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Published in Crop Sci. 44:70-75 (2004).
© 2004 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA

CROP BREEDING, GENETICS & CYTOLOGY

Developing Midstearic Acid Sunflower Lines from a High Stearic Acid Mutant

Begoña Pérez-Vich*, Juan Muñoz-Ruz and José M. Fernández-Martínez

Instituto de Agricultura Sostenible (CSIC), Apartado 4084, E-14080 Córdoba, Spain

* Corresponding author (bperez{at}cica.es).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sunflower (Helianthus annuus L.) genotypes with increased stearic acid (C18:0) content in their seed oil may be useful for food and industrial applications. The objective of this study was to isolate and characterize mid-stearic acid sunflower lines homozygous recessive for single genes from the high stearic acid mutant CAS-3 (250 g kg–1). Crosses between CAS-3 (genotype es1es1es2es2), and the inbred line HA 89, with standard low stearic acid levels (50 g kg–1; Es1Es1Es2Es2), were made to obtain F3 families segregating for either the Es1 or Es2 loci. From these families, F3 half-seeds with putative genotypes es1es1Es2Es2 (188 g kg–1) and Es1Es1es2es2 (90 g kg–1) were selected. F7–lines homozygous for es1 or es2 were developed. These lines were named CAS-19 (es1es1Es2Es2) and CAS-20 (Es1Es1es2es2) and showed mid-stearic acid levels of 168 g kg–1 (CAS-19) and 83 g kg–1 (CAS-20). The fatty acid content was evaluated in all generations by gas-liquid chromatography. The genetic composition of CAS-19 and CAS-20 was verified by evaluating progenies from crosses between both mid-stearic acid lines, and from crosses between the mid-stearic acid lines and HA 89. The new Es1Es1es2es2 and es1es1Es2Es2 genotypes expressing mid-stearic acid levels represent a further advance for the development of sunflower lines for specific edible purposes, and constitute a unique source for agronomic and genetic studies on single alleles controlling increased stearic acid content in sunflower.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
SUNFLOWER LINES with an increased stearic acid (C18:0) content in their seed oil have been developed. Osorio et al. (1995) obtained the sunflower mutants CAS-3, with high stearic acid levels (260 g kg–1, compared with 50 g kg–1 in standard sunflower seed oil), and CAS-4 and CAS-8, with a midstearic acid content (113 g kg–1 in CAS-4 and 99 g kg–1 in CAS-8, respectively). This increased stearic acid content improves the quality of the oil for specific edible purposes. Increased levels of saturated fatty acids are desired for the margarine and related industries for the development of solid or semisolid fats without harmful chemical processes such as hydrogenation or transesterification (Kritchevsky et al., 1995; Ascherio and Willet, 1997). Despite the fact that consumers have become concerned with reducing the saturated fat content in their diets, individual saturated fatty acids can have opposite nutritional effects. Initially, it was considered that all saturated fatty acids, in particular myristic (C14:0) and palmitic (C16:0) acids had the undesirable property of raising serum LDL-cholesterol levels (Zock et al., 1994), which was associated with cardiovascular disease. However, it then became well established that stearic acid does not raise LDL-cholesterol as do other saturates and may actually lower total cholesterol (Dougherty et al., 1995). Stearic acid is therefore generally considered to be at least neutral with respect to risk of cardiovascular disease (Pearson, 1994).

Genetic studies with the CAS-3 mutant indicated that the high stearic phenotype of CAS-3 was controlled by partially recessive alleles at the Es1 and Es2 loci (Pérez-Vich et al., 1999). The proposed genotype for the CAS-3 high stearic acid line was es1es1es2es2. The segregation patterns from crosses between the lines used for the genetic study indicated that the Es1 locus had the greatest effect on the stearic acid levels, but both Es loci had an additive effect on stearic acid content (Pérez-Vich et al., 1999).

