Impact of Exogenous Sugars on the Potency of Selected Secondary Metabolites in Non-Starchy Amaranth (Amaranthus hybridus L.)
Research Article
DOI:
https://doi.org/10.21276/pt.2024.v1.i4.6Keywords:
Enzyme activity, Amaranthus hybridus L, plant biomass, starch–sugar metabolism, flavonoids, phenolsAbstract
The biosynthesis of secondary metabolites plays a significant role in determining the value of medicinal herbs, with sugar metabolism frequently influencing overall metabolic processes. To investigate the regulatory mechanisms, exogenous sugars (sucrose, glucose, and fructose) were applied to the leaves of Amaranthus hybridus L., a highly valued and multifunctional vegetable plant, both individually and in combination (sucrose + glucose + fructose), along with a control (water). Our findings revealed that exogenous sugars enhanced the accumulation of starch and soluble sugars, while also increasing enzyme activities associated with carbohydrate assimilation. Additionally, plant biomass was significantly boosted by combined exogenous sugars, sucrose alone enhanced the photosynthetic rate, and the combined sugars accelerated the accumulation of phenols and flavonoids. Metabolomic analysis further confirmed that exogenous sugars increased the levels of phenolic and flavonoid compounds. The levels of UDP-glucose pyrophosphorylase (UGP) and hexokinase (HKX) were elevated by exogenous sugars and showed a strong correlation with their metabolic activities, which in turn stimulated the synthesis of specific secondary metabolites. These results provide valuable insights into the key factors contributing to the value formation of A. hybridus and suggest a potential approach to enhancing its quality.
References
Abolaji GT, Olooto FM, Ogundele DT, Williams FE. Nutritional Characterization of Grain Amaranth Grown in Nigeria for Food Security and Healthy Living. Agrosearch. 2016; 17:1. https://dx.doi.org/10.4314/agrosh.v17i2.1
Nyonje WA, Yang RY, Kejo D, Makokha AO, Owino WO, Abukutsa-Onyango MO. Exploring the Status of Preference, Utilization Practices, and Challenges to Consumption of Amaranth in Kenya and Tanzania. J Nutr Metab. 2022; 2240724. https://doi.org/10.1155/2022/2240724
Nyonje WA, Makokha AO, Abukutsa-Onyango MO. Anti-Nutrient, Phytochemical and Antiradical Evaluation of 10 Amaranth (Amaranthus spp.) Varieties Before and After Flowering. J Agric Sci. 2014; 6: 68. https://doi.org/10.5539/jas.v6n4p68
Christenhusz MJM, Byng JW. The Number of Known Plants Species in the World and Its Annual Increase. Phytotaxa. 2016; 261: 201. https://doi.org/10.11646/phytotaxa.261.3.1
Waselkov KE, Boleda AS, Olsen KM. A Phylogeny of the Genus Amaranthus (Amaranthaceae) Based on Several Low-Copy Nuclear Loci and Chloroplast Regions. Syst Bot. 2018; 43: 439–458. https://doi.org/10.1600/036364418X697193
Assad R, Reshi ZA, Jan S, Rashid I. Biology of Amaranths. Bot Rev. 2017; 83: 382–436. http://dx.doi.org/10.1007%2Fs12229-017-9194-1
Langyan S, Bhardwaj R, Kumari J, Jacob SR, Bisht IS, Pandravada SR, Singh A, Singh PB, Dar ZA, Kumar A. Nutritional Diversity in Native Germplasm of Maize Collected from Three Different Fragile Ecosystems of India. Front Nutr. 2022; 9: 812599. https://doi.org/10.3389/fnut.2022.812599
Uliano BO, Rice. Role in Diet. In Encyclopedia of Food and Health; Caballero, B., Finglas, P., Toldrá, F., Eds.; Elsevier: Amsterdam, The Netherlands. 2016; pp. 641–645.
