x tepary bean hybrids. J. Hered. 85:174–178.
• Guo, M., D.A. Lightfoot, M.C. Mok, and D.W.S. Mok. 1991. Analyses of Phaseolus vulgaris L. and P. coccineus Lam. hybrids by RFLP: Preferential transmission of P. vulgaris alleles. Theor. Appl. Genet. 81:703–709.
• Guo, M., M.C. Mok, and D.W.S. Mok. 1994. RFLP analysis of preferential transmission in interspecific hybrids of Phaseolus vulgaris and P. coccineus. J. Hered. 85:174–178.[Abstract/Free Full Text]
• Haghighi, Y., and P.D. Ascher. 1988. Fertile intermediate hybrids between P. vulgaris and P. acutifolius from congruity backcrossing. Sex. Plant Reprod. 1:51–58.
• Haghighi, K., S. Zuluaga, and P.D. Ascher. 1984. Hybridization and rapid asexual propagation of Phaseolus vulgaris-P. acutifolius. Annu. Rep. Bean Improv. Coop. 27:42–43.
• Honma, S. 1956. A bean interspecific hybrid. J. Hered. 47:217–220.[Free Full Text]
• Jung, G., P.W. Skroch, D.P. Coyne, J. Nienhuis, E. Arnaud-Santana, H.M. Ariyarathne, S.M. Kaeppler, and M.J. Basset. 1997. Molecular marker based genetic analysis of tepary bean derived common bacterial blight resistance in different developmental stages of common bean. J. Am. Soc. Hortic. Sci. 122:329–337.[Abstract/Free Full Text]
• Khairallah, M., M.V. Adams, and B.B. Sears. 1991. Mitochondrial genome size variation and restriction fragment length polymorphisms in three Phaseolus species. Theor. Appl. Genet. 82:321–328.
• Lashermes, P., S.B. Andrzejewski, B. Betran, M.C. Combes, S. Dussert, G. Graziosi, P. Trouslot, and F. Anthony. 2000. Molecular analyses of introgressive breeding in coffee (Coffea arabica L.). Theor. Appl. Genet. 100:139–146.
• Le Marchand, G., and R. Maréchal. 1977. Chromosome pairing in interspecific hybrids reveals the value of pollen morphology for deducting phylogenic affinities in the genus Phaseolus. p. 335–337. In Interspecific hybridization and plant breeding: Proc. 8th Eucarpia Congress, Madrid.
• Lin, T.Y., and A.H. Markhart. 1996. Phaseolus acutifolius A. Gray is more heat tolerant than P. vulgaris L. in the absence of water stress. Crop Sci. 36:110–114.[Abstract/Free Full Text]
• Maréchal, R. 1970. Données cytologiques sur les espèces de la sous-tribu des Papilionaceae-Phaseolae-Phaseolinae. Deuxieme serie. Bull. Jard. Bot. Nat. Belge. 40:307–348.
• Maréchal, R., J.M. Mascherpa, and F. Stainier. 1978. Etude taxonomique d'un groupe complexe d'espèces des genres Phaseolus et Vigna (Papilonaceae) sur la base des données morphologiques et polliniques traité par l, analyse informatique. Boissera 28:1–273.
• Maughan, P.J., M.A. Saghai, G.R. Buss, and G.M. Huestis. 1996. Amplified length polymorphism (AFLP) in soybean: Species, diversity, inheritance and near-isogenic lines analysis. Theor. Appl. Genet. 93:392–401.[Web of Science]
• Mejía-Jiménez, A., C. Muñoz, H.J. Jacobsen, W.M. Roca, and S.P. Singh. 1994. Interspecific hybridization between common and tepary beans: Increased hybrid embryo growth, fertility, and efficiency of hybridization through recurrent and congruity backcrossing. Theor. Appl. Genet. 88:324–331.[Web of Science]
• Miklas, P.N., D.P. Coyne, K.F. Grafton, N. Mutlu, J. Reiser, and S.P. Singh. 2002. A major QTL for common bacterial blight resistance in GN# 1 sel 27 derives from the great northern landrace Montana No. 5 not tepary bean. Annu. Rep. Bean Improv. 46:52–53.
• Miklas, P.N., J.C. Rosas, J.S. Beaver, L. Telek, and G.F. Freytag. 1994. Field performance of select tepary bean germplasm in the tropics. Crop Sci. 34:1639–1644.[Abstract/Free Full Text]