A stearoyl-acyl carrier protein desaturase locus (SAD17A) has been found to cosegregate with the Es1 locus (Pérez-Vich et al., 2002a). This enzyme desaturates stearate to oleate in the de novo biosynthesis of fatty acids in seed plastids (Somerville et al., 2000). Using linkage maps constructed of AFLP and RFLP markers, the SAD17A locus was found to underlie the major QTL affecting the concentration of stearic acid in CAS-3, explaining around 80% of the phenotypic variance of this fatty acid (Pérez-Vich et al., 2002a). Other minor QTLs affecting stearic acid content were detected in that study. However, they differed depending on the populations or the method used to perform the QTL analyses. Therefore, neither of those minor QTLs was considered a good candidate for the Es2 locus. It was suggested that the highly significant effect of the macromutation Es1 probably reduced the power for identifying other QTL affecting stearic acid levels (Pérez-Vich et al., 2002a).

The development of lines homozygous for either the es1 or the es2 alleles (genotypes for stearic acid content es1es1Es2Es2 and Es1Es1es2es2, respectively) is of great interest for further genetic, agronomic, and biochemical studies, because they would allow the study of each allele independently (i.e., the study of es2 without the effect of es1). Additionally, both types of homozygous lines might produce novel midstearic acid profiles, of great value for specific food applications. The objective of the present work was to isolate and characterize sunflower lines homozygous for es1 or es2 from the high stearic acid mutant CAS-3.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Isolation of Lines Homozygous for es1 or es2
Two sunflower lines were used to generate the F2 population segregating for stearic acid content from which the isolation of lines homozygous for the es1 and es2 alleles was initiated. A high C18:0 mutant line, CAS-3, obtained by Osorio et al. (1995) and an oilseed maintainer line, HA 89, released by the Texas Agricultural Experiment Station and the USDA-ARS in 1971 with the standard low stearic acid fatty acid profile of cultivated sunflower were crossed. The resulting F2 population from the cross HA 89 x CAS-3 was evaluated by analyzing the fatty acid composition of F2 half-seeds by gas-liquid chromatography (GLC), as described by Pérez-Vich et al. (1999). A total of 21 F2 half-seeds, representing the stearic acid range for stearic acid concentration detected in this F2 generation (from 40–260 g kg–1), were selected, germinated, and transplanted into the field at the experimental farm of the Instituto de Agricultura Sostenible at Córdoba (southern Spain) to generate F3 populations segregating for stearic acid content. For the evaluation of the F3 generation, a preliminary screening of 12 F3 half-seeds from each of the 21 F2 plants was done to identify the presence or absence of segregation for stearic acid content. After that, about 96 seeds from each segregating F3 population were analyzed.

The study of the F3 populations segregating for stearic acid content allowed the identification of three F3 families with a stearic acid content ranging from 35 to 200 g kg–1. Our hypothesis was that these populations were segregating for the Es1 locus, the Es2 locus being putatively in a homozygous dominant state. Within these families, nine F3 half-seeds showing the highest stearic acid levels (from 182–200 g kg–1) were selected to isolate the es1es1Es2Es2 genotype. Following a similar approach, an F3 family ranging for stearic acid content from 32 to 95 g kg–1 was identified. This family was hypothesized to segregate for the Es2 locus, the Es1 locus being in a homozygous dominant state. Within this family, four F3 half-seeds with the highest stearic acid content (from 85–95 g kg–1) were selected to isolate the Es1Es1es2es2 genotype.

The selected F3 half-seeds were sown under greenhouse conditions [35/15°C (day/night) with 16-h daylength]. Each F3 plant was self-pollinated. To avoid contamination with external pollen, each plant head was covered with a paper bag at flowering. F4 half-seeds from each F3 plant were analyzed for fatty acid composition, and those non-segregating F3 plants which maintained an average stearic acid content within the range of the original F3 selected half-seeds were selected. The selected F3 plants derived from F3 half-seeds with an hypothesized genotype for stearic acid content es1es1Es2Es2 or Es1Es1es2es2 were named CAS-19 and CAS-20, respectively. F4 half-seeds from selected F3 plants were sown under field conditions and the F4 plants were self-pollinated as described above. Six to 10 F5 half-seeds per F4 plant were also analyzed for fatty acid composition. F5 half-seeds from F4 CAS-19 and CAS-20 plants showing an average stearic acid content within the range for stearic acid observed in the previous generation were sown, and this process was repeated in the F6 and F7 generations. Plants of the parental lines of the original cross, CAS-3 and HA 89, were grown as control lines and analyzed for fatty acid composition in all generations.

