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 Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Huh, M. K. Articles by Huh, H. W. Search for Related Content PubMed Articles by Huh, M. K. Articles by Huh, H. W. Agricola Articles by Huh, M. K. Articles by Huh, H. W. Related Collections Other Legumes Crop Genetics

PLANT GENETIC RESOURCES

Genetic Diversity and Population Structure of Wild Lentil Tare

H.W. Huh, Department of Biology Education, Pusan National University, Pusan, 609-735, The Republic of Korea

* Corresponding author: Man Kyu Huh (e-mail: mkhuh200{at}yahoo.co.kr)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Genetic diversity has been studied extensively in the cultivated faba bean (Vicia faba L.). Compared with other ecologically and economically significant herbaceous species, population structure of lentil tare, Vicia tetrasperma (L.) Schreber (Leguminosae), has not been studied. The objectives of this study were to estimate the level of genetic diversity in the species and to describe how its genetic variation is distributed within and among its populations. The percentage of polymorphic loci was 50.0%. Genetic diversity was high at both the species and population levels , whereas the extent of the population divergence was relatively low . In the hierarchical analysis, a great amount of variance was exhibited among populations with respect to regions and a large component of the value was explained by variance among regions with respect to the total . The results were consistent with the strong geographic effect indicated by unweighted pairwise groups method using arithmetic average (UPGMA) and Mantel's test. The correlation between genetic distance and geographic distance by Mantel's test was high and significant . F_is, a measure of the deviation from random mating within populations, was 0.503, indicating that V. tetrasperma is an inbreeding species. An indirect estimate of the number of migrants per generation indicated that gene flow was high among populations. Nearly 88.4% of the total genetic diversity in V. tetrasperma was apportioned within populations. The wide geographic ranges, wild condition of the species, and high fecundity are proposed as possible factors contributing to high genetic diversity.

Abbreviations: UPGMA, unweighted pairwise groups method using arithmetic average

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
THE GENUS VICIA is comprised of approximately 140 widely distributed species most commonly in temperate regions of Europe, Asia, and America (Weber and Schifino-Wittman, 1999). Vicia tetrasperma is distributed mostly in the temperate regions of both hemispheres. It is typically found in low mountain regions in Korea and Japan, where it grows at elevations as low as 300 m above sea level. In addition, wild lentil tare plants grow in fallow fields, under hedgerows, and along roadsides and riverbanks. Populations of V. tetrasperma are typically small and distributed in patches.

Many studies have been conducted on the cultivated faba bean (Amet, 1986; Mancini et al., 1989; Przybylska et al., 1992; Suso et al., 1993; Torres et al., 1995), but there are only a few isozyme studies in other lentil tare species (Yamamoto and Plitmann, 1980; Yamamoto, 1986; Leonards and Muller, 1990). Most of the isozyme analyses of Vicia have been used in evolutionary and taxonomic studies (Yamamoto, 1975; Yamamoto and Plitmann, 1980), inbred-line recognition (Bassri and Rouhani, 1977; Kaser and Steiner, 1983), and outcrossing rate estimation (Peat and Adham, 1984; Suso et al., 1993; Zhang and Mosjidis, 1998). Zhang and Mosjidis (1998) reported that most Vicia species were mix-mating system. Although molecular and biochemical approaches are now increasingly being applied to address the taxonomic and phylogenetic relationships within the subgenus Vicia (Potokina et al., 1999), no population genetics studies have been conducted, especially on the population genetic structure of lentil tare species.

