Abstract
Background
At least eight structurally related forms of vitamin E occur in nature, four tocopherols and four tocotrienols, all of which are potent membrane-soluble antioxidants. In this study, we detected two major isoforms in sesame (Sesamum indicum L.) seed: γ-tocopherol and β-tocotrienol. The objective of this study is to investigate the genetic basis of these vitamin E isoforms.
Methods
We conducted a genome-wide association study (GWAS) using 5962 genome-wide markers, acquired from 96 core sesame accessions. The GWAS was performed using generalized linear (GLM) and mixed linear (MLM) models.
Results
LG08_6621957, on chromosome 8, was detected as having a significant association with γ-tocopherol in both models. It explained 20.9% of γ-tocopherol variation in sesame. For β-tocotrienol, no significant loci were detected according to the two models, but one locus, SLG03_13104062, explained 17.8% of the phenotypic variation. Based on structure and phylogenetic studies, the 96 accessions were clearly clustered into two subpopulations.
Conclusion
This study on sesame demonstrates and provides an evidence that genotyping by sequencing (GBS) based GWAS can be used to identifying important loci for small growing crops. The significant SNPs or genes could be useful for improving the vitamin E content in sesame breeding programs.
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References
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3(10):e3376
Brigelius-Flohe R, Traber MG (1999) Vitamin E: function and metabolism. FASEB J 13(10):1145–1155
Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21(9):1082–1087
Chen S, Li H, Liu G (2006) Progress of vitamin E metabolic engineering in plants. Transgenic Res 15(6):655–665
Cho EA, Lee CA, Kim YS, Baek SH, Reyes BG, Yun SJ (2005) Expression of γ-tocopherol methyltransferase transgene improves tocopherol composition in lettuce (Latuca sativa L.). Mol Cells 19(1):1
Collakova E, DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp. PCC 6803 and Arabidopsis. Plant Physiol 127(3):1113–1124
Collakova E, DellaPenna D (2003) Homogentisate phytyltransferase activity is limiting for tocopherol biosynthesis in Arabidopsis. Plant Physiol 131(2):632–642
Cook WB, Miles D (1992) Nuclear mutations affecting plastoquinone accumulation in maize. Photosynth Res 31(2):99–111
DellaPenna D (2005) Progress in the dissection and manipulation of vitamin E synthesis. Trends Plant Sci 10(12):574–579
Demurin Y, Skoric D, Karlovic D (1996) Genetic variability of tocopherol composition in sunflower seeds as a basis of breeding for improved oil quality. Plant Breed 115(1):33–36
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(5):e19379
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Falk J, Krauß N, Dähnhardt D, Krupinska K (2002) The senescence associated gene of barley encoding 4-hydroxyphenylpyruvate dioxygenase is expressed during oxidative stress. J Plant Physiol 159(11):1245–1253
Garcia I, Rodgers M, Lenne C, Rolland A, Sailland A, Matringe M (1997) Subcellular localization and purification of a p-hydroxyphenylpyruvate dioxygenase from cultured carrot cells and characterization of the corresponding cDNA. Biochem J 325(3):761–769
Garcia I, Rodgers M, Pepin R, Hsieh T-F, Matringe M (1999) Characterization and subcellular compartmentation of recombinant 4-hydroxyphenylpyruvate dioxygenase from Arabidopsis in transgenic tobacco. Plant Physiol 119(4):1507–1516
Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Zhang Z (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42(11):961–967
Jiang Q, Christen S, Shigenaga MK, Ames BN (2001) γ-Tocopherol, the major form of vitamin E in the US diet, deserves more attention. Am J Clin Nutr 74(6):714–722
Kamal-Eldin A, Appelqvist L-Å (1996) The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 31(7):671–701
Karunanandaa B, Qi Q, Hao M, Baszis SR, Jensen PK, Wong Y-HH, Moshiri F (2005) Metabolically engineered oilseed crops with enhanced seed tocopherol. Metab Eng 7(5):384–400
Kumar R, Raclaru M, Schüßeler T, Gruber J, Sadre R, Lühs W, Frentzen M (2005) Characterisation of plant tocopherol cyclases and their overexpression in transgenic Brassica napus seeds. FEBS Lett 579(6):1357–1364
Li G-X, Lee M-J, Liu AB, Yang Z, Lin Y, Shih WJ, Yang CS (2011) δ-tocopherol is more active than α-or γ-tocopherol in inhibiting lung tumorigenesis in vivo. Cancer Prevention Res 4(3):404–413
