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Crop Science 42:37-44 (2002)
© 2002 Crop Science Society of America

CROP BREEDING, GENETICS & CYTOLOGY

Genotype x Environment Interactions, Stability, and Agronomic Performance of Soybean with Altered Fatty Acid Profiles

Valerio S. Primomoa,b, Duane E. Falka, Gary R. Ablettb, Jack W. Tannera and Istvan Rajcan*,a

a Dep. of Plant Agriculture, Crop Science Division, Univ. of Guelph, Guelph, ON, N1G 2W1 Canada
b M.S. degree from the Dep. of Plant Agriculture, Crop Science Division at the Univ. of Guelph

* Corresponding author (irajcan{at}uoguelph.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
There has been a major effort to produce soybean [Glycine max (L.) Merr.] lines with modified fatty acid profiles in order to improve quality and develop new uses for soybean oil. Utilization of the lines depends on their agronomic traits and stability of the fatty acid profiles in diverse environments. The objectives of this study were to (i) evaluate the influence of years and locations on the fatty acid composition of soybean genotypes with unique fatty acid profiles, (ii) determine which fatty acids and fatty acid profiles are the most stable, and (iii) evaluate agronomic and seed quality traits of mutant soybean lines. Genotypes were evaluated over three years (1996, 1997, and 1998) at four locations in Southern Ontario, Canada. Year effects had the largest impact on all fatty acid levels. Location effects were significant only for oleic and linolenic acids. Genotype x year interaction effect was significant for all fatty acids whereas genotype x location and genotype x year x location interaction effects were significant only for oleic, linoleic, and linolenic acids. Mutants with reduced or elevated palmitic, elevated oleic, or reduced linolenic acid concentrations exhibited average or higher stability than lines with normal levels of these fatty acids. Therefore, these lines may be suitable for growing in a wide range of environments. Maturity, plant height, lodging, seed size, and seed quality were significantly different between mutants and cultivars. Seed yield was significantly reduced in mutants compared to cultivars.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
THE END USE OF SOYBEAN [Glycine max (L.) Merr.] oil is influenced by its fatty acid composition. The seed oil of common soybean cultivars consists of {approx}110 g kg -1 palmitic, 40 g kg-1 stearic, 240 g kg-1 oleic, 540 g kg-1 linoleic, and 70 g kg-1 linolenic acid. Genetic manipulation of soybean fatty acid composition can produce soybean oil with specific industrial and nutritional value. New soybean genotypes with elevated or reduced levels of palmitic acid, elevated stearic and oleic acids, and lowered linolenic acid have been developed by chemical mutagenesis at the University of Guelph. Although these new genotypes can be of commercial value, their commercialization will depend on agronomic performance and fatty acid profile stability in different years and locations.

Development of cultivars with different fatty acid profiles will depend on the associations of specific alleles affecting levels of fatty acids with agronomic and seed traits of economic importance. Several studies have shown that alleles affecting levels of fatty acids have a negative influence on these agronomically important traits. Comparisons between reduced ({approx}40 g kg-1) and normal ({approx}110 g kg-1) palmitic acid families showed a significant decrease in seed yield (Rebetzke et al., 1998; Ndzana et al., 1994) and total oil content (Ndzana et al., 1994) in the reduced palmitic acid lines. Lundeen et al. (1987) reported that there were significant differences between the means of the elevated and normal stearic acid lines for maturity, lodging, plant height, and protein and oil contents, however, it was of little agronomic importance.

Other studies have shown that mutant alleles do not have a significant effect on agronomic traits. Horejsi et al. (1994) used backcrossing to develop reduced palmitic acid families with seed yields similar to the recurrent parent. Lundeen et al. (1987) and Hartmann et al. (1997) reported that there were lines with elevated stearic acid contents that were not significantly different in seed yield than the highest yielding line in the population. Increasing oleic acid content in soybean by recurrent selection was correlated with increases in seed size and a reduction in time to maturity, but seed yield, seed oil, and protein content seemed to be unaffected (Carver et al., 1986). Wilcox et al. (1993) and McClure (1999) both indicated that the fan allele was not associated with agronomic traits desired in commercial soybean cultivars with low levels of linolenic acid.