• Nei, M., and W. Li. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. (USA) 76:5269–5273.[Abstract/Free Full Text]
• Parker, J.P., and T.E. Michaels. 1986. Simple genetic control of hybrids plant development in interspecific crosses between Phaseolus vulgaris and P. acutifolius A. Gray. Plant Breed. 97:315–323.
• Pratt, R.C., and G.P. Nabhan. 1988. Evolution and diversity of Phaseolus acutifolius genetic resources. p.409–440. In P. Gepts (ed.) Genetic resources of Phaseolus beans. Kluwer Academic Publishers, Boston.
• Prendota, K., J.P. Baudoin, and R. Marechal. 1982. Fertile allopolyploides from the cross P. acutifolius x P. vulgaris. Bull. Rech. Agron. Gembloux 17:177–190.
• Rohlf, F.J. 1993. NTSYS-PC numerical taxonomy and multivariate analysis system. Version 2.02. Exeter Publ., Setauket, NY.
• SAS. Institute.1989. SAS/STAT users guide. 6.09 ed. SAS Inst., Cary, NC.
• Singh, S,P. 1992. Common bean improvement in the tropics. Plant. Breed. Rev. 10:199–269.
• Singh, S.P., and C.G. Muñoz. 1999. Resistance to common bacterial blight among Phaseolus species and common bean improvement. Crop Sci. 39:80–89.[Abstract/Free Full Text]
• Smart, J. 1981a. Gene pools in Phaseolus and Vigna cultigens. Euphytica 30:445–449.
• Smart, J. 1981b. Evolving gene pools in crop plants. Euphytica 30:415–418.
• Tohme, J., F.D. Orlando, S. Beebe, and M.C. Duque. 1996. AFLP analysis of gene pools of a wild bean core collection. Crop Sci. 6:1375–1384.
• Urrea, C., P.N. Miklas, and S. Beaver. 1999. Inheritance of resistance to common bacterial blight in four tepary bean lines. J. Am. Soc. Hortic. Sci. 124:24–27.[Abstract/Free Full Text]
• Vallejos, C.E., N.S. Sakima, and C.D. Chase. 1992. A plant DNA minipreparation. Version II. Plant Mol. Biol. 1:19–21.
• Van Toai, T.T., J. Peng, and S.K.S. Martín. 1997. Using AFLP markers to determine the genomic contributions of parents to populations. Crop Sci. 37:1370–1373.[Abstract/Free Full Text]
• Vroh Bi, I., A. Maquet, J.P. Baudoin, P. Du Jardin, J.M. Jacquemin, and G. Mergai. 1999. Breeding for low-gossypol seed and high gossypol plants. Upland cotton tri-species hybrids and backcross progenies. Theor. Appl. Genet. 99:1233–1244.
• Waines, J.G., R.M. Manshardt, and W.C. Wells. 1988. Interspecific hybridization between Phaseolus vulgaris and P. acutifolius. p. 485–502. In P. Gepts (ed.) Genetic resources of Phaseolus beans. Kluwer Academic Publishers, Boston.

This article has been cited by other articles:

				S. P. Singh, H. Teran, H. F. Schwartz, K. Otto, and M. Lema Introgressing White Mold Resistance from Phaseolus Species of the Secondary Gene Pool into Common Bean Crop Sci., August 7, 2009; 49(5): 1629 - 1637. [Abstract] [Full Text] [PDF]

				L. C. Munoz, M. C. Duque, D. G. Debouck, and M. W. Blair Taxonomy of Tepary Bean and Wild Relatives as Determined by Amplified Fragment Length Polymorphism (AFLP) Markers Crop Sci., June 20, 2006; 46(4): 1744 - 1754. [Abstract] [Full Text] [PDF]

This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (3) Citing Articles via Google Scholar Google Scholar Articles by Muñoz, L. C. Articles by Roca, W. Search for Related Content PubMed Articles by Muñoz, L. C. Articles by Roca, W. Agricola Articles by Muñoz, L. C. Articles by Roca, W. Related Collections Other Legumes Cell Biology & Molecular Genetics Crop Genetics