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CELL BIOLOGY & MOLECULAR GENETICS

Putative Quantitative Trait Loci for Physical and Chemical Components of Common Bean

^a Unidad de Biotecnología del Bajío, Campo Experimental Bajío-INIFAP, Km. 6.0 Carretera Celaya-San Miguel Allende, Celaya, Gto., México
^b Centro de Investigación y de Estudios Avanzados del IPN, Unidad Irapuato, Apartado Postal 629, Irapuato, Gto., 36500, México

^* Corresponding author (oparedes{at}ira.cinvestav.mx)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
In common bean (Phaseolus vulgaris L.), some nutritional traits such as proteins and mineral content are lower in the cultivated form as compared with the wild counterpart. To assess the feasibility of wild bean as the putative source of desirable traits such as minerals or tannins, this study was performed to identify quantitative trait loci (QTL) associated with seed mass, Ca, Fe, Zn, and tannin content in bean seed. Two-hundred-ninety-one amplified fragment length polymorphism (AFLP) markers were scored in 120 F_2:3 segregating individuals derived from a cross between cultivated ‘Bayo Baranda’ and wild common bean accession G-22837. Seed weight and minerals and tannin contents were quantified on the seed harvested from the 120 individual plants. Significant transgressive segregation was observed among the F_2:3 individuals for some characteristics. A total of 57 AFLP markers were distributed among five linkage groups with a coverage of 497 centiMorgans (cM). Five putative QTL were significantly associated with seed mass, two with Ca, two with Fe, one with Zn, and four with tannin content in the seed. These QTL explained 42, 25, 25, 15, and 42% of the phenotypic variance, respectively. Due to known environmental effect on most nutritional traits, the use of QTL with larger effects could be used to screen segregating populations that include wild genotypes, wild populations, and ancestral landraces from the region where outstanding wild populations are identified.

Abbreviations: AFLP, amplified fragment length polymorphism • cM, centiMorgan • LG, linkage groups • LOD, logarithm of odds • QTL, quantitative trait loci • TAE, tannic acid equivalents

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
INCREASING THE AMOUNT of bioavailable micronutrients in plant foods for human consumption is a challenge that is particularly important in developing countries. Cereal grains and some legumes are the primary and least expensive source of Ca, Fe, and Zn for the population in these countries; however, intakes do not satisfy their mineral requirements (Welch and Graham, 1999). Calcium content in rural diets in developing countries is not adequate (Rosado et al., 1992; Wyatt and Triana-Tejas, 1994) and dietary Ca deficiency has been epidemiologically linked to several chronic diseases, including osteoporosis, hypertension, and colon cancer (Anderson and Allen, 1994).

Recent reports indicate that Fe deficiency is the most prevalent micronutrient problem in the world, affecting over 2 billion people globally, many of whom depend on beans as their staple food (Welch, 1999). Forty percent of Fe intake in developing countries is derived from legumes and cereals (Rosado et al., 1992; Barclay et al., 1996). In addition, accompanying antinutrients (e.g., tannins and phytic acid) reduce the bioavailability of Ca, Fe, and Zn (Frossard et al., 2000).

During the past 25 yr, substantial progress has been made on the clinical, biochemical, and immunological aspects of the role of Zn in humans (Ganapathy and Volpe, 1999). Extensive research has shown that Zn is involved in a myriad of critical reactions in the human body and is associated with cellular growth and repair, appetite, behavior, and susceptibility to infection. Recent studies have identified Zn deficiencies in children who consume diets high in cereals (Ranum, 1999). Moreover, it is recognized that a nutritional deficiency in Zn is common throughout the world, including the USA. (Ganapathy and Volpe, 1999).

Plant breeding has been mainly focused on increasing yield and disease resistance in crops, but not at improving the micronutrient concentration in grain (Frossard et al., 2000). Developing cultivars with higher capacity to accumulate Ca, Fe, and Zn could contribute significantly to the improvement of the micronutrient status of people depending on common bean as a major component of their diet. Beebe et al. (1999) have shown that the genetic differences in Fe and Zn content of common bean seeds are expressed across different seasons and in different environments. In addition, environmental and genetic factors influence Ca accumulation in common bean (Moraghan and Grafton, 1997).