Vicia tetrasperma is a profusely flowering annual, with autogamous magenta flowers that are occasionally visited by some insect species. Genetic diversity has been studied extensively in the cultivated faba bean (Amet, 1986; Yamamoto, 1986; Jaaska, 1997). Grain legume crops contribute significantly to the total farm products in the world (Muehlbauer et al., 1985). Although the numbers of farms have decreased in recent years, the areas sown to lentil have increased in the United States (USA Dry Pea and Lentil Council, 1991). This increase reflects the rising demands from foreign markets, as well as those of an expanding domestic market. Compared with other ecologically and economically significant herbaceous species, population structure of lentil tare has not been studied. The objectives of this study were to estimate the level of genetic diversity in the species and to describe how its genetic variation is distributed within and among its populations.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Sampling Procedure and Enzyme Electrophoresis
Vicia tetrasperma was collected from 17 populations in Korea and Japan (Fig. 1) . One leaf per plant was collected during the period from 1999 to 2000. Forty-five to 64 plants were sampled from each population. All samples were placed on ice until isozyme extraction. Approximately 300 to 500 mg of leaf tissue were ground with a cold mortar and pestle in 300 to 500 µL of extraction buffer (0.05 mL 0.1% 2-mercaptoenthanol, 0.001 M EDTA, 0.01 M KCl, 0.01 M magnesium chloride hexahydrate, 1 g 4% w/v PVP, 0.10 M Tris-HCl buffer, pH 8.0).

View larger version (36K): [in this window] [in a new window]   Fig. 1. Collection localities for populations of Vicia tetrasperma as sources for allozyme analysis.

Isozyme bands were assigned to putative loci based on analysis of observed variation patterns. For example, the most anodal isozyme locus was arbitrarily designated "1" and subsequent isozymes were assigned sequentially higher numbers. Likewise, alleles at each locus were designated sequentially with the most anodally migrating allozyme designated "a" and progressively slower forms "b", "c", and so on. All V. tetrasperma allozymes expressed phenotypes that were consistent in subunit structure and genetic interpretation with most other allozyme studies of plants (Weeden and Wendel, 1989).

Data Analysis
The following genetic parameters were calculated using a computer program developed by Loveless and Schnabel (Edwards and Sharitz, 2000): percentage polymorphic loci (P_p for population level and P_s for species level), mean number of alleles per locus (A), effective number of alleles per locus (A_e), and gene diversity (H_e) (Hamrick et al., 1992). Species (indicated with the subscript _S) and mean population (indicated with the subscript _P) levels of genetic diversity were calculated as in Hamrick and Godt (1989). Observed heterozygosity (H_o) was compared with Hardy–Weinberg expected values using Wright's fixation index (F) or inbreeding coefficients (Wright, 1965). These indices were tested for deviation from zero by ² statistics following Li and Horvitz (1953). Nei's gene diversity formulae (H_t, H_s, D_st, and G_st) were used to evaluate the distribution of genetic diversity within and among populations (Nei, 1973, 1977). The G_st coefficient, in particular, estimates relative degree of population differentiation. In addition, ² statistics were used to detect significant differences in allele frequencies among populations for each locus (Workman and Niswander, 1970).

Nei's genetic identity (I) and genetic distance (D) were calculated for each pairwise combination of populations (Nei, 1972). Populations were clustered via UPGMA (SAS Institute, 1989). Bootstrapping was done using the PAUP (or PHYLIP) program to estimate the relative support for clades (Felsenstein, 1993).

The genetic structure within and among populations was also evaluated using Wright's (1965) F statistics: F_it, F_is, and F_st. F_it and F_is measure excesses of homozygotes or heterozygotes relative to panmictic expectations, within samples and within populations, respectively. Deviations of F_it and F_is from zero were tested using ² statistics (Li and Horvitz, 1953). Two indirect estimates of gene flow were calculated. Estimates of the number of migrants per generation (N_m) were based on G_st or the average frequency of private alleles, found in only one population (Slatkin, 1985). Genetic diversity was tested against regions by Spearman rank to seek any correlation between genetic variation in populations and the regions (Zar, 1984). Correlation between geographical and genetic distances was tested using a modified Mantel's test (Smouse et al., 1986).

