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Molecular Breeding

, 36:146 | Cite as

Characterization of fragrance in sorghum (Sorghum bicolor (L.) Moench) grain and development of a gene-based marker for selection in breeding

  • Rahul Zanan
  • Kiran Khandagale
  • Vidya Hinge
  • M. Elangovan
  • Robert J. Henry
  • Altafhusain NadafEmail author
Article

Abstract

Fragrance is one of the most important and valued quality characters in sorghum and other foods and attracts a premium price in local and global trade. The allele of the SbBADH2 gene in fragrant sorghum cultivar E228 was characterized. A 1441 bp deletion extending from exon 13 to 15 was found rather than a deletion from exon 12 to 15 as had been reported earlier. This allowed the development and validation of a new perfect PCR-based marker for identification of fragrant sorghum accessions in breeding. The concentration of 2-acetyl-1-pyrroline (2AP) in the grain of this cultivar was estimated to be 6.5 ± 0.4 ppb using headspace solid-phase microextraction (HS-SPME) coupled with GC-MS. Flavor components of fragrant sorghum accession E228 (IC 568489) were analyzed and compared with the non-fragrant M35-1 cultivar. PCA analysis revealed that 2AP, benzothiazole, 2,3,5-trimethylpyridine, (1E)-1-ethylidene-1H-indene, cedrene, 2,4-bis(2-methyl-2-propanyl)phenol, 2-hexyl-1-octanol, and 2-butyl-1-octanol were among 25 compounds that were found in sorghum grain that may be contributing toward the aroma of fragrant sorghum. Proline and methylglyoxal contents were found to be higher in E228 than in M35-1, while SbBADH2 expression in E228 was half that in M35-1, suggesting a similar 2AP biosynthetic mechanism to that found in fragrant rice and soybean.

Keywords

Fragrant sorghum Volatile compounds 2-Acetyl-1-pyrroline biosynthesis BADH2 SbBADH2-EX13-15 

Notes

Acknowledgments

RZ acknowledges the Science and Engineering Research Board (SERB), Department of Science and Technology, India (Sanction No. SR/FT/LS-350/2012) and VH the WOS-A scheme of Department of Science and Technology, India (Sanction No. SR/WOS-A/LS433/2011(G)) for financial assistance. KK acknowledges Council of Scientific and Industrial Research (CSIR), India (Sanction No. 09/137/(0541)/2012-EMR-1) for the award of SRF.

