Journal of Plant Research

, Volume 130, Issue 3, pp 611–624 | Cite as

Silicon alleviates salt and drought stress of Glycyrrhiza uralensis seedling by altering antioxidant metabolism and osmotic adjustment

  • Wenjin Zhang
  • Zhicai Xie
  • Lianhong Wang
  • Ming Li
  • Duoyong Lang
  • Xinhui Zhang
Regular Paper


This study was conducted to determine effect and mechanism of exogenous silicon (Si) on salt and drought tolerance of Glycyrrhiza uralensis seedling by focusing on the pathways of antioxidant defense and osmotic adjustment. Seedling growth, lipid peroxidation, antioxidant metabolism, osmolytes concentration and Si content of G. uralensis seedlings were analyzed under control, salt and drought stress [100 mM NaCl with 0, 10 and 20% of PEG-6000 (Polyethylene glycol-6000)] with or without 1 mM Si. Si addition markedly affected the G. uralensis growth in a combined dose of NaCl and PEG dependent manner. In brief, Si addition improved germination rate, germination index, seedling vitality index and biomass under control and NaCl; Si also increased radicle length under control, NaCl and NaCl—10% PEG, decreased radicle length, seedling vitality index and germination parameters under NaCl—20% PEG. The salt and drought stress-induced-oxidative stress was modulated by Si application. Generally, Si application increased catalase (CAT) activity under control and NaCl—10% PEG, ascorbate peroxidase (APX) activity under all treatments and glutathione (GSH) content under salt combined drought stress as compared with non-Si treatments, which resisted to the increase of superoxide radicals and hydrogen peroxide caused by salt and drought stress and further decreased membrane permeability and malondialdehyde (MDA) concentration. Si application also increased proline concentration under NaCl and NaCl—20% PEG, but decreased it under NaCl—10% PEG, indicating proline play an important role in G. uralensis seedling response to osmotic stress. In conclusion, Si could ameliorate adverse effects of salt and drought stress on G. uralensis likely by reducing oxidative stress and osmotic stress, and the oxidative stress was regulated through enhancing of antioxidants (mainly CAT, APX and GSH) and osmotic stress was regulated by proline.


Glycyrrhiza uralensis Silicon Reactive oxygen species Antioxidant enzymes Non-enzyme antioxidants Osmotic adjustment Salt and drought stress 



The authors are grateful for the financial support provided by the project of the National Natural Science Foundation of China (31460330 and 31260304).


