CONCENTRATION OF STEVIOSIDE AND REBAUDIOSIDE-A IN Stevia rebaudiana BERTONI PLANTS IN INTERACTION WITH ARBUSCULAR MYCORRHIZAE AND PHOSPHORUS
DOI:
https://doi.org/10.18633/biotecnia.v26.2280Keywords:
metabolites, glycosides, AM, phosphate, quantificationAbstract
Stevia rebaudiana produces steviol glycosides in its leaves, stevioside and rebaudioside-A are the most important thanks to their sweetening property. Phosphorus is an essential element in the biosynthesis of steviol glycosides and arbuscular mycorrhizae can promote the concentration of glycosides by facilitating the translocation of phosphorus to the plant. Therefore, the concentration of stevioside and rebaudioside-A was quantified by means of 1H-NMR in S. rebaudiana plants inoculated with arbuscular mycorrhizal consortia (RC, TZ and CY consortia) and fertilized with phosphorus levels (25, 50, 75 and 100 %). A 76 % mycorrhizal colonization was obtained with the RC + 25 % phosphorus treatment, where a higher leaf phosphorus content and a higher concentration of stevioside and rebaudioside-A in mg g-1 of dry leaf were also recorded, significantly surpassing conventional fertilization. With this combination, it was possible to improve the yield of stevioside and rebaudioside-A in S. rebaudiana leaves. Furthermore, it is highlighted that the 1H-NMR method was used as a viable alternative to HPLC to quantify the main steviol glycosides in S. rebaudiana, which provides quantitative results in less time and with the same precision.
Downloads
References
Aguilar-Jiménez, D., Piña-Guillén, J., and Silva Díaz, V. 2019. Propagación in vitro de Stevia rebaudiana y análisis preliminar de esteviósidos. Revista mexicana de ciencias agrícolas. 10(1): 197-204. https://doi.org/10.29312/remexca.v10i1.1543
Aranda-González, I., Moguel-Ordoñez, Y., and Betancur-Ancona, D. 2015. Determination of rebaudioside A and Stevioside in leaves of S. rebaudiana Bertoni grown in México by a validated HPLC method. American journal of analytical chemistry. 6(11): 878. https://doi.org/10.4236/ajac.2015.611083
Ahmad, J., Khan, I., Blundell, R., Azzopardi, J., and Mahomoodally, M. F. 2020. Stevia rebaudiana Bertoni: an updated review of its health benefits, industrial applications and safety. Trends in Food Science & Technology. 100: 177-189. https://doi.org/10.1016/j.tifs.2020.04.030
Bagyaraj, D. J., Sharma, M. P., and Maiti, D. 2015. Phosphorus nutrition of crops through arbuscular mycorrhizal fungi. Current Science. 1288-1293. https://www.jstor.org/stable/24905490
Biswapriya, B., M., Ruiz-Hernández, I. M., Hernández-Bolio, G. I., Hernández-Núñez, E., Díaz-Gamboa, R., and Colli-Dula, R., C. 2019. 1H NMR metabolomic analysis of skin and blubber of bottlenose dolphins reveals a functional metabolic dichotomy. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics. 30: 25-32. https://doi.org/10.1016/j.cbd.2019.02.004
Brandle, J., E., and Telmer, P., G. 2007. Steviol glycoside biosynthesis. Phytochemistry. 68(14):1855-1863. https://doi.org/10.1016/j.phytochem.2007.02.010
Cauich Cauich, R., Pérez Gutiérrez, A., Lozano Contreras, M. G., Garruña, R. y Ruíz Sánchez, E. 2018. Productividad de Stevia rebaudiana Bertoni con diferentes láminas de riego e inoculantes microbianos. Nova scientia. 10(20):30-46. https://doi.org/10.21640/ns.v10i20.1166
Chí-Sánchez, F. A., Alvarado-López, C. J., Cristóbal-Alejo, J., González-Moreno, A., and Reyes-Ramírez, A. 2021. Mineral content of landraces maize from Yucatán: analysis by µ-Fluorescence X-ray. Terra Latinoamericana. 39. https://doi.org/10.28940/terra.v39i0.454
Dona, A., C., Kyriakides, M., Scott, F., Shephard, E., A., Varshavi, D., Veselkov, K., and Everett, J. R. 2016. A guide to the identification of metabolites in NMR-based metabonomics/metabolomics ex-periments. Computational and structural biotechnology journal. 14:135-153.