Supplementary material

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References

  1. Adams A, De Kimpe N (2007) Formation of pyrazines and 2-acetyl-1-pyrroline by Bacillus cereus. Food Chem 101:1230–1238. doi: 10.1016/j.foodchem.2006.03.027 CrossRefGoogle Scholar
  2. Ajarayasiri J, Chaiseri S (2008) Comparative study on aroma-active compounds in thai, black and white glutinous rice varieties. Kasetsart J (Nat Sci) 42:715–722Google Scholar
  3. Amarawathi Y, Singh R, Singh AK, Singh VP, Mohapatra T, Sharma TR, Singh NK (2008) Mapping of quantitative trait loci for basmati quality traits in rice (Oryza sativa L.). Mol Breed 21:49–65. doi: 10.1007/s11032-007-9108-8 CrossRefGoogle Scholar
  4. AVRDC (2003) AVRDC progress report 2002. AVRDC-The World Vegetable Center, Shanhua http://203.64.245.61/fulltext_pdf/AR/2002.pdf. Accessed 21 March 2015
  5. Ayyangar GNR (1938) Studies in sorghum. J Madras Univ 11:131–143Google Scholar
  6. Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. doi: 10.1007/BF00018060 CrossRefGoogle Scholar
  7. Beaulieu JC, Lea JM (2006) Characterization and semiquantitative analysis of volatiles in seedless watermelon varieties using solid-phase microextraction. J Agric Food Chem 54(20):7789–7793. doi: 10.1021/jf060663l CrossRefPubMedGoogle Scholar
  8. Bergman CJ, Delgado JT, Bryant R, Grimm C, Cadwallader KR, Webb BD (2000) Rapid gas chromatographic technique for quantifying 2-acetyl-1-pyrroline and hexanal in rice (Oryza sativa L.). Cereal Chem 77:454–458. doi: 10.1094/CCHEM.2000.77.4.454 CrossRefGoogle Scholar
  9. Berner DK, Hoff BJ (1986) Inheritance of scent in American long grain rice. Crop Sci 26:876–878. doi: 10.2135/cropsci1986.0011183X002600050008x CrossRefGoogle Scholar
  10. Bradbury LMT, Gillies SA, Brushett DJ, Waters DLE, Henry RJ (2008) Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Mol Biol 68:439–449. doi: 10.1007/s11103-008-9381-x CrossRefPubMedGoogle Scholar
  11. Bradbury LMT, Henry RJ, Jin Q, Russell FRF, Waters DLE (2005) A perfect marker for fragrance genotyping in rice. Mol Breed 16:279–283. doi: 10.1007/s11032-005-0776-y CrossRefGoogle Scholar
  12. Bryant RJ, Mcclung AM (2011) Volatile profiles of aromatic and non-aromatic rice cultivars using SPME/GC–MS. Food Chem 124:501–513. doi: 10.1016/j.foodchem.2010.06.061 CrossRefGoogle Scholar
  13. Bullard RW, Holguin G (1977) Volatile components of unprocessed rice (Oryza sativa L.). J Agric Food Chem 25(1):99–103CrossRefGoogle Scholar
  14. Buttery RG, Ling LC, Juliano BO (1982) 2-Acetyl-1-pyrroline: an important aroma component of cooked rice. Chem Ind 958–959Google Scholar
  15. Buttery RG, Ling LC, Juliano BO, Turnbauhg JG (1983) Cooked rice aroma and 2-acetyl-1-pyrroline. J Agric Food Chem 31:823–826. doi: 10.1021/jf00118a036 CrossRefGoogle Scholar
  16. Chen S, Yang Y, Shi W, Ji Q, He F, Zhang Z, Cheng Z, Liu X, Xu M (2008) Badh2, encoding betaine aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell 20:1850–1861. doi: 10.1105/tpc.108.058917 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chughtai MFJ, Pasha I, Anjum FM, Nasir MA (2015) Characterization of sorghum and millet with special reference to fatty acid and volatile profile. TURJAF 3(7):515–521Google Scholar