  1. Abbasi GH, Akhtar J, Ahmad R, Jamil M, Anwar-ul-haq M, Ali S, Ijaz M (2015a) Potassium application mitigates salt stress differentially at different growth stages in tolerant and sensitive maize hybrids. Plant Growth Regul 76:111–125CrossRefGoogle Scholar
  2. Abbasi GH, Akhtar J, Anwar-ul-Haq M, Malik W, Ali S, Chen Z, Zhang G (2015b) Morpho-physiological and micrographic characterization of maize hybrids under NaCl and Cd stress. Plant Growth Regul 75:115–122CrossRefGoogle Scholar
  3. Ahmed IM, Dai H, Zheng W, Cao F, Zhang G, Sun D, Wu F (2012) Genotypic differences in physiological characteristics in the tolerance to drought and salinity combined stress between Tibetan wild and cultivated barley. Plant Physiol Biochem 63:49–60CrossRefPubMedGoogle Scholar
  4. Almansouri M, Kinet JM, Lutts S (2001) Effect of salt and osmotic stresses on germination in durum wheat (Triticum durum Desf). Plant Soil 231:243–254CrossRefGoogle Scholar
  5. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:207–216CrossRefGoogle Scholar
  6. Bandani M, Abdolzadeh A (2007) Effects of silicon nutrition on salinity tolerance of (Puccinellia distans). J Sci Food Agric 14:111–119Google Scholar
  7. Bazzaz MM, Hossain MA (2015) Plant water relations and proline accumulations in soybean under salt and water stress environment. J Plant Sci 3:272–278Google Scholar
  8. Bodner G, Nakhforoosh A, Kaul HP (2015) Management of crop water under drought: a review. Agron Sustain Dev 35:401–442CrossRefGoogle Scholar
  9. Bu RF, Xie JM, Yu J, Liao WB, Xiao XM, Lv J, Wang CL, Ye J, Urrea AC (2016) Autotoxicity in cucumber (Cucumis sativus L.) seedling is alleviated by silicon through an increase in the activity of antioxidant enzymes and by mitigating lipid peroxidation. J Plant Biol 59:247–259CrossRefGoogle Scholar
  10. Chołuj D, Karwowska R, Ciszewska A, Jasińska M (2008) Influence of long-term drought stress on osmolyte accumulation in sugar beet (Beta vulgaris L.) plants. Acta Physiol Plant 30:679–687CrossRefGoogle Scholar
  11. Crusciol CA, Pulz AL, Lemos LB, Soratto RP, Lima GP (2009) Effects of silicon and drought stress on tuber yield and leaf biochemical characteristics in potato. Crop Sci 49:949–954CrossRefGoogle Scholar
  12. Dakora FD, Nelwamondo A (2003) Silicon nutrition promotes root growth and tissue mechanical strength in symbiotic cowpea. Funct Plant Biol 30:947–953CrossRefGoogle Scholar
  13. Egamberdieva D, Li L, Lindström K, Räsänen LA (2015) A synergistic interaction between salt-tolerant Pseudomonas and Mesorhizobium strains improves growth and symbiotic performance of liquorice (Glycyrrhiza uralensis Fisch) under salt stress. Appl Microbiol Biotechnol 100:2829–2841CrossRefPubMedGoogle Scholar
  14. Elliot CL, Snyder GH (1991) Autoclave-induced digestion for the colorimetric determination of silicon in rice straw. J Agric Food Chem 39:1118–1119CrossRefGoogle Scholar
  15. Epstein E (1999) Silicon. Annu Rev Plant Physiol 50:641–664CrossRefGoogle Scholar
  16. Epstein E (2009) Silicon: its manifold role in plants. Ann Appl Biol 155:155–160CrossRefGoogle Scholar
  17. Eslami V, Behdani MA, Ali S (2009) Effect of salinity on germination and early seedling growth of canola cultivars. Environ Stress Agri Sci 1:39–46Google Scholar
  18. Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Faiq M (2015) Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul 75:391–404CrossRefGoogle Scholar
  19. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  20. Garg N, Bhandari P (2016) Silicon nutrition and mycorrhizal inoculations improve growth, nutrient status, K+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress. Plant Growth Regul 78:371–387CrossRefGoogle Scholar
  21. Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212CrossRefPubMedGoogle Scholar
  22. Gong HJ, Zhu XY, Chen KM, Wang SM, Zhang CL (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321CrossRefGoogle Scholar
  23. Gong HJ, Chen KM, Zhao ZG, Chen GC, Zhou WJ (2008) Effects of silicon on defense of wheat against oxidative stress under drought at different developmental stages. Biol Plant 52:592–596CrossRefGoogle Scholar