Shi S, Zhao D, Xing J, Pan K, Ma J, Wang X, Liu J, Cao C, Jiang Y Relationship between Rice Grain Protein Content and Key Phenotypes in Rice. Agron J. 2023; 115: 1257–1264. https://ui.adsabs.harvard.edu/link_gateway/2023AgrJ..115.1257S/doi:10.1002/agj2.21250
Kondi´c-Špika A, Mladenov N, Grahovac N, Zori´c M, Miki´c S, Trkulja D, Marjanovi´c-Jeromela A, Miladinovi´c, D, Hristov N. Biometric Analyses of Yield, Oil and Protein Contents of Wheat (Triticum Aestivum L.) Genotypes in Different Environments. Agronomy. 2019; 9: 270. https://doi.org/10.3390/AGRONOMY9060270
Jimoh MO, Afolayan AJ, Lewu FB. Suitability of Amaranthus Species for Alleviating Human Dietary Deficiencies. S Afr J Bot. 2018; 115: 65–73. https://doi.org/10.1016/j.sajb.2018.01.004
Apu A, Muhit M, Tareq S, Pathan A, Jamaluddin A, Ahmed M. Antimicrobial activity and brine shrimp lethality bioassay of the leaves extract of Dillenia indica Linn. J Young Pharm. 2010; 1: pp. 50–53. https://doi.org/10.4103/0975-1483.62213
Asante, DB, Effah-Yeboah E, Barnes. Antidiabetic effect of young and old ethanolic leaf extracts of Vernonia amygdalina: a comparative study. J Diabetes Res. 2016; 8252741:1–13. https://doi.org/10.1155/2016/8252741
Shanmugam B, Shanmugam GV, Subbaiah Reddy KR. Medicinal plants and bioactive compounds for diabetes management: important, K. S. It advances in drug discovery. Curr Pharm Des. 2016; 27: 763–774. https://doi.org/10.2174/1381612826666200928160357
Stamp N. Out of the quagmire of plant defense hypotheses. Q Rev Biol. 2003; 78(1): 23–55. https://doi.org/10.1086/367580
Wu J, Wang X, Bian L, Li Z, Jiang X, Shi F, Tang F, Zhang Z. Starch and sucrose metabolism plays an important role in the stem development in Medicago sativa. Funct Plant Biol. 2024; 51:FP24073. https://doi.org/10.1071/FP24073
Liu Z, Li Y, Wang YB, Liu XL, Ma L, Zhang ZJ, Mu C, Zhang Y, Peng L, Xie SJ, Song CP, Shi HZ, Zhu JK, Wang PC. Initiation and amplification of SnRK2 activationin abscisic acid signaling. Nat Commun. 2021; 12(1): 24-56. https://doi.org/10.1038/s41467-021-22812-x
Dong NQ, Sun Y, Guo T, Shi CL, Zhang YM, Kan Y, Xiang YH, Zhang H, Yang YB, Li YC, Zhao HY, Yu HX, Lu ZQ, Wang Y, Ye WW, Shan XJ, Lin HX. UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat Commun. 2020; 11(1): 2629. https://doi.org/10.1186/s12284-022-00604-1
Smeekens S, Hellmann HA Sugar sensing and signaling in plants. Front Plant Sci. 2014; 5: 113. https://doi.org/10.3389/fpls.2014.00113
Ljung K, Nemhauser JL, Perata P. New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol. 2015; 25: 130–137. https://doi.org/10.1016/j.pbi.2015.05.022
Kanwar P, Jha G. Alterations in plant sugar metabolism: signatory of pathogen attack. Planta. 2019; 249(2):305–318. https://doi.org/10.1007/s00425-018-3018-3
Baque MD, Elgirban A, Lee EJ, Paek KY. Sucrose regulated enhanced induction of anthraquinone, phenolics, flavonoids biosynthesis and activities of antioxidant enzymes in adventitious root suspension cultures of Morinda citrifolia (L.). Acta Physiol Plant. 2012; 34(2): 405–415. https://doi.org/10.1007/s11627-013-9555-3
Dai ZW, Meddar M, Renaud C, Merlin I, Hilbert G, Delrot S, Gomès E. Long-term in vitro culture of grape berries and its application to assess the effects of sugar supply on anthocyanin accumulation. J Exp Bot. 2013; 65(16): 4665–4677. https://doi.org/10.1093/jxb/ert489
Wang Y, Weathers P.J. Sugars proportionately affect artemisinin production. Plant Cell Rep. 2007; 26 (7): 1073–1081. https://doi.org/10.1007/s00299-006-0295-2
Guo J, Yang Y, Wang G, Yang L, Sun X. Ecophysiological responses of Abies fabri seedlings to drought stress and nitrogen supply. Plant Physiol. 2010; 139: 335–347. https://doi.org/10.1111/j.1399-3054.2010.01370.x
Grechi I, Vivin P, Hilbert G, Milin S, Robert T, Gaudillère JP. Effect of light and nitrogen supply on internal C; N balance and control of root-to-shoot biomass allocation in grapevine. Environ Exp Bot. 2007;59:139–149. http://dx.doi.org/10.1016%2Fj.envexpbot.2005.11.002
