Genome-wide association study for starch content and constitution in sorghum (Sorghum bicolor (L.) Moench)

doi:10.1016/S2095-3119(19)62631-6

摘要/Abstract

Abstract: Starch is the most important component in endosperm of sorghum grain. Usually, two types of starch are present: amylose (AM) and amylopectin (AP). The levels of AM and AP contents play a significant role in the appearance, structure, and quality of sorghum grains and in marketing applications. In the present study, a panel of 634 sorghum (Sorghum bicolor (L.) Moench) accessions were evaluated for starch, AM, and AP contents of grain, which included a mini core collection of 242 accessions from the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) in India, and 252 landraces and 140 cultivars from China. The average starch content was 67.64% and the average AM and AP contents were 20.19 and 79.81%, respectively. We developed a total of 260 000 high-confidence single nucleotide polymorphism (SNP) markers in the panel of 634 accessions of S. bicolor using specific locus amplified fragment sequencing (SLAF-seq). We performed genome-wide association studies (GWAS) of starch, AM, and AM/AP of grain and SNP markers based on a mixed linear model (MLM). In total, 70 significant association signals were detected for starch, AM, and AM/AP ratio of grain with P<4.452×10^–7, of which 10 SNPs were identified with significant starch, 51 SNPs were associated with AM, and nine SNPs were associated with the AM/AP ratio. The Gene Ontology (GO) analysis identified 12 candidate genes at five QTLs associated with starch metabolism within the 200-kb intervals, located on chromosomes 1, 5, 6, and 9. Of these genes, Sobic.006G036500.1 encodes peptidyl-prolyl cis-trans-isomerase CYP38 responsible for hexose monophosphate shunt (HMS) and Sobic.009G071800 encodes 6-phospho-fructokinase (PFK), which is involved in the embden-meyerhof pathway (EMP). Kompetitive allele specific PCR (KASP) markers were developed to validate the GWAS results. The C allele is correlated with a high starch content, while the T allele is linked with a low level of starch content, and provides reliable haplotypes for MAS in sorghum quality improvement.

Key words: sorghum , , genome-wide association mapping (GWAS) , , starch content , , amylose (AM) , , candidate genes , , KASP

. [J]. Journal of Integrative Agriculture, 2019, 18(11): 2446-2456.

CHEN Bing-ru, WANG Chun-yu, WANG Ping, ZHU Zhen-xing, XU Ning, SHI Gui-shan, YU Miao, WANG Nai, LI Ji-hong, HOU Jia-ming, LI Shu-jie, ZHOU Yu-fei, GAO Shi-jie, LU Xiao-chun, HUANG Rui. Genome-wide association study for starch content and constitution in sorghum (Sorghum bicolor (L.) Moench)[J]. Journal of Integrative Agriculture, 2019, 18(11): 2446-2456.