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28(18):2397–2399
Liu C, Zhou Q, Dong L, Wang H, Liu F, Weng J, Xie C (2016) Genetic architecture of the maize kernel row number revealed by combining QTL mapping using a high-density genetic map and bulked segregant RNA sequencing. BMC Genomics 17(1):915
Mondal N, Bhat K, Srivastava P, Sen S (2016) Effects of domestication bottleneck and selection on fatty acid desaturases in Indian sesame germplasm. Plant Genetic Resour 14:81–90
Park SH, Ryu SN, Bu Y, Kim H, Simon JE, Kim KS (2010) Antioxidant components as potential neuroprotective agents in sesame (Sesamum indicum L.). Food Rev Int 26(2):103–121
Park JH, Suresh S, Cho GT, Choi NG, Baek HJ, Lee CW, Chung JW (2014) Assessment of molecular genetic diversity and population structure of sesame (Sesamum indicum L.) core collection accessions using simple sequence repeat markers. Plant Genetic Resour 12(01):112–119
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Purru S, Sahu S, Rai S, Rao A, Bhat KJP, Plants MBO (2018) GinMicrosatDb: a genome-wide microsatellite markers database for sesame (Sesamum indicum L.). Physiol Mol Biol Plants 24(5):929–937
Sattler SE, Cheng Z, DellaPenna D (2004) From Arabidopsis to agriculture: engineering improved vitamin E content in soybean. Trends Plant Sci 9(8):365–367
Schwartz H, Ollilainen V, Piironen V, Lampi A-M (2008) Tocopherol, tocotrienol and plant sterol contents of vegetable oils and industrial fats. J Food Compos Anal 21(2):152–161
Soll J, Schultz G, Joyard J, Douce R, Block MA (1985) Localization and synthesis of prenylquinones in isolated outer and inner envelope membranes from spinach chloroplasts. Arch Biochem Biophys 238(1):290–299
Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14(5):748–750
Subramaniam SS, Slater SC, Karberg K, Chen R, Valentin HE, Wong YHH (2008) Nucleic acid sequences to proteins involved in tocopherol synthesis. In: Google Patents
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Zeng H (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8(3):e58700
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Theriault A, Chao J-T, Wang Q, Gapor A, Adeli K (1999) Tocotrienol: a review of its therapeutic potential. Clin Biochem 32(5):309–319
Truong HT, Ramos AM, Yalcin F, de Ruiter M, van der Poel HJ, Huvenaars KH, van Orsouw NJ (2012) Sequence-based genotyping for marker discovery and co-dominant scoring in germplasm and populations. PLoS One 7(5):e37565
Van Eenennaam A, Valentin H, Karunanandaa B, Hao M, Aasen E, Levering C (2003a) Methyltransferase genes and uses thereof. International patent application WO 3:016482
Van Eenennaam AL, Lincoln K, Durrett TP, Valentin HE, Shewmaker CK, Thorne GM, Aasen ED (2003b) Engineering vitamin E content: from Arabidopsis mutant to soy oil. Plant Cell 15(12):3007–3019
Wang L, Yu S, Tong C, Zhao Y, Liu Y, Song C, Hua W (2014) Genome sequencing of the high oil crop sesame provides insight into oil biosynthesis. Genome Biol 15(2):1
Wang X-Q, Yoon M-Y, He Q, Kim T-S, Tong W, Choi B-W, Park Y-J (2015) Natural variations in OsγTMT contribute to diversity of the α-tocopherol content in rice. Mol Genet Genomics 290(6):2121–2135
Wei X, Liu K, Zhang Y, Feng Q, Wang L, Zhao Y, Zhu X (2015) Genetic discovery for oil production and quality in sesame. Nature Commun 6:8609
Wen Z, Tan R, Yuan J, Bales C, Du W, Zhang S, Cregan PB (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genomics 15(1):1
Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Yan J (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(9):e1004573
Yano K, Yamamoto E, Aya K, Takeuchi H, Lo PC, Hu L, Hirano K (2016) Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice. Nature Genet 48:927
Zhang H, Miao H, Wang L, Qu L, Liu H, Wang Q, Yue M (2013) Genome sequencing of the important oilseed crop Sesamum indicum L. Genome Biol 14(1):401
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This work was supported by the research grant of the Kongju National University in 2018.
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He, Q., Xu, F., Min, MH. et al. Genome-wide association study of vitamin E using genotyping by sequencing in sesame (Sesamum indicum). Genes Genom 41, 1085–1093 (2019). https://doi.org/10.1007/s13258-019-00837-3
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DOI: https://doi.org/10.1007/s13258-019-00837-3