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Genetic Diversity
At the species level, 16 of the 32 loci (50.0%) showed detectable polymorphism in at least one population (Table 1). The remaining 16 loci (Acp-4, Got-1, Idh-1, Lap-1, Lap-2, Mdh-2, Mdh-4, Mdh-5, Per-3, Per-4, Pgd-1, Pgd-2, Pgi-1, Pgm-1, Sod-2, and Skd-1) were monomorphic in all populations. An average of 44.7% of the loci were polymorphic within populations, with individual population values ranging from 37.5 to 50.0%. The average number of alleles per locus (A_p) was 1.57 across populations, varying from 1.50 to 1.66. The effective number of alleles per locus (A_e) was similar at the species and population levels . The mean genetic diversity within populations was 0.158. Population KO4 had the highest expected diversity (0.189), while population JP3 had the lowest (0.131). Genetic diversity at the species level was 0.171. Significant differences in allele frequencies among populations of V. tetrasperma were found in 14 of the 16 polymorphic loci.

Genetic diversity of V. tetrasperma is comparable with other Vicia species, although the use of different methods (e.g., the number of loci, populations sampled, and the enzyme systems studied) may preclude meaningful direct comparisons. Yamamoto and Plitmann (1980) analyzed 24 Vicia species by disc electrophoresis. It is impossible to compare the results directly; however, V. sativa had at least a moderate or high level of genetic variation in the four enzyme systems that were used for isozyme analysis. Jaaska (1997) used polyacrylamide gel electrophoresis to study 21 Vicia species of the subgenus Vicia and pale flowered vetch (Vicilla pisiformis L.) of the subgenus Vicilla. P_s of V. tetrasperma was 25% and P_s of V. tetrasperma in this study was 50%. Other parameters cannot be estimated in their tables because no data for gene frequency were shown. Weber and Schifino-Wittman (1999) conducted karyotype, phenological, and morphological analyses of 37 taxa of Vicia. Vicia tetrasperma was found to be widespread and highly polymorphic.

The relatively high level of genetic variation found in V. tetrasperma is consistent with several aspects of its biology. First, geographic range has been shown to be strongly associated with the level of variation maintained within populations and at the species level (Hamrick and Godt, 1989). Widely distributed plant species tend to maintain more variation than more narrowly distributed species. Vicia tetrasperma is found throughout Europe, Asia, and America (Yamamoto and Plitmann, 1980; Potokina, 1997; Weber and Schifino-Wittman, 1999). Secondly, plant species with high fecundity usually maintain high genetic diversity (Huh, 1999). Wild lentil tare flowers profusely. Individual plants produce hundreds of seeds under field conditions (Potokina, 1997). We observed that each mature plant produces 70 to 150 seeds, indicating high reproductive capacity. Thirdly, high genetic diversity is associated with the species' colonizing success (Sun, 1997). Colonizing species are often expected to be markedly depauperate in genetic variation within populations due to founder effects and genetic drift (Sun and Corke, 1992). Vicia tetrasperma has maintained a considerable amount of variation during the colonization process, despite being predominantly inbred. During colonization, individuals with high genetic diversity may survive natural selection. Finally, the presumed progenitors or wild types usually store great amounts of genetic variation and show higher variability than those of most crops (Clegg et al., 1984; Doebley, 1989; Escalante et al., 1994). As has been shown in most cultivated species, the domestication process has eroded the levels of genetic variation of the cultivated populations (Doebley, 1989). Some species of the genus Vicia are included among the oldest domesticated plants (Kupicha, 1976; Hanelt and Mettin, 1989). As wild lentil tare is more long-lived than cultivated lentil tare, opportunities for the accumulation of mutations should be high (Ledig, 1986). Longevity of individuals in annual plants may play an important role in maintaining high levels of genetic variability (Huh, 1999).

Population Structure
F_is, a measure of the deviation from random mating within the 17 populations, was 0.503, ranging from 0.214 (Mdh-3) to 0.697 (Sod-3) (Table 2). The observed significant and positive F_is value (0.503) indicates that there was a significant deficit of heterozygotes in the populations. Analysis of fixation indices, calculated for all polymorphic loci in each population, showed a slight deficiency of heterozygotes relative to Hardy–Weinberg expectations (Table 3). For example, 96.7% of fixation indices were positive (234/242), of which 200 indices (85.5%) departed significantly from zero (P < 0.05). Only eight indices (3.3%) were negative, and none of them deviated significantly from zero.