参考文献

de Alencar Figueiredo L F, Sine B, Chantereau J, Mestres C, Fliedel G, Rami J F, Glaszmann J C, Deu M, Courtois B. 2010. Variability of grain quality in sorghum: Association with polymorphism in Sh2, Bt2, SssI, Ae1, Wx and O2. Theoretical and Applied Genetics, 121, 1171–1185.
Aluko G, Martinez C, Tohme J, Castano C, Bergman C, Oard J H. 2004. QTL mapping of grain quality traits from the interspecific cross Oryza sativa×O. glaberrima. Theoretical and Applied Genetics, 109, 630–639.
Atwell S, Huang Y S, Vilhjalmsson B J, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone A M, Hu T T. 2010. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature, 465, 627–631.
Ayres N M, McClung A M, Larkin P D, Bligh H F J, Jones C A, ParkW D. 1997. Microsatellites and a single-nucleotide polymorphism differentiate apparent amylose classes in an extended rice pedigree of US rice germplasm. Theoretical and Applied Genetics, 94, 773–781.
Boyles R E, Pfeiffer B K, Cooper E A, Rauh L, Zielinski K J, Myers M T, Brenton Z, Rooney W L, Kresovich S. 2017. Genetic dissection of sorghum grain quality traits using diverse and segregating populations. Theoretical and Applied Genetics, 130, 697–716.
Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diver samples. Bioinformatics, 23, 2633–2635.
Cook J P, McMullen M D, Holland J B, Tian F, Bradbury P, RossIbarra J, Buckler E S, Flint-Garcia S A. 2012. Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiology, 158, 824–834.
Cui Z H, Luo J H, Qi ChY, Ruan Y Y, Li J, Zhang A, Yang X H, He Y. 2016. Genome-wide association study (GWAS) reveals the genetic architecture of four husk traits in maize. BMC Genomics, 17, 946–960.
Denyer K, Johnson P, Zeeman S, Smith A M. 2001. The control of amylose synthesis. Journal of Plant Physiology, 158, 479–487.
Fang Q, Hanna M A. 2000. Functional properties of polylactic acid starch-based loose-fill packaging foams. Cereal Chemistry, 77, 779–783.
Flint J, Eskin E. 2012. Genome-wide association studies in mice. Nature Reviews Genetics, 13, 807–817.
Fukunaga K, kawase M, Kato K. 2002. Structural variation in the Waxy gene and differentiation in foxtail millet [Setariaitalica (L.) P. Beauv.]: implication for multiple origins of the waxy phenotye. Molecular Genetics Genomics, 268, 214–222.
Hamblin M T, Salas Fernandez M G,Tuinstra M R, Rooney W L, Kresovich S. 2007. Sequence variation at candidate loci in the starch metabolism pathway in sorghum: prospects for linkage disequilibrium mapping. Crop Science, 47, S125–S134.
Han Y, Zhao X, Liu D, Li Y, Lightfoot D A, Yang Z. 2016.Domestication footprints anchogenomic regions of agronomic importance in soybeans. New Phytologist, 209, 871–884.
Holm S. 1979. A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65–70.
Huang X H, Wei X H, Tao S, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C R, Lu T T, Zhang Z W, Li M, Fan D L, Guo Y L, Wang A H, Wang L, Deng L W, Li W J, Lu Y Q, Weng Q J, Liu K Y, et al. 2010. Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genetics, 42, 961–967.
Huang X H, Zhao Y, Wei X H, Li C Y, Wang A H, Zhao Q, Li W J, Guo Y L, Deng L W, Zhu C R, Fan D L, Lu Y Q, Weng Q J, Liu K Y, Zhou T Y, Jing Y F, Si L Z, Dong G J, Huang T, Lu T T, et al. 2012. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nature Genetics, 44, 32–39.
Huang X Q, Cloutier S, Lycar L, Radovanovic N, Humphreys D G, Noll J S, Somers D J, Brown P D. 2006. Molecular detectionof QTLs for agronomic and quality traits in a doubled haploid population derived from two Canadian wheats (Triticum aestivum L.). Theoretical and Applied Genetics, 113, 753–766.
Jeon J S, Ryoo N, Hahn T R, Walia H, Nakamura Y. 2010.Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry, 48, 383–392.
Jia G Q, Huang X H, Zhi H, Zhao Y, Zhao Q, Li W J, Chai Y, Yang L F, Liu K Y, Lu H Y, Zhu C R, Lu Y Q, Zhou C C, Fan D L, Weng Q J, Guo Y L, Huang T, Zhang L, Lu T T, Feng Q, et al. 2013. A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtailmillet (Setaria italica). Nature Genetics, 45, 957–961.
Karper R E. 1933. Inheritance of waxy endosperm in sorghum. Journal of Heredity, 24, 257–262.
Kawahigashi H, Oshima M, Nishikawa T, Okuizumi H, Kasug S, Yonemaru J I. 2013. A novel waxy allele in sorghum landraces in East Asia. Plant Breeding, 132, 305–310.
Korte A, Farlow A. 2013. The advantages and limitations of trait analysis with GWAS: A review. Plant Methods, 9, 29.
Li C S, Huang Y C, Huang R D, Wu Y R, Wang W Q. 2017.The genetic architecture of amylose biosynthesis in maize kernel. Plant Biotechnology Journal, 16, 688–695.
Li H, Peng Z Y, Yang X H, Wang W D, Fu J J, Wang J H, Han Y J, Chai Y C, Guo T T, Yang N, Liu J, Warburton M L, Cheng Y B , Hao X M, Zhang P, Zhao J Y, Liu Y J, Wang G Y, Li J S, Yan J B. 2013. Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nature Genetics, 45, 43–50.
