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A genomics and multi-platform metabolomics approach to identify new traits of rice quality in traditional and improved varieties

Abstract

Using a novel approach combining four complementary metabolomic and mineral platforms with genome-wide genotyping at 1536 single nucleotide polymorphism (SNP) loci, we have investigated the extent of biochemical and genetic diversity in three commercially-relevant waxy rice cultivars important to food production in the Lao People’s Democratic Republic (PDR). Following cultivation with different nitrogen fertiliser regimes, multiple metabolomic data sets, including minerals, were produced and analysed using multivariate statistical methods to reveal the degree of similarity between the genotypes and to identify discriminatory compounds supported by multiple technology platforms. Results revealed little effect of nitrogen supply on metabolites related to quality, despite known yield differences. All platforms revealed unique metabolic signatures for each variety and many discriminatory compounds could be identified as being relevant to consumers in terms of nutritional value and taste or flavour. For each platform, metabolomic diversity was highly associated with genetic distance between the varieties. This study demonstrates that multiple metabolomic platforms have potential as phenotyping tools to assist breeders in their quest to combine key yield and quality characteristics. This better enables rice improvement programs to meet different consumer and farmer needs, and to address food security in rice-consuming countries.

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References

  1. Allwood, J. W., Erban, A., de Koning, S., Dunn, W., Luedemann, A., Lommen, A., et al. (2009). Inter-laboratory reproducibility of fast gas chromatography-electron impact-time of flight mass spectrometry (GC-EI-OF/MS) based plant metabolomics. Metabolomics, 5, 479–496.

    PubMed  Article  CAS  Google Scholar 

  2. Association, A. D. (2004). Nutrition principles and recommendations in diabetes. Diabetes Care, 27(suppl 1), s36. doi:10.2337/diacare.27.2007.S36.

    Google Scholar 

  3. Baker, D. H. (2005). Comparative nutrition and metabolism: Explication of open questions with emphasis on protein and amino acids. Proceedings of the National Academy of Sciences, 102(50), 17897–17902. doi:10.1073/pnas.0509317102.

    Article  CAS  Google Scholar 

  4. Boualaphanh, C., Calingacion, M., Jothityangkoon, D., Sanitchon, J., Cuevas, R., & Fitzgerald, M. (2011). Yield and quality of non-aromatic and aromatic Lao rice in response to nitrogen fertilizer. Science Asia, 37, 89–97. doi:10.2306/scienceasia1513-1874.2011.37.089.

    Article  CAS  Google Scholar 

  5. Bouché, N., & Fromm, H. (2004). GABA in plants: Just a metabolite? Trends in Plant Science, 9(3), 110–115.

    PubMed  Article  Google Scholar 

  6. Bounphanousay, C. (2007). Use of phenotypic characters and DNA profiling for classification of the genetic diversity in black glutinous rice of the Lao PDR. Thailand: Khon Kaen University.

    Google Scholar 

  7. Bounphanousay, C., Appa Rao, S., Kanyavong, K., Sengthong, B., Schiller, J. M., & Jackson, M. T. (2000). Conservation of Lao rice germplasm at the International Rice Genebank, Part 5 (p. 22). Los Banos, Philippines: IRRI.

    Google Scholar 

  8. Bradbury, L., Gillies, S., Brushett, D., Waters, D., & Henry, R. (2008). Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Molecular Biology, 68(4), 439–449.

    PubMed  Article  CAS  Google Scholar 

  9. Butsat, S., & Siriamornpun, S. (2010). Antioxidant capacities and phenolic compounds of the husk, bran and endosperm of Thai rice. Food Chemistry, 119(2), 606–613.

    Article  CAS  Google Scholar 

  10. Champagne, E. T., Bett-Garber, K. L., Fitzgerald, M. A., Grimm, C., Lea, J., Ohtsubo, K., et al. (2010). Important sensory properties differentiating premium rice varieties. Rice, 3, 270–281.

    Article  Google Scholar 

  11. Cuevas, R., Daygon, V., Corpuz, H., Waters, D. L. E., Reinke, R. F., & Fitzgerald, M. A. (2010). Melting the secrets of gelatinisation temperature. Functional Plant Biology, 37, 439–447.

    Article  CAS  Google Scholar 

  12. De Kimpe, N., & Keppens, M. (1996). Novel syntheses of the major flavor components of bread and cooked rice. Journal of Agricultural and Food Chemistry, 44(6), 1515–1519.

