Published in Crop Sci. 44:2038-2042 (2004).
© 2004 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
CROP BREEDING, GENETICS & CYTOLOGY
Soybean Maturity Gene Effects on Seed Coat Pigmentation and Cracking in Response to Low Temperatures
Eduardo R. Beniteza,
Hideyuki Funatsukib,
Yukio Kanekoa,
Yasuo Matsuzawaa,
Sang W. Banga and
Ryoji Takahashic,*
a Faculty of Agriculture, Utsunomiya Univ., 350 Mine-Machi, Utsunomiya, 321-8505 Japan
b National Agriculture Research Center for Hokkaido Region, Hitsujigaoka 1, Sapporo, 062-8555 Japan
c National Institute of Crop Science, Kannondai 2-1-18, Tsukuba, Ibaraki, 305-8518 Japan
* Corresponding author (masako{at}affrc.go.jp)
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ABSTRACT
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Exposure of soybean [Glycine max (L.) Merr.] to chilling temperatures (about 15°C) at flowering induces browning around the hilum region and cracking of the seed coats. Both pigmentation and cracking degrade the external appearance of soybean seeds and reduce their commercial value. An earlier study showed that some alleles at maturity loci E1 to E5 were associated with intensity of pigmentation and cracking. The objective of this study was to evaluate the effect of alleles at maturity locus E7 and the combination effect of E3 and E4 on the intensity of seed coat pigmentation and cracking. Soybean cv. Harosoy (e1e2E3E4e5E7) and its near-isogenic lines Harosoy-e3, Harosoy-e4, Harosoy-e3e4, and Harosoy-e3e4e7 were exposed to 15°C for 2 wk beginning 8 d after flowering. Control plants were grown in a greenhouse throughout their entire life cycle, whereas the treated plants were transferred from the greenhouse to a phytotron for the chilling treatment. Intensities of both pigmentation and cracking were increased by recessive allele e3 and reduced by recessive allele e4. Harosoy-e3e4 showed an intermediate degree of pigmentation and cracking relative to Harosoy-e3 and Harosoy-e4. These results suggest that effects of maturity genes E3 and E4 may be additive and that combination effects may be roughly estimated from individual gene action. Harosoy-e3e4e7 exhibited a higher degree of pigmentation and cracking than Harosoy-e3e4, suggesting that dominant allele E7 can reduce the degree of pigmentation and cracking, similar to the E1, E2, E3, and E5 loci. These results suggest that selection for the appropriate combination of maturity genes is effective to adjust time to flowering and maturity and to produce high quality seeds at high latitude regions. The e4 allele may be especially useful in reducing seed coat pigmentation and cracking in soybean cultivars adapted to high latitudes.
Abbreviations: DAO, days after opening of individual flowers • NILs, near-isogenic lines
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INTRODUCTION
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SOYBEAN cultivated at high latitudes and/or altitudes are frequently subjected to low temperature stresses during critical phases of development. Chilling stress can retard growth, cause abortion of flowers and immature pods, and reduce final seed yield (Raper and Kramer, 1987). Furthermore, chilling temperatures (about 15°C) during flowering induce browning and cracking of seed coats (Sunada and Ito, 1982). Cultivars with yellow hilum color compared with those with brown hilum are preferred in Japan for confectionery use because of better external appearance. However, yellow hilum cultivars are more susceptible to low temperatures, resulting in reduced seed yield and poor seed quality compared with brown hilum cultivars (Takahashi and Asanuma, 1996; Takahashi, 1997). Seed coat pigmentation as a result of chilling stress occurs only in yellow hilum cultivars and is absent in cultivars with brown hilum (Sunada and Ito, 1982). Both pigmentation and cracking degrade the external appearance of soybean seeds and reduce their commercial value.
