Skip to main content
Log in

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

  • Published:
Molecular Breeding Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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

    Article  CAS  Google Scholar 

  • Ajarayasiri J, Chaiseri S (2008) Comparative study on aroma-active compounds in thai, black and white glutinous rice varieties. Kasetsart J (Nat Sci) 42:715–722

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

  • Ayyangar GNR (1938) Studies in sorghum. J Madras Univ 11:131–143

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Berner DK, Hoff BJ (1986) Inheritance of scent in American long grain rice. Crop Sci 26:876–878. doi:10.2135/cropsci1986.0011183X002600050008x

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bullard RW, Holguin G (1977) Volatile components of unprocessed rice (Oryza sativa L.). J Agric Food Chem 25(1):99–103

    Article  CAS  Google Scholar 

  • Buttery RG, Ling LC, Juliano BO (1982) 2-Acetyl-1-pyrroline: an important aroma component of cooked rice. Chem Ind 958–959

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):515–521

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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):39–44

    CAS  Google Scholar 

  • Elangovan M (2008) Kharif sorghum germplasm collection from Bundelkhand regions of Madhya Pradesh. Sorghum Germplasm Exploration Report. pp. 8.

  • 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 45–108

  • 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 39

  • Girard B, Kopp TG (1998) Physicochemical characteristics of selected sweet cherry cultivars. J Agric Food Chem 46(2):471–476. doi:10.1021/jf970646j

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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. 95–100

    Google Scholar 

  • Jambmathan R (1995) Volatile constituents of mold-susceptible and mold-resistant sorghum [Sorghum bicolor (L.) Moench] grains. J Agric Food Chem 43:215–218

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kottur GL (1919) Classification and description of the jowars of the Bombay and Karnataka. Bulletin Number 92, Department of Agriculture, Bombay, India

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lwande W, Bentley MD (1987) Volatiles of Sorghum bicolor seedlings. J Nat Prod 50(5):950–952

    Article  CAS  Google Scholar 

  • 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. 230

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • Murty DS, Nicodemus KD, House LR (1982) Inheritance of basmati and dimpled seed in sorghum. Crop Sci 22:1080–1082

    Article  Google Scholar 

  • Nawar WW (1996) Lipids. In: Fennema O (ed) Food chemistry, 3rd edn. Marcel Dekker, New York, pp. 255–264

    Google Scholar 

  • 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):650–654

    Google Scholar 

  • Prasada KE, Murty DS (1979) A basmati (scented) sorghum from Madhya Pradesh. Curr Sci 48:824–826

    Google Scholar 

  • 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):65–70

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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: 10.1155/2014/918209

  • Sood BC, Siddiq EA (1978) A rapid technique for scent determination in rice. Ind J Genet Plant Breed 38:268–271

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tsugita T (1985) Aroma of cooked rice. Food Rev Int 1(3):497–520. doi:10.1080/87559128509540781

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 31:299–306

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 50:2001–2004

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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):1295–1298

    CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Altafhusain Nadaf.

Electronic supplementary material

ESM 1

(DOCX 28 kb)

ESM 2

(DOCX 272 kb)

ESM 3

(DOCX 1754 kb)

ESM 4

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zanan, R., Khandagale, K., Hinge, V. et al. Characterization of fragrance in sorghum (Sorghum bicolor (L.) Moench) grain and development of a gene-based marker for selection in breeding. Mol Breeding 36, 146 (2016). https://doi.org/10.1007/s11032-016-0582-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-016-0582-8

Keywords

Navigation