https://doi.org/10.1016/j.csbj.2016.02.005
Eun-Hwa, L., Ju-Kyeong, E., Kang-Hyeon, K. and Ahn-Heum, E. 2013. Diversity of arbuscular mycor-rhizal fungi and their roles in ecosystems. Mycobiology. 41:121–125. https://doi.org/10.5941/MYCO.2013.41.3.121
Ezawa, T., and Saito, K. 2018. How do arbuscular mycorrhizal fungi handle phosphate? New insight into fine‐tuning of phosphate metabolism. New phytologist. 220(4): 1116-1121. https://doi.org/10.1111/nph.15187
Fronza D. and Folegatti M. 2003. Water consumption of the estevia (Stevia rebaudiana (Bert.) Bertoni crop estimated through microlysimeter. Scientia Agricola. 60(3): 595-599. https://doi.org/10.1590/S0103-90162003000300028
Gao, X., Guo, H., Zhang, Q., Guo, H., Zhang, L., Zhang, C. and Zeng, F. 2020. Arbuscular mycorrhizal fungi (AMF) enhanced the growth, yield, fiber quality and phosphorus regulation in upland cotton (Gossypium hirsutum L.). Scientific Reports. 10(1):1-12. https://doi.org/10.1038/s41598-020-59180-3
Giovannetti, M., and Mosse, B. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New phytologist. 489-500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Gerdemann, J. W., and Nicolson, T. H. 1963. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological society. 46(2): 235-244. https://doi.org/10.1016/S0007-1536(63)80079-0
Gupta P., Sharma S., and Saxena S. 2014. Effect of salts (NaCl and Na2CO3) on callus and suspension culture of Stevia rebaudiana for steviol glycoside production. Applied biochemistry and biotech-nology, 172(6), 2894-2906. https://doi.org/10.1007/s12010-014-0736-2
Higo, M., Azuma, M., Kamiyoshihara, Y., Kanda, A., Tatewaki, Y., and Isobe, K. 2020. Impact of phosphorus fertilization on tomato growth and arbuscular mycorrhizal fungal communities. Micro-organisms. 8(2):178. https://doi.org/10.3390/microorganisms8020178
Hoseini, R., Mohammadi, E., and Kalatejari, S. 2015. Effect of bio-fertilizer on growth, development and nutrient content (leaf and soil) of Stevia rebaudiana Bertoni. Journal of Crop Protection. 4(5):691-704. http://jcp.modares.ac.ir/article-3-2883-en.html
Jansa, J., Forczek, S. T., Rozmoš, M., Püschel, D., Bukovská, P., and Hršelová, H. 2019. Arbuscular mycorrhiza and soil organic nitrogen: network of players and interactions. Chemical and Biological Technologies in Agriculture. 6(1):1-10. https://doi.org/10.1186/s40538-019-0147-2
Lima, C. S., Campos, M. A. D. S., and da Silva, F. S. B. 2015. Mycorrhizal Fungi (AMF) increase the content of biomolecules in leaves of Inga vera Willd. seedlings. Symbiosis. 65:117-123.
