Soybean seed oil content: genetic control under different photoperiods

Soybean seed oil content:

genetic control under different photoperiods¹

Zilda F.S. Miranda, Carlos A. Arrabal Arias, José Francisco Ferraz de Toledo and Marcelo Fernandes de Oliveira

Centro Nacional de Pesquisa de Soja, Embrapa, Caixa Postal 231, 86001-970 Londrina, PR, Brasil. Send correspondence to C.A.A.A.

ABSTRACT

The oil content of soybean (Glycine max (L.) Merrill) seeds is a polygenic and complex trait that is responsive to environmental effects that occur during plant development. Our objective was to study the seed oil content of soybeans developed under diverse photoperiod and temperature conditions. Three parental inbred lines with classic (BR-13, FT-2 and BR85-29009) and one with long juvenile flowering type (OCEPAR 8) and the F2, F3, and F9 generations derived from all possible crosses between them (including reciprocals) were sowed in September 27th, October 20th and December 17th in 1993 in Londrina, Paraná State, Brazil (between 23^o08'47" and 23^o55'46" latitude S). The October and December sowing dates are within the period the varietal research personnel recommend for sowing soybeans in Paraná State. The analysis of variance indicated significant differences among sowing dates, among advanced inbred lines, and the sowing date x inbred line interaction. Seed oil content increased from September to October and decreased from October to December in all materials, but the reduction was greater in FT-2 and OCEPAR 8 among the parentals. The additive genetic variance (D) or additive variance among linked genes (D1) was significant for all crosses and sowing dates. Genotype x micro-environment interactions were important in some crosses. The additive [d] effects were greater in September and October, and the additive x additive interaction [i] was important in October among the mean genetic parameters. Significant dominance effects [h] were more frequent in December and October, often in direction of the increased seed oil content. The heritability estimates ranged from 15 to 43%, with the highest values obtained in September. The prediction of cross potential to generate higher seed oil inbred lines indicated that selection is likely to be successful in most crosses. The highest proportion of inbred lines with seed oil percentage above the standard (lines with more than 22% seed oil content) was for BR85-29009 x OCEPAR 8 in September, FT-2 x OCEPAR 8 in October, and in BR85-29009 x OCEPAR 8 and BR-13 x OCEPAR 8 in December.

INTRODUCTION

Soybean (Glycine max (L.) Merrill) is extensively cultivated in Brazil and is an important source of edible oil. Average seed oil content in Brazilian and North-American soybean cultivars are 22.19 and 21.00% (Teixeira et al., 1984; Hartwig, 1973), respectively. The genetic base of soybean is similar in both regions (Hiromoto and Vello, 1986), thus, the causes for this difference in seed oil content must be more environmental than genetic.

Soybean seed oil content is a difficult trait to study because it is under polygenic genetic control, and is sensitive to the environmental effects that influence plant development period. Genetic studies on the seed oil content of North-American cultivars are available. The genetic control of seed oil content in soybeans was found to include primarily additive gene action (Brim and Cockerham, 1961; Hanson and Weber, 1961, 1962; Hanson et al., 1967; McKendry et al., 1985; Wilcox, 1989), but some evidence for epistatic effects has been reported (Hanson and Weber, 1961, 1962). Heritability values reported ranged from moderate (0.51) to high (0.84) (Weber and Moorthy, 1952; Johnson et al., 1955; Hanson and Weber, 1962; Kwon and Torrie, 1964; Shorter et al., 1976). Cianzio et al. (1985) reported high phenotypic and rank correlations between genotypes selected under temperate and tropical conditions, indicating low genotype by environment interaction effect on seed oil content. Burton and Brim (1981) evaluated three cycles of recurrent selection for seed oil content that increased linearly at an average rate of 0.35 ± 0.30% per cycle, but no significant change was observed in total oil produced per hectare.

Evaluation of seed oil content in segregant generations was always a laborious and time-consuming task. Superior commercial cultivars were probably not developed for this trait due to these difficulties. Evaluation for seed oil content was enhanced by use of nuclear magnetic resonance (NMR) spectroscopy (Collins et al., 1967; Fehr et al., 1968; Shorter, 1972). The NMR analysis allows a quick non-destructive evaluation of seed oil content of soybean. Analyzed seeds can be sowed, guaranteeing the use of the full genetic variability.

Photoperiodism and temperature were observed to affect various traits in soybean. Number of days from emergence to flowering was reported to be positively correlated with seed oil content (Johnson et al., 1955).

