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Published in Crop Sci. 43:1602-1609 (2003).
© 2003 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA

CROP BREEDING, GENETICS & CYTOLOGY

Translocation Breakpoints in Soybean Classical Genetic Linkage Groups 6 and 8

A. Assibi Mahama and Reid G. Palmer*

USDA-ARS-CICGR and Dep. of Agronomy and Zoology/Genetics, Iowa State Univ., Ames, IA 50011

* Corresponding author (rpalmer{at}iastate.edu).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Reciprocal chromosome translocations are important for locating genes to linkage groups (LGs). Identifying the chromosomes involved in translocations is necessary for the isolation of tester sets. Our objectives were (i) to determine the location of translocation breakpoints by testing linkage with loci of Classical Linkage Group (CLG) 6 (Df2 and Y11), CLG 8 (Adh1, Ms1, Wm, Ms6, St5, W1, and Y23), and other CLGs, and (ii) to confirm the orientation of these nine marker loci. The ‘KS172-11-3’, ‘KS175-7-3’, ‘Clark T/T’, ‘KS171-31-2’, PI 189866, and ‘L75-0283-4’ soybean lines with homozygous chromosome translocations were crossed to the same genetic marker types. F2 seed was increased at the University of Puerto Rico/Iowa State University soybean nursery near Isabela, PR. Data for the different characters used as marker traits were collected from F2 populations and F2:3 families. Recombination values revealed linkage between the breakpoints in KS172-11-3, KS175-7-3, and Clark T/T, with Df2, Y11, and several loci of CLG 8. Interestingly, these three translocations had a common breakpoint between Y11 and Ms1, but no linkage was identified between these loci and the breakpoints in KS171-31-2, PI 189866, and L75-0283-4. Our data further showed that CLGs 6 and 8 are the same LG, with Df2 and Adh1 at the ends of the chromosome segment. KS172-11-3, KS175-7-3, and Clark T/T share a common translocated chromosome which is different from that in KS171-31-2, PI 189866, and L75-0283-4. This information will facilitate the assignment of CLGs and the isolation of a tester set of translocations, and enhance genetic linkage mapping.

Abbreviations: LG, Linkage Group • CLG, Classical Linkage Group • MLG, Molecular Linkage Group


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
RECIPROCAL TRANSLOCATIONS, also known as chromosomal interchanges, are a type of chromosomal aberration arising from the exchange of broken segments of nonhomologous chromosomes. Thus, an individual with a reciprocal translocation contains a segment of one LG attached to another LG, the breakpoint being the point of attachment of the broken segments. Heterozygous translocations express partial pollen and ovule sterility (40 to 60% sterility), and this character defines the translocation breakpoint which would show linkage with mutants of the two different LGs. Marker loci close to the translocation breakpoint will also show linkage with each other, and where multiple markers are involved, the translocation-marker loci linkage relationships can furnish information needed to determine the orientation of linkage maps. However, accurate determination of the translocation breakpoint, possible with the use of multiple markers, is critical for map orientation. Reciprocal translocations are therefore useful for the location of genes to CLGs, for testing the independence of LGs, and for map orientation. The isolation and identification of a complete tester set of translocations will facilitate classical and molecular genetic linkage mapping in soybean. Sterility due to gene mutation can be complete male-sterility as in the case of Ms1 and Ms6, or complete male- and female-sterility as for St5, thus distinguishing this character from the partial male- and female-sterility character in heterozygous translocations. The flower color locus, W1, (CLG 8) has been assigned to Molecular Linkage Group F (MLG F) (Cregan et al., 1999), but CLG 6 has not yet been associated with a MLG.

