Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Appropriate nitrogen application enhances saponin synthesis and growth mediated by optimizing root nutrient uptake ability

  • Wei, Wei (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Ye, Chen (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Huang, Hui-Chuan (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Yang, Min (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Mei, Xin-Yue (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Du, Fei (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • He, Xia-Hong (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Zhu, Shu-Sheng (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University) ;
  • Liu, Yi-Xiang (State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University)
  • Received : 2018.10.09
  • Accepted : 2019.04.11
  • Published : 2020.07.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Cultivation of medicinal crops, which synthesize hundreds of substances for curative functions, was focused on the synthesis of secondary metabolites rather than biomass accumulation. Nutrition is an important restrict factor for plant growth and secondary metabolites, but little attention has been given to the plasticity of nutrient uptake and secondary metabolites synthesis response to soil nitrogen (N) change. Methods: Two year-field experiments of Sanqi (Panax notoginseng), which can synthesize a high level of saponin in cells, were conducted to study the effects of N application on the temporal dynamics of biomass, nutrient absorption, root architecture and the relationships between these parameters and saponin synthesis. Results: Increasing N fertilizer rates could improve the dry matter yields and nutrient absorption ability through increasing the maximum daily growth (or nutrient uptake) rate. Under suitable N level (225 kg/ha N), Sanqi restricted the root length and surface and enhanced the root diameter and N uptake rate per root length (NURI) to promote nutrient absorption, but the opposite status of Sanqi root architecture and NURI was found when soil N was deficient. Furthermore, increasing N rates could promote the accumulation of saponin in roots through improving the NURI, which showed a significant positive relationship with the content of saponin in the taproots. Conclusion: Appropriate N fertilizer rates could optimize both root architecture and nutrient uptake efficiency, then promote both the accumulation of dry matter and the synthesis of saponins.

