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Identification of SSR markers associated with height using pool-based genome-wide association mapping in sorghum

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Abstract

Sorghum has been proposed as a potential energy crop. However, it has been traditionally bred for grain yield and forage quality, not traits related to bioenergy production. To develop tools for genetic improvement of bioenergy-related traits such as height, genetic markers associated with these traits have first to be identified. Association mapping has been extensively used in humans and in some crop plants for this purpose. However, genome-wide association mapping using the whole association panel is costly and time-consuming. A variation of this method called pool-based genome-wide association mapping has been extensively used in humans. In this variation, pools of individuals with contrasting phenotypes, instead of the whole panel, are screened with genetic markers and polymorphic markers are confirmed by screening the individuals in the pools. Here, we identified several new simple sequence repeats (SSR) markers associated with height using this pool-based genome-wide association mapping in sorghum. After screening the tall and short pools of sorghum accessions from the sorghum Mini Core collection developed at the International Crops Research Institute for the Semi-Arid Tropics with 703 SSR markers, we have identified four markers that are closely associated with sorghum height on chromosomes 2, 6, and 9. Comparison with published maps indicates that all four markers are clustered with markers previously mapped to height or height-related traits and with candidate genes involved in regulating plant height such as FtsZ, Ugt, and GA 2-oxidase. The mapping method can be applied to other crop plants for which a high-throughput genome-wide association mapping platform is not yet available.

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References

  • Abu Assar AH, Uptmoor R, Abdelmula AA, Salih M, Ordon F, Friedt W (2005) Genetic variation in sorghum germplasm from Sudan, ICRISAT, and USA assessed by simple sequence repeats (SSRs). Crop Sci 45:1636–1644

    Article  Google Scholar 

  • Agrama HA, Tuinstra MR (2003) Phylogenetic diversity and relationships among sorghum accessions using SSRs and RAPDs. Afr J Biotechnol 2:334–340

    CAS  Google Scholar 

  • Ali ML, Rajewski JF, Baenziger PS, Gill KS, Eskridge KM, Dweiket I (2008) Assessment of genetic diversity and relationship among a collection of US sweet sorghum germplasm by SSR markers. Mol Breed 21:497–509

    Article  CAS  Google Scholar 

  • Anas, Yoshida T (2004) Genetic diversity among Japanese cultivated sorghum assessed with simple sequence repeats markers. Plant Prod Sci 7:217–223

  • Barnaud A, Deu M, Garine E, McKey D, Joly HI (2007) Local genetic diversity of sorghum in a village in northern Cameroon: structure and dynamics of landraces. Theor Appl Genet 114:237–248

    Article  PubMed  Google Scholar 

  • Bhattramakki D, Dong J, Chhabra K, Hart GE (2000) An integrated SSR and RFLP linkage map of Sorghum bicolor (L.) Moench. Genome 43:988–1002

    PubMed  CAS  Google Scholar 

  • Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265

    Article  PubMed  CAS  Google Scholar 

  • Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–2395

    Article  PubMed  CAS  Google Scholar 

  • Bowers JE, Abbey C, Anderson S, Chang C, Draye X, Hoppe AH, Jessup R, Lemke C, Lennington J, Li Z, Lin YR, Liu SC, Luo L, Marler BS, Ming R, Mitchell SE, Qiang D, Reischmann K, Schulze SR, Skinner DN, Wang YW, Kresovich S, Schertz KF, Paterson AH (2003) A high-density genetic recombination map of sequence-tagged sites for sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics 165:367–386

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Brown PJ, Klein PE, Bortiri E, Acharya CB, Rooney WL, Kresovich S (2006) Inheritance of inflorescence architecture in sorghum. Theor Appl Genet 113:931–942

    Article  PubMed  CAS  Google Scholar 

  • Brown PJ, Rooney WL, Franks C, Kresovich S (2008) Efficient mapping of plant height quantitative trait loci in a sorghum association population with introgressed dwarfing genes. Genetics 180:629–637

    Article  PubMed  Google Scholar 

  • Busov VB, Meilan R, Pearce DW, Ma C, Rood SB, Strauss SH (2003) Activation tagging of a dominant gibberellin catabolism gene (GA 2-oxidase) from poplar that regulates tree stature. Plant Physiol 132:1283–1291

    Article  PubMed  CAS  Google Scholar 

  • Caniato FF, Guimarães CT, Schaffert RE, Alves VM, Kochian LV, Borém A, Klein PE, Magalhaes JV (2007) Genetic diversity for aluminum tolerance in sorghum. Theor Appl Genet 114:863–876

    Article  PubMed  CAS  Google Scholar 

  • Casa AM, Mitchell SE, Hamblin MT, Sun H, Bowers JE, Paterson AH, Aquadro CF, Kresovich S (2005) Diversity and selection in sorghum: simultaneous analyses using simple sequence repeats. Theor Appl Genet 111:23–30