  24. Gunes A, Pilbeam DJ, Inal A, Bagci EG, Coban S (2007) Influence of silicon on antioxidant mechanisms and lipid peroxidation in chickpea (Cicer arietinum L.) cultivars under drought stress. J Plant Interact 2:105–113CrossRefGoogle Scholar
  25. Gunes A, Pilbeam DJ, Inal A, Coban S (2008) Influence of silicon on sunflower cultivars under drought stress, I: growth, antioxidant mechanisms, and lipid peroxidation. Commun Soil Sci Plan 39:1885–1903CrossRefGoogle Scholar
  26. Hajiboland R, Cheraghvareh L (2014) Influence of Si supplementation on growth and some physiological and biochemical parameters in salt-stressed tobacco (Nicotiana rustica L.) plants. J Sci 25:205–217Google Scholar
  27. Hameed A, Sheikh MA, Jamil A, Basra SMA (2013) Seed priming with sodium silicate enhances seed germination and seedling growth in wheat (Triticum aestivum L.) under water deficit stress induced by polyethylene glycol. Pak J Life Soc Sci 11:19–24Google Scholar
  28. Hernandez JA, Jimenez A, Mullineaux P, Sevilia F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  29. Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot 96:1027–1046CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ivanov AA (2015) Response of wheat seedling to combined effect of drought and salinity. In: Stress responses in plants. Springer, New York, pp 159–198CrossRefGoogle Scholar
  31. Jiang J, Su M, Chen Y, Gao N, Jiao C, Sun Z, Wang C (2013) Correlation of drought resistance in grass pea (Lathyrus sativus) with reactive oxygen species scavenging and osmotic adjustment. Biologia 68:231–240CrossRefGoogle Scholar
  32. Kang HM, Saltveit ME (2002) Activity of enzymatic antioxidant defense systems in chilled and heat shocked cucumber seedling radicles. Physiol Plant 113:548–556CrossRefGoogle Scholar
  33. Khan AL, Waqas M, Hussain J, Al-Harrasi A, Lee IJ (2014) Fungal endophyte penicillium janthinellum LK5 can reduce cadmium toxicity in solanum lycopersicum (sitiens and rhe). Biol Fertil Soils 50:75–85CrossRefGoogle Scholar
  34. Khan MSA, Karim MA, Abullah AM, Parveen S, Bazzaz MM, Hossain MA (2015) Plant water relations and proline accumulations in soybean under salt and water stress environment. J Plant Sci 3:272–278Google Scholar
  35. Khawale RN, Singh SK, Patel VS, Singh SP (2003) Changes due to in vitro sodium chloride induced salinity in grape (Vitis vinifera L.). Indian. J Plant Physiol 28:378–382Google Scholar
  36. Kim YH, Khan AL, Waqas M, Jeong HJ, Kim DH, Shin JS, Kim JG, Yeon, MH, Lee IJ (2014). Regulation of jasmonic acid biosynthesis by silicon application during physical injury to Oryza sativa L. J Plant Res 127:525–532CrossRefPubMedGoogle Scholar
  37. Koffler BE, Luschin-Ebengreuth N, Zechmann B (2015) Compartment specific changes of the antioxidative status in Arabidopsis thaliana during salt stress. J Plant Biol 58:8–16CrossRefGoogle Scholar
  38. Li WR, Zhang SQ, Shan L (2007) Physiological and biochemical responses of leaves and root s of alfalfa (Medicago sativa L.) to water stress. Acta Agrest Sin 15:299–305Google Scholar
  39. Li HL, Zhu YX, Hu YH, Han WH, Gong HJ (2015) Beneficial effects of silicon in alleviating salinity stress of tomato seedling grown under sand culture. Acta Physiol Plant 37:1–9CrossRefGoogle Scholar
  40. Li YT, Zhang WJ, Cui JJ, Lang DY, Li M, Zhao QP, Zhang XH (2016) Silicon nutrition alleviates the lipid peroxidation and ion imbalance of Glycyrrhiza uralensis, seedlings under salt stress. Acta Physiol Plant 38:1–9CrossRefGoogle Scholar
  41. Liang YC, Chen Q, Liu Q, Zhang WH, Ding RX (2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). J Plant Physiol 160:1157–1164CrossRefPubMedGoogle Scholar
  42. Liang YC, Zhang WH, Chen Q, Ding RX (2005) Effects of silicon on H+-ATPase and H+-PPase activity, fatty acid composition and fluidity of tonoplast vesicles from roots of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 53:29–37CrossRefGoogle Scholar
  43. Liang YC, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stress in higher plants: a review. Environ Pollut 147:422–428CrossRefPubMedGoogle Scholar
  44. Liu J, Wu L, Wei S, Xiao X, Su C, Jiang P, Yu Z (2007) Effects of arbuscular mycorrhizal fungi on the growth, nutrient uptake and glycyrrhizin production of licorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 52:29–39CrossRefGoogle Scholar
