Metabolite profile of two Allium cepa L. aggregatum group cultivars by Nuclear Magnetic Resonance
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FRANSISKA RENITA ANON BASUNDARI
https://orcid.org/0000-0001-9163-230X
ENDANG SULISTYANINGSIH
♥
RUDI HARI MURTI
https://orcid.org/0000-0002-0791-1750
TRI RINI NURINGTYAS
https://orcid.org/0000-0002-8011-8396
Abstract
Abstract. Basundari FRA, Sulistyaningsih E, Murti RH, Nuringtyas TR. 2021. Metabolite profile of two Allium cepa L. aggregatum group cultivars by Nuclear Magnetic Resonance. Biodiversitas 22: 3127-3135. Shallot, an Allium species with high economic value, is widely cultivated in Indonesia. The species includes numerous cultivars with unique characteristics, such as harvesting time, yield, taste, odor, and bulb color. Tuk Tuk and Trisula, the cultivars used in this experiment, have different bulb colors. Tuk Tuk’s bulb color is light red, while that of Trisula is dark red. This color difference may be attributed to variations in the metabolite contents of the shallot bulbs. The present experiment aimed to reveal differences in the metabolite contents of the two shallot cultivars by using Nuclear Magnetic Resonance (NMR) and then determine the specific metabolites contributing to these differences. Bulbs of Tuk Tuk and Trisula were planted in the field under the same conditions and then collected. The bulb samples were powdered, freeze-dried, and subjected to a two-phase extraction method with CDCl3 and D2O as solvents to separate the nonpolar metabolites from polar ones. The extracts were analyzed by 1H-NMR, and the spectra collected were analyzed using MNOVA software and Metaboanalyst.ca. A total of 23 metabolites were successfully identified and characterized in this experiment. The contents of eight of these metabolites, namely, sucrose, glutamine, citric acid, choline, methiin, propiin, threonine, and formic acid, were significantly higher in Trisula than in Tuk Tuk. These differences may be correlated with variations in the color intensity, pungency, and other traits of the cultivars. The results demonstrate that NMR metabolite profiling could effectively differentiate metabolite profile variations among shallot cultivars.
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References
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Roldan M, Engel B, de Vos RCH, Vereijken P, Astola, L, Groenenboom M, van de Geest H, Bovy A, Molenaar J, van Eeuwijk F, Hall, R. 2014. Metabolomics reveals organ-specific metabolic rearrangements during early tomato seedling development. Metabolomics 10(5): 958–974. https://doi.org/10.1007/s11306-014-0625-2
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Russell BL, Rathinasabapathi B, Hanson AD. 1998. Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiology 116(2): 859–865. https://doi.org/10.1104/pp.116.2.859
Saviano G, Paris D, Melck D, Fantasma F, Motta A, Iorizzi M. 2019. Metabolite variation in three edible Italian Allium cepa L. by NMR-based metabolomics: a comparative study in fresh and stored bulbs. Metabolomics 15(8). https://doi.org/10.1007/s11306-019-1566-6
Schripsema, J., & Dagnino, D. 2018. Two-phase extraction for comprehensive analysis of the plant metabolome by NMR. In GAT et al. (eds). Metabolic Profiling: Methods and Protocols, Methods in Molecular Biology. 1738: 195–202. Springer Science+Business Media, LLC. https://doi.org/10.1007/978-1-4939-7643-0
Shannon S, Yamaguchi M, Howard FD. 1967. Precursors involved in the formation of pink pigments in onion purees. Journal of Agricultural and Food Chemistry 15(3): 423–426. https://doi.org/10.1021/jf60151a027
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Verpoorte R, Choi YH, Kim HK. 2007. NMR-based metabolomics at work in phytochemistry. Phytochemistry Reviews 6(1): 3–14. https://doi.org/10.1007/s11101-006-9031-3
Verpoorte R, Choi YH, Mustafa NR, Kim HK. 2008. Metabolomics: back to basics. Phytochemistry Reviews 7(3): 525–537. https://doi.org/10.1007/s11101-008-9091-7
Wahyuni D. 2021. Thrips resistance in gladiolus: An eco-metabolomic approach. [Dissertation]. Universiteit Leiden. Netherlands.
