Skip to main content
Log in

Autotoxicity in cucumber (Cucumis sativus L.) seedlings is alleviated by silicon through an increase in the activity of antioxidant enzymes and by mitigating lipid peroxidation

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Autotoxicity in plants limits their growth and that of nearby plants of the same species, which has obvious implications in crop yield and quality. Silicon (Si) has been shown to increase plant tolerance to autotoxic stress. However, the physiological mechanisms underlying the effects of Si in alleviating autotoxicity during germination in cucumber (Cucumis sativus L.) are unknown. Cinnamic acid derivatives, such as 3-phenylpropionic acid (PA), are a class of autotoxins present in cucumber root exudates. Our objective was to investigate Si-induced autotoxic stress tolerance in cucumber seedlings by focusing on the effects of Si on the induction of antioxidant defense pathways. We found that PA treatment significantly reduced seed germination, radicle length, lateral root number, fresh weight, AsA and GSH contents, and the activities of SOD, CAT, and APX in cucumber seedlings, while it increased membrane permeability and levels of MDA, proline, O -2 , and H2O2. Application of Si enhanced growth of PA-treated plants and significantly increased germination rate, radicle length, lateral root number, fresh weight, AsA and GSH levels, and SOD, CAT, POD, and APX activities. These results suggest that exogenous Si alleviates autotoxicity caused by PA during seed germination by increasing antioxidant enzyme activities and mitigating lipid peroxidation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F (1998) Effects of silicon on tolerance to water deficit and heat stress in rice plants (Oryza sativa L.), monitored by electrolyte leakage. Plant Prod Sci 1:96–103

    Article  Google Scholar 

  • Al-aghabary K, Zhu Z, Shi Q (2005) Influence of silicon supply on chlorophyll content, chlorophyll fluorescence, and antioxidative enzyme activities in tomato plants under salt stress. J Plant Nutr 27:2101–2115

    Article  Google Scholar 

  • Asada K (1992) Ascorbate peroxidase-a hydrogen peroxide-scavenging enzyme in plants. Physiol Plantarum 85:235–241

    Article  CAS  Google Scholar 

  • Ashraf M, Afzal M, Ahmed R, Mujeeb F, Sarwar A, Ali L (2010) Alleviation of detrimental effects of NaCl by silicon nutrition in salt-sensitive and salt-tolerant genotypes of sugarcane (Saccharum officinarum L.). Plant Soil 326:381–391

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Batish DR, Singh HP, Kaur S, Kohli RK, Yadav SS (2008) Caffeic acid affects early growth, and morphogenetic response of hypocotyl cuttings of mung bean (Phaseolus aureus). J Plant Physiol 165:297–305

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Yao XQ, Cai KZ, Chen JN (2011) Silicon alleviates drought stress of rice plants by improving plant water status, photosynthesis and mineral nutrient absorption. Biol Trace Elem Res 142:67–76

    Article  CAS  PubMed  Google Scholar 

  • Chérif M, Asselin A, Bélanger RR (1994) Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Phytopathology 84:236–242

    Article  Google Scholar 

  • Dai AH, Nie YX, Yu B, Li Q, Lu LY, Bai JG (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Díaz-Vivancos P, Rubio M, Mesonero V, Periago PM, Barceló AR, Martínez-Gómez P, Hernández JA (2006) The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 57:3813–3824

    Article  PubMed  Google Scholar 

  • Ding J, Sun Y, Xiao CL, Shi K, Zhou YH, Yu JQ (2007) Physiological basis of different allelopathic reactions of cucumber and figleaf gourd plants to cinnamic acid. J Exp Bot 58:3765–3773

    Article  CAS  PubMed  Google Scholar 

  • Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620

    Article  CAS  PubMed  Google Scholar 

  • Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci USA 91:11–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Epstein E (1999) Silicon. Ann Rev Plant Biol 50:641–664

    Article  CAS  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acidinduced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plantarum 92:696–717

    Article  CAS  Google Scholar 

  • Foyer CH, Theodoulou FL, Delrot S (2001) The functions of interand intracellular glutathione transport systems in plants. Trends Plant Sci 6:486–492

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (1975) Superoxide dismutases. Annu Rev Biochem 44:147–159

