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Natural variations in stearoyl-acp desaturase genes affect the conversion of stearic to oleic acid in maize kernel

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We identified 11 SAD genes, and mined their natural variations associated with the conservation of stearic to oleic acid, especially ZmSAD1 supported by both the QTL and an expression QTL.

Abstract

Maize oil is generally regarded as a healthy vegetable oil owing to its low abundance of saturated fatty acids. Stearoyl-ACP desaturase (SAD) is a key rate-limiting enzyme for the conservation of stearic (C18:0) to oleic (C18:1) acid. Here, 11 maize SAD genes were identified to have more divergent functions than Arabidopsis SAD genes. The genomic regional associations in a maize panel including 508 inbred lines identified 6 SAD genes significantly associated (P < 0.01) with the C18:0/C18:1 ratio or the level of C18:0 or C18:1, one gene of which co-localized with a quantitative trait locus (QTL) and 5 of which co-localized with an expression QTL. ZmSAD1, supported by both the QTL and an expression QTL, had the largest effect on C18:0/C18:1. One nonsynonymous single-nucleotide polymorphism in exon 3 and one 5-bp insertion/deletion in the 3′ untranslated region were further shown to contribute to the natural variation in C18:0/C18:1 according to ZmSAD1-based association mapping. Finally, selection tests of ZmSAD1 in teosinte, regular maize, and high-oil maize indicated that ZmSAD1 was not a selection target during the process of maize domestication and high-oil maize development. These results will guide the manipulation of the ratio between saturated and unsaturated fatty acids in maize.

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References

  • Alrefai R, Berke TG, Rocheford TR (1995) Quantitative trait locus analysis of fatty acid concentrations in maize. Genome 38:894–901

    Article  CAS  PubMed  Google Scholar 

  • Beló A, Zheng P, Luck S, Shen B, Meyer DJ, Li B, Tingey S, Rafalski A (2008) Whole genome scan detects an allelic variant of fad2 associated with increased oleic acid levels in maize. Mol Genet Genomics 279:1–10

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Chai YC, Hao XM, Yang XH, Allen WB, Li JM, Yan JB, Shen B, Li JS (2012) Validation of DGAT1-2 polymorphisms associated with oil content and development of functional markers for molecular breeding of high-oil maize. Mol Breed 29:939–949

    Article  CAS  Google Scholar 

  • Chen J, Zeng B, Zhang M, Xie SJ, Wang GK, Hauck A, Lai JS (2014) Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol 166:252–264

    Article  PubMed  PubMed Central  Google Scholar 

  • Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doebley J, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du HW, Yang XH, Yan JB, Li JS (2011) Fatty acid elongase 1 (FAE1) promoter as a candidate for genetic engineering of fatty acids to improve seed oil composition. Afr J Biotechnol 10:19615–19622

    Article  CAS  Google Scholar 

  • Edgar RC (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC bioinform 5:113

    Article  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu JJ, Cheng YB, Linghu JJ, Yang XH, Kang L, Zhang ZX, Zhang J, He C, Du XM, Peng ZY, Wang B, Zhai LH, Dai CM, Xu JB, Wang WD, Li XR, Zheng J, Chen L, Luo LH, Liu JJ, Qian XJ, Yan JB, Wang J, Wang GY (2013) RNA sequencing reveals the complex regulatory network in the maize kernel. Nat Commun 4:2832

    PubMed  Google Scholar 

  • Ganal MW, Durstewitz G, Polley A, Bérard A, Buckler ES, Charcosset A, Clarke JD, Graner EM, Hansen M, Joets J, Le Paslier MC, McMullen MD, Montalent P, Rose M, Schon CC, Sun Q, Walter H, Martin OC, Falque M (2011) A large maize (Zea mays L) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One 6:e28334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hudson RR, Kreitman M, Aguadé M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hufford MB, Xu X, van Heerwaarden J, Pyhäjärvi T, Chia JM, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, Lai JS, Morrell PL, Shannon LM, Song C, Springer NM, Swanson-Wagner RA, Tiffin P, Wang J, Zhang GY, Doebley J, McMullen MD, Ware D, Buckler ES, Yang S, Ross-Ibarra J (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 44:808–811

    Article  CAS  PubMed  Google Scholar 

  • Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P (2007) The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol 63:257–271