The usefulness of soybean, with altered fatty acid profiles, in a breeding program also is dependent upon the stability of the mutant allele across different environments. Several studies have investigated the effect of years or locations on the fatty acid content of soybean lines with different fatty acid profiles (Cherry et al., 1985; Schnebly and Fehr, 1993; McClure, 1999). The differences in fatty acid content are likely due to the different weather patterns from year to year and from location to location. Studies have indicated that temperature plays a vital role in the synthesis of fatty acids, especially unsaturated fatty acids, in soybean oil. Studies conducted with common cultivars under extreme temperature conditions have indicated that seeds from soybean plants exposed to high daily temperatures have reduced linoleic and linolenic acids and increased oleic acid contents (Howell and Collins, 1957; Wolf et al., 1982; Dornbos and Mullen, 1992). Levels of palmitic and stearic acids remained essentially unchanged across the range in temperatures evaluated. Rennie and Tanner (1989) investigated the effect of extreme temperature conditions on the fatty acid content of soybean lines with reduced linolenic acid and elevated stearic acid contents. Their results indicated that lower levels of linolenic acid were associated with higher temperatures, and soybean lines with reduced linolenic acid were less sensitive to wide temperature changes. Their data also demonstrated that higher levels of stearic acid were associated with higher temperatures, and that soybean lines with elevated stearic acid were very sensitive to wide temperature changes. Levels of palmitic acid were relatively stable across the range of temperatures in their study. These studies evaluated a limited number of fatty acid profiles, and only within a year across locations or within a location across years.

It is important for breeders and producers to understand the influence of environment on the composition of soybean oil and the influence of mutant alleles on agronomic traits from genotypes with altered fatty acid profiles. The objectives of this study were to (i) evaluate the influence of years and locations on the fatty acid composition of 17 soybean genotypes with unique fatty acid profiles, (ii) determine which fatty acids and fatty acid profiles are the most stable, and (iii) evaluate agronomic and seed quality traits of mutant soybean lines.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Three soybean cultivars (Century, Elgin87, and OAC Shire) and fourteen soybean lines with altered fatty acid profiles were used in this study (Table 1). On the basis of fatty acid content, the mutant genotypes were divided into nine fatty acid profiles: reduced palmitic, elevated palmitic, elevated stearic, elevated oleic, reduced linolenic, reduced palmitic and linolenic, elevated stearic and reduced linolenic, elevated oleic and reduced linolenic, and normal cultivars. In general, the fatty acid contents of the mutant soybean lines were significantly different from the normal fatty acid content of traditional soybean cultivars over 12 environments.


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  		Table 1. Fatty acid profile of 17 soybean genotypes planted in 12 environments.

 
The mutant lines C1726, C1727, and C1640 were developed by chemical mutation of Century with ethyl methanesulfonate (EMS) (Erickson et al., 1988; Wilcox et al., 1984). In 1987, approximately 2000 seeds of the soybean cultivar Elgin87 and low linolenic acid line C1640 were treated with EMS as described by Stojsin et al. (1998a) and Stojsin et al. (1998b), respectively. Single seed descent was used to advance the populations to the M4 generation, subsequently analyzed for fatty acid content. In 1992, several lines with altered fatty acid profiles were identified from both populations. Lines designated as ELLP2, ELHP1, RG6, RG7, and RG9 originated from the mutated Elgin87 population and lines RG10, CLP1, and RG8 originated from the mutated C1640 population (Fig. 1) . In 1994, the crosses ELLP2 x C1726, ELLP2 x CLP1, and A5 x N78-2245 were made in order to combine different mutant alleles. Transgressive segregants originating from the three crosses gave rise to soybean lines designated as RG3, RG1, and AN145-66, respectively.