The objective of this work was to study the responses in seed oil content of soybean developed under diverse photoperiod and temperature conditions. This study analyzes the genetic control of seed oil content in Brazilian soybean materials to obtain estimates of the genetic and environmental parameters including heritability. These estimates were used to predict the results of selection on the materials using the inbred line prediction method of Jinks and Pooni (1976, 1982) and Toledo (1987).

MATERIAL AND METHODS

All possible single crosses, including reciprocals, were made between the cultivars BR-13 (from the cross Bragg (4) x Santa Rosa), OCEPAR 8 (mutant of Paraná for long juvenile period), FT-2 (selection in IAS 5, a sister line of Paraná), and line BR85-29009 (from the cross União (6) x Lo76-1763, where Lo76-1763 is a selection of Industrial). These parentals include highly productive and adapted soybean germplasm (Toledo et al., 1993), which was not particularly selected for their seed oil content. They are representative, however, of the cultivars presently grown in Paraná State, Brazil.

The four parentals and the F2, F3, and F9 generations derived from the 12 crosses between them were sown in September 27, October 20 and December 17, 1993 in Londrina, PR, each date considered a different environment. A total of 13,560 single-plant hill plots were sown in a completely randomized design. Forty plants of each parental, 120 (60 straight and 60 reciprocal derived) of each F2, 150 (15 families of five individuals of each straight and reciprocal crosses) of each F3 and 400 (50 families of four individuals of straight and reciprocal) of the F9 generation were used. The hill plots (plants) were randomized individually and placed in rows at 20-cm intervals. Experimental rows were spaced at 1.5 m and two border rows of bulked remnant seeds were sown between each row and around the experiment. The border rows were sown to facilitate data collection and to keep a plant population similar to the normal field densities of 250,000 to 300,000 plants/ha. Irrigation was used each seven days to allow normal plant development.

The seed oil content was determined by NMR on soybean seed samples weighing from 3.5 to 4.5 g. One sample was obtained from every plot and stored in cold chamber at 18°C and 55% of relative humidity for moisture homogenization in the seed samples. Each sample was analyzed twice by NMR and statistical analyses were performed with the mean values.

The means and variances of seed oil content for each parent and derived generations were calculated. After testing for reciprocal effects, the cross and reciprocal in each generation were pooled. An analysis of variance was conducted to determine the importance of genetic and environmental effects. Genetic and environmental effects were estimated from the means and variances of the generations following the methodology of Cavalli (1952), Hayman (1960) and Mather and Jinks (1982). Additive [d], dominance [h], additive x additive [i] and dominant x dominant [l] epistatic effects were estimated from the generation means. Estimates of [d] are not correlated with [i] and [l], and depend only on the differences between parentals of each cross. Estimates of [h] and [l] are strongly correlated and they often show opposite signals, which makes difficult the interpretation of models including [h] and [l] jointly (Oliveira, 1994).

Estimates of the additive genetic (D), dominance (H), and additive environmental (E) variances were obtained. In the presence of linkage among pairs of genes, the additive genetic variance (D) can be partitioned into D1 and D2, which represent the genetic variances among linked genes of rank 1 and 2, respectively. Rank 1 and 2 denote the generations obtained from meiotic recombination of F1 and F2 plants, respectively (Jinks and Pooni, 1982). Presence of significant estimates of [d] is accompanied by significant estimates of D, but the absence of [d] among the mean estimates does not indicate the absence of its quadratic effect D, because the genes can be dispersed in the parental generation. In the presence of significant genotype x microenvironmental effects, as detected by significant values for the F test of the ratio between the variances (larger variance/smaller variance) of P1, P2 and F9 generations, represented by E1, E2 and E3, respectively, the variance model allowed for them.

Narrow-sense heritability in the F2 was calculated as the ratio additive genetic variance (0.5D) by phenotypic variance (0.5D + 0.25 H + E). The prediction of the crosses potential to generate superior inbred lines (Jinks and Pooni, 1976, 1982; Toledo, 1987) was conducted to evaluate the chances of selection for greater seed oil content in inbred lines derived from these materials. The F9 generation seed oil content was used to check the predictions. The reference used was 22% seed oil content, which is a higher level compared with the presently available cultivars.

RESULTS AND DISCUSSION

Degrees of freedom, means, and variances for seed oil content in the parents, F2, F3, and F9 generations of each cross, and each sowing date are presented in Table I. No reciprocal effects were detected in any case, and the data presented were pooled over reciprocals.