    Article  Google Scholar 

  13. Dodsworth, J. (1997). How Indochina’s economies took off. Finance and Development, 34(1), 20–23.

    Google Scholar 

  14. Eriksson, L., Johansson, E., Kettaneh-Wold, N., Wikström, C., Trygg, J., & Wold, S. (2006). Multi- and megavariate data analysis; part I: Basic principles and applications (2nd ed.). Umea, Sweden: Umetrics Academy.

    Google Scholar 

  15. Fitzgerald, M. A., Martin, M., Ward, R. M., Park, W. D., & Shead, H. J. (2003). Viscosity of rice flour: A rheological and biological study. Journal of Agricultural and Food Chemistry, 51(8), 2295–2299.

    PubMed  Article  CAS  Google Scholar 

  16. Fitzgerald, M. A., McCouch, S. R., & Hall, R. D. (2009). More than just a grain of rice, the global quest for quality [Review]. Trends in Plant Science, 14(3), 133–139. doi:10.1016/j.tplants.2008.12.004.

    PubMed  Article  CAS  Google Scholar 

  17. Garris, A. J., Tai, T. H., Coburn, J., Kresovich, S., & McCouch, S. R. (2005). Genetic structure and diversity in Oryza sativa L. Genetics, 169, 1631–1638.

    PubMed  Article  CAS  Google Scholar 

  18. Hall, R. D. (2006). Plant metabolomics: From holistic hope, to hype, to hot topic. New Phytologist, 169(3), 453–468.

    PubMed  Article  CAS  Google Scholar 

  19. Hall, R. D., Brouwer, I. D., & Fitzgerald, M. A. (2008). Plant metabolomics and its potential application for human nutrition [Review]. Physiologia Plantarum, 132, 162–175. doi:10.1111/j.1399-3054.2007.00989.x.

    PubMed  CAS  Google Scholar 

  20. Hansen, T., Laursen, K., Persson, D., Pedas, P., Husted, S., & Schjoerring, J. (2009). Micro-scaled high-throughput digestion of plant tissue samples for multi-elemental analysis. Plant Methods, 5, 12.

    PubMed  Article  Google Scholar 

  21. Heinemann, R. J. B., Xu, Z., Godber, J. S., & Lanfer-Marquez, U. M. (2008). Tocopherols, tocotrienols, and γ-oryzanol contents in japonica and indica subspecies of rice (Oryza sativa L.) cultivated in Brazil. Cereal Chemistry, 85(2), 243–247.

    Article  CAS  Google Scholar 

  22. Hughes, R., & Carr, A. (2002). A randomized, double-blind, placebo-controlled trial of glucosamine sulphate as an analgesic in osteoarthritis of the knee. Rheumatology, 41(3), 279–284. doi:10.1093/rheumatology/41.3.279.

    PubMed  Article  CAS  Google Scholar 

  23. Hummel, J., Strehmel, N., Selbig, J., Walther, D., & Kopka, J. (2010). Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics, 6, 322–333.

    PubMed  Article  CAS  Google Scholar 

  24. Hyten, D. L., Smith, J. R., Frederick, R. D., Tucker, M. L., Song, Q., & Cregan, P. B. (2009). Bulked segregant analysis using the GoldenGate Assay to locate the Rpp3 locus that confers resistance to soybean rust in soybean. Crop Science, 49(1), 265–271. doi:10.2135/cropsci2008.08.0511.

    Article  CAS  Google Scholar 

  25. Inthapanya, P., Boualaphan, C., Hatsadong, & Schiller, J. M. (2006). The history of lowland rice variety improvements in Laos. In J. M. Schiller, M. B. Chanphengxay, B. Linquist, & S. Appa Rao (Eds.), Rice in Laos (pp. 325–358). Manila: IRRI.

    Google Scholar 

  26. Kerler, J., Vander Ven, J. G. M., & Weenen, H. (1997). α-Acetyl-N-heterocycles in the Maillard reaction [Review]. Food Reviews International, 13(4), 553–575.

    Article  CAS  Google Scholar 

  27. Laursen, K., Hesselhøj Hansen, T., Persson, D., Schjoerring, J., & Husted, S. (2009). Multi-elemental fingerprinting of plant tissue by semi-quantitative ICP-MS and chemometrics. Journal of Analytical Atomic Spectroscopy, 24, 1198–1207.

    Article  CAS  Google Scholar 

  28. Lee, G.-A., Koh, H.-J., Chung, H.-K., Dixit, A., Chung, J.-W., Ma, K.-H., et al. (2009). Development of SNP-based CAPS and dCAPS markers in eight different genes involved in starch biosynthesis in rice. Molecular Breeding, 24(1), 93–101.

