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Theoretical and Applied Genetics

, Volume 127, Issue 1, pp 97–111 | Cite as

Mapping the low palmitate fap1 mutation and validation of its effects in soybean oil and agronomic traits in three soybean populations

  • Andrea J. CardinalEmail author
  • Rebecca Whetten
  • Sanbao Wang
  • Jérôme Auclair
  • David Hyten
  • Perry Cregan
  • Eleni Bachlava
  • Jason Gillman
  • Martha Ramirez
  • Ralph Dewey
  • Greg Upchurch
  • Lilian Miranda
  • Joseph W. Burton
Original Paper

Abstract

Key message

fap 1 mutation is caused by a G174A change in GmKASIIIA that disrupts a donor splice site recognition and creates a GATCTG motif that enhanced its expression.

Abstract

Soybean oil with reduced palmitic acid content is desirable to reduce the health risks associated with consumption of this fatty acid. The objectives of this study were: to identify the genomic location of the reduced palmitate fap1 mutation, determine its molecular basis, estimate the amount of phenotypic variation in fatty acid composition explained by this locus, determine if there are epistatic interactions between the fap1 and fap nc loci and, determine if the fap1 mutation has pleiotropic effects on seed yield, oil and protein content in three soybean populations. This study detected two major QTL for 16:0 content located in chromosome 5 (GmFATB1a, fap nc) and chromosome 9 near BARCSOYSSR_09_1707 that explained, with their interaction, 66–94 % of the variation in 16:0 content in the three populations. Sequencing results of a putative candidate gene, GmKASIIIA, revealed a single unique polymorphism in the germplasm line C1726, which was predicted to disrupt the donor splice site recognition between exon one and intron one and produce a truncated KASIIIA protein. This G to A change also created the GATCTG motif that enhanced gene expression of the mutated GmKASIIIA gene. Lines homozygous for the GmKASIIIA mutation (fap1) had a significant reduction in 16:0, 18:0, and oil content; and an increase in unsaturated fatty acids content. There were significant epistatic interactions between GmKASIIIA (fap1) and fap nc for 16:0 and oil contents, and seed yield in two populations. In conclusion, the fap1 phenotype is caused by a single unique SNP in the GmKASIIIA gene.

Keywords

Simple Sequence Repeat Marker Agronomic Trait Segregation Distortion Maturity Group Palmitic Acid Content 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

16:0

Palmitic acid

18:0

Stearic acid

18:1

Oleic acid

18:2

Linoleic acid

18:3

Linolenic acid

BLUP

Best linear unbiased predictor

DAP

Days after planting

FATB

16:0-ACP thioesterase

KASIII

3-Ketoacyl-ACP synthase enzyme III

R2

Flowering date

R8

Maturity date

Notes

Acknowledgments

The authors would like to thank William Novitzky at the USDA-ARS Soybean and Nitrogen Fixation Research Unit, Raleigh, NC, for providing training and equipment for the fatty acid analysis; James B. Holland for providing technical expertise in QTL analysis and discussion of results; Martha Ramirez for isolating RNA; and Carol Griffin for performing Northern analysis. This project was funded by the United Soybean Board (Grant # 59-.6645-2-071).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Standards

The experiments performed for this publication comply with the current laws of the United States of America.

Supplementary material

122_2013_2204_MOESM1_ESM.xlsx (55 kb)
Supplementary material 1 (XLSX 54 kb)

