ASSOCIATION OF A SEED WEIGHT FACTOR WITH THE PHASEOLIN SEED STORAGE PROTEIN LOCUS ACROSS GENOTYPES, ENVIRONMENTS, AND GENOMES IN Phaseolus-Vigna spp.:
SAX (1923) REVISITED

Originally published in: Journal of Quantitative Trait Loci, then renamed Journal of Agricultural Genomics

Vol. 2, Paper 5 (1996)


William C. Johnson, Cristina Menéndez, Rubens Nodari, Epimaki M.K. Koinange, Steve Magnusson, Shree P. Singh , Paul Gepts

Dept. of Agronomy and Range Science, University of California, Davis, CA 95616

Corresponding author: Paul Gepts (plgepts@ucdavis.edu)



Abbreviations: AG: Population A55 x G122; BJ: Population BAT93 x Jalo EEP558; BTS: Black Turtle Soup; CDRK: California Dark Red Kidney; CY: Population CDRK x Yolano; GH: Greenhouse; LG: linkage group; MG: Population Midas x G12873; NIL: Nearly-isogenic lines; RIP: recombinant inbred population; QTL: quantitative trait locus; SDS/PAGE: polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulfate





ABSTRACT


Karl Sax (1923) presented the first evidence for linkage between genes controlling qualitative traits (seed color or color patterns) and a quantitative trait (seed weight). Subsequent studies have shown that the P locus, which was one of the seed color genes segregating in the common bean (Phaseolus vulgaris) populations used by Sax, is linked to the Phs locus on linkage group D7. The Phs locus codes for phaseolin, the most abundant seed storage protein in common bean. Variation at this locus had previously been correlated with seed weight in one population. Our goal was to examine wether the Phs locus could be a possible candidate locus for the P locus-linked seed weight QTL identified by Sax. If the association between the Phs locus and seed weight would be observed consistently across a wide range of environments and populations, inside and outside P. vulgaris, this consistency would provide strong circumstantial evidence for our hypothesis. An association between seed weight and phaseolin type was observed through univariate ANOVA's in the five populations that were analyzed here, each of which segregated for seed size and phaseolin type, in addition to two populations analyzed previously. Three populations were grown in more than one season (in a greenhouse) or environment (in the field). Across these seasons or environments, the Phs locus remained consistently associated with seed weight. Depending on the population or the environment, the Phs locus accounted for 18-33% of total phenotypic variation for seed weight. Mapping on the common bean linkage map of probes linked to seed weight QTLs in mung bean or cowpea showed that the QTL associated with the Phs locus appeared to be conserved in mungbean, whereas results were inconclusive for cowpea. Other QTLs for seed weight in the three species appeared not to be conserved. The phaseolin locus is an attractive experimental system to investigate the molecular basis of quantitative variation based onextensive amount of information available on genetic diversity and molecular basis for gene expression at this locus.




INTRODUCTION


In his groundbreaking 1923 paper, Karl Sax proposed a method to locate and enumerate quantitative trait loci (QTLs) on a linkage map through association of the trait with qualitative trait (marker) loci. Specifically, he was able to identify QTLs for seed weight in common bean through associations between seed weight (a quantitative trait showing continuous segregation) and seed color or color patterns (qualitative traits showing a discontinuous segregation).

One of the qualitative traits considered by Sax (1923) was seed color, colored vs. whie corresponding to the presence vs. absence, respectively, of anthocyanins (Feenstra 1960). The major seed weight QTL identified by Sax was associated with seed color. The P locus, which controls seed color, has recently been linked to the Phs locus on linkage group D7 at a distance of approximately 10 cM (Gepts et al. 1993).

The Phs locus codes for phaseolin, the major globulin storage protein, which constitutes about 35-50% of the total seed nitrogen in common bean seeds (Ma and Bliss, 1978). Two major and several minor phaseolin types have been identified on the basis of their banding patterns in one-dimensional SDS polyacrylamide gels (reviewed by Osborn, 1988). The major types found in cultivated germplasm are S (for Sanilac, the cultivar in which S type phaseolin was originally characterized), and T (Tendergreen) (Brown et al. 1982). Together, the 'S' and 'T' types are found in 80% of common bean cultivars (Gepts and Bliss 1988; Gepts et al. 1988). Phaseolin type has been used as a tool to differentiate between both wild and cultivated common beans belonging to the Mesoamerican (S phaseolin type) and Andean (T type) gene pools (Gepts and Bliss, 1986; Debouck et al., 1993; reviewed in Gepts, 1993). The linkage between the P and Phs loci, the nature of the gene product and the strict developmental regulation of the Phs locus (an abundant seed protein) suggested that Phs could be a candidate gene for the major seed weight factor identified by Sax (1923).