Verification of the Genetic Composition of the Isolated Lines
Crosses between CAS-19 and CAS-20 were made to verify whether these two lines possessed the hypothesized genotypes. Additionally, crosses of CAS-19 and CAS-20 with the inbred line HA 89, with a standard low stearic acid fatty acid profile, were also made to determine the inheritance of their stearic acid content separately.

F5 half-seeds from CAS-19 and CAS-20 plants, and half-seeds of the inbred line HA 89 and the high stearic acid mutant line CAS-3, both used as a check, were germinated, and after 15 d in a growth chamber [25/15°C (day/night) with 16-h day-length], were transplanted into pots in a mesh-cage at the Instituto de Agricultura Sostenible. Each head was covered with a paper bag to avoid contamination with external pollen. HA 89 and CAS-3 plants were self-pollinated. Crossing between CAS-19 and CAS-20 plants was achieved through the emasculation of florets of the female parent followed by pollination of their stigmas with pollen from the male parent. The fatty acid composition of F1 half-seeds from each cross was analyzed by GLC. Half-seeds from the F1 and both parents were germinated and after fifteen days in a growth chamber, were transplanted into the field at the experimental farm of the Instituto de Agricultura Sostenible. F1 plants were self-pollinated to obtain the F2 seed. A total of 240 F2 seeds were analyzed by GLC.

F6 CAS-19 and CAS-20 plants were crossed with HA 89 under mesh-cage conditions, by means of the same procedure mentioned above for crosses between CAS-19 and CAS-20. F1 half-seeds were analyzed by GLC. A total of 12 F1 plants were transplanted into the field. F1 plants were self-pollinated to obtain the F2 seed. Plants of CAS-3 and HA 89 were also grown in the field as checks. A total of 335 and 336 F2 half-seeds were analyzed by GLC for the HA 89 x CAS-19 and the HA 89 x CAS-20 crosses, respectively.

The stearic acid content of F2 half-seeds was assigned to phenotypic classes on the basis of the appearance of discontinuities in the F2 stearic acid distribution, and on the stearic acid values found in the parental lines grown under the same environment. The observed proportions within each phenotypic class were compared with those expected on the basis of a one-locus segregation for the HA 89 x CAS-19 cross (F2 genetic ratio of 3:1) or a two-loci segregation for the CAS-19 x CAS-20 cross (F2 genetic ratio of 15:1). Goodness of fit of tested ratios to observed ratios was measured by the Chi-square test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Isolation of Lines Homozygous for es1 or es2
CAS-3 had an average stearic acid content of 250 g kg–1, compared with 46 g kg–1 for HA 89 (Fig. 1a). The stearic acid content in the HA 89 x CAS-3 F2 population ranged from 40 to 260 g kg–1, showing an average stearic acid value of 111 g kg–1 (Fig. 1a). Stearic acid phenotypic classes in the F2 population were defined on the basis of the stearic acid content of the parents grown in the same environment. According to this criterion, three stearic acid classes, <55 g kg–1, 55 g kg–1 to 220 g kg–1, and >220 g kg–1, were identified. The observed numbers for the three classes (15:141:14) satisfactorily fit a phenotypic ratio of 1:14:1 ({chi}2 = 3.28, P = 0.19), which indicated segregation of the two genes Es1 and Es2 previously described by Pérez-Vich et al. (1999).