Atif M, Jahanger MA, Amin B, Ghani MI, Ali,M, Cheng Z. 2020. Mechanism of allium crops bulb enlargement in response to photoperiod: A review. International Journal of Molecular Sciences 21(4). https://doi.org/10.3390/ijms21041325
Bregoff HM, Delwiche CC. 1955. The formation of choline and betaine in leaf disks of Beta vulgaris. The Journal of Biological Chemistry 217(2): 819–828. https://doi.org/10.1016/s0021-9258(18)65947-2
Byerrum, R. U., Hamill, R. L., & Ball, C. D. (1954). The incorporation of glycine into nicotine in tobacco plant metabolism. The Journal of Biological Chemistry 210(2): 645–650. https://doi.org/10.1016/s0021-9258(18)65390-6
Darbyshire B, Henry RJ. 1978. The distribution of fructans in onions. New Phytologist 81(1): 29–34. https://doi.org/10.1111/j.1469-8137.1978.tb01600.x
Dhillon, MK, & Kumar S. 2017. Amino acid profiling of Sorghum bicolor vis-à-vis Chilo partellus (Swinhoe) for biochemical interactions and plant resistance. Arthropod-Plant Interactions 11(4): 537–550. https://doi.org/10.1007/s11829-016-9491-3
Dong X, Gao Y, Chen W, Wang W, Gong L, Liu X, Luo J. 2015. Spatiotemporal distribution of phenolamides and the genetics of natural variation of hydroxycinnamoyl spermidine in rice. Molecular Plan, 8(1): 111–121. https://doi.org/10.1016/j.molp.2014.11.003
Fredotovi? Ž, Soldo B, Šprung M, Marijanovi? Z, Jerkovi? I, Puizina J. 2020. Comparison of organosulfur and amino acid composition between triploid onion Allium cornutum clementi ex visiani, 1842, and common onion Allium cepa L., and evidences for antiproliferative activity of their extracts. Plants, 9(1). https://doi.org/10.3390/plants9010098
Hansen SL. 2001. Content of free amino acids in onion (Allium cepa L.) as influenced by the stage of development at harvest and long-term storage. Acta Agriculturae Scandinavica Section B: Soil and Plant Science 51(2)::77–83. https://doi.org/10.1080/090647101753483796
Holmes E, Tang H, Wang Y, Seger C. 2006. The assessment of plant metabolite profiles by NMR-based methodologies. Planta Medica 72(9): 771–785. https://doi.org/10.1055/s-2006-946682
Hong J, Yang L, Zhang D, Shi J. 2016. Plant metabolomics: An indispensable system biology tool for plant science. International Journal of Molecular Sciences 17(6). https://doi.org/10.3390/ijms17060767
Jahangir M, Nuringtyas TR, Ali K, Wilson EG, Choi YH, Verpoorte R. 2018. NMR-based Metabolomics?: Understanding Plant. NMR-Based Metabolomics: Understanding Plant Chemistry and Identification of Biologically Active Compounds January 2018: 246–263. https://doi.org/10.1039/9781849736435-00246
Jo S, Song Y, Jeong JH, Hwang J, Kim Y. 2020. Geographical discrimination of Allium species (garlic and onion) using 1H NMR spectroscopy with multivariate analysis. International Journal of Food Properties, 23(1): 241–254. https://doi.org/10.1080/10942912.2020.1722160
Kan CC, Chung TY, Juo YA, Hsieh MH. 2015. Glutamine rapidly induces the expression of key transcription factor genes involved in nitrogen and stress responses in rice roots. BMC Genomics 16(1): 1–15. https://doi.org/10.1186/s12864-015-1892-7
Kim HK, Choi YH, Verpoorte R. 2010. NMR-based metabolomic analysis of plants. Nature Protocols 5(3): 536–549. https://doi.org/10.1038/nprot.2009.237
Krotkov G, Vittorio P, Reed G. 1954. Synthesis of glucose and starch by tobacco leaves from HC14OOH, CH3C14OOH, CH3CHOH.C14OOH, C14H3. C14HOH. COOH, and C6H5.C14POOHl. Archives of Biochemistry and Biophysics 51(1): 147–154.