  45. Liu JX, Wang JC, Wang RJ, Jia HY (2012) Interactive effects of drought and salinity stresses on growth and osmotica of naked oat seedling. J Soil Water Conserv 26:244–248 (Chinese)Google Scholar
  46. Liu J, Xia J, Fang Y, Li T, Liu J (2014) Effects of salt-drought stress on growth and physiobiochemical characteristics of Tamarix chinensis seedling. Sci World J. Article ID 765840Google Scholar
  47. Loutfy N, El-Tayeb MA, Hassanen AM, Moustafa MF, Sakuma Y, Inouhe M (2012) Changes in the water status and osmotic solute contents in response to drought and salicylic acid treatments in four different cultivars of wheat (Triticum aestivum). J Plant Res 125:173–184CrossRefPubMedGoogle Scholar
  48. Ma HG, Jiang Q, Wang ZJ, Liu H, He JL (2014) Effects of PEG on Glycyrrhiza uralensis seeds germination and seedling growth. Pratacult Sci 31:1487–1492Google Scholar
  49. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  50. Mohammadkhani N, Heidari R (2008) Effects of drought stress on soluble proteins in two maize varieties. Turk J Biol 32:23–30Google Scholar
  51. Moussa HR (2006) Influence of exogenous application of silicon on physiological response of salt-stressed maize (Zea mays L.). Int J Agric Biol 2:293–297Google Scholar
  52. Muneer S, Jeong BR (2015) Proteomic analysis of salt-stress responsive proteins in roots of tomato (Lycopersicon esculentum L.) plants towards silicon efficiency. Plant Growth Regul 77:1–14CrossRefGoogle Scholar
  53. Murillo-Amador B, Lopez-Aguilar R, Kaya C, Larrinaga-Mayoral J, Flores-Hernandez A (2002) Comparative effects of NaCl and polyethylene glycol on germination, emergence and seedling growth of cowpea. J Agron Crop Sci 188:235–247CrossRefGoogle Scholar
  54. Noman A, Ali S, Naheed F, Ali Q, Farid M, Rizwan M, Irshad MK (2015) Foliar application of ascorbate enhances the physiological and biochemical attributes of maize (Zea mays L.) cultivars under drought stress. Arch Agron Soil Sci 61:1659–1672CrossRefGoogle Scholar
  55. Ozgur R, Uzilday B, Sekmen AH, Turkan I (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847Google Scholar
  56. Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 49:157–165CrossRefGoogle Scholar
  57. Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res Int 22:4056–4075CrossRefPubMedGoogle Scholar
  58. Patil SM, Patil MB, Sapkale GN (2009) Antimicrobial activity of Glycyrrhiza glabra Linn roots. Int J Chem Sci 7:585–591Google Scholar
  59. Pei ZF, Ming DF, Liu D, Wan GL, Geng XX, Gong HJ, Zhou WJ (2010) Silicon improves the tolerance to water-deficit stress induced by polyethylene glycol in wheat (Triticum aestivum L.) seedling. J Plant Growth Regul 29:106–115CrossRefGoogle Scholar
  60. Premachandra GS, Saneoka H, Ogta S (1989) Nutrio-physiological evaluation of the polyethylene glycol test of cell membrane stability in maize. Crop Sci 29:1292–1297CrossRefGoogle Scholar
  61. Ranjan R (2015) Adapting to catastrophic water scarcity in agriculture through social networking and inter-generational occupational transitioning. J Nat Resour Policy Res 7:71–92CrossRefGoogle Scholar
  62. Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202CrossRefGoogle Scholar
  63. Rizwan M, Ali S, Ibrahim M, Farid M, Adrees M, Bharwana SA, Abbas F (2015) Mechanisms of silicon-mediated alleviation of drought and salt stress in plants: a review. Environ Sci Pollut Res Int 22:15416–15431CrossRefPubMedGoogle Scholar
  64. Shahid MA, Balal RM, Pervez MA, Abbas T, Aqeel MA, Javaid MM, Garcia-sanchez F (2015) Foliar spray of phyto-extracts supplemented with silicon: an efficacious strategy to alleviate the salinity-induced deleterious effects in pea (Pisum sativum L.). Turk J Bot 39:408–419CrossRefGoogle Scholar
  65. Shen X, Zhou Y, Duan L, Li Z, Eneji AE, Li J (2010) Silicon effects on photosynthesis and antioxidant parameters of soybean seedling under drought and ultraviolet-B radiation. J Plant physiol 167:1248–1252CrossRefPubMedGoogle Scholar
  66. Sohn YG, Lee BH, Kang KY, Lee JJ (2005) Effects of NaCl stress on germination, antioxidant responses, and proline content in two rice cultivars. J Plant Biol 48:201–208CrossRefGoogle Scholar
  67. Solatni Z, Shekari F, Jamshidi K, Fotovat R, Azimkhani R (2012) The effect of silicon on germination and some growth characteristics of salt-stressed canola seedling. Int J Agron Agric Res 2:12–21Google Scholar