Earlier studies (Palmer and Kilen, 1987) have resulted in the isolation of six reciprocal translocations (Table 1). Cytogenetic studies have shown that the translocations KS172-11-3, KS175-7-3, and Clark T/T share a common chromosome that is different from the one shared by KS171-31-2, PI 189866, and L75-0283-4 (Sadanaga and Newhouse, 1982; Sellner, 1990; Mahama et al., 1999). Sadanaga and Grindeland (1984) and Sacks and Sadanaga (1984) used the KS172-11-3 translocation in linkage studies and reported a gene order of W1, Wm, breakpoint, Ms1. Using the Clark T/T translocation, Palmer (1985), and Palmer and Kaul (1983) reported a gene order of W1, Wm, Ms1, breakpoint. In a separate study with CLG 6 loci, Palmer (1985) reported a gene order of Y11, Df2, breakpoint. The T locus (CLG 1) was reported as independent of the breakpoints in KS172-11-3, and Clark T/T (Palmer, 1976; Sadanaga and Grindeland, 1984). Mapping studies with multiple marker loci composed of CLG 6 and CLG 8 showed that these two LGs are the same LG (Mahama et al., 2002).


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  		Table 1. Origin of six translocation lines in soybean.

 
Since a common chromosome is involved in an interchange in three soybean translocations, it would be important to know the locations of the breakpoints to determine the similarities of the translocated segments. The objectives of our study were (i) to determine the location of translocation breakpoints by testing linkage with loci of CLG 6 (Df2 and Y11), CLG 8 (Adh1, Ms1, Ms6, St5, W1, and Y23), and other CLGs, and (ii) to confirm the orientation of these nine marker loci.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Genetic marker types with loci in both coupling and repulsion phase linkage and six translocation lines were used in mapping studies (Tables 1, 2). All loci express complete dominance except the Y11 locus, which expresses incomplete dominance, and plants with the genotype y11y11 are seedling lethal, dying shortly after germination. Plants with the genotype Y11y11 are viable and have greenish yellow leaves. CS is an unknown male-sterile, female-sterile mutant that has not been tested for allelism with the known male-sterile, female-sterile mutants. It is a sterile recessive gene, and dominant genotypes are fertile. Segregating populations were developed from cross-pollinations among different soybean genotypes (Walker et al., 1979). All the crosses were made in the field at the Bruner Farm near Ames, IA (Table 3). The soil was a Clarion-Nicollet Loam soil type (fine-loamy, mixed, superactive, mesic Typic Hapludolls and fine-loamy, mixed, superactive, mesic Aquic Hapludolls).


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  		Table 2. Phenotypic description of alleles of soybean genes studied.

 

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  		Table 3. List of crosses used to generate segregating populations of soybean.

 
Plants of the translocation lines were used as pollen parents in cross-pollinations with the genetic marker types except for plants carrying the st5 allele, in which case they were used as female parents. Plants of the genotype st5st5 are both male and female sterile. Thus, fertile plants of genotype St5st5, identified by progeny testing, were used as pollen parents. Following the procedures described by Mahama et al. (2002), segregation data for the different characters used as marker traits were collected from F2 populations and F2:3 families grown at the Bruner Farm. The F2 populations were generated from multiple F1 crosses. Because of poor survival, small plants, and/or small population sizes, only F2:3 data were collected for some crosses. Because of the amount of work, cost and time involved, only F2 populations were classified for the Adh1 locus. Late maturity and extreme lodging made it difficult to classify certain crosses in the F2:3 generation without serious errors. W1 and Wm are so closely linked that we chose to classify only W1 in the F2:3 generation. Plants homozygous for the nontranslocated and translocated chromosomes are fertile, and under normal conditions of growth will produce mostly three-seeded pods. In contrast, plants heterozygous for the translocated chromosomes are partial male and female sterile and will produce mostly one- and two-seeded pods. Classification for partial sterility from translocation heterozygosity was done by pollen staining with iodine potassium iodide solution (Jensen, 1962) and/or visual observation of seed set at maturity (Mahama et al., 2002).

Data analyses were according to Hanson and Kramer (1950), Joachim (1947), and Kramer et al. (1954) for calculating chi-square values, and linkage intensity values involving translocations, from F2, and F2:3 genetic data. Appropriate coefficients for the different sources of data were entered into a spreadsheet and used to calculate chi-square values to test the independence of loci pairs, as deviations from 50% recombination, and the corresponding recombination values as percentage recombination. Data from F2 and F2:3 families were analyzed separately. The recessive class was not used in the calculations of F2:3 data.