    Article  CAS  Google Scholar 

  29. Lommen, A. (2009). MetAlign: Interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Analytical Chemistry, 81(8), 3079–3086.

    PubMed  Article  CAS  Google Scholar 

  30. Luedemann, A., Strassburg, K., Erban, A., & Kopka, J. (2008). TagFinder for the quantitative analysis of gas chromatography—mass spectrometry (GC-MS) based metabolite profiling experiments. Bioinformatics, 24(5), 732–737.

    PubMed  Article  CAS  Google Scholar 

  31. Moing, A., Maucourt, M., Renaud, C., Gaudillère, M., Brouquisse, R., Lebouteiller, B., et al. (2004). Quantitative metabolomic profiling by 1-dimensional 1H-NMR analyses: Application to plant genetics and functional genomics. Functional Plant Biology, 31, 889–902.

    Article  CAS  Google Scholar 

  32. Newton-Cheh, C., & Hirschhorn, J. N. (2005). Genetic association studies of complex traits: Design and analysis issues [Review]. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis, 573(1–2), 54–69.

    PubMed  Article  CAS  Google Scholar 

  33. Nguyen, Q. H., & Bui, T. P. (1995). Azelaic acid—pharmacokinetic and pharmacodynamic properties and its therapeutic role in hyperpigmentary disorders and acne. International Journal of Dermatology, 34(2), 75–84.

    PubMed  Article  CAS  Google Scholar 

  34. Olle, H. (1986). Putrescine, spermidine, and spermine. Physiology, 1(1), 12–15.

    Google Scholar 

  35. Raghavan, C., Naredo, M. E. B., Wang, H., Atienza, G., Liu, B., Qiu, F., et al. (2007). Rapid method for detectin SNPs on agarose gels and its application in candidate gene mapping. Molecular Breeding, 19(2), 87–101. doi:10.1007/s11032-00609046-x.

    Article  CAS  Google Scholar 

  36. Reyes, R. A. (1997). The role of the state in Laos’ economic management. In Laos’ dilemmas and options (pp. 48–60). Vientiane: Institute of Southeast Asian Studies.

  37. Sakamoto, S., Hayashi, T., Hayashi, K., Murai, F., Hori, M., Kimoto, K., et al. (2007). Pre-germinated brown rice could enhance maternal mental health and immunity during lactation. European Journal of Nutrition, 46(7), 391–396.

    PubMed  Article  CAS  Google Scholar 

  38. Sanacora, G., Mason, G. F., Rothman, D. L., Behar, K. L., Hyder, F., Petroff, O. A. C., et al. (1999). Reduced cortical {gamma}-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Archives of General Psychiatry, 56(11), 1043–1047. doi:10.1001/archpsyc.56.11.1043.

    PubMed  Article  CAS  Google Scholar 

  39. Schiller, J. M., Appa Rao, S., Inthapanya, P., & Hatsadong, (2006). Glutinous rice in Laos. In J. M. Schiller, M. B. Chanphengxay, B. Linquist, & S. Appa Rao (Eds.), Rice in Laos (pp. 197–214). Los Banos, Philippines: International Rice Research Institute.

    Google Scholar 

  40. Sharif, K., & Butt, M. S. (2006). Preparation of fiber and mineral enriched pan bread by using defatted rice bran. International Journal of Food Properties, 9(4), 623–636.

    Article  CAS  Google Scholar 

  41. Shen, Y., Jin, L., Xiao, P., Lu, Y., & Bao, J.-S. (2009). Total phenolics, flavonoids, antioxidant capacity in rice grain and their relations to grain color, size and weight. Journal of Cereal Science, 49(1), 106–111.

    Article  CAS  Google Scholar 

  42. Shih, F. F. (2004). Rice Proteins. In E. T. Champagne (Ed.), Rice chemistry and technology (3rd ed., pp. 143–157). St Paul, Minnesota: American Association of Cereal Chemists Inc.

    Google Scholar 

  43. Shirasawa, K., Shiokai, S., Yamaguchi, M., Kishitani, S., & Nishio, T. (2006). Dot-blot-SNP analysis for practical plant breeding and cultivar identification in rice. Theoretical and Applied Genetics, 113(1), 147–155.

    PubMed  Article  CAS  Google Scholar 

  44. Strehmel, N., Hummel, J., Erban, A., Strassburg, K., & Kopka, J. (2008). Retention index thresholds for compound matching in GC-MS metabolite profiling. Journal of Chromatography, 871, 182–190.