Hartana (1983) developed near-isogenic lines (NILs) for different phaseolin types in a Sanilac genetic background to analyze the effects of phaseolin genotype on the agronomic and biochemical characteristics of cultivars. He demonstrated that the T type (and C type) phaseolin was significantly correlated with higher seed weight, increased overall seed protein, and an increase in the percent phaseolin compared to S type phaseolin. Seed yield, however, was not significantly affected by phaseolin type. These findings raised the question whether the same association between phaseolin type and seed weight would also be displayed in other populations and environments.

In this paper, we provide additional evidence supporting the hypothesis that Phs is a candidate gene for a seed weight QTL. We compared previously published and unpublished information on intraspecific variation for seed weight and phaseolin type in P. vulgaris and in the Phaseolinae subtribe, which includes cowpea (Vigna unguiculata) and mung bean (V. radiata), in addition to common bean. We observed, with only few exceptions, a consistent association between allelic variation at the Phs locus and seed weight across a broad range of genetic backgrounds and environments.

MATERIALS AND METHODS


Plant Materials and Field or Greenhouse Experiments


Seven populations were studied or will be discussed here, all of which represent crosses or backcrosses between members of the typically smaller-seeded Mesoamerican and the larger-seeded Andean gene pools. None of the populations used in this study exhibited F1 hybrid weakness (Gepts and Bliss 1985, Singh and Gutiérrez 1984).

Among the populations studied by Sax (1923), the Improved Yellow Eye 1317 (PP;PhsTPhsT) x White 1228 (pp;PhsSPhsS) population (Table 1) is highlighted because it was the only F2 population for which F3 families were observed - thus allowing a separation of the F2 classes into homozygous dominant PP and heterozygous Pp classes. As far as we are aware, however, the genotypes used by Sax (1923) are not available anymore. Analyses of related materials in the Improved Yellow Eye and White classes showed these materials to have 'T' and 'S' type phaseolins, respectively (Gepts and Bliss 1988).

Hartana (1983) developed six pairs of near isogenic lines (NILs) differing at the Phs locus. BBL 240 (Bush Blue Lake 240: PP;PhsTPhsT) was backcrossed to Sanilac (pp;PhsSPhsS), donating T type phaseolin to six BC5S5 lines. These six lines were then backcrossed again to Sanilac and an analysis was performed on the F3 progeny of homozygous F2 individuals grown near Hancock, Wisconsin (Table 1).

Koinange (1992) developed a recombinant inbred population (RIP) between Midas (an Andean derived snap bean cultivar: pp;PhsTPhsT) and the wild Mesoamerican accession G12873 (PP;PhsSPhsS) (population MG). Agronomic evaluation of this population was performed in Popayán, Colombia, as described in Koinange et al. (1996).

Four additional populations were studied by the authors. These were grown in various field and greenhouse locations (Table 1). The F2 generation of population BTS (PP;PhsSPhsS) x Peru34 (PP;PhsTPhsT) was grown in a Davis greenhouse. Because of space limitations, this population was grown in two batches in different seasons. Hundred-seed weights were taken on an individual plant basis.

The F2 generation of cross BAT93 (PP;PhsSPhsS) x Jalo EEP558 (PP;PhsTPhsT) (population BJ) served as the initial mapping population for common bean in Davis. A linkage was established in this population (Nodari et al. 1993a) and a QTL analysis was conducted among F2-derived F3 families for resistance to common bacterial blight and Rhizobium nodulation (Nodari et al. 1993b). This population was also grown in a Davis greenhouse. Hundred-seed weights were taken on an individual plant basis from the F2 generation grown in a Davis greenhouse.

We developed the CY RIP from a cross between the cultivars California Dark Red Kidney (CDRK, Andean origin: PP;PhsTPhsT) and Yolano (Mesoamerican origin: PP;PhsSPhsS) through single seed descent (Table 1, pop. 6). Evaluation of seed weight was performed on greenhouse grown F4:5 families. In addition, we analyzed seed weight in a subset (50 F4:6 RILs) of this population in replicated field trials at Davis and Salinas CA in 1995. Ten seeds for each of the 50 RILs were space planted per 1.02 m plot, with a two plant in-row border between plots. Hundred-seed weight was measured on a per-plot basis by taking a sample of the harvested seed in each plot. Standard agronomic practices were maintained at each site.