   RESULTS AND DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
KS172-11-3 and Clark T/T have been used in many linkage studies, but this is the first report on the use of KS175-7-3 in linkage studies. The marker loci Y11 and Df2 of CLG 6, Ms1, W1, St5, and Y23 of CLG 8, and T of CLG 1 segregated independently of the breakpoints in KS171-31-2, L75-0283-4, and PI 189866, indicating that the translocation in these three genotypes involves a different chromosome (Tables 4, 5). F2 and F2:3 data showed that Df2, Y11, Ms1, and W1 were linked to the breakpoints in KS172-11-3, KS175-7-3, and Clark T/T (Fig. 1, 2, and 3, respectively) with the breakpoint between Df2, and Y11. The recombination values calculated from F2 and F2:3 data differed greatly in some cases. This is because of the fact that the chance of error is greater in the F2 generation than the F2:3 generation because phenotypic evaluation is based on single plants in the F2 compared with 25 to 50 plants in the F2:3 generation. As expected, the T locus assorted independently of the breakpoints in KS172-11-3, KS175-7-3, and Clark T/T.


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  		Table 4. Percentage recombination values between loci and translocation breakpoints calculated from F2 progeny data in soybean.

 

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  		Table 5. Percentage recombination values between loci and translocation breakpoints calculated from F2:3 progeny data in soybean.

 


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  		Fig. 1. Linkage relationships between the translocation breakpoint in KS172-11-3 (Tr) and loci of Classical Genetic Linkage Groups 6 and 8 in soybean. Data were obtained from multiple cross populations. F2 data are above the chromosome segment (dark line), and F2:3 (bold type) data are below the chromosome segment. Numbers above each line denote map units. I means independent.

 


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  		Fig. 2. Linkage relationships between the translocation breakpoint in KS175-7-3 (Tr) and loci of Classical Genetic Linkage Groups 6 and 8 in soybean. Data were obtained from multiple cross populations. F2 data are above the chromosome segment (dark line), and F2:3 (bold type) data are below the chromosome segment. Numbers above each line denote map units. I means independent.

 


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  		Fig. 3. Linkage relationships between the translocation breakpoint in Clark T/T (Tr) and loci of Classical Genetic Linkage Groups 6 and 8 in soybean. Data were obtained from multiple cross populations. F2 data are above the chromosome segment (dark line), and F2:3 (bold type) data are below the chromosome segment. Numbers above each line denote map units. I means independent.

 
Our data also revealed that Dt1, Ep, Fr1, G, I, K2, Pb, Ms3, Ms4, Rj1, St2, St3, St4, Y9, Y10, Y12, and Y18 were independent of the breakpoint in Clark T/T (Tables 4, 5). This lack of linkage, together with independent assortment between Ms1 and Ep, and W1 and Ep (Mahama et al., 2002) are in agreement with the placement of these loci in different LGs than CLG 6 and CLG 8. The Ep locus was independent of L75-0283-4, while the breakpoint in PI 189866 was linked to the CS male-sterile, female-sterile mutant (R = 24.7 ± 5.3) (Table 5). Additional linkage data are needed to confirm the observed linkage and to assign the CS mutant to a LG.

On the basis of the observation of chromosome number and constitution during meiosis, Sacks and Sadanaga (1984) reported linkage between W1 and the breakpoint (2.0 ± 1.2) and Ms1 and the breakpoint (18.4 ± 3.3), while Sadanaga and Grindeland (1984) reported linkage between the breakpoint and W1 (1.9 ± 0.8) in KS172-11-3, and independent assortment with T and Y10. Both studies placed the breakpoint distal to W1, and Sacks and Sadanaga (1984) placed the breakpoint between W1 and Ms1.