Many traits in plants are quantitatively inherited, showing a continuous variation in phenotype among a population of individuals. Selection in plant breeding programs, designed to improve quantitative traits such as mineral contents in common beans, is complicated because the effects of individual loci influencing those traits are difficult to isolate and characterize. Efforts to improve nutritional quality of common bean have focused mostly on protein and tannin content through traditional breeding techniques without concerted attempts to utilize variation at QTL (Gepts, 1998). Primarily, QTL analyses have so far been used in common bean to study disease resistance traits (Kelly and Miklas, 1998), canning quality (Walters et al., 1997; Posa-Macalincag et al., 2000), seed size (Park et al., 2000), N-fixation (Nodari et al., 1993), drought (Schneider et al., 1997), common bacterial blight (Jung et al., 1999; Park et al., 1999) and white mold (Miklas et al., 2001; Park et al., 2001). Although no QTL for mineral content have been mapped in common bean, they are likely to be widely distributed in the genome, given the quantitative nature of the trait.

A largely unexplored resource is to exploit diversity present in wild common bean. The extreme phenotypic distinctness of wild common bean, as compared with that of cultivated common bean, and their lack of adaptation to long-day environments, make them a likely source of additional diversity (Gepts, 1998). Guzmán-Maldonado et al. (2000) identified accessions of wild and weedy common beans with Ca, Fe, and Zn contents higher than those of cultivated varieties. The wild ancestors of common bean that have a higher ability to accumulate Ca, Fe, and Zn in their seed could be used as parents to increase the mineral concentration in seed through breeding.

To assess the feasibility of wild bean as the putative source of desirable traits, this study was performed to identify QTL associated with seed quality traits such as mass and Ca, Fe, Zn, and tannin content in bean seed derived from a cultivated x wild bean cross.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Plant Material
A population of 120 F_2:3 lines was developed from a cross between cultivated beige-colored common bean cultivar Bayo Baranda, race Durango, and wild black common bean G-22837 collected in the Mexican state of Jalisco. One F₂ seed of each of the 120 F_2:3 lines and 10 seeds of each parent were sown in plastic bags containing 5 kg of sterilized soil and grown under greenhouse conditions to maturity. Greenhouse temperatures were maintained between 18 and 22°C. Five to eight leaves from each F₃ plant were collected and stored at -80°C. Approximately 50 seeds of each of the 120 segregating F₃ plants and 100 seeds from a bulk of each parent were harvested and stored at 5°C for seed weight, mineral, and tannin analysis.

Seed Mass
Weights of 25 randomly selected seeds were determined and extrapolated to weights of 100 seeds. Determinations were performed in triplicate and reported as g 100 seeds^-1 (Paredes-López et al., 1989).

Minerals
Calcium, Fe, and Zn were determined in ground flour of washed (distilled water) and dried bean seeds after digestion with HClO₄:HNO₃ (Jones and Case, 1990). Minerals were determined in triplicate with a Perkin Elmer 3000SC inductively coupled plasma atomic emission spectroscopy analyzer (Norwalk, CT). Certified standards (Perkin Elmer) were run with every determination. To avoid mineral contamination, samples were ground in glassine paper with a pestle. A sample of glassine paper was run to confirm absence of minerals.

Tannin Determination
Samples for tannin quantification were prepared according to the method of Carmona et al. (1991). Triplicate samples of 1 g flour each were extracted for 24 h at room temperature by continuous stirring with 10 mL of 1% HCl in 97% methanol. Aliquots of the crude extracts were assayed for tannins using the Prussian blue method (Price and Butler, 1977). Tannin content was expressed as tannic acid equivalents (mg TAE g^-1).