References

  1. Aguilar F, Montandon PE, Stutz E (1991) Two genes encoding the soybean translation elongation factor eEF-1 alpha are transcribed in seedling leaves. Plant Mol Biol 17:351–360PubMedCrossRefGoogle Scholar
  2. Bachlava E, Dewey RE, Auclair J, Wang S, Burton JW, Cardinal AJ (2008a) Mapping genes encoding microsomal ω-6 desaturase enzymes and their cosegregation with QTL affecting oleate content in soybean. Crop Sci 48:640–650CrossRefGoogle Scholar
  3. Bachlava E, Burton JW, Brownie C, Wang S, Auclair J, Cardinal AJ (2008b) Heritability of oleic acid content in soybean seed oil and its genetic correlation with fatty acid and agronomic traits. Crop Sci 48:1764–1772CrossRefGoogle Scholar
  4. Bachlava E, Dewey RE, Burton JW, Cardinal AJ (2009a) Mapping candidate genes for oleate biosynthesis and their association with unsaturated fatty acid seed content in soybean. Mol Breed 23:337–347CrossRefGoogle Scholar
  5. Bachlava E, Dewey RE, Burton JW, Cardinal AJ (2009b) Mapping and comparison of Quantitative Trait Loci for oleic acid seed content in two segregating soybean populations. Crop Sci 49:1–10CrossRefGoogle Scholar
  6. Brim CA (1966) A modified pedigree method of selection in soybean. Crop Sci 6:220CrossRefGoogle Scholar
  7. Burkey KO, Booker FL, Pursley WA, Heagle AS (2007) Elevated carbon dioxide and ozone effects on peanut: II. Seed yield and quality. Crop Sci 47:1488–1497CrossRefGoogle Scholar
  8. Burton JW, Wilson RF, Brim CA (1983) Recurrent selection in soybean: IV. Selection for increased oleic acid percentage in seed oil. Crop Sci 23:744–747CrossRefGoogle Scholar
  9. Burton JW, Carter TE, Huie EB (1994a) Registration of ‘Brim’ soybean. Crop Sci 34:301CrossRefGoogle Scholar
  10. Burton JW, Wilson RF, Brim CA (1994b) Registration of N79-2077-12 and N87-2122-4, two soybean germplasm lines with reduced palmitic acid in seed oil. Crop Sci 34:313Google Scholar
  11. Burton JW, Wilson RF, Rebetzke GJ, Pantalone VR (2006) Registration of N98-4445A mid-oleic soybean germplasm line. Crop Sci 46:1010–1012CrossRefGoogle Scholar
  12. Cardinal AJ, Lee M, Sharopova N, Woodman-Clikeman WL, Long MJ (2001) Genetic mapping and analysis of quantitative trait loci for resistance to stalk tunneling by the European corn borer in maize. Crop Sci 41:835–845CrossRefGoogle Scholar
  13. Cardinal AJ, Burton JW, Camacho-Roger AM, Yang JH, Wilson RF, Dewey RE (2007) Molecular analysis of soybean lines with low palmitic acid content in the seed oil. Crop Sci 47:304–310CrossRefGoogle Scholar
  14. Cardinal AJ, Dewey RE, Burton JW (2008) Estimating the individual effects of the reduced palmitic acid alleles fap nc and fap1 alleles on agronomic traits in two soybean populations. Crop Sci 48:633–639CrossRefGoogle Scholar
  15. Cardinal AJ, Burton JW, Camacho-Roger A, Whetten R, Chappell AS, Bilyeu KD, Auclair J, Dewey RE (2011) Molecular analysis of GmFAD3A in two soybean populations segregating for the fan, fap1, and fap nc loci. Crop Sci 51:2104–2112CrossRefGoogle Scholar
  16. Cherrak CM, Pantalone VR, Meyer EJ, Ellis DL, Melton SL, West DR, Mount JR (2003) Low-palmitic, low-linolenic soybean development. J Am Oil Chem Soc 80:539–543CrossRefGoogle Scholar
  17. Cooper M, DeLacy IH (1994) Relationships among analytical methods used to study genotypic variation and genotype-by-environment interaction in plant breeding multi-environment experiments. Theor Appl Genet 88:561–572PubMedCrossRefGoogle Scholar
  18. Cregan PB, Jarvik T, Bush AL, Shoemaker RC, Lark KG, Kahler AL, Kaya N, VanToai TT, Lohnes DG, Chung L, Specht JE (1999) An integrated genetic linkage map of the soybean genome. Crop Sci 39:1464–1490CrossRefGoogle Scholar
  19. Fehr WR, Caviness CE (1977) Stages of soybean development. Special Report. Agriculture and Home Economics Experiment Station. Iowa State University 80:11Google Scholar
  20. Fehr WR, Welke GA, Hammond EG, Duvick DN, Cianzio SR (1991) Inheritance of reduced palmitic acid content in seed oil of soybean. Crop Sci 31:88–89CrossRefGoogle Scholar