The AG RIP was developed by Steve Magnusson of Harris Moran Seed Company (San Juan Bautista, CA) from a cross between the Mesoamerican breeding line A55 (PP;PhsSPhsS) and the Andean-derived cultivar G122 (also known as Jatu Rong: PP;PhsTPhsT). A set of 57 RILs was replicated three times in each of the three field locations - at Davis, Salinas, and the Westside Field Station (near Five Points, CA) (Fig. 1). Field conditions were as above for the CY population.


Laboratory and Statistical analyses


Phaseolin type of individual F2 plants or recombinant inbred lines was determined by one-dimensional SDS/PAGE according to the method of Laemmli (1970) as modified by Ma and Bliss (1978). One-way analyses of variance were performed using Minitab and SAS (PROC GLM) to test for statistical significance of the association between seed weight and Phs segregation. Data analysis was performed using Minitab and SAS.



RESULTS


Phaseolin segregation


Segregation at the phaseolin locus was scored by one-dimensional SDS-PAGE in the populations described in Materials and Methods and Table 1. Chi-square tests indicated that segregation fitted an expected 1:2:1 or 1:1 ratio for F2 or RI populations, respectively. Based on these segregation results, populations were then subdivided into subpopulations corresponding to the segregation classes at the Phs locus. Seed weight was measured on an individual plant (F2) or line (RIP) basis.


Association between phaseolin and seed weight segregations


All populations showed a significant association between genotype at the Phs locus and 100-seed-weight. In all cases except one, the association was significant at the P<0.001 level. The exception was the first season of population BTS x Peru 34 where the association had a significance level of P=0.0018.

The Phs locus accounted for between 18 and 46 percent (R2) of the variation in seed weight depending on the population and the environment from which data was collected (Table 1). Substitution of a lower-weight allele by a higher-weight allele resulted in a seed weight increase of 1 to 6 g/100-seed, depending on the genetic background and the environment.

In the F2 populations studied (the first three populations in Table 1), there was evidence for dominance at the Phs locus. In all three populations, the average 100-seed-weight for heterozygotes was significantly different from that of the TT homozygotes but was not significantly different (Fisher's LSD, 0.05 level) from the average for SS homozygotes. Thus, it appears that the S haplotype, associated with lower seed weight, exhibits some degree of dominance over the T haplotype. Sax (1923) came to a different conclusion (albeit using a different population and a different marker) in his original study (Table 1), where he found evidence for additivity for seed weight associated with the P locus.

When averaged across locations, population A55 x G122 exhibited seed weight phenotypes approximating a normal distribution, with the parents falling towards the upper and lower ends of the curve (Fig. 2). At each location, outliers were observed with average 100-seed-weight greater than or less than the high and low parents, suggesting that both parents carry alleles for both high and low seed weight.


Environmental effects


Seed weight was strongly influenced by environment. When population 6 was grown in replicated trials at Five Points, Davis, and Salinas (Fig. 2), the average 100-seed-weight of RILs was 23, 25, and 34 g, respectively (Fig. 2 ). A Duncan's test and a Fischer's LSD test concluded that seed weights across all locations were significantly different. Seed weight appeared to be negatively related with mean growing temperature (Fig. 2 ).

Population 4 was developed from a cross between the same two parents, and was grown at different times in a greenhouse at Davis. Genotypes at the Phs locus accounted for 18% of the variation in seed weight in season 1, but then accounted for 32% of the variation in season 2, presumably due to environmental differences interacting with the same type of population.

Notable G x E interactions were observed for seed weight in population 7 and its parents. Particularly interesting was the behavior of the A55 parent, which averaged 17 g at Davis and 20 g at Five Points. Most genotypes, however, had larger seeds at Davis than at Five Points.

Stability of seed weight across environment was analyzed according to Lin et al. (1986). They suggested that stability can be viewed as a) (Type I) a lack of variability across environments (quantified by Francis and Kannenberg (1978) as the coefficient of variation, CV = Variance/Mean, reflecting the biological concept of homeostasis) or b) (Type II) a response to environmental variations parallel to that of the average of the genotypes under consideration. In the replicated field trials of population 7, several genotypes were notably more stable (Type I) than others: for example, CV (AG 54) = 0.01, while CV (AG 57) = 4.60 [CV(mean) = 1.14, CV(standard deviation) = 0.76). However, an analysis of variance found no evidence for differential Type I stability based on Phs locus genotype (i.e. 'S' vs. 'T' phaseolin genotypes).

