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.
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
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
Baud S, Lepiniec L (2009) Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Biochem 47:448–455
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
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
Broun P, Gettner S, Somerville C (1999) Genetic engineering of plant lipids. Annu Rev Nutr 19:197–216
Browse J, Somerville C (1991) Glycerolipid synthesis: biochemistry and regulation. Annu Rev Plant Physiol Plant Mol Biol 42:467–506
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
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
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
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
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
Eckey EW (1954) Vegetable fats and oils. Reinhold, New York
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
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
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
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
Harwood JL (1996) Recent advances in the biosynthesis of plant fatty acids. Biochim Biophys Acta 1301:7–56
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
Hilditch TP (1956) The chemical constitution of natural fats. Chapman and Hall, London
Hilditch TP, Williams PN (1964) The chemical constitution of natural fats. Wiley, New York
Hobbs DH, Flintham JE, Hills MJ (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol 136:3341–3349
Hsia CC, McGinnis W (2003) Evolution of transcription factor function. Curr Opin Genet Dev 13:199–206
King MC, Wilson AC (1975) Evolution at two levels in humans and chimpanzees. Science 188:107–116
Korstanje R, Paigen B (2002) From QTL to gene: the harvest begins. Nat Genet 31:235–236
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
Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
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
Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750
Lung S, Weselake RJ (2006) Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids 41:1073–1088
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, Massachusetts
Mackay TF (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339
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
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
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
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
Metcalfe LD, Wang CN (1981) Rapid preparation of fatty acid methyl esters using organic base-catalyzed transesterification. J Chromatogr Sci 19:530–535
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
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
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Ohlrogge JB, Jaworski JG (1997) Regulation of fatty acid synthesis. Annu Rev Plant Physiol Plant Mol Biol 48:109–136
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
Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216
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
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
Storey JD, Tibshirani R (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224:149–157
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
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
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
Systat software, Inc (2007) Systat 12 Statistics, Systat Inc. San Jose, CA
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
Ungerer MC, Rieseberg LH (2003) Genetic architecture of a selection response in Arabidopsis thaliana. Evolution 57:2531–2539
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
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
Corresponding author
Additional information
Communicated by C. Quiros.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-011-1742-1