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Proteomic Analysis of Isogenic Rice Reveals Proteins Correlated with Aroma Compound Biosynthesis at Different Developmental Stages

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Abstract

Fragrant rice has a potent flavor compound, 2-acetyl-1-pyrroline (2AP). A better understanding of the 2AP biosynthetic pathway is gained by proteomic analysis of two isogenic lines of Thai jasmine rice, Oryza sativa L. cv. Khao Dawk Mali 105, which differ only in the aromatic gene Os2AP. The protein profiles of two lines, from six growth stages, seedling to grain filling, had 41 identifiable protein spots. Four of these spots were betaine aldehyde dehydrogenase, a key enzyme responsible for 2AP production. This enzyme occurred in every growth stage of the non-aromatic rice line except smaller amount detected in the hard grain-filling stage of the aromatic line. Glyceraldehyde 3-phosphate dehydrogenase and aspartate aminotransferase, observed in the aromatic line, may involve in the metabolism of precursors for 2AP biosynthesis. In addition, glutamine synthetase and 1-cys peroxiredoxin A which function in ammonia reassimilation and hydrogen peroxide detoxification were unique in the aromatic line. However, proteins that correspond to photosynthesis and the nutrient reservoir were only detected in lower abundances. This possibly explains why the aroma rice grain weight is low. Our study proposed the possible role of these remarkable proteins which involved in 2AP biosynthesis in jasmine rice.

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References

  1. Bryant, R. J., & McClung, A. M. (2011). Volatile profiles of aromatic and non-aromatic rice cultivars using SPME/GC-MS. Food Chemistry, 124, 501–513.

    Article  CAS  Google Scholar 

  2. Cho, S., & Kays, S. J. (2013). Aroma-active compounds of wild rice (Zizania palustris L.). Food Research International, 54, 1463–1470.

    Article  CAS  Google Scholar 

  3. Deng, Y., Zhong, Y., Yu, W., Yue, J., Liu, Z., Zheng, Y., et al. (2013). Effect of hydrostatic high pressure pretreatment on flavor volatile profiles of cooked rice. Journal of Cereal Science, 58, 479–487.

    Article  CAS  Google Scholar 

  4. Mahatheeranont, S., Keawsa-ard, S., & Dumri, K. (2001). Quantification of the rice aroma compound, 2-acetyl-1-pyrroline, in uncooked Khao Dawk Mali 105 brown rice. Journal of Agriculture and Food Chemistry, 49, 773–779.

    Article  CAS  Google Scholar 

  5. Yajima, I., Yanai, T., Nakamura, M., Sakakibara, H., & Hayashi, K. (1979). Volatile flavor components of cooked Kaorimai (scent rice, O. sativa japonica). Agricultural and Biological Chemistry, 43, 2425–2429.

    Article  CAS  Google Scholar 

  6. Buttery, R. G., Ling, L. C., Juliano, B. O., & Turnbaugh, J. G. (1983). Cooked rice aroma and 2-acetyl-1-pyrroline. Journal of Agriculture and Food Chemistry, 31, 823–826.

    Article  CAS  Google Scholar 

  7. Yoshihashi, T. (2002). Quantitative analysis on 2-acetyl-1-pyrroline of aromatic rice by stable isotope dilution method and model studies on its formation during cooking. Journal of Food Science, 67, 619–622.

    Article  CAS  Google Scholar 

  8. Yoshihashi, T., Huong, N. T. T., Surojanametakul, V., Tungtrakul, P., & Varanyanond, W. (2005). Effect of storage conditions on 2-acetyl-1-pyrroline content in aromatic rice variety, Khao Dawk Mali 105. Journal of Food Science, 70, S34–S37.

    Article  CAS  Google Scholar 

  9. Nadaf, A. B., Krishnan, S., & Wakte, K. V. (2006). Histochemical and biochemical analysis of major aroma compound (2-acetyl-1-pyrroline) in basmati and other scented rice (Oryza sativa L.). Current Science, 91, 1533–1536.

    CAS  Google Scholar 

  10. Fitzgerald, T. L., Waters, D. L. E., & Henry, R. J. (2009). Betaine aldehyde dehydrogenase in plants. Plant Biology, 11, 119–130.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Bradbury, L. M. T., Fitzgerald, T. L., Henry, R. J., Jin, Q., & Waters, D. L. E. (2005). The gene for fragrance in rice. Plant Biotechnology Journal, 3, 363–370.