The ranking of the mean seed oil content of the parents and their derived generations in a decreasing order was October, December, and September for all generations (Table I). The means for seed oil content in the parents for each sowing date are illustrated in Figure I. The influence of the environment and the genetic effects on the seed oil content was evident (Tables I and ^II). Experimental conditions for soil preparation and moisture content were similar across sowing dates, and results reflect the importance that photoperiod and/or temperature have on the soybean seed oil content. No correlation between photoperiod, temperature, and length of reproductive period (number of days from flowering to physiological maturity) with seed oil content was observed when data from all sowing dates were considered. High temperature is known to have a positive influence in the seed oil content (Hartwig, 1973). The absence of correlation between temperature and seed oil content was probably caused by the differential performance of the materials for the September 27 planting. September is too early for sowing of soybean in Paraná State and plants may have unexpected responses. The length of the reproductive period also was not correlated when all sowing dates were considered. When only data from normal sowing period (October and December) were taken for the correlation analysis, the correlation value between the length of reproductive period and the oil content was positive and significant (r = 0.42). The most probable hypothesis to explain these results is that, within certain limits, photoperiod and temperature affected the reproductive period and the seed oil content in soybean.

Figure 1 - Oil content in seeds of soybean cultivars for three sowing dates in Londrina, PR.

The cultivars FT-2 and OCEPAR 8 had higher seed oil content than cultivars BR-13 and BR85-29009 at the second sowing date. The differences among parental means were smaller in the first and third sowing dates. The cultivars FT-2 and OCEPAR 8 also had greater seed oil content variation among sowing dates, whereas cultivars BR-13 and BR85-29009 had smaller variation in seed oil content among sowing dates (Table I and Figure I). The gene for later flowering under short-day conditions of OCEPAR 8 did not seem to have differentially influenced the seed oil content among sowing dates compared with FT-2.

Differences among inbred lines for each sowing date and cross combination were significant (P < 0.01), indicating genetic differences among inbred lines. Mean squares for sowing dates, inbred lines, and the interactions between them were significant (P < 0.01) for each biparental cross (^{Table II}). These results show that seed oil content in the parental cultivars was affected by sowing date and that there was a specific response for the different sowing dates. The genotypes were classified as more or less responsive to the different environmental conditions.

The genetic parameters adjusted to the seed oil content of the biparental cross means and variances in each sowing date are shown in Table III. Genetic variability for seed oil content was detected for all crosses and sowings. The mean additive genetic effects [d] predominated in the September and October sowings, while non-allelic interaction [i] was present in all crosses in the October sowing and was less important in the remaining ones. Dominance effects [h] were detected in four, three, and one cross in the December, October, and September sowing dates, respectively. Its presence, however, is taken merely as an indicator of the presence of genetic variability since it is not very useful for selection purposes in soybeans, since inbred lines are sought. Additive-dominant genetic models were observed controlling the soybean seed oil content by McKendry et al. (1985), which was similar to the results obtained in September with fewer significant epistatic parameters. Epistatic effects were present in the October sowing, a normal sowing date in Paraná.

The additive (D) or the additive among linked genes (D₁) genetic variances were detected in all crosses and sowings, except BR85-29009 x BR-13, in the December sowing date when a satisfactory variance model was not found. Linkage was detected in three crosses and in association phase (Table III). These results indicate that there was genetic variability within the biparental crosses and that it is possible to select for higher seed oil content. Genotype x microenvironment was detected in the six crosses, three of them in the October sowing, by the model fitting procedure. The October sowing date had greater additive genetic variance for use in selection programs. The observed values for [d] and D in this research were lower and similar, respectively, to the values obtained by McKendry et al. (1985). The D estimates were similar, as expected, because the Brazilian germplasm is of American origin. The smaller [d] values were probably because McKendry et al. (1985) selected divergent parents for their study while our parents were selected for their high yield capacity.

The heritability estimates ranged from 0.15 in cross FT2 x OCEPAR 8 in the December sowing to 0.43 in the cross BR8529009 x OCEPAR 8 in the September sowing (Table IV). Heritability estimates in October showed intermediate magnitudes compared with those of September and December. These values were lower than reported by Weber and Moorthy (1952), Johnson et al. (1955), Hanson and Weber (1962), Kwon and Torrie (1964) and Shorter et al. (1976).

The higher estimates of heritability obtained in September were expected since additive genetic effects predominated among the mean and variance parameters. The October sowing showed higher additive variance but the non-additive, such as dominance, epistatic and genotype x micro-environment effects caused the heritability values to be similar or smaller than those of September. The genetic variability decreased in December as indicated by the smaller estimates of D.

