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Stability and genetic control of morphological, biomass and biofuel traits under temperate maritime and continental conditions in sweet sorghum (Sorghum bicolour)

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Key message

Eight morphological, biomass and biofuel traits were found with high broad-sense heritability and 18 significant QTLs discovered including one locus controlling the stem juice trait for sorghum grown in Denmark and China. Sweet sorghum with tall plant, fast maturation and high stem Brix content can be bred as a biofuel crop for Northern Europe.


Sweet sorghum (Sorghum bicolour), a native tropical C4 crop, has attracted interest as a bioenergy crop in northern countries due to its juice-rich stem and high biomass production. Little is known about the traits important for its adaptation to high altitude climatic conditions and their genetic controls. Recombinant inbred lines derived from a cross between a sweet and a grain kaoliang sorghum were used in five field trials in Denmark and in China to identify the stability and genetic controls of morphological, biomass and biofuel traits during three consecutive summers with short duration, cool temperatures and long days. Eight out of 15 traits were found with high broad-sense heritability. Strong positive correlations between plant height and biomass traits were observed, while Brix and juice content were under different genetic controls. Using newly developed PAV (presence and absence variant) markers, 53 QTLs were detected, of which 18 were common for both countries, including a locus controlling stem juice (LOD score = 20.5, r 2 = 37.5 %). In Denmark, the heading stage correlated significantly with biomass and morphology traits, and two significant maturity QTLs detected on chromosomes SBI01 and SBI02 co-localised with QTLs previously associated with early-stage chilling tolerance, suggesting that accelerating maturation might be a means of coping with low-temperature stress. Our results suggest that selection for tall and fast maturating sorghum plants combined with high Brix content represents a high potential for breeding bioenergy crop for Northern Europe.

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  1. Bekele WA, Fiedler K, Shiringani A, Schnaubelt D, Windpassinger S, Uptmoor R, Friedt W, Snowdon RJ (2014) Unravelling the genetic complexity of sorghum seedling development under low-temperature conditions. Plant Cell Environ 37:707–723

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

  3. Bickel PJ, Lehmann EL (1975a) Descriptive statistics for nonparametric models. 1. Introduction. Ann Stat 3:1038–1044

  4. Bickel PJ, Lehmann EL (1975b) Descriptive statistics for nonparametric models. 2. Location. Ann Stat 3:1045–1069

  5. 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

  6. 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

  7. Burow G, Burke JJ, Xin ZG, Franks CD (2011) Genetic dissection of early-season cold tolerance in sorghum (Sorghum bicolor (L.) Moench). Mol Breed 28:391–402

  8. Caddel JL, Weibel DE (1971) Effect of photoperiod and pemperature on development of sorghum. Agron J 63:799–803

  9. Chapman A, Pantalone VR, Ustun A, Allen FL, Landau-Ellis D, Trigiano RN, Gresshoff PM (2003) Quantitative trait loci for agronomic and seed quality traits in an F(2) and F(4: 6) soybean population. Euphytica 129:387–393

  10. Childs K, Miller F, Cordonnier-Pratt M, Pratt L, Morgan P, Mullet J (1997) The sorghum photoperiod sensitivity gene, Ma3, encodes a phytochrome B. Plant Physiol 113:611–619

  11. Clerget B, Dingkuhn M, Chantereau J, Hemberger J, Louarn G, Vaksmann M (2004) Does panicle initiation in tropical sorghum depend on day-to-day change in photoperiod? Field Crops Res 88:21–37

  12. Doggett H (1988) Sorghum. 2nd edn. Longman, London

  13. Downes RW (1972) Effect of temperature on phenology and grain yield of Sorghum bicolor. Aust J Agr Res 23:585–594

  14. Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19(11):15

  15. Fehr W (1987) Principales of cultivars development. MacMillan, New York

  16. 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

  17. Franks CD, Burow GB, Burke JJ (2006) A comparison of US and Chinese sorghum germplasm for early season cold tolerance. Crop Sci 46:1371–1376

  18. Goulden CH (1939) Problems in plant selection. Proceedings of 7th International Genetical, Congress Edinburgh, Scotland, pp 132–133

  19. Grafius JE (1965) Short cuts in plant breeding. Crop Sci 5:377

  20. Harlan JR, Dewet JMJ (1972) Simplified classification of cultivated sorghum. Crop Sci 12:172–176

  21. Hart GE, Schertz KF, Peng Y, Syed NH (2001) Genetic mapping of Sorghum bicolor (L.) Moench QTLs that control variation in tillering and other morphological characters. Theor Appl Genet 103:1232–1242

  22. Hemamalini GS, Shashidhar HE, Hittalmani S (2000) Molecular marker assisted tagging of morphological and physiological traits under two contrasting moisture regimes at peak vegetative stage in rice (Oryza sativa L.). Euphytica 112:69–78