    Article  CAS  Google Scholar 

  13. Amarawathi, Y., Singhm, R., Singh, A. K., Singh, V. P., Mohapatra, T., Sharma, T. R., et al. (2008). Mapping of quantitative trait loci for basmati quality traits in rice (Oryza sativa L.). Molecular Breeding, 21, 49–65.

    Article  CAS  Google Scholar 

  14. Lin, D.-G., Chou, S.-Y., Wang, A. Z., Wang, Y.-W., Kuo, S.-M., Lai, C.-C., et al. (2014). A proteomic study of rice cultivar TNG67 and its high aroma mutant SA0420. Plant Science, 214, 20–28.

    Article  CAS  Google Scholar 

  15. Bourgis, F., Guyot, R., Gherbi, H., Tailliez, E., Amabile, I., Salse, J., et al. (2008). Characterization of the major fragrance gene from an aromatic japonica rice and analysis its diversity in Asian cultivated rice. Theoretical and Applied Genetics, 117, 353–368.

    Article  CAS  Google Scholar 

  16. Myint, K. M., Arikit, S., Wanchana, S., Yoshihashi, T., Choowongkomon, K., & Vanavichit, A. (2012). A PCR-based marker for a locus conferring the aroma in Myanmar rice (Oryza sativa L.). Theoretical and Applied Genetics, 125, 887–896.

    Article  CAS  Google Scholar 

  17. Vanavichit, A., Tragoonrung, S., Toojinda, T., Wanchana, S. and Kamolsukyunyong, W. (2008). Transgenic rice plants with reduced expression of Os2AP and elevated levels of 2-acetyl-1-pyrroline. United State Patent 7319181B2 Jan 15, 2008.

  18. Vanavichit, A., & Yoshihashi, T. (2010). Molecular aspects of fragrance and aroma in rice. In J.-C. Kader & M. Delseny (Eds.), Advances in botanical research (Vol. 56, pp. 50–73). London: Elsevier.

    Google Scholar 

  19. Yoshihashi, T., Huong, N. T. T., & Inatomi, H. (2002). Precursors of 2-acetyl-1-pyrroline, a potent flavor compound of an aromatic rice variety. Journal of Agriculture and Food Chemistry, 50, 2001–2004.

    Article  CAS  Google Scholar 

  20. Huang, T.-C., Teng, C.-S., Chang, J.-L., Chuang, H.-S., Ho, C.-T., & Wu, M.-L. (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. Journal of Agriculture and Food Chemistry, 56, 7399–7404.

    Article  CAS  Google Scholar 

  21. Damerval, C., De Vienne, D., Zivy, M., & Thiellement, H. (1986). Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis, 7, 52–54.

    Article  CAS  Google Scholar 

  22. Zhou, Y., Cai, H., Xiao, J., Li, X., Zhang, Q., & Lian, X. (2009). Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theoretical and Applied Genetics, 118, 1381–1390.

    Article  CAS  Google Scholar 

  23. Wadsworth, G. J. (1997). The plant aspartate aminotransferase gene family. Physiologia Plantarum, 100, 998–1006.

    Article  CAS  Google Scholar 

  24. Cai, H., Zhou, Y., Xiao, J., Li, X., Zhang, Q., & Lian, X. (2009). Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Reports, 28, 527–537.

    Article  CAS  Google Scholar 

  25. Hirel, B., & Gadal, P. (1980). Glutamine synthetase in rice: A comparative study of the enzymes from roots and leaves. Plant Physiology, 66, 619–623.

    Article  CAS  Google Scholar 

  26. Wallsgrove, R. M., Turner, J. C., Hall, N. P., Kendall, A. C., & Bright, S. W. J. (1987). Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiology, 83, 155–158.

    Article  CAS  Google Scholar 

  27. Martin, W., & Cerff, R. (1986). Prokaryotic features of a nucleus-encoded enzyme cDNA sequences for chloroplast and cytosolic glyceraldehyde-3-phosphate dehydrogenases from mustard (Sinapis alba). European Journal of Biochemistry, 159, 323–331.