  21. Hallauer AR, Miranda JB (1988) Quantitative genetics in maize breeding, 2nd edn. Iowa State University Press, AmesGoogle Scholar
  22. Hebsgaard SM, Korning PG, Tolstrup N, Engelbrecht J, Rouzé P, Brunak S (1996) Splice site prediction in Arabidopsis thaliana Pre-mRNA by combining local and global sequence information. Nucleic Acids Res 24:3439–3452PubMedCentralPubMedCrossRefGoogle Scholar
  23. Henderson MM (1991) Correlations between fatty acid intake and cancer incidence. In: Nelson GJ (ed) Health effects of dietary fatty acids. American Oil Chemists’ Society, Champaign, pp 136–149Google Scholar
  24. Horejsi TF, Fehr WR, Welke GA, Duvick DN, Hammond EG, Cianzio SR (1994) Genetic control of reduced palmitate content in soybean. Crop Sci 34:331–334. doi: 10.2135/cropsci1994.0011183X003400020003x CrossRefGoogle Scholar
  25. Hu FB, Stampfer MJ, Manson JE, Rimm E, Colditz GA, Rosner BA, Hennekens CH, Willett WC (1997) Dietary fat intake and the risk of coronary heart disease in women. N Engl J Med 337:1491–1499PubMedCrossRefGoogle Scholar
  26. Hyten DL, Choi IY, Song Q, Specht JE, Carter TE, Shoemaker RC, Hwang EY, Matukumalli LK, Cregan PB (2010) A high density integrated genetic linkage map of soybean and the development of a 1,536 Universal Soy Linkage Panel for QTL mapping. Crop Sci 50:960–968. doi: 10.2135/cropsci2009.06.0360 CrossRefGoogle Scholar
  27. Kenworthy WJ (1996) Registration of ‘Corsica” soybean. Crop Sci 36:1078CrossRefGoogle Scholar
  28. Kinoshita T, Rahman SM, Anai T, Takagi Y (1998) Inter-locus relationship between genes controlling palmitic acid contents in soybean mutants. Breed Sci 48:377–381Google Scholar
  29. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln ES, Newburg L (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  30. Li Z, Wilson RF, Rayford WE, Boerma HR (2002) Molecular mapping genes conditioning reduced palmitic acid content in N87-2122-4 soybean. Crop Sci 42(2):373–378CrossRefGoogle Scholar
  31. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS® system for mixed models. SAS Institute Inc, CaryGoogle Scholar
  32. Long M, Deutsch M (1999) Association of intron phases with conservation at splice site sequences and evolution of spliceosomal introns. Mol Biol Evol 16:1528–1534PubMedCrossRefGoogle Scholar
  33. Lorieux M, Perrier X, Goffinet B, Lanaud C, González de León D (1995) Maximum-likelihood models for mapping genetic markers showing segregation distortion. 2. F2 populations. Theor Appl Genet 90:81–89PubMedGoogle Scholar
  34. Moniz de Sa M, Drouin G (1996) Phylogeny and substitution rates of angiosperm actin genes. Mol Biol Evol 13:1198–1212PubMedCrossRefGoogle Scholar
  35. Ndzana X, Fehr WR, Welke GA, Hammond EG, Duvick DN, Cianzio SR (1994) Influence of reduced palmitate content on agronomic and seed traits of soybean. Crop Sci 34:646–649CrossRefGoogle Scholar
  36. Nickell AD, Wilcox JR, Cavins JF (1991) Genetic relationships between loci controlling palmitic and linolenic acids in soybean. Crop Sci 31:1169–1171CrossRefGoogle Scholar
  37. Primomo VS (2000) Inheritance and stability of palmitic acid alleles in soybeans (Glycine max L Merr.). MS Thesis, Department of Plant Agriculture, University of Guelph, Guelph, Ontario, CanadaGoogle Scholar
  38. Primomo VS, Falk DE, Ablett GR, Tanner JW, Rajcan I (2002) Inheritance and interaction of low palmitic and low linolenic soybean. Crop Sci 42:31–36PubMedCrossRefGoogle Scholar
  39. Rahman SM, Kinoshita T, Anai T, Takagi Y (1996) Genetic analysis of palmitic acid content using two soybean mutants. Breed Sci 46:343–347Google Scholar
  40. Rebetzke GJ, Burton JW, Carter TE, Wilson RF (1998a) Changes in agronomic and seed characteristics with selection for reduced palmitic acid content in soybean. Crop Sci 38:297–302CrossRefGoogle Scholar