    Article  CAS  PubMed  Google Scholar 

  • Knutzon DS, Scherer DE, Schreckengost WE (1991) Nucleotide sequence of a complementary DNA clone encoding stearoyl-acyl carrier protein desaturase from castor bean, Ricinus communis. Plant Physiol 96:344–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lambert RJ (2001) High-oil corn hybrids. In: Hallau AR (ed) Special corn. CRC Press Inc, Boca Raton, pp 131–153

  • Li L, Li H, Li Q, Yang XH, Zheng DB, Warburton M, Chai YC, Zhang P, Guo YQ, Yan JB, Li JS (2011) An 11-bp insertion in Zea mays fatb reduces the palmitic acid content of fatty acids in maize grain. PLoS One 6:e24699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Yang XH, Xu ST, Cai Y, Zhang DL, Han YJ, Li L, Zhang ZX, Gao SB, Li JS, Yan JB (2012) Genome-wide association studies identified three independent polymorphisms associated with α-tocopherol content in maize kernels. PLoS One 7:e36807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Peng ZY, Yang XH, Wang WD, Fu JJ, Wang JH, Han YJ, Chai YC, Guo TT, Yang N, Liu J, Warburton ML, Cheng YB, Hao XM, Zhang P, Zhao JY, Liu YJ, Wang GY, Li JS, Yan JB (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–50

    Article  CAS  PubMed  Google Scholar 

  • Li F, Bian CS, Xu JF, Pang WF, Liu J, Duan SG, Lei ZG, Jiwan P, Jin LP (2015) Cloning and functional characterization of SAD genes in potato. PLoS One 10:e0122036

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu ZJ, Yang XH, Fu Y (2009a) SAD, a stearoyl-acyl carrier protein desaturase highly expressed in high-oil maize inbred lines. Russ J Plant Physiol 56:709–715

    Article  Google Scholar 

  • Liu ZJ, Yang XH, Fu Y, Zhang YR, Yan JB, Song TM, Rocheford T, Li JS (2009b) Proteomic analysis of early germs with high-oil and normal inbred lines in maize. Mol Biol Rep 36:813–821

    Article  CAS  PubMed  Google Scholar 

  • Liu HJ, Luo X, Niu LY, Xiao YJ, Chen L, Liu J, Wang XQ, Jin ML, Li WQ, Zhang QH, Yan JB (2016) Distant eQTLs and non-coding sequences play critical roles in regulating gene expression and quantitative trait variation in maize. Mol Plant. doi:10.1016/j.molp.2016.06.016

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López Alonso D, García-Maroto F, Rodríguez-Ruiz J, Garrido JA, Vilches MA (2003) Evolution of the membrane-bound fatty acid desaturases. Biochem Syst Ecol 31:1111–1124

    Article  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci 99:6080–6084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merlo AO, Cowen N, Delate T, Edington B, Folkerts O, Hopkins N, Lemeiux C, Skokut T, Smith K, Woosley A, Yang YJ, Young S, Zwick M (1998) Ribozymes targeted to stearoyl-ACP Δ9 desaturase mRNA produce heritable increases of stearic acid in transgenic maize leaves. Plant Cell 10:1603–1621

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R (2009) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci 106:5019–5024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramsden CE, Zamora D, Leelarthaepin B, Majchrzak-Hong SF, Faurot KR, Suchindran CM, Ringel A, Davis JM, Hibbeln JR (2013) Use of dietary linoleic acid for secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet Heart Study and updated meta-analysis. BMJ 346:e8707

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruddle P II, Whetten R, Cardinal A, Upchurch RG, Miranda L (2014) Effect of Δ9-stearoyl -ACP-desaturase-C mutants in a high oleic background on soybean seed oil composition. Theor Appl Genet 127:349–358

    Article  CAS  PubMed  Google Scholar 

  • Shanklin J, Mullins C, Somerville C (1991) Sequence of a complementary DNA from Cucumis sativus L encoding the stearoyl-acyl-carrier protein desaturase. Plant Physiol 97:467–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shilman F, Brand Y, Brand A, Hedvat I, Hovav R (2011) Identification and molecular characterization of homeologous Δ9-stearoyl acyl carrier protein desaturase 3 genes from the allotetraploid peanut (Arachis hypogaea). Plant Mol Biol Rep 29:232–241

    Article  CAS  Google Scholar 

  • Somerville C, Browse J, Jaworski JG, Ohlrogge JB (2000) Lipids. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologist, Rockville, pp 456–526