    Article  CAS  Google Scholar 

  28. Wu, M.-L., Chou, K.-L., Wu, C.-R., Chen, J.-K., & Huang, T.-C. (2009). Characterization and the possible formation mechanism of 2-acetyl-1-pyrroline in aromatic vegetable soybean (Glycine max L.). Journal of Food Science, 74, 192–197.

    Article  Google Scholar 

  29. Romanczyk, L. J., McClelland, C. A., Post, L. S., & Aitken, W. M. (1995). Formation of 2-acetyl-1-pyrroline by several Bacillus cereus strains isolated from cocoa fermentation boxes. Journal of Agriculture and Food Chemistry, 43, 469–475.

    Article  CAS  Google Scholar 

  30. Costello, P. J., & Henschke, P. A. (2002). Mousy off-flavor of wine: Precursors and biosynthesis of the causative N-heterocycles 2-ethyltetrahydropyridine, 2-acetyltetrahydropyridine, and 2-acetyl-1-pyrroline by Lactobacillus hilgardii DSM 20176. Journal of Agriculture and Food Chemistry, 50, 7079–7087.

    Article  CAS  Google Scholar 

  31. Kleczkowski, L. A. (1994). Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry, 37, 1507–1515.

    Article  CAS  Google Scholar 

  32. Tenhaken, R., & Thulke, O. (1996). Cloning of an enzyme that synthesizes a key nucleotide-sugar precursor of hemicellulose biosynthesis from soybean: UDP-glucose dehydrogenase. Plant Physiology, 112, 1127–1134.

    Article  CAS  Google Scholar 

  33. Grudkowska, M., & Zagdańska, B. (2004). Multifunctional role of plant cysteine proteinases. Acta Biochimica Polonica, 51, 609–624.

    CAS  Google Scholar 

  34. Simões, I., & Faro, C. (2004). Structure and function of plant aspartic proteinases. European Journal of Biochemistry, 271, 2067–2075.

    Article  Google Scholar 

  35. Chen, L., Chan, S. Y., & Cossins, E. A. (1997). Distribution of folate derivatives and enzymes for synthesis of 10-formyltetrahydrofolate in cytosolic and mitochondrial fractions of pea leaves. Plant Physiology, 115, 299–309.

    Article  CAS  Google Scholar 

  36. Jabrin, S., Ravanel, S., Gambonnet, B., Douce, R., & Rébeillé, F. (2003). One-carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development. Plant Physiology, 131, 1431–1439.

    Article  CAS  Google Scholar 

  37. Collakova, E., Goyer, A., Naponelli, V., Krassovskaya, I., Gregory, J. F, 3rd, Hanson, A. D., et al. (2008). Arabidopsis 10-formyl tetrahydrofolate deformylase are essential for photorespiration. Plant Cell, 20, 1818–1832.

    Article  CAS  Google Scholar 

  38. Li, R., Moore, M., & King, J. (2003). Investigating the regulation of one-carbon metabolism in Arabidopsis thaliana. Plant and Cell Physiology, 44, 233–241.

    Article  CAS  Google Scholar 

  39. Popov, V. O., & Lamzin, V. S. (1994). NAD+-dependent formate dehydrogenase. Biochemical Journal, 301, 625–643.

    Article  CAS  Google Scholar 

  40. Alekseeva, A. A., Savin, S. S., & Tishkov, V. I. (2011). NAD+-dependent formate dehydrogenase from plants. Acta Naturae, 3, 38–54.

    CAS  Google Scholar 

  41. Kim, S. Y., Paeng, S. K., Nawkar, G. M., Maibam, P., Lee, E. S., Kim, K.-S., et al. (2011). The 1-Cys peroxiredoxin, a regulator of seed dormancy, functions as a molecular chaperone under oxidative stress conditions. Plant Science, 181, 119–124.

    Article  CAS  Google Scholar 

  42. Al-Quraan, N. A., Locy, R. D., & Singh, N. K. (2011). Implications of paraquat and hydrogen peroxide-induced oxidative stress treatments on the GABA shunt pathway in Arabidopsis thaliana calmodulin mutants. Plant Biotechnology Report, 5, 225–234.

    Article  Google Scholar 

  43. Maruta, T., Ojiri, M., Noshi, M., Tamoi, M., Ishikawa, T., & Shigeoka, S. (2013). Activation of γ-aminobutyrate production by chloroplastic H2O2 is associated with the oxidative stress response. Bioscience, Biotechnology, and Biochemistry, 77, 422–425.