To clarify the genetic basis of varietal differences in chilling tolerance, Takahashi and Asanuma (1996) and Takahashi (1997) evaluated the roles of gene T (responsible for pubescence and hilum color) and gene I (responsible for distribution of seed coat color) using near-isogenic lines (NILs) for the two loci. Independent of the genotypes at I locus, the dominant allele T completely suppressed the development of pigmentation around the hilum region and partly suppressed seed coat cracking. Dominant allele I also suppressed seed coat pigmentation and cracking under the genotype of tt, although its inhibitory effect was not as obvious as gene T. Genes T and I are involved in flavonoid biosynthesis (Palmer and Kilen, 1987). Gene T is presumed to encode a flavonoid 3'-hydroxylase that hydroxylates the 3'-position of the B-ring in flavonoids (Buttery and Buzzell, 1973; Toda et al., 2002). Flavonoids with 3', 4'-dihydroxy configuration possessed a higher antioxidant activity than those with a single hydroxyl group on the B-ring (Pratt, 1976). Most likely, the dominant allele T suppresses pigmentation by inhibiting the oxidation of phenolic compounds. Dominant allele I encodes three tandem repeats of chalcone synthase, a key enzyme for flavonoid biosynthesis. The expression of chalcone synthase genes may be inhibited by a naturally occurring, homology-dependent gene silencing process that leads to a complete absence of coloration (Todd and Vodkin, 1996). Seed coats of soybean with recessive allelic combination of the two loci (i and t, or i-k and t) were severely cracked irrespective of environmental conditions (Nicholas et al., 1993). Increased levels of chilling stress appear to surmount the function of allele I and consequently cause both pigmentation around the hilum region and cracking of the seed coat (Takahashi, 1997).
In addition to genes T and I, there is genetic variation in the tolerance to pigmentation among cultivars with yellow hilum (I) and gray pubescence (t). Genetic analysis using F1 hybrids between chilling temperature sensitive and tolerant cultivars and their F2 population revealed that susceptibility to pigmentation was partially dominant to tolerance as a whole, and a few major genes were involved in tolerance (Takahashi and Abe, 1994). Takahashi and Abe (1994) further found that one of the genes for tolerance was closely associated with a dominant gene for late maturity, the recessive allele of which was involved in floral induction under artificially induced long days by means of incandescent lamps.
Most soybean cultivars are sensitive to long daylength and flower only when the daylength is less than a specific threshold value. Soybean cultivars are generally adapted within a narrow north-south band primarily because of photoperiodic response: southern cultivars remain vegetative under long days and are too late-maturing in the north, whereas northern cultivars flower in response to the shorter days and mature too early in the south (Scott and Aldrich, 1970). Thus, different cultivars are grown at different latitudes to obtain timing of flowering and maturity necessary to achieve a maximum commercial production.
Eight loci have been reported to control time to flowering and maturity in soybean: E1, E2 (Bernard, 1971), E3 (Buzzell, 1971), E4 (Buzzell and Voldeng, 1980), E5 (McBlain and Bernard, 1987), E6 (Bonato and Vello, 1999), E7 (Cober and Voldeng, 2001a), and J (Ray et al., 1995). Of these, E3, E4, and E7 are involved in the response of flowering to long daylength. The e3 locus controls the insensitivity to fluorescent long daylength obtained by extending natural daylength to 20 h using cool white fluorescent lamps with a low FR/R ratio, whereas e4 combines with e3 to control the insensitivity to incandescent long daylength (ILD) accomplished by extending natural daylength to 20 h with incandescent lamps with a high FR/R ratio (Buzzell, 1971; Buzzell and Voldeng, 1980).
To evaluate the separate effects of five maturity genes (E1–E5) on the intensity of seed coat pigmentation and cracking, Takahashi and Abe (1999) treated Harosoy (e1e2E3E4e5E7) and its near-isogenic lines for E1 to E5 loci with chilling temperatures. Intensity of pigmentation was not affected by e3, slightly reduced by E2 and e4, and profoundly reduced by E1 and E5. Degree of cracking was slightly increased by e3 and drastically reduced by e4, E1, and E5. The results suggest that some of the soybean maturity genes have inhibitory effects on the intensity of seed coat pigmentation and cracking in response to low temperatures. Dominant alleles E1 and E5 were most effective in suppressing both pigmentation and cracking.