  41. Rebetzke GJ, Burton JW, Carter TE, Wilson RF (1998b) Genetic variation for modifiers controlling reduced saturated fatty acid content in soybean. Crop Sci 38:303–308CrossRefGoogle Scholar
  42. Rebetzke GJ, Pantalone VR, Burton JW, Carter TE, Wilson RF (2001) Genetic background and environmental influence palmitate content of soybean seed oil. Crop Sci 41:1731–1736CrossRefGoogle Scholar
  43. Rose AB, Elfersi T, Parra G, Korfa I (2008) Promoter-proximal introns in Arabidopsis thaliana are enriched in dispersed signals that elevate gene expression. Plant Cell 20:543–551PubMedCentralPubMedCrossRefGoogle Scholar
  44. Sambrook J, Russell DW (2001) Molecular cloning, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  45. SAS Institute (2010) SAS/STAT software. Release 9.2. SAS Institute, CaryGoogle Scholar
  46. SAS Institute Inc (2004) SAS/STAT software: release 9.1. SAS Institute Inc, CaryGoogle Scholar
  47. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  48. Schnebly SR, Fehr WR, Welke GA, Hammond EG, Duvick DN (1994) Inheritance of reduced and elevated palmitate in mutant lines of soybean. Crop Sci 34:829–833CrossRefGoogle Scholar
  49. Song QJ, Marek LF, Shoemaker RC, Lark KG, Concibido VC, Delanay X, Specht JE, Cregan PB (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128PubMedCrossRefGoogle Scholar
  50. Song Q, Gaofeng J, Zhu Y, Grant D, Nelson R, Hwang EY, Hyten DL, Cregan PB (2010) Abundance of SSR motifs and development of candidate polymorphic SSR markers (BARCSOYSSR-1.0) in soybean. Crop Sci 50:1950–1960CrossRefGoogle Scholar
  51. Stojšin D, Ablett GR, Luzzi BM, Tanner JW (1998) Use of gene substitution values to quantify partial dominance in low palmitic acid soybean. Crop Sci 38:1437–1441CrossRefGoogle Scholar
  52. Vandesompele JK, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–12. doi: 10.1186/gb-2002-3-7-research0034 CrossRefGoogle Scholar
  53. Vries BD, Fehr WR, Welke GA, Dewey RE (2011) Molecular characterization of the mutant fap3(A22) allele for reduced palmitate concentration in soybean. Crop Sci 51:1611–1616CrossRefGoogle Scholar
  54. Wilcox RF, Cavins JF (1990) Registration of C1726 and C1727 soybean germplasm with altered levels of palmitic acid in seed oil of soybean. Crop Sci 30:240CrossRefGoogle Scholar
  55. Wilcox JR, Athow KL, Abney TS, Laviolette FA, Richards TL (1980) Registration of century soybean1 (Reg. No. 135). Crop Sci 20:415. doi: 10.2135/cropsci1980.0011183X002000030043x CrossRefGoogle Scholar
  56. Wilcox JR, Burton JW, Rebetzke GJ, Wilson RF (1994) Transgressive segregation for palmitic acid in seed oil of soybean. Crop Sci 34:1248–1250CrossRefGoogle Scholar
  57. Wilson RF, Burton JW, Novitzky WP, Dewey RE (2001a) Current and future innovations in soybean (Glycine max L. Merr.) oil composition. J Oleo Sci 50:353–358CrossRefGoogle Scholar
  58. Wilson RF, Marquardt TC, Novitzky WP, Burton JW, Wilcox JR, Kinney AJ, Dewey RE (2001b) Metabolic mechanisms associated with alleles governing the 16:0 concentration of soybean oil. J Am Oil Chem Soc 78:335–340CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Andrea J. Cardinal
    • 1
    Email author
  • Rebecca Whetten
    • 1
  • Sanbao Wang
    • 1
  • Jérôme Auclair
    • 2
  • David Hyten
    • 3
    • 4
  • Perry Cregan
    • 3
  • Eleni Bachlava
    • 5
  • Jason Gillman
    • 6
  • Martha Ramirez
    • 7
  • Ralph Dewey
    • 1
  • Greg Upchurch
    • 7
  • Lilian Miranda
    • 7
  • Joseph W. Burton
    • 7
  1. 1.Department of Crop ScienceNorth Carolina State UniversityRaleighUSA
  2. 2.La Coop fédéréeMontrealCanada
  3. 3.Soybean Genomics and Improvement LaboratoryU.S. Department of Agriculture, Agricultural Research ServiceBeltsvilleUSA
  4. 4.DuPont PioneerJohnstonUSA
  5. 5.Monsanto Vegetable SeedsWoodlandUSA
  6. 6.Plant Genetics Research UnitUSDA-ARS, University of MissouriColumbiaUSA
  7. 7.Soybean and Nitrogen Fixation Research UnitUSDA-ARSRaleighUSA

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