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  		Fig. 1. The origin of mutant soybean lines with different fatty acid composition. The major alleles controlling the genotype of the mutant soybeans are given in bold.

 
The fourteen soybean lines with modified fatty acid composition and three normal cultivars were grown in 1996, 1997, and 1998 at four locations in Southern Ontario, Canada (Woodstock, Talbotville, Ridgetown, and Tilbury). Weather data across each year and location was provided by Environment Canada (Table 2). The soil texture in Tilbury was clay, with clay loam at all other locations. A randomized complete block design was used with three replications in each year, and at each location. The plots at Woodstock and Talbotville consisted of four rows, each 6 m long, with 37.5 cm between rows within the plots and also between adjacent plots. The plots at Ridgetown and Tilbury consisted of five rows, each 4 m long, with 42 cm between rows within the plots and between adjacent plots. Approximately 500 seeds were planted per plot.


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  		Table 2. Monthly high, low, and mean temperatures and total precipitation for the 1996, 1997 and 1998 growing seasons in Woodstock (WS), Talbotville (TV), Ridgetown (RG), and Tilbury (TB), Ontario, Canada.

 
The following agronomic traits were measured on all plots at each location and each year: seed yield, days to maturity, plant lodging, and plant height. Seed quality traits (seed size and quality) were measured as a bulk of the three replications at each location. In 1996 and 1997, Ridgetown and Tilbury experienced hailstorms that resulted in poor and unreliable agronomic data and thus were not included in the data analysis. However, this did not affect fatty acid profiles and therefore lines were still analyzed for fatty acid composition. The seed yield at Woodstock and Talbotville was measured as mature seed harvested and threshed from 5.4 m lengths of the four rows. The seed yield at Ridgetown and Tilbury in 1998 was measured as mature seed harvested and threshed from 2.5 m lengths of the three middle rows. Days to maturity were recorded when 95% of the pods matured. Lodging was scored from 1 (all plants in a plot erect) to 5 (all plants in a plot prostrate). Plant height was estimated as the distance from the soil surface to the tip of the main stem for a representative plant. Seed size was recorded as the weight of 100 randomly selected seeds from a bulk at each location. Seed quality was rated from 1 (seed surface smooth with no evidence of shriveling) to 5 (seed very shriveled).

Four plants were randomly selected from each plot for gas chromatography analysis to determine fatty acid profile. The fatty acid composition of each randomly selected plant was measured by bulking four seeds per plant. Each four-seed sample was placed in an envelope, and manually crushed with a hammer. A small sample was taken from each individual envelope, and placed in separate test tubes for fatty acid extraction.

Fatty Acid Analysis
For fatty acid extraction, each crushed sample was placed in a separate glass test tube (13 x 100 cm). The samples were dried overnight in an oven at 90°C. To each test tube 0.6 mL of 0.25 M KOH solution (250 mL methanol, 250 mL ethyl-ether, and 7.01 g KOH) was added. The samples were vortexed for 15 sec and then heated in a hot water bath, at 60°C, for 1 min. The heated samples were allowed to cool for 5 min. Two mL of saturated NaCl solution and 1.5 mL of iso-octane were added to each reaction test tube. Each sample was vortexed for 30 sec. The phases were allowed to separate for 45 min and then 0.85 mL of supernatant was pipetted into a 12 x 32 mm (2 mL) autosampling vial capped with an aluminum seal. Gas chromatograph fitted with a capillary column (15 m long and 0.25 mm diameter) (J&W Scientific, Folsom, CA) was used for fatty acid analysis. The oven, injection, and detector temperatures were adjusted to 180°C, 290°C, and 330°C, respectively. The air, hydrogen, and helium (carrier gas) flow rates were set to 400 mL/min, 30 mL/min, and 0.7 mL/min, respectively. Standard fatty acid mixtures (D102 and D103) from Serdary Research Laboratories (London, ON, Canada) were used as controls and to calibrate a standard curve. Peaks were recorded and integrated by the Hewlett Packard ChemStation Software (Hewlett Packard, Mississauga, ON, Canada). Five fatty acids, palmitic, stearic, oleic, linoleic, and linolenic were evaluated.

