Skip to main content
Log in

Quantitative trait loci involved in regulating seed oil composition in Arabidopsis thaliana and their evolutionary implications

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Fatty acid composition is an important determinant of seed oil quality. Overall, 72 QTL for 12 fatty acid traits that control seed oil composition were identified in four recombinant inbred line (RIL) populations (Ler-0 × Sha, Ler-0 × Col-4, Ler-2 × Cvi, Ler-0 × No-0) of Arabidopsis thaliana. The identified QTL explained 3.2–79.8% of the phenotypic variance; 33 of the 59 QTL identified in the Ler-0 × Sha and the Ler-0 × Col RIL populations co-located with several a priori candidate genes for seed oil composition. QTL for fatty acids 18:1, 18:2, 22:1, and fatty acids synthesized in plastids was identified in both Ler-0 × Sha and Ler-0 × Col-4 RIL populations, and QTL for 16:0 was identified in the Ler-0 × Sha and Ler-0 × No-0 RIL populations providing strong support for the importance of these QTL in determining seed oil composition. We identified melting point QTL in three RIL populations, and fatty acid QTL collocated with two of them, suggesting that the loci could be under selection for altering the melting point of seed oils to enhance adaptation and could be useful for breeding purposes. Nuclear-cytoplasmic interactions and epistasis were rare. Analysis of the genetic correlations between these loci and other fatty acids indicated that these correlations would tend to strongly enhance selection for desirable fatty acids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alonso-Blanco C, Peeters AJ, Koornneef M, Lister C, Dean C et al (1998) Development of an AFLP based linkage map of Ler, Col and Cvi Arabidopsis thaliana ecotypes and construction of a Ler/Cvi recombinant inbred line population. Plant J 14:259–271

    Article  PubMed  CAS  Google Scholar 

  • Barker GC, Larson TR, Graham IA, Lynn JR, King GJ (2007) Novel insights into seed fatty acid synthesis and modification pathways from genetic diversity and quantitative trait Loci analysis of the Brassica C genome. Plant Physiol 144:1827–1842

    Article  PubMed  CAS  Google Scholar 

  • Baud S, Lepiniec L (2009) Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Biochem 47:448–455

    Article  PubMed  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300

    Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  PubMed  CAS  Google Scholar 

  • Broun P, Gettner S, Somerville C (1999) Genetic engineering of plant lipids. Annu Rev Nutr 19:197–216

    Article  PubMed  CAS  Google Scholar 

  • Browse J, Somerville C (1991) Glycerolipid synthesis: biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42:467–506

    Article  CAS  Google Scholar 

  • Cahoon EB, Lindqvist Y, Schneider G, Shanklin J (1997) Redesign of soluble fatty acid desaturases from plants for altered substrate specificity and double bond position. Proc Natl Acad Sci USA 94:4872–4877

    Article  PubMed  CAS  Google Scholar 

  • Canvin DT (1965) The effect of temperature on the oil content and fatty acid composition of the oils from several oil seed crops. Can J Bot 43:63–69

    Article  CAS  Google Scholar 

  • Capelle V, Remoue C, Moreau L, Reyss A, Mahe A et al (2010) QTLs and candidate genes for desiccation and abscisic acid content in maize kernels. BMC Plant Biology 10:2

    Article  PubMed  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Djemel N, Guedon D, Lechevalier A, Salon C, Miquel M et al (2005) Development and composition of the seeds of nine genotypes of the Medicago truncatula species complex. Plant Physiol Biochem 43:557–566

    Article  PubMed  CAS  Google Scholar 

  • Eckey EW (1954) Vegetable fats and oils. Reinhold, New York

    Google Scholar 

  • El-Lithy ME, Clerkx EJ, Ruys GJ, Koornneef M, Vreugdenhil D (2004) Quantitative trait locus analysis of growth-related traits in a new Arabidopsis recombinant inbred population. Plant Physiol 135:444–458

    Article  PubMed  CAS  Google Scholar 

  • Gurr MI (1980) The biosynthesis of triacylglycerols. In: Stumpf PK, Conn EE (eds) Lipids: structure and function, Vol. 4. The biochemistry of plants: a comprehensive treatise. Academic Press, New York, pp 205–248

