Abstract
High-oil maize is a useful genetic resource for genomic investigation in plants. To determine the genetic basis of oil concentration and composition in maize grain, a recombinant inbred population derived from a cross between normal line B73 and high-oil line By804 was phenotyped using gas chromatography, and genotyped with 228 molecular markers. A total of 42 individual QTL, associated with fatty acid compositions and oil concentration, were detected in 21 genomic regions. Five major QTL were identified for measured traits, one each of which explained 42.0% of phenotypic variance for palmitic acid, 15.0% for stearic acid, 27.7% for oleic acid, 48.3% for linoleic acid, and 15.7% for oil concentration in the RIL population. Thirty-six loci were involved in 24 molecular marker pairs of epistatic interactions across all traits, which explained phenotypic variances ranging from 0.4 to 6.1%. Seven of 18 mapping candidate genes related to lipid metabolism were localized within or were close to identified individual QTL, explaining 0.7–13.2% of the population variance. These results demonstrated that a few major QTL with large additive effects could play an important role in attending fatty acid compositions and increasing oil concentration in used germplasm. A larger number of minor QTL and a certain number of epistatic QTL, both with additive effects, also contributed to fatty acid compositions and oil concentration.
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References
Alrefai R, Berke TG, Rocheford TR (1995) Quantitative trait locus analysis of fatty acid concentration in maize. Genome 38:894–901
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Barton NH, Keightley PD (2002) Understanding quantitative genetic variation. Nat Rev 3:11–21
Beisson F, Koo AJK, Ruuska S, Schwender J, Pollard M, Thelen JJ, Paddock T, Salas JJ, Savage L, Milcamps A, Mhaske VB, Cho Y, Ohlrogge JB (2003) Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol 132:681–697
Benitez JA, Gernat AG, Murillo JG, Araba M (1999) The use of high oil corn in broiler diets. Poult Sci 78:861–865
Berberich T, Harada M, Sugawara K, Kodama H, Iba K, Kusano T (1998) Two maize genes encoding ω-3 fatty acid desaturase and their differential expression to temperature. Plant Mol Biol 36:297–306
Berke T, Rocheford TR (1995) Quantitative trait loci for flowering, plant and ear height, and kernel traits in maize. Crop Sci 35:1542–1549
Bhattramakki D, Dolan M, Hanafey M, Wineland R, Vaske D, Register JC III, Tingey SV, Rafalski A (2002) Insertion-deletion polymorphisms in 3′ regions of maize genes occur frequently and can be used as highly informative genetic markers. Plant Mol Biol 48:539–547
Borevitz JO, Maloof JN, Lutes J, Dabi T, Redfern JL, Trainer GT, Werner JD, Asami T, Berry CC, Weigel D, Chory J (2002) Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana. Genetics 160:683–696
Carlborg O, Haley CS (2004) Epistasis: too often neglected in complex trait studies. Nat Rev Genet 5:618–625
Champoux MC, Wang G, Sarkarung S, Mackill DJ, O’Toole JC, Huang N, McCouch SR (1995) Locating genes associated with root morphology and drought avoidance in rice via linkage to molecular markers. Theor Appl Genet 90:969–981
Chase K, Adler FR, Lark KG (1997) Epistat: A computer program for identifying and testing interactions between pairs of quantitative trait loci. Theor Appl Genet 94:724–730
Clark D, Dudley JW, Rocheford TR, Ledeaux JR (2006) Genetic analysis of corn kernel chemical composition in the random mated 10 generation of the cross of generation 70 of IHO × ILO. Crop Sci 46:807–819
Clarke KR, Gorley RN (2001) PRIMER v5: user manual/tutorial. Plymouth: PRIMER-E Ltd., 91
Doebley J, Stec A (1993) Inheritance of the morphological differences between maize and teosinte: comparison of results for two F2 populations. Genetics 134:559–570
Doebley J, Stec A, Wendel J, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc Natl Acad Sci USA 87:9888–9892
Doebley J, Stec A, Gustus C (1995) Teosinte branched 1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346
Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294
Dudley JW (1977) Seventy-six generation of selection for oil and protein percentage in maize. In: Pollak E (ed) Proceedings of international conference on quantitative genetics. Iowa State University Press, Ames, pp 459–473