Finlay and Wilkinson (1963) quantified Type II stability as the regression coefficient of the trait on an environmental index for the trait (the average of all genotypes across the set of experimental environments). The values for Type II stability of the RILs lead to different conclusions - the R2 value for AG 54 was the lowest at 0.58, while the R2 value for AG57 was among the highest at 0.99 (average R2 = 0.92, R2 (std. dev.) = 0.09). An analysis of variance found no significant relationship between Type II stability and genotype at the Phs locus.


Association between seed weight and yield.


When the data for all three locations was analyzed jointly there was a statistically significant yet small positive association between yield and 100-seed-weight (R2 = 0.17, P = 0.000) and between yield/day (adjusted yield) and 100-seed weight (R2 = 0.08, P = 0.000). This was apparently due to the association of larger seed weight with higher yield across, rather than within locations. Analyzed separately, no significant associations were observed at Davis and Five Points. However, in one location (Salinas) average 100-seed-weight was negatively correlated with adjusted yield (R2 = 0.09, P = 0.02).

Closer examination of the data revealed that most of the largest-seeded RILs in Salinas were also lines exhibiting symptoms of partial infertility (extremely low harvest index, production of parthenocarpic pods). Problems with viability and fertility in the progeny of crosses between the gene pools of common bean are well documented (Coyne, 1965 and 1969; Finke et al.,1986; Gepts and Bliss, 1985; Singh and Gutiérrez, 1984; Singh and Molina, 1991).

Because reduced seed set can lead to increased seed size through yield component compensation, we hypothesized that the negative association of seed yield and seed weight in Salinas was due to statistical outliers (low yield / high seed weight) caused by the relatively few lines exhibiting reduced fertility. To test this hypothesis, we removed the five lines exhibiting the most severe symptoms of infertility at Salinas from the data set (those with an adjusted yield per plot of less than 1.5 grams per day) and performed the analysis again. In the second analysis, no significant associations between yield and seed weight could be observed (R2 = 0.008, P = 0.517).

Relationship with seed weight factors in related legume genomes


Phaseolin is a vicilin-like protein that is conserved among a wide range of taxa inside and outside the Fabaceae (Borroto and Dure 1987). In particular, it is conserved within the Phaseolinae subtribe, which includes both Phaseolus and Vigna (Panella et al. 1993; Kami and Gepts, unpubl. results). The conservation of phaseolin in these two genera raises the possibility that phaseolin (or vignin as it is known in Vigna spp.) would be associated with an effect on seed weight not only in P. vulgaris but also in Vigna spp. [Vigna unguiculata (cowpea) and V. radiata (mung bean)]. Fatokun et al. (1992) had identified an apparent conservation of a major seed weight QTL between cowpea and mung bean. We were therefore interested in determining whether any of the Vigna seed weight QTLs would map near the phaseolin locus.

In P. vulgaris, seed weight QTLs have been identified in two populations, BAT93 x Jalo EEP 558 and Midas x G12873. In the latter population (population 3) (Koinange et al. 1996), two QTLs for seed weight explaining 27 and 18% of the variation for this trait were mapped to linkage groups D7 and D1, respectively. Two major QTLs mapped to the same regions on linkage groups D1 (accounting for 17% of the variance) and D7 (28%) in the BAT93 x Jalo EEP558 population (5) (Nodari 1992). The location of the overlapping QTLs on linkage group D7 on the common bean map span the phaseolin locus. Two additional QTLs with smaller effects were detected on linkage groups D7 (15%) and D11 (16%) in population Midas x G12873 (Koinange et al. 1996) and on linkage groups D3 (11%) and D4 (10%) in population BAT93 x Jalo EEP558 (Nodari 1992) (Table 2).

To correlate the QTLs identified in P. vulgaris with those identified in V. unguiculata and V. radiata (Fatokun et al. 1992), probes linked to QTLs in mungbean and cowpea were mapped in a P. vulgaris recombinant inbred population derived from the cross BAT93 x Jalo EEP558 (population 5). Their map location was then compared with that of the previously identified seed weight QTLs in P. vulgaris (Nodari 1992; Koinange et al. 1996).