    Google Scholar 

  • Harris HC, Mcwilliam JR, Mason WK (1978) Influence of temperature on oil content and composition of sunflower seed. Aust J Agr Res 29:1203–1212

    Article  CAS  Google Scholar 

  • Harwood JL (1980) Plant acyl lipids: structure, distribution, and analysis. In: Stumpf PK, Conn EE (eds) Lipids: structure and function Vol 4 of The biochemistry of plants: a comprehensive treatise. Academic Press, New York, pp 2–55

    Google Scholar 

  • Harwood JL (1996) Recent advances in the biosynthesis of plant fatty acids. Biochim Biophys Acta 1301:7–56

    PubMed  Google Scholar 

  • Hasan M, Friedt W, Pons-Kühnemann J, Freitag NM, Link K, Snowdon RJ (2008) Association of gene-linked SSR markers to seed glucosinolate content in oilseed rape (Brassica napus ssp. napus). Theor Appl Genet 116:1035–1049

    Article  PubMed  CAS  Google Scholar 

  • Hilditch TP (1956) The chemical constitution of natural fats. Chapman and Hall, London

    Google Scholar 

  • Hilditch TP, Williams PN (1964) The chemical constitution of natural fats. Wiley, New York

    Google Scholar 

  • Hobbs DH, Flintham JE, Hills MJ (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol 136:3341–3349

    Article  PubMed  CAS  Google Scholar 

  • Hsia CC, McGinnis W (2003) Evolution of transcription factor function. Curr Opin Genet Dev 13:199–206

    Article  PubMed  CAS  Google Scholar 

  • King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116

    Article  PubMed  CAS  Google Scholar 

  • Korstanje R, Paigen B (2002) From QTL to gene: the harvest begins. Nat Genet 31:235–236

    Article  PubMed  CAS  Google Scholar 

  • Lagercrantz U, Putterill J, Coupland G, Lydiate D (1996) Comparative mapping in Arabidopsis and Brassica, fine-scale genome collinearity and congruence of genes controlling flowering time. Plant J 9:13–20

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    PubMed  CAS  Google Scholar 

  • Linder CR (2000) Adaptive evolution of seed oils in plants: accounting for the biogeographic distribution of saturated and unsaturated fatty acids in seed oils. Am Nat 156:442–458

    Article  Google Scholar 

  • Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750

    Article  CAS  Google Scholar 

  • Lung S, Weselake RJ (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41:1073–1088

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Mackay TF (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339

    Article  PubMed  CAS  Google Scholar 

  • Magliano TM, Botto JF, Godoy AV, Symonds VV, Lloyd AM et al (2005) New Arabidopsis recombinant inbred lines (Landsberg erecta × Nossen) reveal natural variation in phytochrome-mediated responses. Plant Physiol 138:1126–1135

    Article  PubMed  CAS  Google Scholar 

  • Malkin T (1954) The polymorphism of glycerides. In: Holman RT, Lundberg WO, Malkin T (eds) Progress in the chemistry of fats and other lipids. Pergamon, New York, pp 1–50

    Google Scholar 

  • Marsalkiene N, Sliessaravicius A, Karpaviciene B, Dastikaite A (2009) Oil content and fatty acid composition of seeds of some Lithuanian wild crucifer species. Agron Res 7:654–661

    Google Scholar 

  • Mekhedov S, Oskar Martínez de Ilárduya OM, Ohlrogge J (2000) Toward a functional catalog of the plant genome. A survey of genes for lipid biosynthesis. Plant Physiol 122:389–401

    Article  PubMed  CAS  Google Scholar 

  • Metcalfe LD, Wang CN (1981) Rapid preparation of fatty acid methyl esters using organic base-catalyzed transesterification. J Chromatogr Sci 19:530–535

    CAS  Google Scholar 

  • Millar AA, Kunst L (1999) The natural genetic variation of the fatty-acyl composition of seed oils in different ecotypes of Arabidopsis thaliana. Phytochemistry 52:1029–1033