Dudley JW (2008) Epistatic interactions in crosses of Illinois High Oil × Illinois Low Oil and of Illinois High Protein × Illinois Low Protein corn strains. Crop Sci 48:59–68
Dudley JW, Lambert RJ (1992) Ninety generations of selection for oil and protein in maize. Maydica 37:81–87
Dudley JW, Lambert RJ (2004) 100 generations of selection for oil and protein in corn. Plant Breed Rev 24:79–110
Egli MA, Lutz SM, Somers DA, Gengenbach BG (1995) A maize acetyl-coenzyme a carboxylase cDNA sequence. Plant Physiol 108:1299–1300
Falque M, Décousset L, Dervins D, Jacob AM, Joets J, Martinant JP, Raffoux X, Ribière N, Ridel C, Samson D, Charcosset A, Murigneux A (2005) Linkage mapping of 1454 new maize candidate gene loci. Genetics 170:957–1966
Fan CC, Xing YZ, Mao HL, Lu TT, Han B, Xu CG, Li XH, Zhang QF (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171
Fisher RA (1918) The correlations between relatives on the supposition of Mendelian inheritance. Trans R Soc Edinb 52:399–433
Gadau J, Page RE, Werren JH (2002) The genetic basis of the interspecific differences in wing size in Nasonia (Hymenoptera; Pteromalidae): major quantitative trait loci and epistasis. Genetics 161:673–684
Goldman IL, Rocheford TR, Dudley JW (1994) Molecular markers associated with maize kernel oil concentration in an Illinois High Protein × Illinois Low Protein cross. Crop Sci 34:908–915
Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987
Groh S, González-de-León D, Khairallah MM, Jiang C, Bergvinson D, Bohn M, Hoisington DA, Melchinger AE (1998) QTL mapping in tropical maize: III. Genomic regions for resistance to Diatraea spp. and associated traits in two RIL populations. Crop Sci 38:1062–1072
Han Y, Parsons CM, Alexander DE (1987) Nutritive value of high oil for poultry. Poult Sci 66:103–111
Hobbs DH, Flintham JE, Hills MJ (2004) Genetic control of storage oil synthesis in seeds of Arabidopsis. Plant Physiol 136:3341–3349
Holland JB (1998) Epistacy: a SAS program for detecting two-locus epistatic interactions using genetic marker information. J Hered 89:374–375
Jeppe RA, Thomas L (2003) Functional markers in plants. Trends Plant Sci 8:552–560
Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216
Knapp SJ, Stroup WW, Ross WM (1985) Exact confidence intervals for heritability on a progeny mean basis. Crop Sci 25:192–194
Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations co-dominant ecotype-specific PCR based markers. Plant J 4:403–410
Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312:1392–1396
Lambert RJ (2001) High-oil corn hybrids. In: Hallau AR (ed) Special corn. CRC Press, Boca Raton, pp 131–153
Lambert RJ, Alexander DE, Mejaya IJ (2004) Single kernel selection for increased grain oil in maize synthetics and high-oil hybrid development. Plant Breed Rev 24:153–175
Laurie CC, Chasalow SD, LeDeaux JR, McCarroll R, Bush D, Hauge B, Lai CQ, Clark D, Rocheford TR, Dudley JW (2004) The genetic architecture of response to long-term artificial selection for oil concentration in the maize kernel. Genetics 168:2141–2155
Lee K, Huang AH (1994) Genes encoding oleosins in maize kernel of inbreds Mo17 and B73. Plant Mol Biol 26:1981–1987
Li CB, Zhou AL, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936–1939
Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMAKER/EXP Version 3.0: A tutorial and reference manual. A Whitehead Institute for Biomedical Research Technical Report
Lionneton E, Ravera S, Sanchez L, Aubert G, Delourme R, Ochatt S (2002) Development of an AFLP-based linkage map and localization of QTLs for seed fatty acid content in condiment mustard (Brassica juncea). Genome 45:1203–1215
Lukens LN, Doebley J (1999) Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genet Res 74:291–302
Malmberg RL, Held S, Waits A, Mauricio R (2005) Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field. Genetics 171:2013–2027
Mangolin CA, de Souza CL Jr, Garcia AAF, Garcia AF, Sibov ST, de Souza AP (2004) Mapping QTLs for kernel oil content in a tropical maize population. Euphytica 137:251–259
Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932