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  		Fig. 1. Mean and range of stearic acid (C18:0) content in the sunflower parental lines CAS-3 and HA 89 and in the F2 to F7 generations from their cross. (a) Isolation of CAS-19; (b) Isolation of CAS-20. The square symbols represent the average stearic acid value in each generation. The circular symbols represent the maximum and minimum C18:0 values in each generation.

 
The analysis of the stearic acid content in the F3 generation from the HA 89 x CAS-3 cross allowed for the identification of three F3 families with a stearic acid range from 35 to 200 g kg–1 (Fig. 1a), and one F3 family with stearic acid content ranging from 32 to 95 g kg–1 (Fig. 1b). These F3 families were hypothesized to segregate for Es1, Es2 being in a homozygous dominant state (Fig. 1a), or for Es2, Es1 being in a homozygous dominant state (Fig. 1b), respectively. F3 half-seeds with the highest stearic acid content in the stearic acid distribution from these two groups of F3 families were selected to isolate the es1es1Es2Es2 or the Es1Es1es2es2 genotypes (Table 1). The stearic acid range of these selected F3 half-seeds was outside that observed in the parental lines grown in the same environment (Table 1).


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  		Table 1. Pedigree, mean, and range of the stearic acid (C18:0) content in F3, F4, F5, F6, and F7 half-seeds with hypothesized genotypes es1es1Es2Es2 or Es1Es1es2es2, and in the HA 89 and CAS-3 sunflower lines grown in the same environment.

 
Four F3 plants with a putative genotype es1es1Es2Es2 had F4 half-seeds with a stearic acid content between 127 and 225 g kg–1 in the following generation (Fig. 1a and Table 1). These plants were selected and designated CAS-19. The other F3 plants analyzed coming from the selected F3 half-seeds were discarded, since they showed a stearic acid range of variation similar to the parental line CAS-3 (from 230–290 g kg–1), or they segregated from low (50 g kg–1) to high (290 g kg–1) stearic acid values. Average stearic acid values of CAS-19 in the F5, F6, and F7 generations were 149, 153, and 168 g kg–1, respectively, showing a similar stearic acid range (Fig. 1a and Table 1), which indicates that stearic acid content was fixed in the F4 generation. CAS-19 had a three-fold increase in its stearic acid content compared with the standard-low stearic acid line HA 89 (Table 2). This increased stearic acid content was developed at the expense of oleic acid (C18:1) (Table 2).


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  		Table 2. Fatty acid composition of the sunflower lines CAS-3, HA 89, CAS-19, and CAS-20, and of F1 half-seeds from crosses of HA 89 with CAS-19 and CAS-20.

 
The analysis of F4 half-seeds from F3 plants derived from selected F3 half-seeds with a putative genotype Es1Es1es2es2 showed a stearic acid range between 79 g kg–1 and 124 g kg–1, with an average stearic acid value of 98 g kg–1 (Fig. 1b and Table 1). The F3 plants analyzed were selected and designated CAS-20. The F5, F6, and F7 half-seeds of CAS-20 maintained similar stearic acid average values (98, 77, and 83 g kg–1, respectively) and ranges of variation for stearic acid content (Fig. 1b and Table 1) through the different generations, which indicated that the stearic acid content was fixed in the F4 generation. The stearic acid content in CAS-20 represents a two-fold increase compared with that of HA 89 (Table 2). This increased stearic acid content was developed at the expense of linoleic acid (C18:2) (Table 2).