Li J, Xiao J, Grandillo S, Jiang L, Wan Y, Deng Q, Yuan L, McCouch S R. 2004. QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African
(O. glaberrima S.) rice. Genome, 47, 697–704.
Liu N, Xue Y, Guo Z, Li W, Tang J. 2016. Genome-wide association study identifies candidate genes for starch content regulation in maize kernels. Frontiers in Plant Science, 7, 1–8.
McCartney C A, Somers D J, Lukow O, Ames N, Noll J, Cloutier S, Humphreys D G, McCallum B D. 2006. QTL analysis of quality traits in the spring wheat cross RL4452×“AC Domain”. Plant Breeding, 125, 565–575.
McIntyre C L, Drenth J, Gonzalez N, Henzell R G, Jordan D R. 2008. Molecular characterization of the waxy locus in sorghum. Genome, 51, 524–533.
Ni X L, Zhao G L, Wang X K, Liu T P, Chen G M, Ding G X. 2015. The genetic diversity analysis of 42 glutinous sorghum germplasm, resources using SSR markers. Molecular Plant Breeding, 9, 1962–1969. (in Chinese)
National Bureau of Statistics of the People’s Republic of China. 2015. China Statistical Yearbook. China Statistics Press, Beijing. (in Chinese)
Olsen K M, Purugganan M D. 2002. Molecular evidence on the origin and evolution of glutinous rice. Genetics, 162, 941–950.
Olsen H G, Hayes B J, Kent M P, Nome T, Svendsen M, Larsgard A G, Lien S. 2011. Genome-wide association mapping in Norwegian Red cattle identifies quantitative trait loci for fertility and milk production on BTA12. Animal Genetics, 42, 466–474.
Rooney L W, Pflugfelder R L.1986. Factors affecting starch digestibility with special emphasis on sorghum and corn. Journal of Animal Science, 63, 1607–1623.
Schultz J A, Juvik J A. 2004. Current models for starch synthesis and the sugary enhancer1 (se1) mutation in Zea mays. Plant Physiology and Biochemistry, 42, 457–464.
Séne M, Causse M, Damerval C, Thévenot C, Prioul J L. 2000.Quantitative trait loci affecting amylose, amylopectin and starch content in maize recombinant inbred lines. Plant Physiology and Biochemistry, 38,459–472.
Semagn K, Babu R, Hearne S, Michael O. 2013. Single nucleotide polymorphism genotyping using Kompetitive Allele Speci?c PCR (KASP): overview of the technology and its application in crop improvement. Moleular Breeding, 33, 1–14.
Sherrod L B, Albin R C, Furr R D. 1969. Net energy of regular and waxy sorghum grains for finishing steers. Journal of Animal Science, 29, 997–1000.
Sukumaran S, Xiang W, Bean S R, Pedersen J F, Kresovich S, Tuinstra M R, Tesso T T, Hamblin M T, Yu J. 2012.Association mapping for grain quality in a diverse sorghum collection. Plant Genome, 5, 126–135.
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W. 2013. SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS ONE, 8, e58700.
Pasquini C. 2003. Near infrared spectroscopy: Fundamentals, practical aspects and analytical applications. Journal of the Brazilian Chemical Society, 14,198–219.
Pedersen J, Bean S, Graybosch R, Park S, Tilley M. 2005.Characterization of waxy grain sorghum lines in relation to granule–bound starch synthase. Euphytica, 144, 151–156.
Udachan I S, Sahu A K, Hend F M. 2012. Extraction and characterization of sorghum (Sorghum bicolor L. Moench) starch. International Food Research Journal, 19, 315–319.
Upadhyaya H D, Pundir R P S, Dwivedi S L, Gowda C L L, Reddy V G, Singh S. 2009. Developing a mini core collection of sorghum for diversified utilization of germplasm. Crop Science, 49, 1769–1780.
Wang D, Bean S, McLaren J, Seib P, Madl R, Tuinstra M, Shi Y, Lenz M, Wu X, Zhao R. 2008. Grain sorghum is aviable feedstock for ethanol production. Journal of Industrial Microbiology Biotechnology, 35, 313–320.
De Wet J M J. 1978. Systematics and evolution of Sorghum Sect. Sorghum (Gramineae). American Journal of Botany, 65, 477–484.
Wilson L M, Whitt S R, Ibanez A M, Rocheford T R, Goodman M M, Buckler E S. 2004. Dissection of maize kernel composition andstarch production by candidate gene association. The Plant Cell, 16, 2719–2733.
Wong J H, Lau T, Cai N, Singh J, Pedersen J F, Vensel W H, Hurkman W J, Wilson J D, Lemaux P G, Buchanan B B. 2009. Digestibility of protein and starch from sorghum (Sorghum bicolor) is linked to biochemical and structural features of grain endosperm. Journal of Cereal Science, 49, 73–82.
Wu X, Ren C, Joshi T, Vuong T, Xu D, Nguyen H. 2010. SNP discovery by high throughput sequencing in soybean. BMC Genomics, 11, 469.
Yan S, Wu X, Bean S, Pedersen J, Tesso T, Chen Y, Wang D. 2011. Evaluation of waxy grain sorghum for ethanol production. Cereal Chemistry, 88, 589–595.
Zheng X M, Gong T T, Hong L, Ou H L, Xue D Y, Qiao W H, Wang J R, Liu S, Yang Q W, Olsen K M. 2018. Genome-wide association study of rice grain width variation. Genome, 61, 233–240.
Zhu F. 2014. Structure, physicochemical properties, modifications, and uses of sorghum starch. Comprehensive Reviews in Food Science and Food Safety, 13, 597–610.