Marker Bng199, closely linked to markers A955 and A515, which mark a seed weight QTL on mung bean linkage group 4 (Fatokun et al. 1992; N. Young, pers. comm.), mapped to common bean linkage group D7 at approximately 10 cM of the Phs locus. While the common bean QTL on linkage group D7 was the major seed weight QTL in that species, it was only a minor QTL in mung bean (Fatokun et al. 1992). There was no apparent QTL matching this seed weight QTL in cowpea (Table 2).

Marker O103 located near a major QTL for seed weight in cowpea (36.5%) and mungbean (32.5%) (Fatokun et al. 1992) mapped to common bean linkage group D3. The mapping distance was 45 cM between O103 and D1132, the marker most closely linked to a common bean seed weight QTL (Nodari 1992). The large linkage distance suggests that these may actually be different QTLs.

The other two QTLs identified in mung bean, on linkage groups 3 and 11, mapped to common bean linkage group D2 and D5 or D7, respectively. No common bean QTLs for seed weight have so far been identified in these regions (Table 2). Likewise, an additional QTL in cowpea for seed weight on linkage group 7, mapped to common bean linkage group D8, to which no seed weight QTL had been mapped in that species thus far.

Inspection of Table 2 revealed that generally QTLs for seed weight were not conserved across the populations used for these three species with the possible exception of the QTL associated with the Phs locus.



DISCUSSION


Phs as the candidate locus for a seed weight QTL identified by Sax (1923)


Our results show that in all of the P. vulgaris populations analyzed here the Phs locus was associated with seed weight differences. Although the parents of these populations - and the populations studied by Sax (1923), Hartana (1983), and Koinange (1992) - represent a diverse germplasm, they shared one characteristic, namely segregation at the Phs locus. One of the parents had an 'S' or 'M' phaseolin type (of Mesoamerican origin) and the other a 'T' phaseolin type (of Andean origin).

The P locus, initially identified by Sax (1923) as marking a genomic region carrying a QTL for seed weight, was segregating in only three out of 8 populations listed in Table 1 (IYE 1713 x White 1228, Sanilac x BBL 240, and Midas x G12873). This suggests strongly that some other gene or genes in the vicinity of P rather than P itself is involved in seed weight differences. The results of Hartana (1983) indicating a correlation between phaseolin type and seed weight, suggest that Phs may be the QTL for seed weight that was segregating in Sax's (1923) populations. Alternatively, any locus tightly linked to Phs could also be a candidate locus. This latter suggestion is perhaps less likely because it assumes that the linkage disequilibrium between Phs and the QTL for seed weight would have been maintained throughout the evolutionary history of common bean. Indeed, the relationship between Phs and seed weight was observed also in the cross between G12873 and Midas, representing a wild common bean from the Mesoamerican gene pool and a cultivar from the Andean gene pool, respectively. In that cross, both the Phs and P loci were segregating. The magnitude of the effect (R2) on seed weight associated with the Phs locus was slightly higher (27%) than that associated with the P locus (22%) consistent with the hypothesis that the seed weight factor is not associated with the P locus but rather with the Phs locus.

More definitive evidence on the role of the Phs locus as a candidate locus for a seed weight QTL should come from transformation experiments. For example, S phaseolin genotypes could be transformed with T phaseolin genes under control of the appropriate regulatory sequences. The transformants could then be observed for any increase in seed weight.

Beavis et al. (1991) suggested that most QTLs are in close proximity to mapped qualitative genetic loci and that "qualitative genetic loci are the same loci that affect quantitative traits." This statement was based on the observation that a number of QTLs affecting plant height in maize mapped to chromosomal regions known to carry genes conditioning dwarfism. Mansur et al. (1993) also implicitly speculated on the association of qualitative and quantitative genes, noting that "the markers associated with the QTL explaining the major portion of the phenotypic variance for seed oil mapped to linkage group 3, which also contains the structural gene for thiol protease, a protein associated with seed oil bodies." The association between seed weight in common beans and the phaseolin locus is additional evidence that, in some cases, genes conditioning quantitative traits may indeed be genes with discreet qualitative effects.