View larger version (13K): [in this window] [in a new window]   Fig. 2. A dendrogram, based on genetic distance data, showing the genetic relationships among the 17 populations of Vicia tetrasperma.

Mean genetic identity between populations is very high , but it is unclear how the populations are genetically homogeneous. It is highly probable that directional movement toward genetic similarity in a relatively homogeneous habitat (i.e., fallow fields, hill habitats, open ground, and colonizing sites) operates among the populations of V. tetrasperma.

In addition, the correlation between genetic distance and geographic distance was high and significant , indicating that geographically close populations tended to be genetically similar and about 64% (1 - r²) of the variation in genetic distance is due to unknown factors other than distance.

In the hierarchical analysis, the large variance exhibited among populations with respect to regions and a large component of the value was explained by variance among regions with respect to the total , a result consistent with the strong geographic effect indicated by UPGMA and Mantel's test (the correlation between geographic and genetic distances). Although genetic diversity was not significantly correlated with regions (r_s = 0.514, Spearman rank correlation), measures of genetic diversity for the Japanese populations were lower than those for Korean populations (Table 1). As revealed by earlier studies (Yamamoto and Plitmann, 1980; Potokina, 1997; Weber and Schifino-Wittman, 1999; Zhang and Mosjidis, 1998), the genus Vicia could have originated in the Mediterranean region and Western Asia. If this hypothesis is correct, it is possible that the Japanese V. tetrasperma populations trace to introductions from Western Asia via Korea or China.

A substantial heterozygote deficiency occurred in some populations and at some loci . Population structuring is not obvious, and, as a result, a sample may consist of a group of heterogeneous subsamples from a population. If there are fairly large differences in allelic frequencies among these subsamples, when they are lumped together there will be a net deficiency of heterozygotes and an excess of homozygotes even if Hardy–Weinberg proportions exist within each subsample (Wahlund, 1928). Our sampling included individuals from several patches per population, resulting in an overall deficiency of heterozygotes. This sampling method created a Wahlund effect in our results (Hartl and Clark, 1989). It is probable that the combination of these factors may contribute to heterozygote deficiencies within these populations. In addition, if breeding systems and a Wahlund effect affect the population genetic structure, all F values for polymorphic loci should show similar patterns in a single population. The F values were nonsignificant among polymorphic loci (Bartlett test, P < 0.05). This suggests that for V. tetrasperma the evolutionary forces (e.g., selection factor) were similar in their impact upon 16 polymorphic loci.

	CONCLUSIONS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 
Vicia tetrasperma maintained high levels of allozyme variation. A striking feature of this study is the lack of intrapopulation variation. The most variation was exhibited within populations with respect to regions. A combination of wide geographical distribution, wild species, and a propensity for high fecundity may explain the high level of genetic diversity within populations. These factors should be taken into account both in conservation programs and for the genetic improvement of this economically very important wild Vicia species.

Received for publication December 14, 2000.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSIONS REFERENCES

 