Kubec R, Hrbá?ová M, Musah R, Velíšek J. 2004. Allium discoloration: the nature of onion pinking and garlic greening. Czech Journal of Food Sciences, 22: S109–S112. https://doi.org/10.17221/10629-cjfs
Kubec R, Velíšek J. 2007. Allium discoloration: The color-forming potential of individual thiosulfinates and amino acids: Structural requirements for the color-developing precursors. Journal of Agricultural and Food Chemistry 55(9): 3491–3497. https://doi.org/10.1021/jf070040n
Lee EJ, Yoo KS, Jifon J, Patil BS. 2009. Characterization of shortday onion cultivars of 3 pungency levels with flavor precursor, free amino acid, sulfur, and sugar contents. Journal of Food Science 74(6). https://doi.org/10.1111/j.1750-3841.2009.01243.x
Lee J, Harnly JM. 2005. Free amino acid and cysteine sulfoxide composition of 11 garlic (Allium sativum L.) cultivars by gas chromatography with flame ionization and mass selective detection. Journal of Agricultural and Food Chemistry 53(23): 9100–9104. https://doi.org/10.1021/jf051228e
Lukes TM. 1986. Factors governing the greening of garlic puree. Journal of Food Science 51(6):1577–1577. https://doi.org/10.1111/j.1365-2621.1986.tb13869.x
Pan Q, Dai Y, Nuringtyas TR, Mustafa NR, Schulte AE, Verpoorte R, Choi YH. 2014. Investigation of the chemomarkers correlated with flower colour in different organs of catharanthus roseus using nmr-based metabolomics. Phytochemical Analysis 25(1): 66–74. https://doi.org/10.1002/pca.2464
Ritota M, Casciani L, Han BZ, Cozzolino S, Leita L, Sequi P, Valentini M. 2012. Traceability of Italian garlic (Allium sativum L.) by means of HRMAS-NMR spectroscopy and multivariate data analysis. Food Chemistry 135(2): 684–693. https://doi.org/10.1016/j.foodchem.2012.05.032
Ritsema T, Smeekens S. 2003. Fructans: Beneficial for plants and humans. Current Opinion in Plant Biology 6(3): 223–230. https://doi.org/10.1016/S1369-5266(03)00034-7
Roldan M, Engel B, de Vos RCH, Vereijken P, Astola, L, Groenenboom M, van de Geest H, Bovy A, Molenaar J, van Eeuwijk F, Hall, R. 2014. Metabolomics reveals organ-specific metabolic rearrangements during early tomato seedling development. Metabolomics 10(5): 958–974. https://doi.org/10.1007/s11306-014-0625-2
Rose P, Whiteman M, Moore K, Zhun Y. 2005. Bioactive S-alk(en)yl cysteine sulfoxide metabolites in the genus Allium?: the chemistry of potential therapeutic agents. Nat. Prod. Rep, 22: 351–368.
Russell BL, Rathinasabapathi B, Hanson AD. 1998. Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiology 116(2): 859–865. https://doi.org/10.1104/pp.116.2.859
Saviano G, Paris D, Melck D, Fantasma F, Motta A, Iorizzi M. 2019. Metabolite variation in three edible Italian Allium cepa L. by NMR-based metabolomics: a comparative study in fresh and stored bulbs. Metabolomics 15(8). https://doi.org/10.1007/s11306-019-1566-6
Schripsema, J., & Dagnino, D. 2018. Two-phase extraction for comprehensive analysis of the plant metabolome by NMR. In GAT et al. (eds). Metabolic Profiling: Methods and Protocols, Methods in Molecular Biology. 1738: 195–202. Springer Science+Business Media, LLC. https://doi.org/10.1007/978-1-4939-7643-0
Shannon S, Yamaguchi M, Howard FD. 1967. Precursors involved in the formation of pink pigments in onion purees. Journal of Agricultural and Food Chemistry 15(3): 423–426. https://doi.org/10.1021/jf60151a027
Shelp BJ, Bown AW, Faure D. 2006. Extracellular ?-aminobutyrate mediates communication between plants and other organisms. Plant Physiology 142(4): 1350–1352. https://doi.org/10.1104/pp.106.088955
Soininen TH, Jukarainen N, Auriola SOK, Julkunen-Tiitto R, Karjalainen R, Vepsäläinen JJ. 2014. Quantitative metabolite profiling of edible onion species by NMR and HPLC-MS. Food Chemistry, 165, 499–505. https://doi.org/10.1016/j.foodchem.2014.05.132
Tolbert NE. 1955. Formic acid metabolism in barley leaves. The Journal of Biological Chemistry 215(1): 27–34. https://doi.org/10.1016/s0021-9258(18):66013-2
Trejo-Téllez LI, Gómez-Merino FC, Schmitt JM. (2012). Citric acid: Biosynthesis, properties and applications on higher plants. In D. Vargas & J. Medina (Eds.), Citric Acid: Synthesis, Properties and Applications April:43–70). Nova Science Publishers, Inc.
Verpoorte R, Choi YH, Kim HK. 2007. NMR-based metabolomics at work in phytochemistry. Phytochemistry Reviews 6(1): 3–14. https://doi.org/10.1007/s11101-006-9031-3
Verpoorte R, Choi YH, Mustafa NR, Kim HK. 2008. Metabolomics: back to basics. Phytochemistry Reviews 7(3): 525–537. https://doi.org/10.1007/s11101-008-9091-7
Wahyuni D. 2021. Thrips resistance in gladiolus: An eco-metabolomic approach. [Dissertation]. Universiteit Leiden. Netherlands.
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