The objective of this study was to investigate the effects of the combination of the E3, E4, and E7 loci in a common background on seed coat pigmentation and cracking when subjected to chilling stress during early seed development.
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MATERIALS AND METHODS
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Soybean cv. Harosoy (e1e2E3E4e5E7) and its NILs Harosoy-e3 (L62-667: e1e2e3E4e5E7), Harosoy-e4 (OT94-41: e1e2E3e4e5E7), Harosoy-e3e4 (OT89-5: e1e2e3e4e5E7), and Harosoy-e3e4e7 (OT94-47: e1e2e3e4e5e7) were used (Table 1). Seeds of L62-667 were provided by the USDA Soybean Germplasm Collections. It was produced by crossing Harosoy with line T204 having the e3 allele and backcrossing the progeny to Harosoy up to BC6 (Bernard et al., 1991). Seeds of OT94-41, OT89-5, and OT94-47 were obtained from Plant Res. Ctr., Agric. Agri-Food Canada, Ottawa. OT94-41 was selected from a cross between Harosoy isolines, OT89-5 (e1e2e3e4e5E7) and L67-153 (e1e2E3E4e5E7) as described by Cober et al. (1996). OT94-47 was selected for early maturity from a cross between OT89-5 and X2479-K1 (e1e2e3E4e5e7) (Cober and Voldeng, 2001a). All soybean lines used in this report have yellow hilum (I) and gray pubescence (t).
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Table 1. Harosoy and near-isogenic soybean lines used to study the relationship between maturity genes and seed coat pigmentation and cracking in response to low temperatures.
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Experiments were conducted from June to October in 2003 at the National Agriculture Research Center, Tsukuba, Japan (36°06'N, 140°05'E). On 14 June, eight seeds were planted in pots (15.5-cm diameter) filled with 4 kg soil (low-humic andosols) supplemented with ammonium sulfate (2 g), monocalcium phosphate (2 g), fused magnesium phosphate (4 g), and potassium sulfate (1 g). One week after emergence, seedlings were thinned to two per pot and grown in an unheated vinyl plastic greenhouse. Because early-maturing NILs generally produce fewer seeds than late-maturing NILs, 20 pots for Harosoy-e3e4e7, 14 pots for Harosoy-e3e4, and 12 pots each for Harosoy, Harosoy-e3, and Harosoy-e4 were subjected to chilling treatment. In addition, five pots per line were grown continuously in the greenhouse.
The chilling treatment was done by transferring plants from the greenhouse to a phytotron set at 15 ± 0.5°C (day/night). Light was supplied at a photosynthetic photon flux density (400–700 nm) of 200 µmol m–2 s–1 by metal halide lamps (DR 400/T(L), Toshiba Co., Tokyo, Japan) at a 14/10 h light/dark regime. The mean temperatures in the control greenhouse during the chilling treatment were 23.4°C. Earlier chilling induced seed coat studies revealed that pigmentation was most intense when flowers from 5 to 10 d after opening of individual flowers (DAO) were exposed to a 15°C treatment for more than 10 d (Oka et al., 1989). Therefore, plants were exposed to chilling for 14 d beginning 8 d after flowering of individual plants. Because the flowering period in soybean spans over 2 wk, the chilling treatment of an individual plant leads to exposure of flowers at various stages of development. Accordingly, flowers were individually labeled with the date of opening and only the flowers that opened before the beginning of the chilling treatment were used for analysis. Pots were randomized both in the phytotron and the greenhouse and repositioned twice a week in the greenhouse and daily in the phytotron. After 14 d of the chilling treatment, pots were returned to the greenhouse.
The number of days from planting to opening of the first flower (R1, Fehr et al., 1971), and from planting to maturity (R8), when 95% of pods had mature color, were recorded for individual plants. Means of days from planting to flowering and maturity among NILs were compared with Tukey's HSD test by the Statistica software (StatSoft, Inc. Tulsa, OK).