    PubMed  Article  CAS  Google Scholar 

  45. Tarpley, L., & Roessner, U. (2007). Metabolomics: Enabling systems-level phenotyping in rice functional genomics. In N. M. Upadhyaya (Ed.), Rice functional genomics: Challenges, progress and prospects (pp. 91–107). New York: Springer.

    Chapter  Google Scholar 

  46. Tikunov, Y., Lommen, A., de Vos, C. H. R., Verhoeven, H. A., Bino, R. J., Hall, R. D., et al. (2005). A novel approach for nontargeted data analysis for metabolomics. Large-scale profiling of tomato fruit volatiles. Plant Physiology, 139(3), 1125–1137. doi:10.1104/pp.105.068130.

    PubMed  Article  CAS  Google Scholar 

  47. van Berloo, R. (2008). GGT 2.0: Versatile software for visualization and analysis of genetic data. Journal of Heredity, 99(2), 232–236. doi:10.1093/jhered/esm109.

    PubMed  Article  Google Scholar 

  48. Verhoeven, H. A., Jonker, H. H., de Vos, R. C. H., & Hall, R. D. (2011). Solid-phase micro-extraction (SPME) GC-MS analysis of natural volatile components in melon and rice. In N. G. Hardy, & R. D. Hall (Eds.), Plant metabolomics methods. Ithaca: Humana Press (in press).

  49. Wheeler, M. L., & Pi-Sunyer, F. X. (2008). Carbohydrate issues: Type and amount. Journal of the American Dietetic Association, 108(4), S34–S39.

    PubMed  Article  CAS  Google Scholar 

  50. Wright, M., Tung, C.-W., Zhao, K., Reynolds, A., McCouch, S. R., & Bustamante, C. D. (2010). ALCHEMY: A reliable method for automated SNP genotype calling for small batch sizes and highly homozygous populations. Bioinformatics (Oxford), 26(23), 2952–2960. doi:10.1093/bioinformatics/btq533.

    Article  CAS  Google Scholar 

  51. Yokoyama, W. H. (2004). Nutritional properties of rice and rice bran. In E. T. Champagne (Ed.), Rice chemistry and technology (pp. 595–606). Minneapolis: American Association of Cereal Chemists, Inc.

    Google Scholar 

  52. Yu, S., Nehus, Z. T., Badger, T. M., & Fang, N. (2007). Quantification of vitamin E and y-oryzanol components in rice germ and bran. Journal of Agricultural and Food Chemistry, 55, 7308–7313.

    PubMed  Article  CAS  Google Scholar 

  53. Zeisel, S. H., Da Costa, K. A., Franklin, P. D., Alexander, E. A., Lamont, J. T., Sheard, N. F., et al. (1991). Choline, an essential nutrient for humans. The FASEB Journal, 5(7), 2093–2098.

    CAS  Google Scholar 

  54. Zhao, K., Wright, M., Kimball, J., Eizenga, G., McClung, A., Kovach, M., et al. (2010). Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS ONE, 5(5), e10780. doi:10.1371/journal.pone.0010780.

    PubMed  Article  Google Scholar 

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Acknowledgments

All the authors acknowledge funding from the EU for the project META-PHOR (FOOD-CT-2006-036220) which was part of FP VI. RDH, RCHV and RM acknowledge additional support from the Centre for BioSystems Genomics, an initiative under the auspices of the Netherlands Genomics Initiative. MAF acknowledges additional support from the International Rice Research Institute (IRRI). CB acknowledges support from IRRI, KKU and NAFRI. University of Copenhagen acknowledges additional support from HarvestPlus to the Danish Plant Research Network entitled ‘Supporting the Foundation for Iron and Zinc Biofortification in Beans, Rice and Wheat’. Bordeaux Metabolome Facility acknowledge additional support from IBiSA and INRA CNOC, and Daniel Jacob for developing and maintaining the MeRy-B database.

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Correspondence to M. A. Fitzgerald.

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Calingacion, M.N., Boualaphanh, C., Daygon, V.D. et al. A genomics and multi-platform metabolomics approach to identify new traits of rice quality in traditional and improved varieties. Metabolomics 8, 771–783 (2012). https://doi.org/10.1007/s11306-011-0374-4

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Keywords

  • Rice
  • Volatile compounds
  • Primary polar compounds
  • Minerals
  • Flavour
  • Nutrition