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 60. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225

    Article  CAS  PubMed  Google Scholar 

  • Thambugala D, Cloutier S (2014) Fatty acid composition and desaturase gene expression in flax (Linum usitatissimum L). J Appl Genet 55:423–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson GA, Scherer DE, Foxall-Van Aken S, Kenny JW, Young HL, Shintani DK, Kridl JC, Knauf VC (1991) Primary structures of the precursor and mature forms of stearoyl-acyl carrier protein desaturase from safflower embryos and requirement of ferredoxin for enzyme activity. Proc Natl Acad Sci 88:2578–2582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM, Gonzalez S, de Jesus J, Ross-Ibarra J (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proc Natl Acad Sci 108:1088–1092

    Article  PubMed  Google Scholar 

  • Wang H, Nussbaum-Wagler T, Li BL, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wassom JJ, Mikkelineni V, Bohn MO, Rocheford TR (2008) QTL for fatty acid composition of maize kernel oil in Illinois high oil × B73 backcross-derived lines. Crop Sci 48:69–78

    Article  CAS  Google Scholar 

  • Weber EJ (1987) Lipids of the kernel. In: Watson SA, Ramstad PE (eds) Corn: chemistry and technology. American Association of Ceral Chemists St Paul, Minn, pp 311–349

    Google Scholar 

  • Yang XH, Guo YQ, Yan JB, Zhang J, Song TM, Rocheford T, Li JS (2010a) Major and minor QTL and epistasis contribute to fatty acid compositions and oil concentration in high-oil maize. Theor Appl Genet 120:665–678

    Article  CAS  PubMed  Google Scholar 

  • Yang XH, Yan JB, Shah T, Warburton ML, Li Q, Li L, Gao YF, Chai YC, Fu ZY, Zhou Y, Xu ST, Bai GH, Meng YJ, Zheng YP, Li JS (2010b) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431

    Article  PubMed  Google Scholar 

  • Yang XH, Gao SB, Xu ST, Zhang ZX, Prasanna BM, Li L, Li JS, Yan JB (2011) Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breed 28:511–526

    Article  Google Scholar 

  • Yang N, Lu YL, Yang XH, Huang J, Zhou Y, Ali F, Wen WW, Liu J, Li JS, Yan JB (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10:e1004573

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu JM, Pressoir G, Briggs WH, Vroh Bi I, 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang YF, Maximova SN, Guiltinan MJ (2015) Characterization of a stearoyl-acyl carrier protein desaturase gene family from chocolate tree, Theobroma cacao L. Front Plant Sci 6:239

    PubMed  PubMed Central  Google Scholar 

  • Zheng PZ, Allen WB, Roesler K, Williams ME, Zhang SR, Li JM, Glassman K, Ranch J, Nubel D, Solawetz W, Bhattramakki D, Llaca V, Deschamps S, Zhong GY, Tarczynski MC, Shen B (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40:367–372

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We greatly appreciate Dr. Jianbing Yan and Mr. Haijun Liu for providing the genotyping-by-sequencing data for the maize association panel. We also appreciate the helpful comments on the manuscript from three anonymous reviewers. This research was supported by the National Natural Science Foundation of China (Grant Number 31361140362) and the Program for New Century Excellent Talents in University of the Ministry of Education of China (Grant Number 2014FG049).

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Authors and Affiliations

  1. Beijing Key Laboratory of Crop Genetic Improvement, National Maize Improvement Center of China, China Agricultural University, Beijing, 100193, China

    Yingjia Han, Gen Xu, Jieyun Hu, Jiansheng Li & Xiaohong Yang

  2. College of Life Science, Yangtze University, Jingzhou, 434025, Hubei, China

    Hewei Du

  3. Shandong Cotton Research Center, Shandong Academy of Agricutural Sciences, Jinan, 250100, China

    Zhanji Liu

  4. School of Biological Science and Technology, University of Jinan, Jinan, 250022, Shandong, China

    Hui Li

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  1. Yingjia Han
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  2. Gen Xu
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Correspondence to Xiaohong Yang.

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Communicated by A. A. Franco Garcia.

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Han, Y., Xu, G., Du, H. et al. Natural variations in stearoyl-acp desaturase genes affect the conversion of stearic to oleic acid in maize kernel. Theor Appl Genet 130, 151–161 (2017). https://doi.org/10.1007/s00122-016-2800-5

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