  18. Dai do N, Thang TD, Ogunwande IA (2014) Chemical composition of essential oils from the leaves and stem barks of Vietnamese species of Polyalthia harmandii, Polyalthia jucunda and Polyalthia thorelii. Nat Prod Res 28(8):555–562. doi: 10.1080/14786419.2014.886209 CrossRefPubMedGoogle Scholar
  19. Dong X, Wang Y, Sun Y (2011) Comparative analysis of chemical compositions of volatile oils from Rhizoma Pinelliae Fermentata and its unfermented production. Asian J Tradit Med 6(1):39–44Google Scholar
  20. Elangovan M (2008) Kharif sorghum germplasm collection from Bundelkhand regions of Madhya Pradesh. Sorghum Germplasm Exploration Report. pp. 8.Google Scholar
  21. Elangovan M, Tonapi VA (2015) Sorghum and millet genetic resources. In: Tonapi VA, Patil JV (Eds.) Millets – Ensuring Climate Resilience and Nutritional Security, Daya Publishing House – A division of Astral International Pvt. Ltd. pp 45–108Google Scholar
  22. Fushimi T, Masuda R (2001) 2-Acetyl-1-pyrroline concentration of the vegetable soybean. In: Lumpkin T, Shanmugasundaram S (eds) Proceeding of the 2nd international vegetable soybean conference. Washington State University, Pullman, p 39Google Scholar
  23. Girard B, Kopp TG (1998) Physicochemical characteristics of selected sweet cherry cultivars. J Agric Food Chem 46(2):471–476. doi: 10.1021/jf970646j CrossRefPubMedGoogle Scholar
  24. Grimm CC, Bergman C, Delgado JT, Bryant R (2001) Screening for 2-acetyl-1-pyrroline in the headspace of Rice using SPME/GC-MS. J Agric Food Chem 49:245–249. doi: 10.1021/jf0008902 CrossRefPubMedGoogle Scholar
  25. Hinge V, Patil H, Nadaf A (2015) Comparative characterization of aroma volatiles and related gene expression analysis at vegetative and mature stages in basmati and non-basmati rice (Oryza sativa L.) cultivars. Appl Biochem Biotech 178(4):619–639. doi: 10.1007/s12010-015-1898-2 CrossRefGoogle Scholar
  26. Hinge V, Patil HB, Nadaf AB (2016) Aroma volatile analyses and 2AP characterization at various developmental stages in basmati and non-basmati scented rice (Oryza sativa L.) cultivars. Rice. doi: 10.1186/s12284-016-0113-6 PubMedPubMedCentralGoogle Scholar
  27. Huang TC, Huang YW, Hung HJ, Ho CT, Wu ML (2007) Δ1-Pyrroline-5-carboxylic acid formed by proline dehydrogenase from the Bacillus subtilis ssp. natto expressed in Escherichia coli as a precursor for 2-acetyl-1-pyrroline. Agric Food Chem 55:5097–5102. doi: 10.1021/jf0700576 CrossRefGoogle Scholar
  28. Huang TC, Teng CS, Chang JL, Chuang HS, Ho CT, Wu ML (2008) Biosynthetic mechanism of 2-acetyl-1-pyrroline and its relationship with Δ1-pyrroline-5-carboxylic acid and methylglyoxal in aromatic rice (Oryza sativa L.) callus. Agric Food Chem 56:7399–7404. doi: 10.1021/jf8011739 CrossRefGoogle Scholar
  29. Hussain A, Naqvi SHM, Hammerschimdt FJ (1987) Isolation and identification of volatile components from basmati rice (Oryza sativa L). In: Martens M, Dalen GA, Russwurm H (eds) Flavor science and technology. John Wiley & Sons, New York & Toronto pp, pp. 95–100Google Scholar
  30. Jambmathan R (1995) Volatile constituents of mold-susceptible and mold-resistant sorghum [Sorghum bicolor (L.) Moench] grains. J Agric Food Chem 43:215–218CrossRefGoogle Scholar
  31. Joshi R, Sharma P, Sharma V, Prasad R, Sud RK, Gulati A (2013) Analysis of the essential oil of large cardamom (Amomum subulatum Roxb.) growing in different agro-climatic zones of Himachal Pradesh, India. J Sci Food Agric 93(6):1303–1309. doi: 10.1002/jsfa.5886 CrossRefPubMedGoogle Scholar