    Article  CAS  PubMed  Google Scholar 

  • Gezi L, Xiaoqi P, Liting W, Guozhang K (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321–325

    Article  Google Scholar 

  • 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 Plantarum 52:592–596

    Article  CAS  Google Scholar 

  • Gong HJ, Zhu XY, Chen KM, Wang SM, Zhang CL (2005) Silicon alleviates oxidative damage of wheat plants in pots under drought. Plant Sci 169:313–321

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Bagci E G, Coban S, Pilbeam DJ (2007a) Silicon mediates changes to some physiological and enzymatic parameters symptomatic for oxidative stress in spinach (Spinacia oleracea L.) grown under B toxicity. Sci Hortic 113:113–119

    Article  CAS  Google Scholar 

  • Gunes A, Inal A, Bagci EG, Coban S, Sahin O (2007b) Silicon increases boron tolerance and reduces oxidative damage of wheat grown in soil with excess boron. Biol Plantarum 51:571–574

    Article  CAS  Google Scholar 

  • Guri A (1983) Variation in glutathione and ascorbic acid content among selected cultivars of Phaseolus vulgaris prior to and after exposure to ozone. Can J Plant Sci 63:733–737

    Article  CAS  Google Scholar 

  • Hwang SY, Lin HW, Chern RH, Lo HF, Li L (1999) Reduced susceptibility to waterlogging together with high-light stress is related to increases in superoxide dismutase and catalase activities in sweet potato. Plant Growth Regul 27:167–172

    Article  CAS  Google Scholar 

  • Hodson MJ, White PJ, Mead A, Broadley MR (2005) Phylogenetic variation in the silicon composition of plants. Ann Bot (Lond.) 96:1027–1046

    Article  CAS  Google Scholar 

  • Jarvis SC (1987) The uptake and transport of silicon by perennial ryegrass and wheat. Plant Soil 97:429–437

    Article  CAS  Google Scholar 

  • Jiménez A, Hernández JA, Pastori G, Río LAD, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones LHP, Handreck KA (1967) Silica in soils, plants and animals. Adv Agron 19:107–149

    Article  CAS  Google Scholar 

  • Kampfenkel K, Vanmontagu M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  CAS  PubMed  Google Scholar 

  • Kauss H, Seehaus K, Franke R, Gilbert S, Dietrich RA, Kröger N (2003) Silica deposition by a strongly cationic proline-rich protein from systemically resistant cucumber plants. Plant J 33:87–95

    Article  CAS  PubMed  Google Scholar 

  • Kim SG, Kim KW, Park EW, Choi D. (2002) Silicon-induced cell wall fortification of rice leaves: a possible cellular mechanism of enhanced host resistance to blast. Phytopathology 92(10):1095–1103

    Article  PubMed  Google Scholar 

  • Kumar GNM, Knowles NR (1993) Changes in lipid peroxidation and lipolytic and free-radical scavenging enzyme activities during aging and sprouting of potato (Solanum tuberosum) seed-tubers. Plant Physiol 102:115–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    Article  CAS  PubMed  Google Scholar 

  • Liang Y (1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant Soil 209:217–224

    Article  CAS  Google Scholar 

  • Liang Y, Si J, Römheld V (2005a) Silicon uptake and transport is an active process in Cucumis sativus. New Phytol 167(3):797–804

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of siliconmediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut 147:422–428

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Wong JWC, Wei L (2005c) Silicon-mediated enhancement of cadmium tolerance in maize (Zea mays L.) grown in cadmium contaminated soil. Chemosphere 58:475–483

    Article  CAS  PubMed  Google Scholar 

  • Liang YC, Shen QR, Shen ZG, Ma TS (1996) Effects of silicon on salinity tolerance of two barley cultivars. J Plant Nutr 19:173–183

    Article  CAS  Google Scholar 

  • Liang YC, Zhang WH, Chen Q, Ding RX (2005b) Effects of silicon on tonoplast H+-ATPase and H+-PPase activity, fatty acid composition and fluidity in roots of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 53:29–37