    Article  PubMed  CAS  Google Scholar 

  • Casa AM, Pressoir G, Brown PJ, Mitchell SE, Rooney WL, Tuinstra MR, Franks CD, Kresovich S (2008) Community resources and strategies for association mapping in sorghum. Crop Sci 48:30–40

    Article  Google Scholar 

  • Chittenden LM, Schertz KF, Lin YR, Wing RA, Paterson AH (1994) A detailed RFLP map of Sorghum bicolor × S. propinquum, suitable for high-density mapping, suggests ancestral duplication of sorghum chromosomes or chromosomal segments. Theor Appl Genet 87:925–933

    Article  CAS  Google Scholar 

  • Deu M, Sagnard F, Chantereau J, Calatayud C, Hérault D, Mariac C, Pham JL, Vigouroux Y, Kapran I, Traore PS, Mamadou A, Gerard B, Ndjeunga J, Bezançon G (2008) Niger-wide assessment of in situ sorghum genetic diversity with microsatellite markers. Theor Appl Genet 116:903–913

    Article  PubMed  CAS  Google Scholar 

  • Dillon SL, Kawrence PK, Henry RJ (2005) The new use of Sorghum bicolor-derived SSR markers to evaluate genetic diversity in 17 Australian Sorghum species. Plant Genet Resour 3:19–28

    Article  CAS  Google Scholar 

  • Drgon T, Zhang PW, Johnson C, Walther D, Hess J, Nino M, Uhl GR (2010) Genome wide association for addiction: replicated results and comparisons of two analytic approaches. PLoS One 5(1):e8832

    Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Feltus FA, Hart GE, Schertz KF, Casa AM, Kresovich S, Abraham S, Klein PE, Brown PJ, Paterson AH (2006) Alignment of genetic maps and QTLs between inter- and intra-specific sorghum populations. Theor Appl Genet 112:1295–1305

    Article  PubMed  CAS  Google Scholar 

  • Folkertsma RT, Rattunde HFW, Chandra S, Raju GS, Hash CT (2005) The pattern of genetic diversity of Guinea-race Sorghum bicolor (L.) Moench landraces as revealed with SSR markers. Theor Appl Genet 111:399–409

    Article  PubMed  CAS  Google Scholar 

  • Ghebru B, Schmidt R, Bennetzen J (2002) Genetic diversity of Eritrean sorghum landraces assessed with simple sequence repeat (SSR) markers. Theor Appl Genet 105:229–236

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni JJ, Wing RA, Ganal MW, Tanksley SD (1991) Isolation of molecular markers from specific chromosomal intervals using DNA pools from existing mapping populations. Nucl Acids Res 19:6553–6558

    Article  PubMed  CAS  Google Scholar 

  • Haussmann B, Hess D, Seetharama D, Welz H, Geiger H (2002) Construction of a combined sorghum linkage map from two recombinant inbred populations using AFLP, SSR, RFLP, and RAPD markers, and comparison with other sorghum maps. Theor Appl Genet 105:629–637

    Article  PubMed  CAS  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Li W, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  PubMed  CAS  Google Scholar 

  • Jeong WJ, Jeong SW, Min SR, Yoo OL, Liu JR (2002) Growth retardation of plank transform by overexpression of NtFtsZ1–2 in tobacco. J Plant Biol 45:107–111

    Article  CAS  Google Scholar 

  • Klein PE, Klein RR, Cartinhour SW, Ulanch PE, Dong J, Obert JA, Morshige DT, Schlueter SD, Childs KL, Ale M, Mullet JE (2000) A high-throughput AFLP-based method for constructing integrated genetic and physical maps: Progress toward a sorghum genome map. Genome Res 10:789–807

    Article  PubMed  CAS  Google Scholar 

  • Klein RR, Mullet JE, Jordan DR, Miller FR, Rooney WL, Menz MA, Franks CD, Klein PE (2008) The effect of tropical sorghum conversion and inbred development on genome diversity as revealed by high-resolution genotyping. Plant Genome S1:S12–S26

    Google Scholar 

  • Knoll J, Ejeta G (2008) Marker-assisted selection for early-season cold tolerance in sorghum: QTL validation across populations and environments. Theor Appl Genet 116:541–553

    Article  PubMed  Google Scholar 

  • Kong L, Dong J, Hart GE (2000) Characteristics, linkage-map positions and allelic differentiation of Sorghum bicolor (L.) Moench DNA simple-sequence repeats (SSRs). Theor Appl Genet 101:438–448

    Article  CAS  Google Scholar 

  • Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Wang J, Sun SS, Zhang G (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42:1053–1059