  68. Sonobe K, Hattori T, An P, Tsuji W, Eneji AE, Kobayashi S, Kawamura Y, Tanaka K, Inanaga S (2011) Effect of silicon application on sorghum root responses to water stress. J Plant Nutr 34:71–82CrossRefGoogle Scholar
  69. Soylemezoglu G, Demir K, Inal A, Gunes A (2009) Effect of silicon on antioxidant and stomatal response of two grapevine (Vitis vinifera L.) rootstocks grown in boron toxic, saline and boron toxic-saline soil. Sci Hortic 123:240–246CrossRefGoogle Scholar
  70. Sreenivasulu N, Grimm B, Wobus U, Weschke W (2000) Differential response of antioxidant compounds to salinity stress in salt-tolerant and salt-sensitive seedling of foxtail millet (Setaria italica). Physiol Plant 109:435–442CrossRefGoogle Scholar
  71. Tian Z, Wang F, Zhang W, Liu C, Zhao X (2012) Antioxidant mechanism and lipid peroxidation patterns in leaves and petals of marigold in response to drought stress. Hortic Environ Biotechnol 53:183–192CrossRefGoogle Scholar
  72. Wang WB, Kim YH, Lee HS, Kim KY, Deng XP, Kwak SS (2009). Analysis of antioxidant enzyme activity during germination of alfalfa under salt and drought stresses. Plant Physiol Biochem 47:570–577CrossRefPubMedGoogle Scholar
  73. Wang D, Yu Z, White PJ (2013) The effect of supplemental irrigation after jointing on leaf senescence and grain filling in wheat. Field Crop Res 151:35–44CrossRefGoogle Scholar
  74. Wang L, Chen W, Zhou W (2014) Assessment of future drought in Southwest China based on CMIP5 multimodel projections. Adv Atmos Sci 31:1035–1050CrossRefGoogle Scholar
  75. White JW, Izquierdo J (1991) Physiology of yield potential and stress tolerance. Common beans: research for crop improvement 287–382Google Scholar
  76. Wu CH, Wang QZ, Xie B, Wang ZW, Cui J, Hu TM (2012) Effects of drought and salt stress on seed germination of three leguminous species. Afr J Biotechnol 10:17954–17961Google Scholar
  77. Wu S, Hu C, Tan Q, Nie Z, Sun X (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol Biochem 83:365–374CrossRefPubMedGoogle Scholar
  78. Yang F, Xu X, Xiao X, Li C (2009) Responses to drought stress in two poplar species originating from different altitudes. Biol Plant 53:511–516CrossRefGoogle Scholar
  79. Yin L, Wang S, Liu P, Wang W, Cao D, Deng X, Zhang S (2014) Silicon-mediated changes in polyamine and 1-aminocyclopropane-1-carboxylic acid are involved in silicon-induced drought resistance in Sorghum bicolor L. Plant Physiol Biochem 80:268–277CrossRefPubMedGoogle Scholar
  80. Zhang XH, Zhou D, Cui JJ, Ma HL, Lang DY, Wu XL, Li M (2015) Effect of silicon on seed germination and the physiological characteristics of Glycyrrhiza uralensis under different levels of salinity. J Hortic Sci Biotechnol 90:439–443CrossRefGoogle Scholar
  81. Zhou YH, Yu JQ, Huang LF, Nogués S (2004) The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. Plant Cell Environ 27:1503–1514CrossRefGoogle Scholar
  82. Zhu Y, Gong H (2014) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472CrossRefGoogle Scholar
  83. Zhu Z, Wei G, Li J, Qian Q, Yu J (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533CrossRefGoogle Scholar
  84. Zhuang WW, Li J, Cao MH, Feng WJ, Li YP (2010) Effects of salt-drought intercross stress on physiological and biochemical characteristics of Ammodendron argenteum (Pall) Kuntze seedling. J Wuhan Bot Res 28:730–736 (Chinese)Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2017

Authors and Affiliations

  • Wenjin Zhang
    • 1
  • Zhicai Xie
    • 1
  • Lianhong Wang
    • 3
  • Ming Li
    • 5
  • Duoyong Lang
    • 4
  • Xinhui Zhang
    • 1
    • 2
  1. 1.College of PharmacyNingxia Medical UniversityYinchuanChina
  2. 2.Ningxia Engineering and Technology Research Center of Hui Medicine Modernization, Ningxia Collaborative Innovation Center of Hui Medicine, Laboratory of Hui Ethnic Medicine Modernization, Ministry of EducationNingxia Medical UniversityYinchuanChina
  3. 3.Yantai Institute of Forestry ScienceYantaiChina
  4. 4.Laboratory Animal CenterNingxia Medical UniversityYinchuanChina
  5. 5.Desertification Control InstituteNingxia Academy of Agriculture and Forestry SciencesYinchuanChina

Personalised recommendations