• Amet, T.A. 1986. Geographical patterns of allozyme variation in a germplasm collection of faba bean (Vicia faba L.). FABIS Newsl. 16:5–12.
• Bassri, A., and I. Rouhani. 1977. Identification of broad-bean cultivars based on isoenzyme patterns. Euphytica 26:279–286.
• Clegg, M.T., A.H.D. Brown, and P.R. Whitfield. 1984. Chloroplast DNA diversity in wild and cultivated barley: implications for genetic conservation. Genet. Res. 43:339–343.[ISI]
• Doebley, J. 1989. Isozymic evidence and the evolution of crop plants. p. 165–191. In D.E. Soltis and P.S. Soltis (ed.) Isozymes in plant biology. Dioscorides, Portland, OR.
• Edwards, A.L., and R.R. Sharitz. 2000. Population genetics of two rare perennials in isolated wetlands: Sagittaria isoetiformis and S. teris (Alismataceae). Am. J. Bot. 87:1147–1158.[Abstract/Free Full Text]
• Escalante, A.M., G. Coello, L.E. Eguiarte, and D. Piñero. 1994. Genetic structure and mating systems in wild and cultivated populations of Phaseolus coccineus and P. vulgaris (Fabaceae). Am. J. Bot. 81:1096–1103.[ISI]
• Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package) version 3.5s. Distributed by the author. Department of Genetics, Univ. Washington, Seattle, WA.
• Hamrick, J.L. 1987. Gene flow and distribution of genetic variation in plant species. p. 53–67. In K. Urbanska (ed.) Differentiation patterns in higher plants. Academic Press, New York, NY.
• Hamrick, J.L., and M.J.W. Godt. 1989. Allozyme diversity in plant species. p. 43–63. In A.D.H. Brown et al. (ed.) Plant population genetics, breeding and genetic resources. Sinauer, Sunderland, MA.
• Hamrick, J.L., M.J.W. Godt, and S.L. Sherman-Broyles. 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6:95–124.
• Hanelt, P., and D. Mettin. 1989. Biosystematics of the genus Vicia L. (Leguminosae). Annu. Rev. Ecol. Syst. 20:199–223.[ISI]
• Hartl, D.L., and A.G. Clark. 1989. Principles of population genetics. 2nd ed. Sinauer Assoc., Sunderland, MA.
• Huh, M.K. 1999. Genetic diversity and population structure of Korean alder (Alnus japonica: Betulaceae). Can. J. For. Res. 29:1311–1316.
• Jaaska, V. 1997. Isozyme diversity and phylogenetic affinities in Vicia subgenus Vicia (Fabaceae). Genet. Resour. Crop Evol. 44:557–574.
• Kaser, H.R., and A.M. Steiner. 1983. Subspecific classification of Vicia faba L. by protein and isozyme patterns. FABIS Newsl. 7:19–20.
• Kupicha, F.K. 1976. The infrageneric structure of Vicia. Edinburgh J. Bot. 34:287–326.
• Ledig, F.T. 1986. Heterozygosity, heterosis, and fitness in outbreeding plants. p. 77–104. In M.E. Soule (ed.) Conservation biology. Sinauer Press, Sunderland, MA.
• Leonards, C., and H.P. Muller. 1990. Populationsgenetik und artenshutz-untersuchungen zur genetischen variabilitat in wild populationen der gattung Vicia in Rheinland und in der Eifel. Dechenia 143:196–208.
• Li, C.C., and D.G. Horvitz. 1953. Some methods of estimating the inbreeding coefficient. Am. J. Hum. Genet. 5:107–117.[ISI][Medline]
• Mancini, R., C. De Pace, G.T. Scaracia-Mugnozza, V. Delre, and D. Vittori. 1989. Isozyme genetic markers in Vicia faba L. Theor. Appl. Genet. 77:657–667.
• Muehlbauer, F.J., J.I. Cubero, and R.J. Summerfield. 1985. Lentil. p. 266–311. In R.J. Summerfield and E.H. Roberts (ed.) Grain legume crops. Collins, London, UK.
• Nei, M. 1972. Genetic distance between populations. Am. Nat. 106:282–292.
• Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA 70:3321–3323.[Abstract/Free Full Text]
• Nei, M. 1977. F-statistics and analysis of gene diversity in subdivided populations. Ann. Hum. Genet. 41:225–233.[ISI][Medline]
• Peat, W.E., and J.Y. Adham. 1984. The use of isozyme genes as markers in the population genetics of Vicia faba L. p. 109–117. In G.P. Chapman and S.A. Tarawai (ed.) Systems for cytogenetic analysis in Vicia faba L. Nijhoff, Dordrecht, the Netherlands.