The possibility of selection success is given by the estimates of the cross potential to generate superior inbred lines (Jinks and Pooni, 1976, 1982; Toledo, 1987). The correlation values between expected and observed superior inbred lines were higher for the October (r = 0.84) and December (r = 0.96) sowing dates (Table IV). The correlation for September was not significant because of the lower frequency of superior inbred lines above the reference of 22%. Higher proportions of superior inbred lines were observed in the October sowing date (Table IV). The highest proportion of superior inbred lines was observed in cross FT2 x OCEPAR 8, but all crosses showed potential to generate inbred lines above 22% for seed oil content. Crosses FT-2 x OCEPAR 8 and BR8529009 x OCEPAR 8 showed potential to generate inbred lines with seed oil percentage above 22% in all sowings. Lines that are stable in oil percentage across sowings could be sought from these two crosses. In spite of the smaller percentage of superior lines expected in September, selection efficiency is expected to be high given the predominance of additive genetic effects. Dominance, epistatic, and genotype by micro-environment effects were more frequently observed in December, but of greater importance in October sowing date. Cultivar OCEPAR 8 could be considered a good parent because the three crosses were consistent across sowing dates for generating superior lines. The late flowering gene did not seem to affect OCEPAR 8 performance itself, and the late flowering gene cannot be associated with the higher seed oil content.

ACKNOWLEDGMENTS

The authors are grateful to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and FBB (Fundação Banco do Brasil) for the financial support provided for this work.

RESUMO

O teor de óleo em grãos de soja (Glycine max (L.) Merrill) é um caráter poligênico e complexo, responsivo aos efeitos ambientais presentes durante o desenvolvimento da planta. O objetivo deste trabalho foi estudar as respostas no teor de óleo em grãos de soja cultivada sob diferentes condições de fotoperíodo e temperatura. Três cultivares com florescimento clássico (BR13, FT2 e BR8529009) e uma com período juvenil longo (OCEPAR 8) e as gerações descendentes F2, F3 e F9 obtidas dos possíveis cruzamentos entre elas (incluindo os recíprocos) foram semeadas em 27 de setembro, 20 de outubro e 17 de dezembro de 1993 em Londrina, Estado do Paraná, Brasil (latitude entre 23^o08'47" e 23^o55'46" S). As datas de semeadura de outubro e de dezembro estão dentro da época recomendada pela pesquisa para a cultura da soja no Paraná. Pela análise de variância, houve significância para diferenças entre épocas de semeadura, linhagens e para a interação entre linhagens com épocas de semeadura. O teor de óleo nas sementes aumentou de setembro para outubro e diminuiu de outubro para dezembro para todos os materiais, com maior redução para FT-2 e OCEPAR 8 entre os parentais. A variância genética aditiva (D) ou aditiva entre genes ligados (D1) foi significativa para todos os cruzamentos e épocas de semeadura. Interações do tipo genótipo por micro-ambiente foram importantes para alguns cruzamentos. Entre os parâmetros genéticos de médias, os efeitos aditivos [d] foram maiores em setembro e outubro e a interação do tipo aditivo x aditivo [i] foi importante em outubro. Efeitos significativos para a dominância [h] foram mais freqüentes em dezembro e outubro, geralmente no sentido de aumentar o teor de óleo nas sementes. As estimativas da herdabilidade variaram de 15% a 43%, com maiores valores para a semeadura de setembro. As previsões do potencial dos cruzamentos para gerar linhas puras superiores para teor de óleo nas sementes indicaram que a seleção pode ser efetiva para a maioria dos cruzamentos. A maior proporção de linhas puras acima da referência (linhagens com mais de 22% de óleo) foi observada para BR85-29009 x OCEPAR 8 em setembro, FT2 x OCEPAR 8 em outubro e em BR85-29009 x OCEPAR 8 e BR-13 x OCEPAR 8 em dezembro.

(Received April 17, 1997)