Keywords

References

  1. Wang T, Guo R, Zhou G, Zhou X, Kou Z, Sui F, Li C, Tang L, Wang Z. Traditional uses, botany, phytochemistry, pharmacology and toxicology of Panax notoginseng (Burk.) F.H. Chen: a review. J Ethnopharmacol 2016;188:234-58. https://doi.org/10.1016/j.jep.2016.05.005
  2. Yang M, Zhang X, Xu Y, Mei X, Jiang B, Liao J, Yin Z, Zhen J, Zhao Z, Fan L, et al. Autotoxic ginsenosides in the rhizosphere contribute to the replant failure of Panax notoginseng. PLoS One 2015;10:e0118555. https://doi.org/10.1371/journal.pone.0118555
  3. He Y, Song SY, Yong-Hua XU, Gao YG, Zhang LX. Research progress on triterpenoid saponins in Panax ginseng and its ecological effects. Chinese Tradi Herb Drugs 2017;48:1692-8.
  4. Chung AS, Park KM. Chapter 4. Anticancer and antineurodegenerative effects of ginsenosides. Stud Nat Prod Chem 2016;50.
  5. Leung KW, Wong ST. Pharmacology of ginsenosides: a literature review. Chin Med 2010;5:20. https://doi.org/10.1186/1749-8546-5-20
  6. Liu Y, Zhang W, Sun J, Li X, Christie P, Li L. High morphological and physiological plasticity of wheat roots is conducive to higher competitive ability of wheat than maize in intercropping systems. Plant Soil 2015;397:387-99. https://doi.org/10.1007/s11104-015-2654-7
  7. Trinder C, Brooker R, Davidson H, Robinson D. Dynamic trajectories of growth and nitrogen capture by competing plants. New Phytol 2012;193:948-58. https://doi.org/10.1111/j.1469-8137.2011.04020.x
  8. Trinder CJ, Brooker RW, Robinson D. Plant ecology's guilty little secret: understanding the dynamics of plant competition. Func Ecol 2013;27:918-29. https://doi.org/10.1111/1365-2435.12078
  9. Sun Y, Chen Z, Wei M. Effects of various nitrogen fertilizers on the yield and quality of Panax notoginseng. Soil Fertil Sci China 2008;26:22-5.
  10. Wang C, Chen Z, Sun Y. Effect of different proportion fertilizing on the growth and yield of Panax notoginseng. Res Pract Chinese Med 2007;21:5-7. https://doi.org/10.3969/j.issn.1673-6427.2007.01.002
  11. Wei M, Sun Y, Huang T. Effects on the growth and the contents of saponin with different level of nitrogen applied in Panax notoginseng. Res Pract Chinese Med 2008;22:17-20.
  12. Andersen M, Hauggaardnielsen H, Jacob W, Eriksteen J. Competitive dynamics in two- and three-component intercrops. J Appl Ecol 2007;44:545-51. https://doi.org/10.1111/j.1365-2664.2007.01289.x
  13. Gaude N, Brehelin C, Tischendorf G, Kessler F, Dormann P. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytylesters. Plant J 2007;49:729-39. https://doi.org/10.1111/j.1365-313X.2006.02992.x
  14. Kang JH. Study on the relationship between the main secondary metabolites and polysaccharide in fruits of Lycium barbarum at different application amounts of nitrogen. J Anhui Agr Sci 2008;36:16008-10.
  15. Gershenzon J. Changes in the levels of plant secondary metabolites under water and nutrient stress. In: Timmermann BN, Steelink C, Loewus FA, editors. Phytochemical adaptations to stress. Boston: Springer; 2002. p. 273-320.
  16. Szakiel A, Pa˛czkowski C, Henry M. Influence of environmental biotic factors on the content of saponins in plants. Phytochem Rev 2011;10:493-502. https://doi.org/10.1007/s11101-010-9164-2
  17. Fan W, Yang H. Effect of soil type on root architecture and nutrient uptake by roots of young apple rootstocks. Acta Horticulturae 2011:885-90.
  18. Forde B, Lorenzo H. The nutritional control of root development. Plant Soil 2001;232:51-68. https://doi.org/10.1023/A:1010329902165
  19. Yan HT, Beyrouty CA, Norman RJ, Gbur EE. Nutrient uptake relationship to root characteristics of rice. Plant Soil 1995;171:297-302. https://doi.org/10.1007/BF00010285
  20. Gruber BD, Giehl RF, Friedel S, von Wiren N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 2013;163:161-79. https://doi.org/10.1104/pp.113.218453
  21. Mou P, Jones RH, Tan Z, Bao Z, Chen H. Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous. Plant Soil 2013;364:373-84. https://doi.org/10.1007/s11104-012-1336-y
  22. Sultan SE. Phenotypic plasticity for plant development, function and lifehistory. Trends Plant Sci 2001;5:537-42. https://doi.org/10.1016/S1360-1385(00)01797-0
  23. Pigliucci M, Hayden K. Phenotypic plasticity is the major determinant of changes in phenotypic integration in Arabidopsis. New Phytol 2001;152:419-30. https://doi.org/10.1046/j.0028-646X.2001.00275.x
  24. Hunt R. Plant growth analysis. Suffolk: The Lavenham Press; 1982.
  25. Page AL, Miller RH, Keeney DR. Methods of soil analysis. Part 2: chemical and microbiological properties. 2nd ed. Madison: ASA and SSSA; 1982. p. 643-98.
  26. Ou X, Yang Y, Guo L, Zhu D, Liu D. Effect of organic-inorganic N sources on growth, Npk nutrients and secondary metabolites of Panax notoginseng (Burk.) F. H. Chen. Emir J Food Agr 2017:629-38. https://doi.org/10.9755/ejfa.2015.04.016
  27. Brokaw N, Busing RT. Niche versus chance and tree diversity in forest gaps. Trends Ecol Evol 2000;15:183. https://doi.org/10.1016/S0169-5347(00)01822-X