    Article  PubMed  CAS  Google Scholar 

  • Li M, Yuyama N, Luo L, Hirata M, Cai H (2009) In silico mapping of 1758 new SSR markers developed from public genomic sequences for sorghum. Mol Breed 24:41–47

    Article  Google Scholar 

  • Lin YR, Schertz KF, Paterson AH (1995) Comparative analysis of QTLs affecting plant height and maturity across the poaceae, in referecence to an interspecific sorghum population. Genetics 141:391–411

    PubMed  CAS  Google Scholar 

  • Lind PA, Macgregor S, Vink JM, Pergadia ML, Hansell NK, de Moor MH, Smit AB, Hottenga JJ, Richter MM, Heath AC, Martin NG, Willemsen G, de Geus EJ, Vogelzangs N, Penninx BW, Whitfield JB, Montgomery GW, Boomsma DI, Madden PA (2010) A genomewide association study of nicotine and alcohol dependence in Australian and Dutch populations. Twin Res Hum Genet 13:10–29

    Article  PubMed  Google Scholar 

  • Mazzucato A, Papa R, Bitocchi E, Mosconi P, Nanni L, Negri V, Picarella ME, Siligato F, Soressi GP, Tiranti B, Veronesi F (2008) Genetic diversity structure and marker-trait associations in a collection of Italian tomato (Solanum lycopersicum L.) landraces. Theor Appl Genet 116:657–669

    Article  PubMed  Google Scholar 

  • Menz MA, Klein RR, Unruh NC, Rooney RL, Klein PE, Mullet JE (2004) Genetic diversity of public inbreds of sorghum determined by mapped AFLP and SSR markers. Crop Sci 44:1236–1244

    Article  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    Article  PubMed  CAS  Google Scholar 

  • Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS (2003) Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302:81–84

    Article  PubMed  CAS  Google Scholar 

  • Murray SC, Rooney WL, Mitchell SE, Sharma A, Klein PE, Mullet JE, Kresovich S (2008) Genetic improvement of sorghum as a biofuel feedstock: II. QTL for stem and leaf structural carbohydrates. Crop Sci 48:2180–2193

    Article  Google Scholar 

  • Murray SC, Rooney WL, Mitchell SE, Kresovich S (2009) Sweet sorghum diversity and association mapping for brix and height. Plant Genome 2:48–62

    Article  CAS  Google Scholar 

  • Nielsen DA, Ji F, Yuferov V, Ho A, He C, Ott J, Kreek MJ (2010) Genome-wide association study identifies genes that may contribute to risk for developing heroin addiction. Psychiatr Genet 20:207–214

    Article  PubMed  Google Scholar 

  • Paterson AH, Lin YR, Li Z, Schertz KF, Doebley JF, Pinson SRM, Liu SC, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269:1714–1717

    Article  PubMed  CAS  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman Ware D, Westhoff P, Mayer KF, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  PubMed  CAS  Google Scholar 

  • Pei Z, Gao J, Chen Q, Wei J, Li Z, Luo F, Shi L, Ding B, Sun S (2010) Genetic diversity of elite sweet sorghum genotypes assessed by SSR markers. Biol Planta 54:653–658

    Article  CAS  Google Scholar 

  • Pereira MG, Lee M (1995) Identification of genomic regions affecting plant height in sorghum and maize. Theor Appl Genet 90:380–388

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quinby JR, Karper RE (1954) Inheritance of height in Sorghum. Agron J 46:211–216

    Article  Google Scholar 

  • Ramu P, Kassahun B, Senthilvel S, Kumar CA, Jayashree B, Folkertsma RT, Reddy LA, Kuruvinashetti MS, Haussmann BIG, Hash CT (2009) Exploiting rice–sorghum synteny for targeted development of EST-SSRs to enrich the sorghum genetic linkage map. Theor Appl Genet 119:1193–1204

    Article  PubMed  CAS  Google Scholar 

  • Ritter KB, Jordan DR, Chapman SC, Godwin ID, Mace ES, McIntyre CL (2008) Identification of QTL for sugar-related traits in a sweet × grain sorghum (Sorghum bicolor L. Moench) recombinant inbred population. Mol Breed 22:367–384

    Article  Google Scholar 

  • Rooney W (2004) Sorghum improvement—integrating traditional and new technology to produce improved genotypes. Adv Agron 83:37–109

    Article  Google Scholar 

  • Rooney WL, Blumenthal J, Bean B, Mullet JE (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofuels Bioprod Biorefin 1:147–157

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386

    Google Scholar 

  • Saballos A (2008) Development and utilization of sorghum as a bioenergy crop. In: Vermerris W (ed) Genetic improvement of bioenergy crops. Springer, New York, pp 209–248

    Google Scholar 

  • Salas Fernandez MG, Becraft PW, Yin Y, Lübberstedt T (2009) From dwarves to giants? Plant height manipulation for biomass yield. Trends Plant Sci 14:454–461