Deoxyribonucleic Acid Extraction
Bean leaves of F₃ lines were frozen in liquid N and ground to a fine powder with sterilized mortar and pestle. Extraction buffer (0.05 M Tris-HCl, 7.0 M urea, 0.35 M NaCl, 0.02 M EDTA, 1% N-lauroylsarcosine) was added, and after mixing, samples were extracted once with phenol:chloroform:isoamyl alcohol (25:24:1, v/v/v) and centrifuged at 13 000 x g for 15 min. The supernatant was treated with RNase (30 min, 37°C) and again extracted with phenol:chloroform:isoamyl alcohol. Deoxyribonucleic acid was precipitated with isopropanol, and washed twice in 70 and 100% ethanol. Deoxyribonucleic acid was resuspended in Tris-EDTA buffer (0.01 M Tris-HCl, pH 8.0, 0.01 M EDTA) and quantified visually in agarose gel using lambda DNA/HindIII fragments as molecular weight markers.

Amplified Fragment Length Polymorphism Analysis
Amplified fragment length polymorphism was determined according to the method reported by Vos et al. (1995). The AFLP protocol consists of total bean genomic DNA digestion with restriction enzymes EcoRI and MseI. Adaptor molecules specific for the restriction fragment ends were then ligated to the mixture of restriction fragments. The adaptor molecules and nucleotides adjacent to the site of ligation serve as a template for the annealing of specific oligonucleotide primers used for polymerase chain reaction amplification reactions. Oligonucleotide primers used for the amplification step were EcoRI 5'-GACTGCGTACCAATTC/A-3' (EcoRI + A) and MseI 5'-GACGATGAGTCCTGAGTAA/C-3' (MseI + C). The preamplification step was followed by a second selective amplification step with two selective nucleotides. The EcoRI oligonucleotide primers for the second amplification were 5'-AGACTGCGTACCAATTC/AGA-3' (EcoRI + AGA) and MseI oligonucleotides were 5'-GATGAGTCCTGAGTAA/CAC, /CAA, /CAT and /CAG. The EcoRI + AGA primer used was radioactively labeled by using T4 kinase, and the products of the second amplification were visualized after electrophoresis on a polyacrylamide sequencing gel and autoradiography. The EcoRI + AGA primer was chosen because it generated the highest fragment polymorphism among common bean cultivars (Tohme et al., 1996).

Data Analysis
A molecular marker linkage map was constructed using Joinmap 1.4 (Stamp, 1993). The grouping file was obtained using logarithm of odds 3 (LOD), and for recombination and mapping analysis, a LOD threshold of 0.05 and a recombination threshold of 0.5 were used.

Number, sizes of effect, and positions of QTL in the segregating population were determined by regression mapping (Haley and Knott, 1992; Martínez and Curnow, 1994). This approach consists in regressing the phenotypic value on the probability of having a QTL genotype at a given position in the genome, estimating the coefficients of the model by the least square method. As F₂ plants were used, three QTL genotypes are possible for each locus, say aa, Aa, or AA. In all cases, the allele from the wild parent was labeled as a and the one from the cultivated parent was labeled as A (no dominance implication in this notation). The general form of the regression model is

where Y is the quantitative value, ß₀ estimates a reference point corresponding to the effect of all wild alleles, P[A_r A_r/m] and P[A_r a_r/m] are the probabilities of having the QTL genotypes AA and Aa, given the information from the flanking markers at a given position, and thus ß_1r and ß_2r estimate the effect of the AA and Aa QTL genotypes, and the sum is across all the QTL fitted in the model; r = 1,2, ... k, with k representing the number of QTL fitted. As a first step in the analysis, all the linkage groups were scanned looking for significant effects and thus the position of a putative QTL was estimated where a significant effect was found. As a second step, a set of models including all possible combinations of putative QTL for a character were fitted, and the best model was selected by the maximum R² criteria. The global variation explained by all QTL fitted was reported.