    Article  PubMed  CAS  Google Scholar 

  • O’Neill CM, Gill S, Hobbs D, Morgan C, Bancroft I (2003) Natural variation for seed oil composition in Arabidopsis thaliana. Phytochemistry 64:1077–1090

    Article  PubMed  Google Scholar 

  • Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    Article  PubMed  CAS  Google Scholar 

  • Ohlrogge JB, Jaworski JG (1997) Regulation of fatty acid synthesis. Annu Rev Plant Physiol Plant Mol Biol 48:109–136

    Article  PubMed  CAS  Google Scholar 

  • Pelgas B, Bousquet J, Meirmans PG, Ritland K, Nathalie I (2011) QTL mapping in white spruce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genomics 12:145

    Article  PubMed  Google Scholar 

  • Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216

    Article  PubMed  CAS  Google Scholar 

  • Qiu D, Morgan C, Shi J, Long Y, Liu J, Li R, Zhuang X, Wang Y, Tan X, Dietrich E, Weihmann T, Everett C, Vanstraelen S, Beckett P, Fraser F, Trick M, Barnes S, Wilmer J, Schmidt R, Li J, Li D, Meng J, Bancroft I (2006) A comparative linkage map of oilseed rape and its use for QTL analysis of seed oil and erucic acid content. Theor Appl Genet 114:67–80

    Article  PubMed  CAS  Google Scholar 

  • Sharma N, Anderson M, Kumar A, Zhang Y, Giblin EM et al (2008) Transgenic increases in seed oil content are associated with the differential expression of novel Brassica-specific transcripts. BMC Genomics 9:619

    Article  PubMed  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224:149–157

    PubMed  CAS  Google Scholar 

  • Storey J, Taylor J, Siegmund D (2004) Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. J R Stat Soc Ser B (Stat Methodol) 66:187–205

    Article  Google Scholar 

  • Stumpf PF (1980) Biosynthesis of saturated and unsaturated fatty acids. In: Stumpf PK, Conn EE (eds) Lipids: structure and function, edited by P. K. The biochemistry of plants: a comprehensive treatise, vol 4. Academic Press, New York, pp 177–204

    Google Scholar 

  • Symonds VV, Godoy AV, Alconada T, Botto JF, Juenger TE et al (2005) Mapping quantitative trait loci in multiple populations of Arabidopsis thaliana identifies natural allelic variation for trichome density. Genetics 169:1649–1658

    Article  PubMed  CAS  Google Scholar 

  • Systat software, Inc (2007) Systat 12 Statistics, Systat Inc. San Jose, CA

    Google Scholar 

  • Tonsor SJ, Alonso-Blanco C, Koornneef M (2005) Gene function beyond the single trait: natural variation, gene effects, and evolutionary ecology in Arabidopsis thaliana. Plant Cell Environ 28:2–20

    Article  CAS  Google Scholar 

  • Ungerer MC, Rieseberg LH (2003) Genetic architecture of a selection response in Arabidopsis thaliana. Evolution 57:2531–2539

    PubMed  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)

  • Welch RM, House WA, Beebe S, Cheng Z (2000) Genetic selection for enhanced bioavailable levels of iron in bean (Phaseolus vulgaris L.) seeds. J Agric Food Chem 48:3576–3580

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Thomas E. Juenger for his advice on experiments and comments on this manuscript. We thank Maarten Koornneef and Vaughan Symonds for sharing the mapping information of the Ler-0 × Sha and Ler-0 × No-0 RIL populations. We thank Dr. Samuel Trachsel for his valuable comments on the manuscript. We also thank Anandita Agarwal, Petko Ivanov, Sandra Sipe and Sheila Shapouri for their help with data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anushree Sanyal.

Additional information

Communicated by C. Quiros.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary tables (PDF 211 kb)

Supplementary figures (PDF 469 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sanyal, A., Randal Linder, C. Quantitative trait loci involved in regulating seed oil composition in Arabidopsis thaliana and their evolutionary implications. Theor Appl Genet 124, 723–738 (2012). https://doi.org/10.1007/s00122-011-1742-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-011-1742-1

Keywords

Navigation