The degree of pigmentation and cracking of each seed was scored by a pigmentation index (0 = not pigmented to 4 = severely pigmented) and a cracking index (0 = not cracked to 4 = severely cracked) as previously described (Takahashi, 1997; Takahashi and Abe, 1999). The effect of a 14-d chilling treatment initiated at different flower stages on pigmentation and cracking was evaluated by averaging the indices of seeds obtained from flowers that were exposed to chilling stress at the same developmental stage. Pigmentation and cracking indices were subjected to two-way analysis of variance by considering each pot as a replicate to evaluate effects of NILs, DAO, and their interactions.
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RESULTS AND DISCUSSION
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Harosoy took the longest days to flowering followed by the other NILs having recessive maturity alleles in the order of Harosoy-e4 > Harosoy-e3 > Harosoy-e3e4 > Harosoy-e3e4e7 (Table 2). The genes E3, E4, and E7 probably have additive delaying effects on time to flowering. Days to maturity were not significantly different among Harosoy, Harosoy-e3, and Harosoy-e4, but Harosoy-e3e4 and Harosoy-e3e4e7 required significantly fewer days to reach maturity than Harosoy and the other two NILs. Thus, E3 and E4 genes showed additive effects on time to maturity as well. Daylength at the location of this experiment may not be long enough for E3, E4 and E7 to exhibit distinct delaying effects, because neither E3, E4, nor E7 loci delayed flowering and maturity under a 12-h photoperiod (Cober et al., 1996; Cober and Voldeng, 2001b).
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Table 2. Days from planting to flowering (R1) and maturity (R8) in Harosoy and its soybean near-isogenic lines at Tsukuba, Japan, in 2003.
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Seed coat pigmentation was observed only in chilling-treated plants (Table 3). Development of pigmentation in response to the age of flowers (0–8 DAO) at the beginning of chilling treatment was different among the NILs (Fig. 1)
. Their pigmentation indices were relatively stable from 0 to 3 DAO but decreased thereafter. The results suggest that pigmentation is most severe when recently opened flowers are exposed to chilling. A two-way analysis of variance indicated that main effects of both NILs and flower stages on the pigmentation index were significant at the 1% level. Tukey's HSD test revealed that the mean of pigmentation index differed significantly among the NILs except between Harosoy and Harosoy-e3e4, and between Harosoy-e3e4e7 and Harosoy-e3. On the basis of the degree of pigmentation, the NILs can be ranked as follow: Harosoy-e4 (average of pigmentation index = 1.04) < Harosoy (1.78) = Harosoy-e3e4 (1.94) < Harosoy-e3e4e7 (2.23) = Harosoy-e3 (2.23).
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Table 3. Frequency of pigmented or cracked seeds in Harosoy and its near-isogenic soybean lines under control and chilling treatments at Tsukuba, Japan, in 2003. Data are means ± SE.
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Fig. 1. Effects of chilling treatments and age of flowers on seed coat pigmentation in Harosoy and its near-isogenic soybean lines, Harosoy-e3, Harosoy-e4, Harosoy-e3e4, Harosoy-e3e4e7. Pigmentation index (0, not pigmented to 4, severely pigmented), bars indicate standard error of the mean, numbers at each data point represent the number of seeds obtained from flowers exposed to chilling at a similar stage.
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The proportion of cracked seeds in plants continuously grown in the greenhouse was less than 1% and was substantially increased by chilling treatment (Table 3). In contrast to the pigmentation indices, cracking indices generally increased with the age of flowers from 0 to 8 DAO (Fig. 2)
. Probably, the same maturity genes influence pigmentation and cracking, but the response mechanisms or thresholds may be different between the two characters. The main effects of both NILs and flower stage on the cracking index and their interaction were significant at the 1% level. Tukey's HSD test showed that the mean cracking indices were significantly different among NILs except between Harosoy and Harosoy-e3e4, and between Harosoy-e3e4e7 and Harosoy-e3. On the basis of the degree of cracking, the NILs could be ranked as follow: Harosoy-e4 (average of cracking index = 0.83) < Harosoy (1.64) = Harosoy-e3e4 (1.88) < Harosoy-e3 (2.20) = Harosoy-e3e4e7 (2.51).
