Crop Science 41:698-701 (2001)
© 2001 Crop Science Society of America
CROP BREEDING, GENETICS & CYTOLOGY
A New Soybean Maturity and Photoperiod-Sensitivity Locus Linked to E1 and T
Elroy R. Cober* and
Harvey D. Voldeng
Eastern Cereal and Oilseed Research Centre, Agric. & Agri-Food Canada, Bldg. #110, Central Exp. Farm, Ottawa, Ontario, Canada, K1A 0C6
* Corresponding author (coberer{at}em.agr.ca)
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ABSTRACT
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An association between early maturity and tawny pubescence has been observed in short-season soybean [Glycine max (L.) Merr.]. The objectives of this study were to determine if a single locus controls early maturity; and if there is a new locus linked to E1 and T or, alternatively, a third allele at the E1 locus. A cross was made between ‘Harosoy’ isolines OT89-5 (e3e3 e4e4) and OT94-47. PI 196529 was the donor of early maturity in the backcrossing program which developed OT94-47. A total of 229 F2 plants and the parents were grown under 20-h photoperiods produced by incandescent lamps. OT94-47 flowered in 43 ± 1.4 d, OT89-5 flowered later in 57 ± 4.2 d, and the F2 population fit a 3 late: 1 early flowering ratio. Early-flowering F2 plants produced F3 families that flowered similarly to OT94-47. Later-flowering F2 plants either segregated for flowering date or flowered similarly to OT89-5. To test for allelism with E1 and linkage with T, a cross was made between OT93-26 (E1E1 e3e3 e4e4 TT) and OT94-47. F2 plants were classified as parental types or intermediate and equivalent to OT89-5 in maturity. Maturity and pubescence color were recorded in 376 F3 progeny rows. The data did not fit a single locus model or a two loci dominant epistasis model (12:3:1). The E7 allele was partially, but not completely, dominant over the e7 allele. Therefore, a new locus E7 is proposed. Using the F3 segregation data, linkage between T and E1 was estimated to be 1.3 ± 0.6 centimorgan (cM). Linkage between E1 and E7 was estimated to be 6.2 cM and linkage between E7 and T was estimated to be 3.9 cM. E7 is a new flowering, maturity, and photoperiod sensitivity locus tightly linked to both E1 and T. E7E7 results in later flowering and maturity, and sensitivity to long photoperiods produced by incandescent lamps when compared to e7e7.
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INTRODUCTION
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IN SOYBEAN, five loci with two alleles at each locus have been reported to control time to flowering and maturity: E1 and E2 (Bernard, 1971), E3 (Buzzell, 1971), E4 (Buzzell and Voldeng, 1980), and E5 (McBlain and Bernard, 1987). Some of these genes (E1, E3, E4) are also involved in photoperiod sensitivity (Cober et al., 1996). Backcross-derived, near-isogenic lines (isolines) of the cultivars Harosoy (genotype e1e1 e2e2 E3E3 E4E4 e5e5) and Clark (genotype e1e1 E2E2 E3E3 E4E4 e5e5) have been developed to identify and study these genes by means of various germplasm sources with alternative alleles. A Harosoy isoline (OT89-5) containing early-maturity alleles at all five of the reported loci is classified as maturity group 0 when grown in short-season areas in Canada. Two shorter-season maturity groups (00 and 000) exist and a genetic model for this earlier maturity is not yet available. We have developed an earlier-maturing Harosoy isoline (OT94-47) with the early maturity originating from the donor parent PI 196529 which was identified as daylength neutral by Polson (1972).
Tawny pubescence seems to be a favorable trait in short-season soybean cultivars (Morrison et al., 1994; Morrison et al., 1997). We hypothesized (Cober et al., 1997) that another genetic factor controlling maturity might be linked to pubescence color in addition to the reported tight linkage between pubescence color and the E1 locus (Weiss, 1970).
The objectives of this study were to determine if a single locus controls early maturity; and if there is a new locus linked to E1 and T or, alternatively, a third allele at the E1 locus.