https://doi.org/10.1007/s13199-015-0325-3
Libik-Konieczny, M., Capecka, E., Tuleja, M., and Konieczny, R. 2021. Synthesis and production of steviol glycosides: recent research trends and perspectives. Applied Microbiology and Biotechnology. 105(10):3883-3900. https://doi.org/10.1007/s00253-021-11306-x
Mandal, S., Upadhyay, S., Singh, V. P., and Kapoor, R. 2015. Enhanced production of steviol glycosides in mycorrhizal plants: a concerted effect of arbuscular mycorrhizal symbiosis on transcription of bi-osynthetic genes. Plant Physiology and Biochemistry. 89:100-106. https://doi.org/10.1016/j.plaphy.2015.02.010
Mandal, S., Evelin, H., Giri, B., Singh, V. P., and Kapoor, R. 2013. Arbuscular mycorrhiza enhances the production of stevioside and rebaudioside-A in Stevia rebaudiana via nutritional and non-nutritional mechanisms. Applied soil ecology. 72:187-194. https://doi.org/10.1016/j.apsoil.2013.07.003.
Mamta R. P., Pathania V., Gulati A., Singh B., Bhanwra R. K., and Tewari R. 2010. Stimulatory effect of phosphate-solubilizing bacteria on plant growth, stevio-side and rebaudioside-A contents of Stevia rebaudiana Bertoni. Applied Soil Ecology. 46:222–229. https://doi.org/10.1016/j.apsoil.2010.08.008
Maniruzzaman, M., Chowdhury, T., Rahman, M. A., and Chowdhury, M. A. H. 2017. Phosphorus use efficiency and critical P content of stevia grown in acid and non-calcareous soils of Bangladesh. Re-search in Agriculture Livestock and Fisheries. 4(2):55-68. https://doi.org/10.3329/ralf.v4i2.33717
Marcinek, K., and Krejpcio, Z. 2016. Stevia rebaudiana Bertoni: health promoting properties and thera-peutic applications. Journal für Verbraucherschutz und Lebensmittelsicherheit. 11(1):3-8.
https://doi.org/10.1007/s00003-015-0968-2
Malz, F., and Jancke, H. 2005. Validation of quantitative NMR. Journal of pharmaceutical and biomedical analysis. 38(5):813-823. https://doi.org/10.1016/j.jpba.2005.01.043
Mohamed, A. A., Ceunen, S., Geuns, J. M., Van den Ende, W., and De Ley, M. 2011. UDP-dependent glycosyltransferases involved in the biosynthesis of steviol glycosides. Journal of plant physiology. 168(10):1136-1141. https://doi.org/10.1016/j.jplph.2011.01.030
Perrier, J. D., Mihalov, J. J., and Carlson, S. J. 2018. FDA regulatory approach to steviol glycosides. Food and Chemical Toxicology. 122:132-142. https://doi.org/10.1016/j.fct.2018.09.062
Pieri, V., Belancic, A., Morales, S., and Stuppner, H. 2011. Identification and quantification of major steviol glycosides in Stevia rebaudiana purified extracts by 1H NMR spectroscopy. Journal of agricultural and food chemistry. 59(9):4378-4384. https://doi.org/10.1021/jf104922q
Phillips, J. M., and Hayman, D. S. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British mycological Society. 55(1):158-161. https://doi.org/10.1016/s0007-1536(70)80110-3
Ramírez-Jaramillo, G. y Lozano-Contreras, M. G. 2017. La producción de Stevia rebaudiana Bertoni en Mexico. AgroProductividad. 10(8):84-90.