  32. Juwattanasomran R, Somta P, Kaga A, Chankaew S, Shimizu T, Sorajjapinun W, Srinives P (2012) Identification of a new fragrance allele in soybean and development of its functional marker. Mol Breed 29:13–21. doi: 10.1007/s11032-010-9523-0 CrossRefGoogle Scholar
  33. Kottur GL (1919) Classification and description of the jowars of the Bombay and Karnataka. Bulletin Number 92, Department of Agriculture, Bombay, IndiaGoogle Scholar
  34. Kovach MJ, Calingacion MN, Fitzgerald MA, Mccouch SR (2009) The origin and evolution of fragrance in rice (Oryza sativa L.). PNAS 106:14444–14449. doi: 10.1073/pnas.0904077106 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lam HS, Proctor A (2003) Milled rice oxidation volatiles and odor development. J Food Sci 68:2676–2681. doi: 10.1111/j.1365-2621.2003.tb05788.x CrossRefGoogle Scholar
  36. Liu X, Park JH, Abd El-Aty AM, Assayed ME, Shimoda M, Shim JH (2013) Isolation of volatiles from Nigella sativa seeds using microwave-assisted extraction: effect of whole extracts on canine and murine CYP1A. Biomed Chromatogr 27(7):938–945. doi: 10.1002/bmc.2887 CrossRefPubMedGoogle Scholar
  37. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408. doi: 10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  38. Lwande W, Bentley MD (1987) Volatiles of Sorghum bicolor seedlings. J Nat Prod 50(5):950–952CrossRefGoogle Scholar
  39. Mahajan RK, Sapra RL, Srivastava U, Singh M, Sharma GD (2000) Minimal descriptors (for characterization and evaluation) of agri-horticultural crops (part I). National Bureau of Plant Genetic Resources, New Delhi, p. 230Google Scholar
  40. Mahatheeranont S, Keawsaard S, Dumri K (2001) Quantification of the rice aroma compound, 2-acetyl-1-pyrroline, in uncooked Khao Dawk Mali 105 brown rice. J Agric Food Chem 49(2):773–779. doi: 10.1021/jf000885y CrossRefPubMedGoogle Scholar
  41. Mathure SV, Jawali N, Thengane RJ, Nadaf AB (2014) Comparative quantitative analysis of headspace volatiles and their association with BADH2 marker in non-basmati scented, basmati and non-scented rice (Oryza sativa L.) cultivars of India. Food Chem 142:383–391. doi: 10.1016/j.foodchem.2013.07.066 CrossRefPubMedGoogle Scholar
  42. Mathure SV, Wakte KV, Jawali N, Nadaf AB (2010) Quantification of 2-acetyl-1-pyrroline and other rice aroma volatiles among Indian scented rice cultivars by HS-SPME/GC-FID. Food Anal Methods. doi: 10.1007/s12161-010-9171-3 Google Scholar
  43. Monsoor MA, Proctor A (2004) Volatile component analysis of commercially milled head and broken rice. J Food Sci 69(8):C632–C636. doi: 10.1111/j.1365-2621.2004.tb09911.x CrossRefGoogle Scholar
  44. Murty DS, Nicodemus KD, House LR (1982) Inheritance of basmati and dimpled seed in sorghum. Crop Sci 22:1080–1082CrossRefGoogle Scholar
  45. Nawar WW (1996) Lipids. In: Fennema O (ed) Food chemistry, 3rd edn. Marcel Dekker, New York, pp. 255–264Google Scholar
  46. Pattanashetti SK, Biradar BD, Salimath PM (2005) Comparative performance of Milo v/s Maldandi based rabi sorghum hybrids in the northern dry zone of Karnataka. Karnataka J Agric Sci 18(3):650–654Google Scholar
  47. Prasada KE, Murty DS (1979) A basmati (scented) sorghum from Madhya Pradesh. Curr Sci 48:824–826Google Scholar
  48. Rzama A, Arreguy-San-Miguel B, Ettalibi M (2002) Lipids metabolites and essential oil from the green alga Chara vulgaris. Actes Inst Agron Vet (Maroc) 22(2):65–70Google Scholar