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MATERIALS AND METHODS
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Six Harosoy isolines were used in this study (Table 1). The isolines with an L prefix have been described by Bernard et al. (1991). The remaining lines were developed at the Eastern Cereal and Oilseed Research Centre, Ottawa, Ontario, Canada. L62-667, an early-maturing BC5 isoline of Harosoy, was developed by transferring the e3 allele from line T204 (Bernard et al., 1991). L62-667 was then used as the recurrent parent in the development of two even earlier-maturing isolines, OT89-5 with the e4 allele from PI 438477 (Voldeng and Saindon, 1991) and X2749-K1 with early maturity derived from PI 196529. Crossing OT89-5 and X2749-K1 and selecting for early maturity produced OT94-47. During the development of X2749-K1, there appeared to be a linkage between tawny pubescence and early maturity in the donor PI 196529.
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Table 1. Harosoy isolines used as parents to develop early-maturing soybean isolines and isolines used in this study of early maturity and photoperiod response.
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To determine if a single locus controls early maturity, a cross was made between OT89-5 and OT94-47. Two hundred twenty-nine F2 plants and the parents, followed by 22 selected F3 families and the parents were grown in a growth room under a 20-h photoperiod produced by 60-W incandescent lamps. Eight F3 plants were grown from each of 22 families which allowed a 90% probability of detecting a recessive individual in a family segregating 3:1. Under incandescent lamps, the red:far-red quantum ratio (R:FR) was 0.56 and the photosynthetic photon flux was 36 µmol m-2 s-1. Light quality was measured 50 cm from the source with a radiometer/photometer and a monochromometer. Incident radiation was measured in 10-nm bandwidths centered at 660 and 730 nm. Quantum spectral ratios were calculated as 89.4% of energy spectral ratios since red light (660 nm) has 10.6% more energy per mole of quanta than far-red (730 nm). Photosynthetic photon flux was measured with a LI-COR quantum sensor (Model LI-1000, LI-COR Inc., Lincoln, NE). Seeds were germinated in vermiculite and seedlings were transplanted into 13-cm pots filled with standard phytotron potting mix (3 parts loam: 2 parts vermiculite: 1.5 parts peat moss: 1 part crushed brick). The date of the first open flower was recorded for each plant.
Since E1 is linked to T (Weiss, 1970) and an association was observed between early maturity and pubescence color in the development of OT94-47 and in breeding lines (Cober et al., 1997), it was necessary to determine if there is a new locus linked to E1 and T or if there is a third allele at the E1 locus. As E2 and E5 had been previously shown to be unlinked with E1 (Bernard, 1971; McBlain and Bernard, 1987), no crosses were made involving these loci.
A cross was made between OT93-26 (PI 591429, TT E1E1 e3e3 e4e4; Voldeng et al., 1996) and OT94-47 to test for allelism at the E1 locus and to test for linkage with the T locus in the winter of 1994/1995. The F2 population was planted in the field at the Central Experimental Farm, Ottawa, Ontario, Canada, on 1 June 1995 and 376 F3 progeny rows were planted 27 May 1996. Populations, progeny rows, and check isolines were planted in 4-m rows with 50 cm between rows at a seeding rate of about 15 seeds m-1. As F2 plants matured, they were harvested and labeled as early, intermediate, or late maturing. The date of maturity (95% of pods with mature color) and the pubescence color of F3 progeny rows were recorded. The chi-square test was used to test the goodness of fit of observed to expected ratios. Linkage estimates were made by LINKEM (Vowden et al., 1995) or the square root method where the double recessive class was used to estimate non-crossover gametes (coupling phase) and linkage is estimated by the following formula: linkage estimate = 1 - 2 (frequency of double recessives)1/2.
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RESULTS AND DISCUSSION
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Under 20-h photoperiods produced by incandescent lamps, OT94-47 flowered in 43 ± 1.4 d (mean ± standard error) and OT89-5 flowered in 57 ± 4.2 d. Long photoperiods with low red:far-red quantum ratios allowed discrimination between flowering time of the two parents. The maturity of these two isolines differed by only 5 d under field conditions (Table 2), probably because a less extreme photoperiod was imposed. Both time-to-flowering and time-to-maturity is conditioned by these loci and where small differences are observed, time-to-maturity is the more discriminating trait (Cober et al., 1996).
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Table 2. The number of F3 soybean families from a cross of OT93-26 x OT94-47 in each maturity class, the pubescence color, and the mean and range of maturity of these families and the maturity of check isolines grown in the field at Ottawa, ON, Canada in 1996.