    Article  PubMed  CAS  Google Scholar 

  • Sham P, Bader JS, Craig I, O’Donovan M, Owen M (2002) DNA pooling: a tool for large scale association studies. Nat Rev Genet 3:862–871

    Article  PubMed  CAS  Google Scholar 

  • Shehzad T, Iwata H, Okuno K (2009a) Genome-wide association mapping of quantitative traits in sorghum (Sorghum bicolor (L.) Moench) by using multiple models. Breed Sci 59:217–227

    Article  CAS  Google Scholar 

  • Shehzad T, Okuizumi H, Kawase M, Okuno K (2009b) Development of SSR-based sorghum (Sorghum bicolor (L.) Moench) diversity research set of germplasm and its evaluation by morphological traits. Genet Res Crop Evol 56:809–827

    Article  CAS  Google Scholar 

  • Smith JSC, Kresovich S, Hopkins MS, Mitchell SE, Dean RE, Woodman RL, Lee M, Porter K (2000) Genetic diversity among elite sorghum inbred lines assessed with simple sequence repeats. Crop Sci 40:226–232

    Article  CAS  Google Scholar 

  • Srinivas G, Satish K, Madhusudhana K, Seetharama N (2009) Exploration and mapping of microsatellite markers from subtracted drought stress ESTs in Sorghum bicolor (L.) Moench. Theor Appl Genet 118:703–717

    Article  PubMed  CAS  Google Scholar 

  • Upadhyaya HD, Ortiz R (2001) A mini core subset for capturing diversity and promoting utilization of chickpea genetic resources in crop improvement. Theor Appl Genet 102:1292–1298

    Article  Google Scholar 

  • Upadhyaya HD, Pundir RPS, Dwivedi SL, Gowda CLL, Reddy VG, Singh S (2009) Developing a mini core collection of sorghum for diversified utilization of germplasm. Crop Sci 49:1769–1780

    Article  Google Scholar 

  • Wang ML, Barkley NA, Jenkins TM (2009a) Microsatellite markers in plants and insects. Part I: applications of biotechnology. Genes Genome Genomics 3:54–67

    Google Scholar 

  • Wang ML, Zhu C, Barkley NA, Chen Z, Erpelding JE, Murray SC, Tuinstra MR, Tesso T, Pederson GA, Yu J (2009b) Genetic diversity and population structure analysis of accessions in the US historic sweet sorghum collection. Theor Appl Genet 120:13–23

    Article  PubMed  Google Scholar 

  • Williams CE, Ronald PC (1994) PCR template-DNA isolated quickly from monocot and dicot leaves without tissue homogenization. Nucl Acids Res 22:1917–1918

    Article  PubMed  CAS  Google Scholar 

  • Woo HH, Orbach MJ, Hirsch AM, Hawes MC (1999) Meristem-localized inducible expression of a UDP-glycosyltransferase gene is essential for growth and development in pea and alfalfa. Plant Cell 11:2303–2315

    Article  PubMed  CAS  Google Scholar 

  • Wu YQ, Huang Y (2006) An SSR genetic map of Sorghum bicolor (L.) Moench and its comparison to a published genetic map. Genome 50:84–89

    Google Scholar 

  • Yonemaru J, Ando T, Mizubayashi T, Kasuga S, Matsumoto T, Yano M (2009) Development of genome-wide simple sequence repeat markers using whole-genome shotgun sequences of sorghum (Sorghum bicolor (L.) Moench). DNA Res 16:187–193

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160

    Article  PubMed  CAS  Google Scholar 

  • Yu JM, 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

    Article  PubMed  CAS  Google Scholar 

  • Zhao YL, Dolat A, Steinberger Y, Wang X, Osman A, Xie GH (2009) Biomass yield and changes in chemical composition of sweet sorghum cultivars grown for biofuel. Field Crops Res 111:55–64

    Article  Google Scholar 

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Acknowledgments

This work was supported by the University of Louisiana at Lafayette. We thank Jonathan A. Groomer, Chuanqin Xu and William H. Welsh for technical assistance.

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  1. Department of Biology, University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Yi-Hong Wang

  2. Laboratory of Bioinformatics, Center for Advanced Computer Studies, University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Paul Bible & Rasiah Loganantharaj

  3. Gene Bank, International Crops Research Institute for the Semi Arid Tropics (ICRISAT), Patancheru, Andhra Pradesh, 502 324, India

    Hari D. Upadhyaya

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  1. Yi-Hong Wang
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Correspondence to Yi-Hong Wang.

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Wang, YH., Bible, P., Loganantharaj, R. et al. Identification of SSR markers associated with height using pool-based genome-wide association mapping in sorghum. Mol Breeding 30, 281–292 (2012). https://doi.org/10.1007/s11032-011-9617-3

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