  49. Sánchez L, Albores-Velasco M, Rio F (1991) Volatile compounds of Sargentia gregii. Phytochemistry 30(6):1915–1916. doi: 10.1016/0031-9422(91)85039-3 CrossRefGoogle Scholar
  50. Sarıkahya NB, Kayce P, Halay E, Göktürk RS, Sümbül H, Kırmızıgül S (2013) Phytochemical analysis of the essential oils of 10 endemic Cephalaria species from Turkey. Nat Prod Res 27(9):830–833. doi: 10.1080/14786419.2012.701216 CrossRefPubMedGoogle Scholar
  51. Sassi AB, Skhiri FH, Chraief I, Bourgougnon N, Hammami M, Aouni M (2014) Essential oils and crude extracts from Chrysanthemum trifurcatum leaves, stems and roots: chemical composition and antibacterial activity. J Oleo Sci 63(6):607–617. doi: 10.5650/jos.ess13228 CrossRefPubMedGoogle Scholar
  52. Shao GN, Tang A, Tang SQ, Luo J, Jiao GA, Wu JL, Hu PS (2011) A new deletion mutation of fragrant gene and the development of three molecular markers for fragrance in rice. Plant Breed 130:172–176. doi: 10.1111/j.1439-0523.2009.01764.x CrossRefGoogle Scholar
  53. Shi WW, Yang Y, Chen SH, Xu ML (2008) Discovery of a new fragrance allele and the development of functional markers for the breeding of fragrant rice varieties. Mol Breed 22:185–192. doi: 10.1007/s11032-008-9165-7 CrossRefGoogle Scholar
  54. Shi Y, Zhao G, Xu X, Li J (2013) Discovery of a new fragrance allele and development of functional markers for identifying diverse fragrant genotypes in rice. Mol Breed. doi: 10.1007/s11032-013-9986-x PubMedPubMedCentralGoogle Scholar
  55. Shimoda M, Shiratsuchi H, Nakada Y, Wu Y, Osajima Y (1996) Identification and sensory characterization of volatile flavor compounds in sesame seed oil. J Agric Food Chem 44:3309–3912. doi: 10.1021/jf960115f Google Scholar
  56. Singh S, Das SS, Singh G, Schuff C, de Lampasona MP, Catalán CA (2014) Composition, in vitro antioxidant and antimicrobial activities of essential oil and oleoresins obtained from black cumin seeds (Nigella sativa L.). Biomed Res Int 918209. doi: 10.1155/2014/918209Google Scholar
  57. Sood BC, Siddiq EA (1978) A rapid technique for scent determination in rice. Ind J Genet Plant Breed 38:268–271Google Scholar
  58. Sugisawa H, Nakamura K, Tamura H (1990) The aroma profile of the volatiles in marine green algae (Ulva pertusa). Food Rev Int 6(4):573–589. doi: 10.1080/87559129009540893 CrossRefGoogle Scholar
  59. Suvarnalatha G, Narayan MS, Ravishankar GA, Venkataraman LV (1994) Flavour production in plant cell cultures of basmati rice (Oryza sativa L). J Sci Food Agr 66(4):439–442. doi: 10.1002/jsfa.2740660403 CrossRefGoogle Scholar
  60. Thimmaraju R, Bhagyalakshmi N, Narayan MS, Venkatachalam L, Ravishankar GA (2005) In vitro culture of Pandanus amaryllifolius and enhancement of 2-acetyl-1-pyrroline, the major flavouring compound of aromatic rice, by precursor feeding of L-proline. Sci Food Agric 85:2527–2534. doi: 10.1002/jsfa.2286 CrossRefGoogle Scholar
  61. Tsugita T (1985) Aroma of cooked rice. Food Rev Int 1(3):497–520. doi: 10.1080/87559128509540781 CrossRefGoogle Scholar
  62. Wakte KV, Kad TD, Zanan RL, Nadaf AB (2011) Mechanism of 2-acetyl-1-pyrroline biosynthesis in Bassia latifolia Roxb. Flowers Physiol Mol Biol Plants 17(3):231–237. doi: 10.1007/s12298-011-0075-5 CrossRefPubMedGoogle Scholar