Data Analyses
Analyses of variance were conducted for all data collected over the three years by standard statistical procedures. The expected mean squares for the analysis of variance were calculated by PROC GLM in SAS (SAS, 1996) (Table 3). Genotype was considered a fixed effect and all other effects were considered random. Agronomic and fatty acid data were analyzed using PROC GLM in SAS (SAS, 1996). The estimates of the variance components were calculated using PROC MIXED in SAS (SAS, 1996). The stability regression coefficient (b-value) was calculated for each fatty acid and for each genotype according to Finlay and Wilkinson (1963) to determine if the altered fatty acid levels were stable across different environments. In general, genotypes with b-values (i) <0.70 were considered unresponsive to different environments or had above average stability; (ii) between 0.70 and 1.30 had average stability; and (iii) >1.30 were considered responsive to good environments or had below average stability (Lin and Binns, 1985).


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  		Table 3. Expected mean squares for the sources of variation assuming a random model for all effects except genotype.

 

   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Our study is different from other studies in that we used soybean with a wide range of fatty acid profiles, and tested them for fatty acid stability and agronomic performance in a number of diverse environments. The genotypes were tested across different years and locations, which has not been done in other studies. In addition, several of the fatty acid combinations used in this study have never been reported.

Genotype x Environment Interactions of Fatty Acids
The combined analysis of variance indicated that year effects were significant for all fatty acids considered (Table 4). Years accounted for a large proportion of the total variance for stearic (26%) and the unsaturated fatty acids (46, 50, and 52%, respectively) but had a less marked effect on palmitic acid (13%). In 1998, all genotypes had higher stearic and oleic, and lower linoleic and linolenic acid levels relative to 1997 and 1996 (Table 5). Palmitic acid levels were relatively the same suggesting that this fatty acid was likely the most stable and that the differences were of minor importance.


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  		Table 4. Combined analysis of variance and estimate of variance components (VC) for fatty acid composition over 17 genotypes and 12 environments.

 

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  		Table 5. Fatty acid composition of 17 soybean genotypes planted at four locations (Woodstock, Talbotville, Ridgetown, and Tilbury, Ontario, Canada) during 1996, 1997, and 1998.

 
Location effects were not significant for palmitic, stearic, and linoleic acids but were significant for oleic and linolenic acids (Table 4). Location effects accounted for 4% and 10% of the total oleic and linolenic acid variances, respectively. The results indicated that fatty acid content in soybean was more affected by year than by location effects and that oleic and linolenic acids were more sensitive to environmental changes than the other fatty acids. It was found that genotypes grown in Woodstock generally had the lowest oleic and highest linolenic acid levels while the reverse was observed for Tilbury. This suggested that temperature could be playing a significant role in oleic and linolenic acid concentrations because locations further south generally have higher temperatures.

Genotype x year interaction effects were significant for all fatty acids in the combined analyses over years and locations, especially stearic acid (Table 4). Genotype x location and genotype x year x location effects were significant only for oleic, linoleic, and linolenic acids. Although the genotype x location and genotype x year x location effects for oleic, linoleic, and linolenic acids were significant, the variance components for these effects were small in comparison to year and genotype x year variances. Thus, the genotype x location and genotype x year x location effects for oleic, linoleic, and linolenic acids, although statistically significant, were relatively less important than the year and genotype x year effects.