• Potokina, E.K. 1997. Vica sativa L. aggregate (Fabaceae) in the flora of the former USSR. Genet. Resour. Crop Evol. 44:199–209.
• Potokina, E.K., N. Tomooka, D.A. Vaughan, T. Alexandrova, and R.Q. Xu. 1999. Phylogeny of Vicia subgenus (Fabaceae) based on analysis of RAPDs and RFLP of PCR-amplified chloroplast genes. Genet. Resour. Crop Evol. 46:149–161.
• Przybylska, J., Z. Zimniak-Przybylska, and P. Krajewski. 1992. Isozyme variation in the genetic resources of Vicia faba L. Genet. Polon. 33:17–25.
• SAS Institute. 1989. SAS/STAT user's guide: Ver. 6. SAS Inst., Cary, NC.
• Slatkin, M. 1985. Rare alleles as indicators of gene flow. Evolution 39:53–65.[ISI]
• Smouse, P.E., J.C. Long, and R.R. Sokal. 1986. Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst. Zool. 35:627–632.
• Soltis, D.E., C.H. Haufler, D.C. Darrow, and G.J. Gastony. 1983. Starch gel electrophoresis of ferns: A compilation of grinding buffers, gel and electrode buffers, and staining schedules. Am. Fern J. 73:9–27.[ISI]
• Sun, M. 1997. Population genetic structure of yellow starchistle (Centaurea solstitialis), a colonizing weed in the western United States. Can. J. Bot. 75:1470–1478.
• Sun, M., and H. Corke. 1992. Population genetics of colonizing success of weedy rye in northern California. Theor. Appl. Genet. 83:321–329.
• Suso, M.J., M.T. Moreno, and J.I. Cubero. 1993. New isozyme markers in Vicia faba—Inheritance and linkage. Plant Breed. 111:170–172.
• Torres, A.M., Z. Satovic, J. Canovas, S. Cobos, and J.I. Cubero. 1995. Genetics and mapping of new isozyme loci in Vicia faba L. using trisomics. Theor. Appl. Genet. 91:783–789.
• USA Dry Pea and Lentil Council. 1991. USA Dry Pea and Lentil Updates, 1990–1991. USA Dry Pea and Lentil Industry, Moscow, ID.
• Wahlund, S. 1928. Zusammersetung von populationen und korrelation-sercheiunungen von standpunkt der verebungslehre aus betrachtet. Hereditas 11:65–106.[ISI]
• Weber, L.H., and M.T. Schifino-Wittman. 1999. The Vicia sativa L. aggregate (Fabaceae) in Southern Brazil. Genet. Resour. Crop Evol. 46:207–211.
• Weeden, N.F., and J.F. Wendel. 1989. Genetics of plant isozymes. p. 42–72. In D.E. Soltis and P.S. Soltis (ed.) Isozymes in Plant Biology. Dioscorides, Portland, OR.
• Workman, P.L., and J.D. Niswander. 1970. Population studies on southern Indian tribes. II. local genetic differentiation in the Papago. Am. J. Hum. Genet. 22:24–49.[ISI][Medline]
• Wright, S. 1951. The genetical structure of populations. Ann. Eug. 15:313–354.
• Wright, S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395–420.[ISI]
• Yamamoto, K. 1975. Estimation of genetic homogeneity by isozymes from interspecific hybrids of Vicia. I. Japan. J. Breed. 29:59–65.
• Yamamoto, K. 1986. Interspecific hybridization among Vicia narbonensis and its related species. Biol. Zbl. 105:181–187.
• Yamamoto, K., and U. Plitmann. 1980. Isozyme polymorphism in species of the genus Vicia (Leguminosae). Japan. J. Genet. 55:151–164.
• Zar, J.H. 1984. Biostatistical analysis. 2nd ed. Prentice-Hall, Englewood Cliffs, NJ.
• Zhang, X., and J.A. Mosjidis. 1998. Rapid prediction of mating system of Vicia species. Crop Sci. 38:872–875.[Abstract/Free Full Text]

This article has been cited by other articles:

				B. S. Bushman, S. R. Larson, M. D. Peel, and M. E. Pfrender Population Structure and Genetic Diversity in North American Hedysarum boreale Nutt. Crop Sci., May 31, 2007; 47(3): 1281 - 1288. [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 Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Huh, M. K. Articles by Huh, H. W. Search for Related Content PubMed Articles by Huh, M. K. Articles by Huh, H. W. Agricola Articles by Huh, M. K. Articles by Huh, H. W. Related Collections Other Legumes Crop Genetics