For the selection of putative QTL, the F test of variance analysis for the regression model was used with an = 0.002 for the five linkage groups obtaining an approximate 0.01 experiment-wise probability of Type I error (probability of proclaiming a false positive). It is important to notice that when many QTL are fitted in a model, the number of genotype effects estimated grows geometrically. For example, a model including 5 QTL will be trying to estimate 3⁵ = 243 different genotypes that surely will not be sufficiently represented if the plant population is small. In that case, the estimates of the coefficients become unreliable, and we can consider that a quantitative trait locus was in fact located, but we will not have trustworthy estimations of the QTL effects in the genetic background of the segregating population.

Statistical Analysis
An analysis of variance was applied to seed mass, and Ca, Fe, Zn and tannin content. Differences (P < 0.05) among common bean parents were determined by Tukey's test means comparison (Steel and Torrie, 1982).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Physical and Chemical Characteristics
The wild bean parent was characterized by a small seed mass as compared with the cultivated variety (Table 1). Protein, Ca, Fe, and Zn content of cultivated and wild parental beans were similar in amount to values previously reported by Guzmán-Maldonado et al. (2000) and Moraghan and Grafton (1997). These traits were higher (P < 0.05) in the wild bean progenitor than those in the cultivated bean (Table 1). Small-sized bean seeds possess a higher protein content because of a reduction in starch content (Shellie-Dessert and Bliss, 1991). The contribution of genetic and environmental factors to mineral accumulation in wild and cultivated common beans is poorly understood (Moraghan and Grafton, 1997). These marked differences that distinguish wild bean progenitors, and the lack of information about the genetic inheritance of distinguished traits, have limited the utilization of wild germplasm for crop improvement (Koinange et al., 1996).

In most traits, transgressive F_2:3 families were observed (as determined by the Student's t test at = 0.05; analyses not shown), the exception was in seed mass since the cultivated parent displayed the largest seed mass. Heterosis was observed in Zn content (Table 1). Heterosis has been reported previously for common bean by Nienhuis and Singh (1986) and Singh (1991). The existence of transgressive variation and heterosis above the high parent, such as that observed for Zn content, should encourage plant breeders as it indicates that gene combination exists, which can result in enhanced characteristic performance in the absence of overdominance. From the distribution figures (data not shown), segregation among F_2:3 families for all selected traits was close to normal with a minimal number of families, two to four, displaying larger values than the parents and overall mean. Most probably, those values were the effect of overdominance. To capitalize on transgressive segregation, individual families at the extreme of the normal distribution must be chosen for further advance of generation and testing. We are confident that QTL were not overestimated since very few of the segregating families displayed values higher than two standard deviations above the mean value; in other words, most families were under the normal curve.

Significant positive correlations were observed among Ca, Zn, and Fe contents (Table 2). Calcium content was not correlated with seed mass, as suggested by Moraghan and Grafton (1997), nor was Zn or Fe. Currently, there is no plausible explanation for the correlation among minerals found in the present work, so further studies are necessary. However, both environment and genotype affect Fe, Zn, and Ca contents in common bean (Moraghan and Grafton, 1997; Frossard et al., 2000). Tannin content was negatively associated with seed mass. Since tannin is restricted to the seed coat, analysis of tannin content based on whole seed flour could contribute to the negative correlation observed.

Genetic Map
A total of 57 AFLP markers were genetically linked resulting in five linkage groups (LG) with a coverage of 497 cM (Kosambi) (Fig. 1). Linkage groups ranged in size from 39.8 to 141.6 cM: LG I = 141.6 cM, LG II = 116.4 cM, LG III = 72.5 cM, LG IV = 125.7 cM, and LG V = 39.8 cM. Estimations of the total genome size of common bean, reported by Vallejos et al. (1992) and Gepts et al. (1993), have generated values of 1200 cM and 1250 cM in length, respectively. Hence, our current map covered 41% of the estimated bean genome.