A discrepant observation


Vallejos and Chase (1991) attempted to associate seed weight data with a number of segregating isozyme markers and the Phs locus in a cross between a breeding line (XR-235) and an Andean cultivar (Diacol Calima). In this population, they determined that a locus linked to the Adh-1 and Got-2 isozyme loci accounted for 30 to 50 % of the seed weight difference between the parents. Surprisingly, the Phs locus did not have a significant association with seed weight in this population. It is important to note that the XR-235 breeding line is the inbred progeny of an interspecific cross between P. vulgaris and P. coccineus (Freytag et al., 1982). As a result, this population may be segregating for a number of seed storage proteins not normally expressed in cultivated P. vulgaris or for which the species is monomorphic. A related possibility is that the introgression of factors affecting seed weight from the related species P. coccineus has resulted in a major shift in patterns of gene expression. Seed weight among cultivated P. coccineus is notably larger than that of cultivated P. vulgaris. The factors affecting seed weight which were selected for in the domestication of these two species resulted in much greater gain from selection in P. coccineus than in P. vulgaris. The seed weight exhibited by the inbred progeny of a single cross between these two species is undoubtedly a function of genes from both species, and the factors contributed by the P. coccineus parent may have a far stronger affect on seed weight than those contributed by P. vulgaris.

Evolutionary conservation (or the lack thereoff) of seed weight QTLs


The major conclusion of the comparative mapping studies of seed weight QTLs among the genomes of common bean, cowpea, and mung bean, is that these QTLs are generally not conserved. There are many possible reasons for this observation, including the differences in genetic background and environmental conditions prevailing during the experiments.

A possible exception to the lack of conservation is the QTL associated with the Phs locus, which was observed in all P. vulgaris populations and in mung bean but not cowpea. The absence of any detectable QTL in cowpea around the locus equivalent to phaseolin may be due to absence of segregation at or near that locus for seed weight factors, or the presence of a QTL below the detection limits of the experiment conducted by Fatokun et al. (1992).

Seed weight in common bean as a quantitative trait model system

If factor(s) affecting seed weight are in fact located at or near the Phs locus, this relatively tight linkage could explain why Sax observed a significant association between seed color and seed weight characters. The associations between Phs genotype and seed weight and between Phs genotype and phaseolin expression, as well as observations of environmental and genetic background components to the expression of these traits, suggest that seed weight and phaseolin expression exhibit many of the characteristics of classical quantitative traits. In addition, the availability of accessions with presumed ancestral phaseolin sequences (Kami et al. 1995), genomic and cDNA clones of the Phs locus (Slightom et al. 1985, Kami and Gepts 1994), sequence information for the Phs locus (Slightom et al. 1985, Kami and Gepts 1994), regulation and gene organization information from transgenic expression studies (Kawagoe and Murai, 1992, van der Geest et al. 1994), agronomic data from multilocation field tests (Hartana 1983, Singh et al. 1992 a,b, and present data), and a number of populations segregating for this trait provides an opportunity to attempt to characterize the expression of a quantitative trait at the molecular level. Hence, seed weight in common bean represents an attractive model system for the molecular analysis of quantitative trait variation.


Acknowledgements We are grateful to Robert Lewellen of the USDA Agricultural Research Station, Salinas, CA, and Steve Temple and Donald Helms of UC Davis, for providing space, maintenance, and agronomic advice for the field tests. Additional field help was kindly provided by David Posner, Leslie Goldberg, Denise Flanahan, Christhiam Cano, Asgar Shirmohamadali, Rosanna Freyre, Christa Haney, and Hau Truong. This work was supported in part by the US AID Bean/Cowpea CRSP and the California Dry Bean Advisory Board.



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Table 1. Relationship between seed weight and segregation at the P or Phs locia

Table 2. Putative seed weight QTL correspondence among common bean, cowpea, and mung beana

_________________________________________________________________
          Common bean        
________________________________________     Cowpea      Mungbean
LG   Markers                MG      BJ         LG           LG
_________________________________________________________________

D1   D1492-3, Pal-1        Yes      Yes         No           No
D2   M78                   No       No          No           3
D3   D1132                 No       Yes         No           No
D3   D1009,O103            No       No          2            1
D4   D1011                 No       Yes         No           No
D7   Phs,Bng199            Yes      Yes         No           4
D7   Uri-2                 Yes      No          No           No
D8   Bng7, Bng138, A816    No       No          7            No
D11  D0252                 Yes      No          No           No
D5 (Bng166) or D7 (Bng222) No       No          No           11 
_________________________________________________________________
a Based on results of Koinange et al. (1996) and Nodari (1992)
for common bean and Fatokun et al. (1992) for cowpea and mungbean