Studies conducted in controlled environments have shown that temperature (Wolf et al., 1982) and precipitation (Dornbos and Mullen, 1992) are environmental factors that have a major impact on soybean fatty acid levels in the seed. Therefore, temperature and precipitation could be the underlying factors that have contributed to the year and location effects observed in this study. For this reason, temperature and precipitation differences between 1998 and the previous two years were considered (Table 2). In general, 1998 was substantially drier than 1997 and 1996 growing season. We also observed that May, August, and September of 1998 were warmer in comparison with the same months in 1997 and 1996 (Table 2). All other months were relatively the same for temperature across the three years. These climatic conditions likely contributed to most of the differences observed among years. Studies have also revealed that temperature and precipitation do not significantly affect palmitic acid levels in soybean (Wolf et al., 1982; Dornbos and Mullen, 1992). The fact that palmitic acid content was affected by year in this study suggested that environmental factors other than temperature and precipitation might have an effect on this and the other fatty acids. Factors such as planting date (Wilcox and Cavins, 1992; Schnebly and Fehr, 1993), cultural practices, soil type, or weed, disease or insect pressure also could affect fatty acid content but these factors were not investigated in our study.

From a biochemical standpoint, our results are consistent with Cheesbrough (1989) who showed that some of the enzymes involved in the fatty acid synthesis pathway are influenced by temperature. Their study indicated that temperatures >35°C nearly abolished oleoyl and linoleoyl desaturase activities, stearoyl-ACP desaturase activity decreased six-fold between 20 and 35°C, and palmitoyl-ACP elongation showed little change with respect to temperature.

Stability of Soybean Genotypes
Although the fatty acid content of genotypes were influenced by year and location the fluctuations for a majority of the them were considered stable on the basis of Finlay-Wilkinson analyses (Table 6). It was not surprising to find that the fatty acid b-values for cultivars were indicative of average stability since these represent the normal levels found in soybean seed. Surprisingly, we found that most of the altered fatty acid levels in soybean were more stable than the normal levels except for elevated stearic acid content.


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  		Table 6. Fatty acid stability parameters (b-value) of 17 soybean genotypes planted in 12 environments.

 
The b-values for genotypes with reduced or elevated palmitic acid content ranged from 0.35 (RG3) to 1.48 (ELHP1). This indicated that palmitic acid content was very stable in these genotypes with the exception of ELHP1. Palmitic acid content in ELHP1 by year also was significantly different, however, the differences were considered of minor importance (Table 5). Therefore, the fap mutant alleles found in genotypes with altered palmitic acid content were considered stable.

Stearic acid content was considered of above average stability in all genotypes with normal levels because of their low b-values. Hawkins et al. (1983) also demonstrated that normal stearic acids levels were relatively stable in response to different environments. However, elevated stearic acid content in genotypes RG6, RG7, and RG8 had very high b-values, and thus, were considered unstable (Table 6). This suggested that fas alleles are unstable particularly in low temperature environments. Therefore, future research will require development of more stable mutations in order to minimize significant decreases in stearic acid content.

The elevated oleic acid content of genotypes RG9 and AN145-66 had b-values of 1.15 and 1.63, respectively (Table 6). This indicated that the oleic acid level of RG9 was stable whereas that of AN145-66 was very responsive to different environments. The difference in the two genotypes was likely due to the origin of the oleic acid content. In AN145-66, several minor genes were probably responsible for the high oleic acid content because it was derived from a recurrent selection population, whereas in RG9 it was more likely due to a single major gene. In general it was found that most of the genotypes with normal levels of oleic acid had average stability.

All reduced linolenic acid genotypes had linolenic acid b-values ranging from 0.20 to 0.68 which implied above average stability (Table 6). In addition, each fatty acid for genotypes RG10, C1640, RG1, and CLP1 also had average or above average stability. This suggested that fan alleles are less environmentally sensitive than the normal alleles. Therefore, reduced linolenic acid genotypes could be grown in cool areas without a significant increase in linolenic acid.

Agronomic Performance of Soybean Genotypes
Although our study was not designed to test the influence of mutant alleles on agronomic traits, comparisons can be made between these new genotypes and commercially available cultivars. The 17 soybean genotypes were significantly different for the agronomic traits measured in this study (Table 7). The results were not unexpected because EMS can randomly mutate any gene in the soybean genome including those that control agronomic or fatty acid traits. Although the soybean genotypes were significantly different for agronomic traits, the differences were of minor importance except for yield.