  28. Hauggaard-Nielsen H, Jensen ES. Evaluating pea and barley cultivars for complementarity in intercropping at different levels of soil N availability. Field Crop Res 2001;72:185-96. https://doi.org/10.1016/S0378-4290(01)00176-9
  29. Cui X, Wang c. Study on the growth and dry matter accumulation dynamics of Panax notoginseng. Chinese Herb Med 1991;9:9-11.
  30. Liu Z, Li S, Sun Y, Xiu L, Zhang H, Lu j. Dynamic changes of dry matter accumulation and distribution of ginseng. Spec Wild Econ Anim Plant Res 1994;4:32-5.
  31. Lindhauer MG, Fekete MARD. Starch synthesis in potato (Solanum tuberosum) tubers: activity of selected enzymes in dependence of potassium content in storage tissue. Plant Soil 1990;124:291-5. https://doi.org/10.1007/BF00009275
  32. Wang S, Yu Z, Wang D. Effect of potassium on sucrose content of flag leaves and starch accumulation of kernels in wheat. Acta Phytoecologica Sinica 2003;27:196-201.
  33. Grime JP. Plant strategies and vegetation processes. Biologia Plantarum 1979;23:254. https://doi.org/10.1007/BF02895358
  34. Zhang W, Liu G, Sun J, Zhang L, Weiner J, Li L. Growth trajectories and interspecific competitive dynamics in wheat/maize and barley/maize intercropping. Plant Soil 2015;397:227-38. https://doi.org/10.1007/s11104-015-2619-x
  35. Wei W, Yang M, Liu Y, Huang H, Ye C, Zheng J, Guo C, Hao M, He X, Zhu S. Fertilizer N application rate impacts plant-soil feedback in a sanqi production system. Sci Total Environ 2018;633:796-807. https://doi.org/10.1016/j.scitotenv.2018.03.219
  36. Croft SA, Hodge A, Pitchford JW. Optimal root proliferation strategies: the roles of nutrient heterogeneity, competition and mycorrhizal networks. Plant Soil 2012;351:191-206. https://doi.org/10.1007/s11104-011-0943-3
  37. Giehl RFH, Gruber BD, Von Wiren N. It's time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 2014;65:769-78. https://doi.org/10.1093/jxb/ert421
  38. Cahill JF, Mcnickle GG, Haag JJ, Lamb EG, Nyanumba SM, Clair CCS. Plants integrate information about nutrients and neighbors. Science 2010;328:1657. https://doi.org/10.1126/science.1189736
  39. Orians CM, Babst B, Zanne AE. 17 - Vascular constraints and long distance transport in dicots. Vasc Transport 512 Plant 2005:355-71.
  40. Robinson D. The responses of plants to nonuniform supplies of nutrients. New Phytol 1994;127:635-74. https://doi.org/10.1111/j.1469-8137.1994.tb02969.x
  41. Arena ME, Postemsky PD, Curvetto NR. Changes in the phenolic compounds and antioxidant capacity of Berberis microphylla G. Forst. berries in relation to light intensity and fertilization. Sci Hortic 2017;218:63-71. Amsterdam. https://doi.org/10.1016/j.scienta.2017.02.004
  42. Virjamo V, Sutinen S, Julkunen-Tiitto R. Combined effect of elevated UVB, elevated temperature and fertilization on growth, needle structure and phytochemistry of young Norway spruce (Picea abies) seedlings. Global Change Biol 2014;20:2252-60. https://doi.org/10.1111/gcb.12464
  43. Woodrow P, Ciarmiello LF, Annunziata MG, Pacifico S, Iannuzzi F, Mirto A, D'Amelia L, Dell'Aversana E, Piccolella S, Fuggi A, et al. Durum wheat seedling responses to simultaneous high light and salinity involve a fine reconfiguration of amino acids and carbohydrate metabolism. Physiol Plantarum 2016;159:290. https://doi.org/10.1111/ppl.12513
  44. Ibrahim MH, Jaafar HZ, Rahmat A, Rahman ZA. The relationship between phenolics and flavonoids production with total non structural carbohydrate and photosynthetic rate in Labisia pumila Benth. under high $CO_{2}$ and nitrogen fertilization. Molecules 2011;16:162-74. https://doi.org/10.3390/molecules16010162
  45. Ciesiolka D, Gulewicz P, Martinezvillaluenga C, Pilarski R, Bednarczyk M, Gulewicz K. Products and biopreparations from alkaloid-rich lupin in animal nutrition and ecological agriculture. Folia Biol-Prague 2005;53:59-66. https://doi.org/10.3409/173491605775789443
  46. Zhou L, Yue Q, Zhao L, Cui R, Liu X. Effect of nitrogen level on growth and metabolism of Allium fistulosum L. In: International Conference on Energy, Environment and Sustainable Development; 2018.
  47. Flemotomou E, Molyviatis T, Zabetakis I. The effect of trace elements accumulation on the levels of secondary metabolites and antioxidant activity in carrots, onions and potatoes. Food Nutr Sci 2011;2:1071-6. https://doi.org/10.4236/fns.2011.210143

Cited by

  1. A Panax notoginseng Root Tip Meristem Biosensor and Its Sensing Kinetics for Five Important Nitrogen Nutrients vol.2021, 2020, https://doi.org/10.1155/2021/5526850
  2. Microalgae biofilm cultured in nutrient-rich water as a tool for the phycoremediation of petroleum-contaminated water vol.23, pp.11, 2021, https://doi.org/10.1080/15226514.2021.1882934
  3. Growth, Yield, Quality, and Phytochemical Behavior of Three Cultivars of Quinoa in Response to Moringa and Azolla Extracts under Organic Farming Conditions vol.11, pp.11, 2020, https://doi.org/10.3390/agronomy11112186
  4. Enrichment of Burkholderia in the Rhizosphere by Autotoxic Ginsenosides to Alleviate Negative Plant-Soil Feedback vol.9, pp.3, 2020, https://doi.org/10.1128/spectrum.01400-21