Abstract
We used whole genome scan association mapping to identify loci with major effect on oleic acid content in maize kernels. Single nucleotide polymorphism haplotypes at 8,590 loci were tested for association with oleic acid content in 553 maize inbreds. A single locus with major effect on oleic acid was mapped between 380 and 384 cM in the IBM2 neighbors genetic map on chromosome 4 and confirmed in a biparental population. A fatty acid desaturase, fad2, identified ∼2 kb from the associated genetic marker, is the most likely candidate gene responsible for the differences in the phenotype. The fad2 alleles with high- and low-oleic acid content were sequenced and allelic differences in fad2 RNA level in developing embryos was investigated. We propose that a non-conservative amino acid polymorphism near the active site of fad2 contributes to the effect on oleic acid content. This is the first report of the use of a high resolution whole genome scan association mapping where a putative gene responsible for a quantitative trait was identified in plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alrefai R, Berke T, Rocheford T (1995) Quantitative trait locus analysis of fatty acid concentrations in maize. Genome 38:894–901
Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:e60
Broadwater JA, Whittle E, Shanklin J (2002) Desaturation and hydroxylation. Residues 148 and 324 of Arabidopsis fad2, in addition to substrate chain length, exert a major influence in partitioning of catalytic specificity. J Biol Chem 277:15613–15620
Broun P, Shanklin J, Whittle E, Somerville C (1998) Catalytic plasticity of fatty acid modification enzymes underlying chemical diversity of plant lipids. Science 282:1315–1317
Buhr T, Sato S, Ebrahim F, Xing A, Zhou Y, Mathiesen M, Schweiger B, Kinney A, Staswick P (2002) Ribozyme termination of RNA transcripts down-regulate seed fatty acid genes in transgenic soybean. Plant J 30:155–163
Covello PS, Reed DW (1996) Functional expression of the extraplastidial Arabidopsis thaliana oleate desaturase gene (fad2) in Saccharomyces cerevisiae. Plant Physiol 111:223–226
Devlin B, Risch N (1995) A comparison of linkage disequilibrium measures for fine-scale mapping. Genomics 29:311–322
Fernie AR, Tadmor Y, Zamir D (2006) Natural genetic variation for improving crop quality. Curr Opin Plant Biol 9:196–202
Flint-Garcia SA, Thornsberry JM, Buckler ES4 (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374
Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461–485
Hansen M, Kraft T, Ganestam S, Sall T, Nilsson NO (2001) Linkage disequilibrium mapping of the bolting gene in sea beet using AFLP markers. Genet Res 77:61–66
Hauser MT, Harr B, Schlotterer C (2001) Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol Biol Evol 18:1754–1763
Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108
Hobbs DH, Flintham JE, Hills MJ (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol 136:3341–3349
Hu X, Sullivan-Gilbert M, Gupta M, Thompson SA (2006) Mapping of the loci controlling oleic and linolenic acid contents and development of fad2 and fad3 allele-specific markers in canola (Brassica napus L.). Theor Appl Genet 113:497–507
Jadhav A, Katavic V, Marillia E, Michael Giblin E, Barton DL, Kumar A, Sonntag C, Babic V, Keller WA, Taylor DC (2005) Increased levels of erucic acid in Brassica carinata by co-suppression and antisense repression of the endogenous fad2 gene. Metab Eng 7:215–220
Jung M, Ching A, Bhattramakki D, Dolan M, Tingey S, Morgante M, Rafalski A (2004) Linkage disequilibrium and sequence diversity in a 500-kbp region around the adh1 locus in elite maize germplasm. Theor Appl Genet 109:681–689
Kimchi-Sarfaty C, Oh JM, Kim I, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM (2007) A “silent” polymorphism in the MDR1 gene changes substrate specificity. Science 315:525–528
Kinney AJ, Cahoon EB, Hitz WD (2002) Manipulating desaturase activities in transgenic crop plants. Biochem Soc Trans 30:1099–1103
Kynast RG, Riera-Lizarazu O, Vales MI, Okagaki RJ, Maquieira SB, Chen G, Ananiev EV, Odland WE, Russell CD, Stec AO, Livingston SM, Zaia HA, Rines HW, Phillips RL (2001) A complete set of maize individual chromosome additions to the oat genome. Plant Physiol 125:1216–1227
Liu Q, Singh SP, Green AG (2002) High-stearic and high-oleic cottonseed oils produced by hairpin RNA-mediated post-transcriptional gene silencing. Plant Physiol 129:1732–1743
Mayer KM, McCorkle SR, Shanklin J (2005) Linking enzyme sequence to function using conserved property difference locator to identify and annotate positions likely to control specific functionality. BMC Bioinformatics 6:284
McCartney AW, Dyer JM, Dhanoa PK, Kim PK, Andrews DW, McNew JA, Mullen RT (2004) Membrane-bound fatty acid desaturases are inserted co-translationally into the ER and contain different ER retrieval motifs at their carboxy termini. Plant J 37:156–173
Mikkilineni V, Rocheford TR (2003) Sequence variation and genomic organization of fatty acid desaturase-2 (fad2) and fatty acid desaturase-6 (fad6) cDNAs in maize. Theor Appl Genet 106:1326–1332
Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196
Okagaki RJ, Kynast RG, Livingston SM, Russell CD, Rines HW, Phillips RL (2001) Mapping maize sequences to chromosomes using oat-maize chromosome addition materials. Plant Physiol 125:1228–1235
Palaisa KA, Morgante M, Williams M, Rafalski A (2003) Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795–1806
Palaisa K, Morgante M, Tingey S, Rafalski A (2004) Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc Natl Acad Sci USA 101:9885–9890
Patel M, Jung S, Moore K, Powell G, Ainsworth C, Abbott A (2004) High-oleate peanut mutants result from a mite insertion into the fad2 gene. Theor Appl Genet 108:1492–1502
Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical recipes in C, 2nd edn. Cambridge University Press, Cambridge, 336p
Pritchard JK, Stephens M, et al (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES4 (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Rostoks N, Ramsay L, Mackenzie K, Cardle L, Bhat P, Roose M, Svensson J, Stein N, Varshney R, Marshall D, Graner A, Close T, Waugh R (2006) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc Natl Acad Sci USA 103:18656–18661
Stoutjesdijk PA, Hurlestone C, Singh SP, Green AG (2000) High-oleic acid Australian Brassica napus and B. juncea varieties produced by co-suppression of endogenous delta12-desaturases. Biochem Soc Trans 28:938–940
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES4 (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Weigel D, Nordborg M (2005) Natural variation in Arabidopsis. How do we find the causal genes? Plant Physiol 138:567–568
Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES4 (2002) Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 99:12959–12962
Wilson LM, Whitt SR, Ibanez AM, Rocheford TR, Goodman MM, Buckler ES4 (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719–2733
Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Waugh.
Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession number EF687907.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Beló, A., Zheng, P., Luck, S. et al. Whole genome scan detects an allelic variant of fad2 associated with increased oleic acid levels in maize. Mol Genet Genomics 279, 1–10 (2008). https://doi.org/10.1007/s00438-007-0289-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-007-0289-y