Mei HW, Li ZK, Shu QY, Guo LB, Wang YP, Yu XQ, Ying CS, Luo LJ (2005) Gene actions of QTLs affecting several agronomic traits resolved in a recombinant inbred rice population and two backcross populations. Theor Appl Genet 110:649–659
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
Murry MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970
Ohlrogge J, Mhaske VB, Beisson F, Ruuska S (2004) Genomics approaches to lipid biosynthesis. In: Proceedings of the 4th international crop science congress, 26 Sep to 1 Oct 2004, Brisbane, Australia
Pérez-Vich B, Fernández-Martínez JM, Grondona M, Knapp SJ, Berry ST (2002) Stearoyl-ACP and oleoyl-PC desaturase genes cosegregate with quantitative trait loci underlying high stearic and high oleic acid mutant phenotypes in sunflower. Theor Appl Genet 104:338–349
Redoňa ED, Mackill DJ (1998) Quantitative trait locus analysis for rice panicle and grain characteristics. Theor Appl Genet 96:957–963
Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304
SAS Institute (1999) SAS software. Cary, NC
Schreiber L, Skrabs M, Hartmann K, Becker D, Cassagne C, Lessire R (2000) Biochemical and molecular characterization of corn (Zea mays L.) root elongases. Biochem Soc Trans 28:647–649
Sen S, Churchill GA (2001) A statistical framework for quantitative trait mapping. Genetics 159:371–387
Song TM, Chen SJ (2004) Long term selection for oil concentration in five maize populations. Maydica 49:9–14
Song TM, Kong F, Li CJ, Song GH (1999) Eleven cycles of single kernel phenotypic recurrent selection for percent oil in Zhongzong no. 2 maize synthetics. J Genet Breed 53:31–35
Song XF, Song TM, Dai JR, Rocheford TR, Li JS (2004) QTL mapping of kernel oil concentration with high-oil maize by SSR markers. Maydica 49:41–48
Sukhija PS, Palmquist DL (1988) Rapid method for determination of total fatty acid content and composition of feedstuffs and feces. J Agric Food Chem 36:1202–1206
Wang CS, Rutledge JJ, Gianola D (1994) Bayesian analysis of mixed linear models via Gibbs sampling with an application to litter size in Iberian pigs. Genet Sel Evol 26:91–115
Wang SC, Basten CJ, Zeng ZB (2005) Windows QTL Cartographer 2.5 user manual. North Carolina State University, Raleigh
Wassom JJ, Wong JC, Martinez E, King JJ, DeBaene J, Hotchkiss JR, Mikkilineni V, Bohnh MO, Rocheford TR (2008a) QTL associated with maize kernel oil, protein, and starch concentrations; kernel mass; and grain yield in Illinois High Oil × B73 backcross-derived lines. Crop Sci 48:243–252
Wassom JJ, Mikkelineni V, Bohn MO, Rocheford TR (2008b) QTL for fatty acid composition of maize kernel oil in Illinois High Oil × B73 backcross-derived lines. Crop Sci 48:69–78
Xu SZ, Jia ZY (2007) Genome-wide analysis of epistatic effects for quantitative traits in barley. Genetics 175:1955–1963
Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536
Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang QF, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231
Zhang J, Lu XQ, Song XF, Yan JB, Song TM, Dai JR, Rocheford T, Li JS (2008) Mapping quantitative trait loci for oil, starch, and protein concentrations in grain with high-oil maize by SSR markers. Euphytica 162:335–344
Zhao JY, Becker HC, Zhang DQ, Zhang YF, Ecke W (2005) Oil content in a European × Chinese rapeseed population: QTL with additive and epistatic effects and their genotype–environment interactions. Crop Sci 41:51–59
Zhao JY, Becker HC, Zhang DQ, Zhang YF, Ecke W (2006) Conditional QTL mapping of oil content in rapeseed with respect to protein content and traits related to plant development and grain yield. Theor Appl Genet 113:33–38
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
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Financial support was provided by the National Natural Science Foundation of China and Chinese High Technology Project. We gratefully acknowledge Prof. Jun Zhu’s guidance for using QTLNetwork Version 2.0 software and Professor R. A. McIntosh for language editing.
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Yang, X., Guo, Y., Yan, J. et al. Major and minor QTL and epistasis contribute to fatty acid compositions and oil concentration in high-oil maize. Theor Appl Genet 120, 665–678 (2010). https://doi.org/10.1007/s00122-009-1184-1
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DOI: https://doi.org/10.1007/s00122-009-1184-1