  23. Hittalmani S, Shashidhar HE, Bagali PG, Huang N, Sidhu JS, Singh VP, Khush GS (2002) Molecular mapping of quantitative trait loci for plant growth, yield and yield related traits across three diverse locations in a doubled haploid rice population. Euphytica 125:207–214

  24. Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135:205–211

  25. Jansen RC (1994) Controlling the type-I and type-II errors in mapping quantitative trait loci. Genetics 138:871–881

  26. Jansen RC, Stam P (1994) High-resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455

  27. Jo YD, Park J, Kim J, Song W, Hur CG, Lee YH, Kang BC (2011) Complete sequencing and comparative analyses of the pepper (Capsicum annuum L.) plastome revealed high frequency of tandem repeats and large insertion/deletions on pepper plastome. Plant Cell Rep 30:217–229

  28. Klein RR, Rodriguez-Herrera R, Schlueter JA, Klein PE, Yu ZH, Rooney WL (2001) Identification of genomic regions that affect grain-mould incidence and other traits of agronomic importance in sorghum. Theor Appl Genet 102:307–319

  29. 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

  30. Kresovich S, Barbazuk B, Bedell JA, Borrell A, Buell CR, Burke J, Clifton S, Cordonnier-Pratt MM, Cox S, Dahlberg J, Erpelding J, Fulton TM, Fulton B, Fulton L, Gingle AR, Hash CT, Huang YH, Jordan D, Klein PE, Klein RR, Magalhaes J, McCombie R, Moore P, Mullet JE, Ozias-Akins P, Paterson AH, Porter K, Pratt L, Roe B, Rooney W, Schnable PS, Stelly DM, Tuinstra M, Ware D, Warek U, Workshop SGP (2005) Toward sequencing the sorghum genome. A US National Science Foundation-Sponsored Workshop Report. Plant Physiol 138:1898–1902

  31. Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119:561–601

  32. Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

  33. Lê SJ, Husson JF (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18

  34. Lebreton C, Lazicjancic V, Steed A, Pekic S, Quarrie SA (1995) Identification of Qtl for drought responses in maize and their use in testing causal relationships between traits. J Exp Bot 46:853–865

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

  36. Lu QS, Dahlberg JA (2001) Chinese sorghum genetic resources. Econ Bot 55:401–425

  37. Maiti RK (1996) Germination and seedling establishment. Sorghum science Science Publishers Inc, Lebanon, pp 41–98

  38. Maulana F, Tesso TT (2013) Cold temperature episode at seedling and flowering stages reduces growth and yield components in sorghum. Crop Sci 53:564–574

  39. Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, Dugas DV, Klein PE, Mullet JE (2011) Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci USA 108:16469–16474

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

  41. Murray SC, Sharma A, Rooney WL, Klein PE, Mullet JE, Mitchell SE, Kresovich S (2008b) Genetic improvement of sorghum as a biofuel feedstock: I. QTL for stem sugar and grain nonstructural carbohydrates. Crop Sci 48:2165

  42. Natoli A, Gorni C, Chegdani F, Marsan PA, Colombi C, Lorenzoni C, Marocco A (2002) Identification of QTLs associated with sweet sorghum quality. Maydica 47:311–322

  43. Osuna-Ortega J, Mendoza-Castillo MD, Mendoza-Onofre LE (2003) Sorghum cold tolerance, pollen production, and seed yield in the central high valleys of Mexico. Maydica 48:125–132

  44. Pao C, Morgan P (1986) Genetic regulation of development in Sorghum bicolar: I. Role of the maturity genes. Plant Physiol 82:575–580

  45. Parh DK, Jordan DR, Aitken EA, Mace ES, Jun-ai P, McIntyre CL, Godwin ID (2008) QTL analysis of ergot resistance in sorghum. Theor Appl Genet 117:369–382

  46. Paterson AH, Lin YR, Li Z, Schertz KF, Doebley JF, Pinson SR, Liu SC, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic Loci. Science 269:1714–1718

  47. Peacock JM (1982) Response and Tolerance of Sorghum to Temperature Stress. Sorghum in the Eighties: Proceedings of the International Symposium on Sorghum. International Crops Research Institute for the Semi-Arids Tropics, Patancheru, A.P., India, ICRISAT

  48. Pennisi E (2009) Plant genetics. How sorghum withstands heat and drought. Science 323:573

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

  50. Prasad PVV, Pisipati SR, Mutava RN, Tuinstra MR (2008) Sensitivity of grain sorghum to high temperature stress during reproductive development. Crop Sci 48:1911–1917

  51. Quarrie SA, Laurie DA, Zhu JH, Lebreton C, Semikhodskii A, Steed A, Witsenboer H, Calestani C (1997) QTL analysis to study the association between leaf size and abscisic acid accumulation in droughted rice leaves and comparisons across cereals. Plant Mol Biol 35:155–165