• Brim, C.A. and Cockerham, C.C. (1961). Inheritance of quantitative characters in soybean. Crop Sci. 1: 187-190.
• Burton, J.W. and Brim, C.A. (1981). Recurrent selection in soybeans. III. Selection for increased percent of oil in seeds. Crop Sci. 21: 31-34.
• Cavalli, L.L. (1952). An analysis of linkage in quantitative inheritance. In: Quantitative Inheritance (Reeve, E.C.R. and Waddington, C.D., eds.). HMSO, London, pp. 135-144.
• Cianzio, S.R., Cavins, J.F. and Fehr, N.R. (1985). Protein and oil percentage of temperate soybean genotypes evaluated in tropical enviroments. Crop Sci. 25: 602-606.
• Collins, F.I., Alexander, D.E., Rodgers, R.C. and Silvela, S.L. (1967). Analysis of oil content of soybeans by wide line NMR. J. Am. Oil Chem. Soc. 44: 708-710.
• Fehr, W.R., Collins, F.I. and Weber, C.R. (1968). Evaluation of methods for protein and oil determination in soybean seed. Crop. Sci. 8: 47-49.
• Hanson, W.D. and Weber, C.R. (1961). Resolution of genetic variability in self-pollinated species with an application to the soybean. Genetics 46: 1425-1434.
• Hanson, W.D. and Weber, C.R. (1962). Analysis of genetic variability from generations of plant-progeny lines in soybeans. Crop Sci. 1: 63-67.
• Hanson, W.D., Probst, A.H. and Caldwell, B.E. (1967). Evaluation of a population of soybean genotypes with implications for improving self-pollinated crops. Crop Sci. 7: 99-103.
• Hartwig, E.E. (1973). Varietal development. In: Soybeans: Improvement, Production and Uses (Caldwell, B.E., ed). ASA, Madison, pp. 187-210.
• Hayman, B.I. (1960). Maximun likelihood estimation of genetic components of variation. Biometrics 16: 369-381.
• Hiromoto, D.M. and Vello, N.A. (1986). The genetic base of Brazilian soybean (Glycine max (L.) Merrill) cultivars. Braz. J. Genet. 9: 295-306.
• Jinks, J.L. and Pooni, H.S. (1976). Predicting the properties of recombinant inbred lines derived by single seed descent. Heredity 36: 253-266.
• Jinks, J.L. and Pooni, H.S. (1982). Predicting the properties of pure breeding lines extractable from a cross in the presence of linkage. Heredity 49: 265-270.
• Johnson, H.W., Robinson, H.F. and Comstock, R.E. (1955). Genotypic and phenotypic correlations in soybeans and their implications in selection. Agron. J. 47: 477-483.
• Kwon, S.H. and Torrie, J.H. (1964). Heritability and interrelationships among traits of two soybean populations. Crop Sci. 4: 196-198.
• Mather, K. and Jinks, J.L. (1982). Biometrical Genetics. 3rd edn. Chapman and Hall, London.
• McKendry, A.L., McVetty, P.B.E. and Voldeng, H.D. (1985). Inheritance of seed protein and seed oil content in early maturing soybean. Can. J. Genet. Citol. 27: 603-607.
• Oliveira, M.F. (1994). Análise e previsăo do potencial genético de um cruzamento de soja usando vários delineamentos em tręs épocas de semeadura. Master's thesis, Universidade Estadual de Londrina.
• Shorter, R. (1972). Influence of genotype and environment on chemical composition of soybean seed (Glycine max (L.) Merrill). Magister Agronomy Scientiae thesis, University of Queensland.
• Shorter, R., Byth, D.E. and Mungomery, V.E. (1976). Estimates of selection parameters associated with protein and oil content of soybean seeds (Glycine max (L.) Merril). Aust. J. Agric. Res. 28: 211-222.
• Teixeira, J.P.F., Ramos, M.T.B., Miranda, M.A.C. and Mascarenhas, H.A.A. (1984). Relaçăo entre os principais constituintes químicos da soja. In: Seminário Nacional de Pesquisa de Soja, 3., Anais EMBRAPA-CNPSo, Londrina, pp. 898-908.
• Toledo, J.F.F. de (1987). Predicting the inbreeding and the outcrossing potential of soybean (Glycine max (L.) Merril) varieties. Rev. Bras. Genet 10: 543-558.
• Toledo, J.F.F., Oliveira, M.F., Tsutida, A.C. and Kiihl, R.A.S. (1993). Genetic analysis of growth of determinate soybean genotypes under three photoperiods. Rev. Bras. Genet. 16: 713-748.
• Weber, C.R. and Moorthy, B.R. (1952). Heritable and nonheritable relationships and variability of oil content and agronomic characteristics in F2 generation of soybean crosses. Agron. J. 44: 202-209.
• Wilcox, J.R. (1989). Soybean protein and oil quality. In: World Soybean Research Conference IV, Proceedings. Associatión Argentina de la Soja, Buenos Aires, pp. 28-39.

¹

Research approved for publication by the Technical Director of Embrapa Soja as manuscript number 005/97.

Publication Dates

• Publication in this collection
  23 Feb 1999
• Date of issue
  Sept 1998

History

• Received
  17 Apr 1997