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The F2 population distribution, from a cross between OT94-47 and OT89-5, appears to have three peaks corresponding approximately to the parental means and the mid-parent value (Fig. 1). However, the later-flowering parent mean ± 2 S.E. overlapped the intermediate peak, so a 3:1 ratio was fitted to the data. The early flowering parent (OT94-47) mean + 2 S.E. was used to divide the data into two classes. The F2 population had an observed ratio of 182:47 which fit a 3:1 ratio (n = 229, 
2 = 2.21, P = 0.14). Five plants from each of the parental-maturity ranges and 12 plants of intermediate maturity were selected for progeny testing in the F3 generation. The F2 plants identified as OT94-47 types produced F3 families similar to OT94-47, the early-maturing parent (Fig. 2). Plant 70 was identified as an intermediate-maturing F2 plant but appeared ambiguous or early maturing in the F3 generation. If one plant in 17 of the late-flowering plants was misclassified then a corrected ratio for the F2 population would be 171:58 which also fits a 3:1 ratio (2 = 0.01, P = 0.94). It appears in Fig. 2 that there are five or six families homozygous for OT94-47 type maturity and six families homozygous for OT89-5 type maturity. These true-breeding families would not be present in high frequencies if two or more loci were controlling flowering time. The OT94-47/OT89-5 cross confirmed monogenic inheritance of early maturity. The gene symbol E7 e7 has been assigned by the Soybean Genetics Committee since the E6 gene symbol has been assigned in an as yet unpublished study. In this cross the early maturity of OT94-47 is conditioned by e7e7.
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Fig. 1. A frequency distribution of an F2 soybean population from the cross OT89-5 x OT94-47 segregating for days to first flower under a 20-h photoperiod produced by incandescent lamps. The parents flowered in 43.2 (OT94-47) and 57.3 d (OT89-5) and are shown as mean ± 2 S.E.
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Fig. 2. Tukey box plots for 22 F3 soybean families (n = 8) from the cross OT89-5 x OT94-47 and the two parents for days to first flower under a 20-h photoperiod produced by incandescent lamps alone plotted according to the maturity of the F2 plant, from earliest to latest. The box shows the 25th and 75th percentile with the light bar in the box showing the 50th percentile and the bold bar showing the family mean; the error bars show the 10th and 90th percentile; the dashed line shows the mid-parent value. The families developed from F2 plants designated early maturing are prefixed with "a," those late maturing are prefixed with "b," and the intermediate maturing do not have a prefix.
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Since tawny pubescence segregated with early maturity in the development of the early-maturing isoline OT94-47 and early maturity was found to be associated with tawny pubescence in early-maturing (e1e1) germplasm (Cober et al., 1997), it was necessary to test for allelism of e7 at the E1 locus. The F2 plants from a cross between OT93-26 (TT E1E1 e3e3 e4e4 E7E7) and OT94-47 (tt e1e1 e3e3 e4e4 e7e7) were classified, at maturity, into the two parental classes and an intermediate class. In 1995, OT93-26 matured in 122 ± 2.1 d, OT89-5 matured in 108 ± 1.0 d, and OT94-47 matured in 99 ± 0.7 d. We hypothesized that the late-maturing class had the genotype (E1_ __, that the early class was e1e1 e7e7, and that the intermediate class was e1e1 E7_. This model hypothesized dominant epistasis with E1 epistatic to e7. The maturity and pubescence color of F3 progeny rows was observed in 1996 (Table 2). On the basis of data from 376 F3 progeny rows, 11 F2 plants were misclassified: 1 plant classified as late (E1_ __) matured intermediately (e1e1 E7_), and 10 plants classified as intermediate (e1e1 E7_) matured late E1_ __. The occurrence of segregants intermediate to the parental isolines in both the F2 and F3 generation indicate that e7 is at a second locus and not allelic to E1. If e7 was allelic to E1, and the intermediate class was the heterozygote class in the F2, then the population should fit a 1:2:1 ratio. Also, because of the close linkage between E1 and T (Weiss, 1970), the intermediate class should be heterozygous at the T locus and the progeny should be segregating for pubescence color in the F3. This was not the case. The F2 population, classified using the F3 data, with observed values of 278:14:84 (n = 376, 2 = 522.3, P < 0.0001) did not fit a 1:2:1 ratio. The data were then examined by a two loci dominant epistasis model. The observed values of 278:14:84 did not fit a 12:3:1 ratio (n = 376, 2 = 201.1, P < 0.0001). The failure to fit this model results from lack of independence of the E1 and e7 loci.