View larger version (38K): [in this window] [in a new window]   Fig. 1. Linkage groups (LG) and QTL marker associations with seed mass (SM), Ca, tannins (TA), Fe, and Zn in a common bean population, ‘Bayo Baranda’ x G-22837. Map distance (in cM) is shown in parentheses and indicates the distance of a marker (M) from the top of the LG.

The two QTL associated with Ca content, located in LG I and IV, explained 25% of the variance of Ca concentration in bean seed (Fig. 1 and Table 3). A similar level of variance was obtained for QTL significantly associated with Fe content; whereas QTL associated with Zn concentration explained only 15% of the variance of Zn content in bean seed. The two QTL associated with Fe content were on LG II and III. LG IV grouped QTL associated with Zn, Ca, and tannin contents as well as with seed mass (Fig. 1). Interestingly, all QTL associated with Ca, Fe, and Zn contribute negatively to the regression model (Table 3).

Apparently, the wild parental alleles significantly affect the accumulation of Ca, Fe, and Zn in seed of the segregating populations, in view that intercept ß₀ values contributed to the regression model with 4903.23, 102.62, and 43.83 µg of Ca, Fe, and Zn, respectively (Table 3). One possible explanation for this positive effect is the higher capacity of the wild progenitor to accumulate Ca, Fe, and Zn similar to data reported by Guzmán-Maldonado et al. (2000). In this respect, the Ca content of the wild parental was 275% higher than that of the cultivated one; whereas Fe and Zn contents were 158 and 180% higher than those of the cultivated beans, respectively.

Four QTL significantly associated with tannin content were identified. The QTL were located on LG I (two QTL), and in LG II and III (one quantitative trait locus each) (Fig. 1). Collectively, all four QTL explained 42% of the tannin concentration variance (Table 3). QTL2 contributed positively to the regression model with 50.22 g TAE from QTL2AA and 102.9 g TAE from QTL2Aa (Table 3). No other QTL contributed in such a way with exception to QTL1Aa, which contributed with 85.9 g TAE to the regression model. There is no explanation to the higher contribution of these QTL; probably this is the consequence of estimating four QTL at once and the low number of F_2:3 individuals included in this study. The other QTL for tannin content contributed negatively to the regression model.

In spite of a higher tannin content (212%) in the wild progenitor than in the cultivated bean, apparently both wild and cultivated beans have a similar capacity to accumulate tannin, because previous reports indicate that beige or white cultivated beans showed similar or higher tannin content than levels in wild or cultivated black beans (Reyes-Moreno and Paredes-López, 1993; Guzmán-Maldonado et al., 2000).

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
We constructed a partial linkage map and identified putative QTL significantly related to seed mass and Ca, Fe, Zn, and tannin content in seeds of common bean derived from a cultivated x wild bean cross. QTL2 for tannin content was the QTL which has the greatest positive effect. Further studies are needed to assess the value of these QTL for breeding for better lines of common bean cultivars with improved micronutrient contents. However, we have demonstrated the feasibility of identifying QTL associated with mineral content, which has been neglected because breeders have mainly focused on increasing yield and disease resistance, among other traits, but not on improving micronutrient concentrations in been seeds.

Dry beans are an integral part of diets in a significant portion of the world population, but the potential benefits of consuming beans from a nutraceutical standpoint has been largely overlooked (Hosfield, 2001). Tannins can be potent inhibitors of Fe bioavailability in humans and are also responsible for decreases in feed intake, growth rate, and protein digestibility (Frossard et al., 2000; Guzmán-Maldonado et al., 2000); however, Carbonaro et al. (2000) suggested that the structural properties of the storage protein and not their binding of tannins, are the main determinants of the extent of protein digestibility. Tannins have many important roles in plant physiology, and have been suggested as antimutagenic agents (de Mejía et al., 1999). Therefore, it would seem unwise at the present time to attempt to decrease their content in bean seeds.

	ACKNOWLEDGMENTS

 
Financial support from Consejo Nacional de Ciencia y Tecnología-México is acknowledged.

Received for publication April 17, 2002.

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TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

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