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Fig. 2. Effects of chilling treatments and age of flowers on seed coat cracking in Harosoy and its near-isogenic soybean lines, Harosoy-e3, Harosoy-e4, Harosoy-e3e4, Harosoy-e3e4e7. Cracking index (0, not cracked to 4, severely cracked), bars indicate standard error of the mean, numbers at each data point represent the number of seeds obtained from flowers exposed to chilling at a similar stage.
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Intensity of both pigmentation and cracking was increased by the recessive allele e3, but reduced by the recessive allele e4. Harosoy-e3e4 showed an intermediate degree of pigmentation and cracking relative to Harosoy-e3 and Harosoy-e4. The intensity of pigmentation and cracking in Harosoy-e3e4 was not significantly different from Harosoy. These results suggest that the effects of the genotypes at E3 and E4 loci on the low-temperature induced seed coat deterioration might be additive. Harosoy-e3e4e7 exhibited a higher degree of pigmentation and cracking than Harosoy-e3e4, suggesting that the dominant allele at the E7 locus has an ability to reduce the degree of pigmentation and cracking, similar to the E1, E2, E3 and E5 loci. Only the e4 locus exhibited a unique response to the low-temperature induced seed coat deterioration similar to the previous study (Takahashi and Abe, 1999).
Treatments were initiated in the late-flowering NILs only 3 d later than in the early-flowering ones. It is unlikely that this delay brought about any large differences in environmental conditions such as daylength and temperatures or the plant's stage of development. It would appear unlikely, therefore that environmental factors during pre- or post-treatment periods or growth stage caused major differences in responses among the NILs. The linked E1 and E7, E2, E3, and E4 loci were presumed to locate in molecular linkage groups C2, O, L, and I, respectively (Cregan et al., 1999; Cober and Voldeng, 2001a; Abe et al., 2003). It is unlikely that gene(s) responsible for tolerance to seed coat pigmentation and cracking are located proximal to the maturity genes located at various positions in the genome. Each maturity gene may therefore have a specific influence on chilling induced seed coat pigmentation and cracking.
Multiple environmental and endogenous inputs regulate timing of transition from vegetative to reproductive growth in plants. The molecular genetic dissection of flowering time control in Arabidopsis has identified an integrated network of pathways that quantitatively control the timing of this developmental switch (Simpson and Dean, 2002). Some of the integrated pathways may partly be shared by the low-temperature induced process somewhere between perception of low temperatures to the development of brown pigment. Molecular cloning of the soybean maturity genes may lead to unraveling the underlying physiological mechanisms of how the maturity genes affect the low-temperature induced seed coat deterioration.
Insensitivity of flowering to long daylength is an essential trait in adaptation of soybean to high latitudes with short growing seasons and long daylengths. The double recessive genotype e3e4 is insensitive to incandescent long daylength and flowers under long daylength conditions (Saindon et al., 1989). The additive effect of E3 and E4 alleles observed in this experiment suggests that the combination effect of maturity genes on low-temperature induced seed coat deterioration may roughly be estimated by the individual gene actions. Selection for the appropriate combination of maturity genes may be effective in improving location-specific adaptation and producing high quality seeds at high latitude regions. The e4 allele may be especially useful in reducing seed coat pigmentation and cracking in soybean cultivars adapted to high latitudes.
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ACKNOWLEDGMENTS
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We thank Dr. R.L. Nelson at USDA/ARS Univ. of Illinois, and Dr. H.D. Voldeng and Dr. E.R. Cober at Plant Res. Ctr., Agric. Agri-Food Canada for supplying the seeds of the isolines. We are grateful to Dr. Y. Yogo (Natl. Agric. Research Center) for allowing the use of the phytotron and Dr. Joseph G. Dubouzet (Natl. Inst. Crop Sci.) for critical reading of the manuscript.
Received for publication February 3, 2004.
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TOP
ABSTRACT
INTRODUCTION