    Article  CAS  Google Scholar 

  44. Lee, K. O., Jang, H. H., Jung, B. G., Chi, Y. H., Lee, J. Y., Choi, Y. O., et al. (2000). Rice 1Cys-peroxiredoxin over-expressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity. FEBS Letters, 486, 103–106.

    Article  CAS  Google Scholar 

  45. Andersson, I. (2008). Catalysis and regulation in Rubisco. Journal of Experimental Botany, 59, 1555–1568.

    Article  CAS  Google Scholar 

  46. Fitzgerald, T. L., Waters, D. L. E., Brooks, L. O., & Henry, R. J. (2010). Fragrance in rice (Oryza sativa) is associated with reduced yield under salt treatment. Environmental and Experimental Botany, 68, 292–300.

    Article  CAS  Google Scholar 

  47. Breen, J., & Bellgard, M. (2010). Germin-like proteins (GLPs) in cereal genomes: Gene clustering and dynamic roles in plant defence. Functional & Integrative Genomics, 10, 463–476.

    Article  CAS  Google Scholar 

  48. Zhang, X. Y., Nie, Z. H., Wang, W. J., Leung, D. W. M., Xu, D. G., Chen, B. L., et al. (2013). Relationship between disease resistance and rice oxalate oxidases in transgenic rice. PLoS One, 8, e78348.

    Article  CAS  Google Scholar 

  49. Yoshioka-Nishimura, M., & Yamamoto, Y. (2014). Quality control of photosystem II: The molecular basis for the action of FtsH protease and the dynamics of the thylakoid membranes. Journal of Photochemistry and Photobiology B: Biology, 137, 100–106.

    Article  CAS  Google Scholar 

  50. Hoffmann, L., Besseau, S., Geoffroy, P., Ritzenthaler, C., Meyer, D., Lapierre, C., et al. (2004). Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell, 16, 1446–1465.

    Article  CAS  Google Scholar 

  51. Hu, Y., Gai, Y., Yin, L., Wang, X., Feng, C., Feng, L., et al. (2010). Crystal structures of a Populus tomentosa 4-coumarate:coA ligase shed light on its enzymatic mechanisms. Plant Cell, 22, 3093–3104.

    Article  CAS  Google Scholar 

  52. Sun, H., Li, Y., Feng, S., Zou, W., Guo, K., Fan, C., et al. (2013). Analysis of five rice 4-coumarate:coenzyme A ligase enzyme activity and stress response for potential roles in lignin and flavonoid biosynthesis in rice. Biochemical and Biophysical Research Communications, 430, 1151–1156.

    Article  CAS  Google Scholar 

  53. Riendeau, D., & Meighen, E. (1985). Enzymatic reduction of fatty acids and acyl-CoAs to long chain aldehydes and alcohols. Experientia, 41, 707–713.

    Article  CAS  Google Scholar 

  54. Rowland, O., Zheng, H., Hepworth, S. R., Lam, P., Jetter, R., & Kunst, L. (2006). CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiology, 142, 866–877.

    Article  CAS  Google Scholar 

  55. Wakte, K. V., Kad, T. D., Zanan, R. L., & Nadaf, A. B. (2011). Mechanism of 2-acetyl-1-pyrroline biosynthesis in Bassia latifolia Roxb. flowers. Physiology and Molecular Biology of Plants, 17, 231–237.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to Assoc. Prof. Dr. Aphichart Vanavichit of the Rice Science Center and Rice Gene Discovery Unit, Kasetsart University, Thailand, for providing the isogenic rice seeds used in this research. We also appreciate use of the MS facilities of Kagawa University, Japan, and Genome Institute, BIOTEC, Thailand. Financial support for this research was given by the Center of Excellence for Innovation in Chemistry (PERCH-CIC) and by the Graduate School, Chiang Mai University.

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Correspondence to Hataichanoke Niamsup.

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Wongpia, A., Roytrakul, S., Nomura, M. et al. Proteomic Analysis of Isogenic Rice Reveals Proteins Correlated with Aroma Compound Biosynthesis at Different Developmental Stages. Mol Biotechnol 58, 117–129 (2016). https://doi.org/10.1007/s12033-015-9906-x

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