Verification of the Genetic Composition of the Isolated Lines
Crosses between CAS-19 and CAS-20 were made to verify that the selected lines had the proposed genotype for stearic acid content. The evaluation of these crosses was based on a model of two independent loci because each of the parents was hypothesized to have a major allele for increased stearic acid content. The average stearic acid content of the F1 seeds from the CAS-19 x CAS-20 cross (87 g kg–1) was significantly different and lower than that observed in both parents grown in the same environment (98 g kg–1 for CAS-20 and 149 g kg–1 for CAS-19). This transgressive F1 value suggested that CAS-19 and CAS-20 had alleles for stearic acid content at different loci. The F2 generation was evaluated to verify this hypothesis. The stearic acid content in F2 half-seeds in three different F2 families from the CAS-19 x CAS-20 cross ranged from 35 to 227 g kg–1, showing in all cases transgressive stearic acid values (Fig. 2a). F2 half-seeds with a stearic acid content lower than any seed of CAS-20 (low-transgressive), as well as F2 half-seeds with stearic acid values higher than any half-seed of CAS-19 grown in the same environment were detected (Fig. 2a). While low-transgressive, and parental stearic acid classes overlapped and could not be separated clearly, a group of F2 half-seeds with a stearic acid content higher than any seed of CAS-19 (≥200 g kg–1) could be distinguished (Fig. 2a). In the three F2 families evaluated, the stearic acid content fit a 15:1 (<200 g kg–1: ≥200 g kg–1) ratio (Table 3), that would be expected for segregation of alleles at two independent loci.



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  		Fig. 2. (a) Distribution of stearic acid (C18:0) content in individual seeds of the sunflower parental lines CAS-19 and CAS-20 and in F2 seeds from their cross. Seeds of HA 89 and CAS-3 were included as control lines; (b) Distribution of C18:0 content in individual seeds of the sunflower parental lines HA 89 and CAS-19, and in F2 seeds from their cross. Seeds of CAS-3 were included as a control line; (c) Distribution of C18:0 content in individual seeds of the sunflower parental lines HA 89 and CAS-20, and in F2 seeds from their cross. Seeds of CAS-3 were included as a control line.

 

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  		Table 3. Number of sunflower seeds having different stearic acid (C18:0) content and Chi-square analyses in the F2 generation from crosses between CAS-19 and CAS-20, and from crosses of HA 89 with CAS-19.

 
Crosses of HA 89 with CAS-19 and CAS-20 were also studied to determine the inheritance of the stearic acid content in these lines separately. The stearic acid content of F1 seeds from the HA 89 x CAS-19 cross (64 g kg–1) was significantly different from that of both parents (153 g kg–1 for CAS-19, and 46 g kg–1 for HA 89) and lower than the midparent value (99 g kg–1) (Table 2). The mean stearic acid content in the F1 seeds from the cross between HA 89 and CAS-20 was 41 g kg–1, which was not statistically different from the stearic acid value in the parent HA 89 (Table 2). These results indicated that alleles controlling low stearic acid content in HA 89 are partially dominant to those determining increased stearic acid in CAS-19, and dominant to those for increased stearic acid content in CAS-20.

The stearic acid content in individual F2 half-seeds from the cross between HA 89 and CAS-19 plants ranged from 35 to 170 g kg–1 (Fig. 2b), and showed a bimodal distribution (Fig. 2b). The first class ranged from 35 to 90 g kg–1, which was similar to the range observed in HA 89 and the F1, and the second class ranged from 120 to 172 g kg–1, which was coincident with the range observed in CAS-19 (Fig. 2b). In the four F2 families studied, the observed data satisfactorily fit a phenotypic ratio of 3:1 (Table 3), which confirmed that the increased stearic acid content in CAS-19 is controlled by alleles at the single Es1 locus.

The stearic acid content of the F2 seeds from crosses between HA 89 and CAS-20 showed a continuous distribution, ranging from 3.8 to 12.5% (Fig. 2c). It was not possible to detect classes with normal (=HA 89) or increased (=CAS-20) stearic acid content, even though the F2 clearly segregated covering the whole stearic acid range observed in the parental lines (Fig. 2b). In the four F2 families analyzed, the stearic acid content of about 25% of the F2 half-seeds fell within the range of stearic acid values observed for CAS-20 (Fig. 2b). These results, together with those obtained from the CAS-19 x CAS-20 and HA 89 x CAS-19 crosses, suggested that the HA 89 x CAS-20 cross was segregating for the Es2 gene.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
This study resulted in the development of two mid-stearic acid sunflower lines by isolating genotypes homozygous recessive for single genes from the high stearic acid mutant CAS-3. The CAS-19 line is homozygous for the es1 allele from CAS-3 and has an average stearic acid content of 165 g kg–1, whereas the CAS-20 line is homozygous for the es2 allele from CAS-3 and has a stearic acid mean value of 89 g kg–1.