https://revista-agroproductividad.org/index.php/agroproductividad/article/view/1080
Rivera-Avilez, J. A., Jarma-Orozco, A., and Pompelli, M. F. 2021. Stevia rebaudiana Bertoni: The in-teraction of night interruption on gas exchange, flowering delay, and steviol glycosides synthesis. Horticulturae. 7(12):543. https://doi.org/10.3390/horticulturae7120543
Roy-Bolduc, A., and Hijri, M. 2011. The use of mycorrhizae to enhance phosphorus uptake: a way out the phosphorus crisis. Journal of Biofertilizers & Biopesticides. 2(104):1-5. https://doi.org/10.4172/2155-6202.1000104
Samsulrizal, N. H., Zainuddin, Z., Noh, A. L., and Sundram, T. C. 2019. A review of approaches in steviol glycosides synthesis. International Journal of Life Sciences and Biotechnology. 2(3):145-157. https://doi.org/10.38001/ijlsb.577338
Sarmiento-López, L. G., López-Meyer, M., Sepúlveda-Jiménez, G., Cárdenas, L., and Rodríguez-Monroy, M. 2021. Arbuscular mycorrhizal symbiosis in Stevia rebaudiana increases trichome development, flavonoid and phenolic compound accumulation. Biocatalysis and Agricultural Biotechnology. 31:101889. https://doi.org/10.1016/j.bcab.2020.101889
Sarmiento-López, L. G., López-Meyer, M., Sepúlveda-Jiménez, G., Cárdenas, L., and Rodríguez-Monroy, M. 2020. Photosynthetic performance and stevioside concentration are improved by the arbuscular mycorrhizal symbiosis in Stevia rebaudiana under different phosphate concentrations. PeerJ. 8:1-23. https://doi.org/10.7717/peerj.10173
Sahodaran, N. K., Arun, A. K., and Ray, J. G. 2019. Native arbuscular mycorrhizal fungal isolates (Funneliformis mosseae and Glomus microcarpum) improve plant height and nutritional status of banana plants. Experimental Agriculture. 55(6):924-933. https://doi.org/10.1017/S0014479719000036
Sieverding, E. 1990. Ecology of VAM fungi in tropical agrosystems. Agriculture, Ecosystems and En-vironment. 29(1-4):369-390. https://doi.org/10.1016/0167-8809(90)90303-U
Sbrana, C., Avio, L., and Giovannetti, M. 2014. Beneficial mycorrhizal symbionts affecting the production of health‐promoting phytochemicals. Electrophoresis. 35(11):1535-1546. https://doi.org/10.1002/elps.201300568
Smith, S. E., Jakobsen, I., Grønlund, M., and Smith, F. A. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant physiology. 156(3):1050-1057. https://doi.org/10.1104/pp.111.174581
Spatafora, J., W., Chang, Y., Benny, G., L., Lazarus, K., Smith, M., E., Berbee, M., L., and Stajich, J., E. 2016. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 108(5):1028-1046. https://doi.org/10.3852/16-042
Tavarini, S., Passera, B., Martini, A., Avio, L., Sbrana, C., Giovannetti, M., and Angelini, L., G. 2018. Plant growth, steviol glycosides and nutrient uptake as affected by arbuscular mycorrhizal fungi and phosphorous fertilization in Stevia rebaudiana Bert. Industrial Crops and Products. 111:899-907. https://doi.org/10.1016/j.indcrop.2017.10.055
Tangpaisarnkul, N., Tuchinda, P., Wilairat, P., Siripinyanond, A., Shiowattana, J., and Nobsathian, S. 2018. Development of pure certified reference material of stevioside. Food chemistry. 255:75-80. https://doi.org/10.1016/j.foodchem.2018.02.029
Zimmerman, E., St-Arnaud, M., and Hijri, M. 2009. Sustainable agriculture and the multigenomic model: how advances in the genetics of arbuscular mycorrhizal fungi will change soil management practices. In Molecular plant-microbe interactions. F. BKBNaD (ed.), pp. 269-287. CAB International., Oxford-shire, UK.
Zubek, S., Mielcarek, S., and Turnau, K. 2012. Hypericin and pseudohypericin concentrations of a valuable medicinal plant Hypericum perforatum L. are enhanced by arbuscular mycorrhizal fungi. Mycorrhiza. 22:149-156. https://doi.org/10.1007/s00572-011-0391-1
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
The journal Biotecnia is licensed under the Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) license.