  63. Wanchana S, Kamolsukyunyong W, Ruengphayak S, Toojinda T, Tragoonrung S, Vanavichit A (2005) A rapid construction of a physical contig across a 4.5 cM region for rice grain aroma facilitates marker enrichment for positional cloning. Sci Asia 31:299–306CrossRefGoogle Scholar
  64. Widjaja R, Craske JD, Wootton M (1996) Comparative studies on volatile components of non-fragrant and fragrant Rices. J Sci Food Agri 70:151–161. doi: 10.1002/(SICI)1097-0010(199602)70:2<151::AID-JSFA478>3.0.CO;2-U CrossRefGoogle Scholar
  65. Wild R, Ooi L, Srikanth V, Münch G (2012) A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-L-cysteine assay. Anal Bioanal Chem 403:2577–2581. doi: 10.1007/s00216-012-6086-4 CrossRefPubMedGoogle Scholar
  66. Withycombe DA, Lindsay RC, Stuiber DA (1978) Isolation and identification of volatile components from wild rice grain (Zizania aquatica). J Agric Food Chem 26(4):816–822. doi: 10.1021/jf60218a052 CrossRefGoogle Scholar
  67. Wu ML, Chou KL, Wu CR, Chen JK, Huang TC (2009) Characterization and the possible formation mechanism of 2-acetyl-1-pyrroline in aromatic vegetable soybean (Glycine max L.). J Food Sci 74(5):192–197. doi: 10.1111/j.1750-3841.2009.01166.x CrossRefGoogle Scholar
  68. Yadav SK, Singla-Pareek SL, Ray M, Sopory SK (2005) Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. Biochem Biophys Res Commun 337:61–67. doi: 10.1016/j.bbrc.2005.08.263 CrossRefPubMedGoogle Scholar
  69. Yajima I, Yani T, Nakamura M, Sakakibara H, Hayashi K (1979) Volatile flavor components of cooked Kaorimai (scented rice, O. sativa japonica). Agri Bio Chem 43:2425–2429. doi: 10.1080/00021369.1979.10863850 Google Scholar
  70. Yang DS, Lee KS, Jeong OY, Kim KJ, Kays SJ (2008) Characterization of volatile aroma compounds in cooked black rice. J Agric Food Chem 56:235–240. doi: 10.1021/jf072360c CrossRefPubMedGoogle Scholar
  71. Yoshihashi T (2002a) Quantitative analysis on 2-acetyl-1-pyrroline of aromatic rice by stable isotope dilution method and model studies on its formation during cooking. Food Sci 67(2):619–622. doi: 10.1111/j.1365-2621.2002.tb10648.x CrossRefGoogle Scholar
  72. Yoshihashi T, Huong NTT, Inatomi H (2002b) Precursors of 2-acetyl-1-pyrroline, a potent flavour compound of an aromatic rice variety. Agri Food Chem 50:2001–2004CrossRefGoogle Scholar
  73. Yu J, Wang C, Wang Y, Yang Z (2011) Deoxy-liquefaction products obtained from Crofton weed at different temperatures. J Anal Appl Pyrol 92:68–75. doi: 10.1016/j.jaap.2011.04.009 CrossRefGoogle Scholar
  74. Yundaeng C, Prakit S, Sithichoke T, Sugunya W, Peerasak S (2013) Gene discovery and functional marker development for fragrance in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet. doi: 10.1007/s00122-013-2180-z PubMedGoogle Scholar
  75. Zhang Y, Wang Z (2010) Comparative analysis of essential oil components of two Pinus species from Taibai Mountain in China. Nat Prod Commun 5(8):1295–1298PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Rahul Zanan
    • 1
  • Kiran Khandagale
    • 1
  • Vidya Hinge
    • 1
  • M. Elangovan
    • 2
  • Robert J. Henry
    • 3
  • Altafhusain Nadaf
    • 1
    Email author
  1. 1.Department of BotanySavitribai Phule Pune UniversityPuneIndia
  2. 2.ICAR-Indian Institute of Millets ResearchHyderabadIndia
  3. 3.Queensland Alliance for Agriculture and Food InnovationUniversity of QueenslandBrisbaneAustralia

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