From the segregation data (E1_ TT, 90; E1_ Tt, 184; E1_ tt, 4; e1e1 TT, 0; e1e1 Tt, 1; e1e1 tt, 97), linkage between T and E1 was estimated by LINKEM (Vowden et al., 1995) to be 1.3 ± 0.6 cM, which is similar to the estimate reported by Weiss (1970) of 3.9 ± 0.4 cM and the estimate reported by Hanson (1961) of 2.0 ± 0.3. Since it was not possible to distinguish the E1_ E7_ and E1_ e7e7 classes, the double recessive class (e1e1 e7e7) was used to estimate non-crossover gametes (coupling phase) and the square root method was used to estimate linkage between E1 and E7. From the observed 83 e1e1 e7e7 rows from a total of 376 rows, linkage between E1 and E7 was estimated at 6.0 cM. Linkage estimates between the E7 and T loci were confounded by the effects of E1 and the inability to identify the double recessive class, e7e7 tt. In the absence of double crossovers, the E1_ tt class would also be e7e7. Therefore, the E1_ tt and e1e1 e7e7 tt classes were used to estimate the double recessive class (e7e7 tt), an observed 86 from a total of 376 rows, resulting in a linkage estimate of 4.4 cM between E7 and T. The combination of these linkage estimates places these loci in the following order: E1-1.3-T --------- 4.4 --------- E7.
Another approach to determine gene order involves consideration of crossover families. Gene order E1-E7-T is ruled out by the occurrence of 15 e1e1 E7_ tt families which would be double crossovers with this order. Gene order E1-T-E7 would require one double crossover (e1e1 Tt e7e7) and no appearances of the expected single crossover family e1e1 Tt E7_. Gene order T-E1-E7 would result in three distinguishable single crossover families (tt E1_ __, tt e1e1 E7_, Tt e1e1 e7e7), which are reported in Table 2. The occurrence of 14 tt e1e1 E7_ families supports the gene order T-E1-E7 since some of these families would be expected to be Tt in the case of a E1-T-E7 gene order. A definitive gene order for these three loci must await fine mapping of this region of the genome by molecular techniques.
In summary, E7 is a new maturity and photoperiod-sensitivity locus which is closely linked to E1 and T. E7E7 results in later flowering and maturity, and sensitivity to long photoperiods produced by incandescent lamps, while e7e7 results in early flowering and maturity, and less sensitivity to long photoperiods produced by incandescent lamps. The e1e1 e2e2 e3e3 e4e4 e5e5 e7e7 Harosoy isoline extends the genetic model for maturity to early MG 0. The e7 allele originated from PI 196529 which had been identified as day-neutral by Polson (1972). The linkage between E7 and T is likely responsible for the association between maturity and pubescence color reported by Cober et al. (1997).
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NOTES
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ECORC Contribution no. 991424.
Received for publication September 24, 1999.
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REFERENCES
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- Bernard, R.L. 1971. Two major genes for time of flowering and maturity in soybeans. Crop Sci. 11:242–244.[Abstract/Free Full Text]
- Bernard, R.L., R.L. Nelson, and C.R. Cremeens. 1991. USDA soybean genetic collection: Isoline collection. Soybean Genet. Newsl. 18: 27–57.
- Buzzell, R.I. 1971. Inheritance of a soybean flowering response to fluorescent-daylength conditions. Can. J. Genet. Cytol. 13:703–707.[ISI]
- Buzzell, R.I., and H.D. Voldeng. 1980. Inheritance of insensitivity to long daylength. Soybean Genet. Newsl. 7:26–29.
- Cober, E.R., J.W. Tanner, and H.D. Voldeng. 1996. Genetic control of photoperiod response in early-maturing, near-isogenic soybean lines. Crop Sci. 36:601–605.[Abstract/Free Full Text]
- Cober, E.R., H.D. Voldeng, and M.J. Morrison. 1997. Maturity and pubescence color are associated in short-season soybean. Crop Sci. 37:424–427.[Abstract/Free Full Text]
- Hanson, W.D. 1961. Effect of calcium and phosphorus nutrition on genetic recombination in the soybean. Crop Sci. 1:384.[Free Full Text]
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- Morrison, M.J., H.D. Voldeng, and R.J.D. Guillemette. 1994. Soybean pubescence color influences seed yield in cool-season climates. Agron. J. 86:796–799.[Abstract/Free Full Text]
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ABSTRACT
INTRODUCTION