CAS-19 and CAS-20 constitute novel sources of midstearic acid seed oil in sunflower. Osorio et al. (1995) reported the development of the sunflower mutants CAS-4 and CAS-8 with average stearic acid contents of 113 and 99 g kg–1, respectively, which are different from the stearic acid values of the CAS-19 and CAS-20 lines. Increased stearic acid content in CAS-4 was reported to be controlled by alleles at the Es1 and the Es2 loci (genotype es1bes1bes2es2; Pérez-Vich et al., 2002b). In the case of the line CAS-19, increased stearic acid levels are determined by alleles at the single loci Es1. Monogenic inheritance of increased stearic acid content in this line is advantageous for transferring this trait into sunflower hybrids with good agronomic performance, which is a requisite for the commercial use of the new oils.

Although the major gene Es2 is involved in the genetic control of the midstearic acid trait in CAS-20, the continuous F2 distribution for the levels of this fatty acid observed in crosses between CAS-20 and HA 89 suggested that minor genes and environmental effects also are important in the expression of this character in this line. A similar behavior has been described for stearic acid concentration in the sunflower mutant CAS-4 (Pérez-Vich et al., 2002b), and other fatty acids in other oil crops, for example for the linolenic (C18:3) acid in the soybean [Glycine max (L.) Merr.] mutant line A5 (Rennie and Tanner, 1991; Graef et al., 1988; Fehr et al., 1992). Further characterization of the CAS-20 line and its evaluation under different environmental conditions is required to accurately determine factors other than Es2 affecting the expression of increased stearic acid values in this line. Because of the apparent complexity of the genetic control of increased stearic acid content in CAS-20 and the possible interaction with environment, the use of marker-assisted selection to introgress the desired genes into desirable germplasm might be needed in breeding programs for increasing the stearic acid content in sunflower seed oil from the CAS-20 line.

The isolation process of the CAS-19 and CAS-20 lines as well as the genetic studies conducted with both lines confirmed the differential effects of the Es1 and the Es2 loci on the stearic acid content in sunflower seed oil (Pérez-Vich et al., 1999). The results of the present research also indicated that the larger effect on stearic acid content of the es1 allele partially masked that of the alleles at the Es2 locus, as previously suggested by Pérez-Vich et al. (2002a). A completely recessive effect of the es2 allele has been observed when it has been studied without the presence of the es1 allele (in the HA 89 x CAS-20 cross), whereas Pérez-Vich et al. (1999) found a partially recessive effect of es2 when it was studied in CAS-3 (stearic acid genotype es1es1es2es2). In addition, Osorio et al. (1995) indicated that the high stearic acid concentration in CAS-3 was developed at the expense of oleic acid. According to the results of this research, this seems to be an effect of the Es1 locus, since increased stearic acid content in CAS-20 was developed at the expense of linoleic acid. This masking effect of the Es1 locus probably prevented the identification of molecular markers linked to the Es2 locus (Pérez-Vich et al., 2002a). The use of populations derived from CAS-20 in which the Es2 locus will segregate without the effect of the es1 allele will be of great value for mapping Es2.

In conclusion, the lines CAS-19 and CAS-20 constitute a new valuable material for agronomic, genetic, molecular, and biochemical studies on seed fatty acid biosynthesis in sunflower. In addition, their stearic acid content represents an advance toward the development of sunflower lines with specific fatty acid profiles for edible purposes.

Received for publication October 29, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 


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B. Perez-Vich, L. Velasco, J. Munoz-Ruz, and J. M. Fernandez-Martinez
Inheritance of High Stearic Acid Content in the Sunflower Mutant CAS-14
Crop Sci., December 2, 2005; 46(1): 22 - 29.
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