Bao J, Cai Y, Sun M, Wang G, Corke H. Anthocyanins, flavonols, and free radical scavenging activity of Chinese bayberry (Myrica rubra) extracts and their color properties and stability. J Agric Food Chem. 2005; 53(6): 2327–2332. https://doi.org/10.1021/jf048312z
Singleton VL, Rossi JA. Colorimetry of total phenolics and phosphomolybdic–phosphotungstic acid reagents. Am J Enol Vit. 1965; 16: 144–158. http://www.ajevonline.org/content/16/3/144.full.pdf+html
Chen W, Gong L, Guo Z, Wang W, Zhang H, Liu X, Yu S, Xiong L, Luo J. A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Mol Plant. 2013; 6(6):1769–1780. https://doi.org/10.1093/mp/sst080
Ali S, Hafeez A, Ma X, Tung SA, Liu A, Shah AN, Chattha MS, Zhang Z, Yang G. Potassium relative ratio to nitrogen considerably favors carbon metabolism in late-planted cotton at high planting density. Field Crops Res. 2018; 223: 48–56. https://www.sciencedirect.com/science/article/pii/S0378429018302739
Lei L, Jen S. Dynamic and diverse sugar signaling. Curr Opin Plant Biol. 2016; 33: 116–125. https://doi.org/10.1016/j.pbi.2016.06.018
Patrick JW, Botha FC, Birch RG. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol J. 2013; 11: 142–56. https://doi.org/10.1111/pbi.12002
Rolland F, Baena-gonzalez E, Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol. 2006; 57: 675–709. https://doi.org/10.1146/annurev.arplant.57.032905.105441
Saksena HB, Sharma M, Singh D, Laxmi A. The versatile role of glucose signaling in regulating growth, development and stress responses in plants. J Plant Biochem Biotech .2020; 29(4):687–699. https://doi.org/10.1007/s13562-020-00614-4
McCormick AJ, Watt DA, Cramer MD. Supply and demand: sink regulation of sugar accumulation in sugarcane. J Exp Bot. 2009; 60: 357–64. https://doi.org/10.1093/jxb/ern310
Wang Q, Jiang C, Fang S, Wang J, Ji Y, Shang X, Ni Y, Yin Z, Zhang J. Antihyperglycemic, antihyperlipidemic and antioxidant effects of ethanol and aqueous extracts of Cyclocarya paliurus leaves in type 2 diabetic rats. J Ethnopharmacol. 2013;150(3):1119-27. https://doi.org/10.1016/j.jep.2013.10.040
Jiang W, Ding M, Duan Q, Zhou Q, Huang D. Exogenous glucose preserves the quality of watermelon (Citrullus lanatus) plug seedlings for low-temperature storage. Sci Hortic. 2012;148:23–29. https://doi.org/10.1016/j.scienta.2012.09.016
Chang L, Xiao YM, She LF, Xia YP. Analysis of gene expression and enzyme activities related to starch metabolism in Lycoris sprengeri bulbs of different sizes. Sci Hortic. 2013; 161: 118-124. https://doi.org/10.1016/J.SCIENTA.2013.07.005
Abbas F, Nian X, Zhou Y, Ke Y, Liu L, Yu R, Fan Y. Putative regulatory role of hexokinase and fructokinase in terpenoid aroma biosynthesis in Lilium ‘Siberia’. Plant Physiol Biochem. 2021; 167: 619–629. https://doi.org/10.1016/j.plaphy.2021.08.042
Lloyd JC, Zakhleniuk OV. Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot. 2004; 55:1221–30. https://doi.org/10.1093/jxb/erh143
Chen H, Jones AD, Howe GA. Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Letters. 2006; 580(11):2540–2546. https://doi.org/10.1016/j.febslet.2006.03.070
Yang M, Wang L, Belwal T, Zhang X, Lu H, Chen C, Li L. Exogenous melatonin and abscisic acid expedite the flavonoids biosynthesis in grape berry of Vitis vinifera cv. Kyoho. Molecules. 2019; 25(1) :12. https://doi.org/10.3390/molecules25010012
Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P. Gibberellins, jasmonate and abscisic acid modulate the sucroseinduced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol. 2008; 179(4): 1004–1016. https://doi.org/10.1111/j.1469-8137.2008.02511.x
Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA. Sugar demand, not auxin, is the initial regulator of apical dominance, Proc Natl Acad Sci. 2014; 111: 6092–6097. https://doi.org/10.1073/pnas.1322045111
Downloads
Published
Data Availability Statement
The data supporting the findings of this study are available within the article. The datasets generated and analyzed during the current study are available from the corresponding author upon reasonable request.
Issue
Section
License
Copyright (c) 2025 PhytoTalks
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