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

  53. Rami JF, Dufour P, Trouche G, Fliedel G, Mestres C, Davrieux F, Blanchard P, Hamon P (1998) Quantitative trait loci for grain quality, productivity, morphological and agronomical traits in sorghum (Sorghum bicolor L. Moench). Theor Appl Genet 97:605–616

  54. Ritter KB, Jordan DR, Chapman SC, Godwin ID, Mace ES, Lynne McIntyre C (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

  55. Rooney WL, Aydin S (1999) Genetic control of a photoperiod-sensitive response in Sorghum bicolor (L.) Moench. Crop Sci 39:397–400

  56. Sala RG, Andrade FH, Camadro EL, Cerono JC (2006) Quantitative trait loci for grain moisture at harvest and field grain drying rate in maize (Zea mays L.). Theor Appl Genet 112:462–471

  57. Shen X, Liu Z-Q, Mocoeur A, Xia Y, Jing H-C (2015) PAV markers in Sorghum bicolour: genome pattern, affected genes and pathways, and genetic linkage map construction. Theor Appl Genet 128:623–637

  58. Shiringani AL, Friedt W (2011) QTL for fibre-related traits in grain × sweet sorghum as a tool for the enhancement of sorghum as a biomass crop. Theor Appl Genet 123:999–1011

  59. Shiringani AL, Frisch M, Friedt W (2010) Genetic mapping of QTLs for sugar-related traits in a RIL population of Sorghum bicolor L. Moench. Theor Appl Genet 121:323–336

  60. Srinivas G, Satish K, Madhusudhana R, Reddy RN, Mohan SM, Seetharama N (2009) Identification of quantitative trait loci for agronomically important traits and their association with genic-microsatellite markers in sorghum. Theor Appl Genet 118:1439–1454

  61. Tiryaki I, Andrews DJ (2001) Germination and seedling cold tolerance in sorghum: I. Evaluation of rapid screening methods. Agron J 93:1386–1391

  62. Van Ooijen JW (2004) MapQTL® 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma B.V., Wageningen

  63. Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2004) MapQTLr Software

  64. Veldboom LR, Lee M, Woodman WL (1994) Molecular marker-facilitated studies in an elite maize population. 1. Linkage analysis and determination of QTL for morphological traits. Theor Appl Genet 88:7–16

  65. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New York

  66. Xu W, Subudhi PK, Crasta OR, Rosenow DT, Mullet JE, Nguyen NT (2000) Molecular mapping of QTLs confering stay-green in grain sorghum (Sorghum bicolor L. Moench). Genome 43:461–469

  67. Yano M, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153

  68. Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet 95:1025–1032

  69. Yu JM, Tuinstra MR (2001) Genetic analysis of seedling growth under cold temperature stress in grain sorghum. Crop Sci 41:1438–1443

  70. Yu CZ, Zhai GW, Zou GH, Tao YZ, Wang H (2010) Assessment of genetic diversity among 41 sorghum varieties using SSR markers. Jiangsu J Agric Sci 2:007

  71. Zhang YM, Xu SZ (2004) Mapping quantitative trait loci in F-2 incorporating phenotypes of F-3 progeny. Genetics 166:1981–1993

  72. Zheng LY, Guo XS, He B, Sun LJ, Peng Y, Dong SS, Liu TF, Jiang SY, Ramachandran S, Liu CM, Jing HC (2011) Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol 12:R114

  73. Zou GH, Zhai GW, Feng Q, Yan S, Wang A, Zhao Q, Shao JF, Zhang ZP, Zou JQ, Han B, Tao YZ (2012) Identification of QTLs for eight agronomically important traits using an ultra-high-density map based on SNPs generated from high-throughput sequencing in sorghum under contrasting photoperiods. J Exp Bot 63:5451–5462

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The Sino-Danish Centre for Sustainable Energy, Aarhus, Denmark is greatly acknowledged for its financial support to SKR. Anders Kristian Nørgaard, Louise de Bang, Florian Leplat and Maya Mayek are thanked. We thank the operational staffs at the University of Copenhagen for their assistance with field experiments and phenotyping work. Members of Hai-Chun Jing’s Lab are thanked for their help in the field and for making the collaboration so pleasant. Thanks to Philip Steffan for his assistance with statistical analysis and model construction. This work is partially supported by the grant awarded to Hai-Chun Jing by CNSF (31271797) and MOST (2013BAD22B01).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Correspondence to Søren K. Rasmussen or Hai-Chun Jing.

Additional information

Anne Mocoeur, Yu-Miao Zhang and Zhi-Quan Liu have contributed equally to this work.

Communicated by H. H. Geiger.

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Mocoeur, A., Zhang, Y., Liu, Z. et al. Stability and genetic control of morphological, biomass and biofuel traits under temperate maritime and continental conditions in sweet sorghum (Sorghum bicolour). Theor Appl Genet 128, 1685–1701 (2015). https://doi.org/10.1007/s00122-015-2538-5

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  • Sorghum
  • Sweet Sorghum
  • Negative Additive Effect
  • Stable QTLs
  • Head Stage