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  		Table 7. Overall agronomic means of 17 soybean genotypes planted in 8 environments (two locations in 1996 and 1997, and four locations in 1998).

 
All mutant soybean genotypes were lower in seed yield than the three cultivars, with the exception of ELLP2 (reduced palmitic) and RG7 (elevated stearic), which had yields that were not significantly different from Century and OAC Shire. The lowest yielding genotypes were RG8, RG10, and CLP1, which were all derived from chemical mutations of C1640, a genotype that had been previously mutated with EMS. Exposure to more EMS may have resulted in additional genetic changes having deleterious effects on seed yield. Furthermore, the mutant genotypes RG1 and RG3, which also carry two independent mutant alleles, had seed yields similar to genotypes that had been developed from a population exposed to EMS only once. This suggested that it should be possible to develop soybean lines with altered fatty acid profiles without a yield penalty. Our data supports the results obtained by Wilcox et al. (1993) and McClure (1999) who found that some fan breeding lines had seed yields significantly higher than their Fan counterparts. Lundeen et al. (1987) demonstrated that yield was not significantly different between soybean with normal and elevated stearic acid content. Carver et al. (1986) reported that increased oleic acid content in soybean did not affect yield.

In general, maturity, plant height, lodging, weight, and seed quality of mutant soybean genotypes were similar to the cultivars Elgin87 or Century. This was expected because the mutant soybean genotypes were developed from chemical mutation of either Elgin87 or Century. It is not known whether these agronomic traits are linked to alleles that alter the fatty acid composition of these mutant soybean genotypes, and therefore, further studies are required to address this issue. It has been previously reported, however, that soybean lines with elevated stearic (Hartmann et al., 1997; Lundeen et al., 1987), reduced palmitic (Ndzana et al., 1994; Rebetzke et al., 1998) or reduced linolenic (Wilcox et al., 1993) had minimal effects on agronomic traits in comparison with lines with normal levels. Therefore, it should be possible to develop soybean lines with altered fatty acid content and any of the desired agronomic traits.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
In conclusion, this study has provided an evaluation of the environmental and agronomic performance of a set of soybean lines with altered fatty acid profiles. It was found that year had the most effect on all five fatty acids found in soybean seed, which was likely due to the different weather conditions from 1996 to 1998. However, year had a limited effect on palmitic acid, and therefore, palmitic was considered the most stable of the five fatty acids. Stability analysis has demonstrated that most of these mutant soybean genotypes, particularly those with reduced or elevated palmitic, elevated oleic, and reduced linolenic acid, probably can be grown in different environments without significantly compromising their fatty acid profile. By contrast, genotypes with elevated stearic acid content were shown to be too environmentally sensitive. Although all mutant soybean genotypes were lower yielding in comparison to the cultivar they were derived from, i.e., Elgin87 or Century, other agronomic traits were not considerably different. The lower seed yields were thought to primarily be due to deleterious effects of EMS, and thus, further yield improvements should be possible. High yielding soybean genotypes with altered fatty acid levels could be developed because altered fatty acid contents are known to be controlled by major genes that are easily transferable by using a back-crossing system. Therefore, these mutant lines provide additional sources of germplasm useful in a breeding program aimed at altering soybean oil quality.


   ACKNOWLEDGMENTS
 
The technical assistance of Yesenia Salazar, Wade Montimy, Cal Klager, and Branko Petrusic is greatly appreciated. The authors wish to thank Dr. J.R. Wilcox for providing seeds of C1726, C1727, and C1640. Dr. Steven Bowley is acknowledged for his helpful suggestions regarding stability analysis. Dr. Bruce Luzzi is acknowledged for his initial encouragement and suggestions provided to the senior author. Appreciation is extended to the Ontario Ministry of Agriculture, Food, and Rural Affairs, the Ontario Soybean Growers and the Natural Science and Engineering Research Council of Canada (NSERC) for their generous financial support.

Received for publication October 11, 2000.


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




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