Using standard linkage estimation methods, Palmer (1985) reported linkage between the breakpoint in Clark T/T and Y11 (18.4 ± 0.4) and Df2 (5.8 ± 0.2), and also between the breakpoint and Ms1 (8.5 ± 1.5), Wm (36.8 ± 1.6), and W1 (39.5 ± 2.0), thus placing the breakpoint between Ms1 and Df2. The values reported in our study for CLG 8 are in agreement with those reported by Palmer and Kaul (1983) and Palmer (1985), but different from Sadanaga and Grindeland (1984) and Sacks and Sadanaga (1984). These differences may be reflective of the different methods (F2 and F2:3 segregating data vs. microscope observations) used to obtain linkage data and the different generations of self-pollination that occurred before the translocations were used in the different studies. Whereas Sadanaga and Grindeland (1984) and Sacks and Sadanaga (1984) used the translocations shortly after their isolation following mutagenesis, five generations of self-pollination occurred before they were used in our study. Hence, their recombination values would have been subject more to any unknown instabilities or biases due to differential gametic or genotypic viabilities.

The placement of marker loci in relationship with the translocation breakpoints is based on the recombination values calculated. Linkage maps for KS172-11-3 (Fig. 1), KS175-7-3 (Fig. 2), and Clark T/T (Fig. 3) were developed from our results. Our data placed the breakpoint in all three translocations between Y11 and Ms1. This placement was possible because genotypes carrying both loci were used to generate segregating populations in this study. The orientation of marker loci Df2, Y11, Ms1, W1, Wm, Ms6, Y23, St5, and Adh1 is similar to the reports of Palmer and Hedges (1993) (Ms1, W1, Wm, Ms6, Y23, St5, Adh1) and Mahama et al. (2002) (Y11, Df2, Ms1, Wm, W1, Ms6, Y23, St5, Adh1). Mahama et al. (2002) reported linkage between loci of CLG 6 and CLG 8 and indicated that they are the same LG. The linkage observed between the breakpoints and Y11 and Df2 of CLG 6, and loci of CLG 8 (Ms1, W1) serves as further evidence that the two are the same LG. On the basis of cytogenetic data, KS172-11-3, KS175-7-3, and Clark T/T were reported to share one common interchange chromosome, and KS171-31-2, PI 189866, and L75-0283-4 shared a different common chromosome (Sadanaga and Newhouse, 1982; Sellner, 1990; Mahama et al., 1999). The linkage of loci of CLG 6 and CLG 8 with the breakpoints in KS172-11-3, KS175-7-3, and Clark T/T, and the independent assortment of these loci with the breakpoints in KS171-31-2, PI 189866, and L75-0283-4 observed in this study confirm that the two groups of translocations carry different translocated chromosomes.


   CONCLUSIONS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Recombination values indicated that the loci T, Y9, Y10, and Y18, previously identified as unlinked to CLG 8 loci, as well as Dt1, Ep, Fr1, G, I, K2, Pb, Ms3, Ms4, Rj1, St2, St3, St4 and y12, were independent of the breakpoints in chromosome translocations KS172-11-3, KS175-7-3, and Clark T/T. All three translocations showed linkage with Y11 and Df2, and Ms1, and W1, of CLG 8, with the breakpoint between Y11 and Ms1, while the breakpoints in KS171-31-2, L75-0283-4, and PI 189866 were independent of these loci. These data confirm that KS172-11-3, KS175-7-3, and Clark T/T have a common interchange chromosome, and that KS171-31-2, L75-0283-4, and PI 189866 do not share this common interchange chromosome. Our data are in agreement with the previous report (Mahama et al., 2002), and we propose that CLG 6 and CLG 8 be combined into one LG designated CLG 8 while dropping CLG 6.

The map orientation, once CLG 6 and CLG 8 are combined, is, in general, consistent with reported maps, and our data place Df2 and Adh1 at the opposite ends of the chromosome segment. We report here for the first time linkage between the CS male-sterile, female-sterile mutant and the breakpoint in PI 189866. The data reported in this study will contribute toward the assignment of genes to LGs and reassignment of LGs, the isolation of a tester set of translocations, and will enhance classical and molecular genetic linkage mapping.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Joint contribution J#19834 of the Iowa Agric. and Home Econ. Exp. Stn., Ames, IA, Project No. 3769 and the USDA-ARS, Corn Insects and Crop Genetics Research Unit, and supported by Hatch Act and State of Iowa.

Received for publication July 29, 2002.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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