    Article  CAS  Google Scholar 

  • Liang YC, Zhang WH, Chen Q, Liu YL, Ding RX (2006) Effect of exogenous silicon (Si) on H+-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 57:212–219

    Article  CAS  Google Scholar 

  • Liang YC, Zhu J, Li ZJ, Chu GX, Ding YF, Zhang J, Sun WC (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ Exp Bot 64:286–294

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luster DG, Donaldson RP (1987) Orientation of electron transport activities in the membrane of intact glyoxysomes isolated from castor bean endosperm. Plant Physiol 85:796–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot-London 78:389–398

    Article  CAS  Google Scholar 

  • Ma DY, Sun DX, Wang CY, Qin HX, Ding HN, Li YG, Guo TC (2015) Silicon application alleviates drought stress in wheat through transcriptional regulation of multiple antioxidant defense pathways. J Plant Growth Regul pp. 1–10

    Google Scholar 

  • Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18

    Article  CAS  Google Scholar 

  • Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. Elsevier

    Google Scholar 

  • Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M (2006) A silicon transporter in rice. Nature 440:688–691

    Article  CAS  PubMed  Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397

    Article  CAS  PubMed  Google Scholar 

  • Maksimoviæ JD, Mojoviæ M, Maksimoviæ V, Römheld V, Nikolic M (2012) Silicon ameliorates manganese toxicity in cucumber by decreasing hydroxyl radical accumulation in the leaf apoplast. J Exp Bot 63:2411–2420

    Article  Google Scholar 

  • Mateos-Naranjo E, Andrades-Moreno L, Davy AJ (2013) Silicon alleviates deleterious effects of high salinity on the halophytic grass Spartina densiflora. Plant Physiol Bioch 63:115–121

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stressinduced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Physiol Plantarum 58:166–170

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Pereira GJG, Molina SMG, Lea PJ, Azevedo RA (2002) Activity of antioxidant enzymes in response to cadmium in Crotalaria juncea. Plant Soil 239:123–132

    Article  CAS  Google Scholar 

  • Ramiro DA, Guerreiro-Filho O, Mazzafera P (2006) Phenol contents, oxidase activities, and the resistance of coffee to the leaf miner Leucoptera coffeella. J Chem Ecol 32:1977–1988

    Article  CAS  PubMed  Google Scholar 

  • Richmond KE, Sussman M (2003) Got silicon? The non-essential beneficial plant nutrient. Curr. Opin. Plant Biol 6:268–272

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez R, Redman R (2005) Balancing the generation and elimination of reactive oxygen species. Proc Natl Acad Sci USA 102:3175–3176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan C, He F, Xu G, Han R, Liang Z (2012) Nitric oxide is involved in the regulation of ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Biol Plantarum 56:187–191

    Article  CAS  Google Scholar 

  • Shen XF, Zhou YY, Duan LS, Li ZH, Eneji AE, Li JM (2010) Silicon effects on photosynthesis and antioxidant parameters of soybean seedlings under drought and ultraviolet-B radiation. J Plant Physiol 167:1248–1252

    Article  CAS  PubMed  Google Scholar 

  • Shi QH, Bao ZY, Zhu ZJ, He Y, Qian QQ, Yu JQ (2005) Siliconmediated alleviation of Mn toxicity in Cucumis sativus in relation to activities of superoxide dismutase and ascorbate peroxidase. Phytochemistry 66:1551–1559

    Article  CAS  PubMed  Google Scholar 

  • Song AL, Li ZJ, Zhang J, Xue GF, Fan FL, Liang YC (2009) Siliconenhanced resistance to cadmium toxicity in Brassica chinensis L. is attributed to Si-suppressed cadmium uptake and transport and Si-enhanced antioxidant defense capacity. J Hazard Mater 172:74–83

    CAS  PubMed  Google Scholar 

  • Van der Vorm PDJ (1987) Dry ashing of plant material and dissolution of the ash in HF for the colorimetric determination of silicon. Commun Soil Sci Plan 18:1181–1189

    Article  Google Scholar 

  • Vyas D, Kumar S (2005) Purification and partial characterization of a low temperature responsive Mn-SOD from tea (Camellia sinensis (L.) O. Kuntze). Biochem Bioph Res Co 329(3):831–838

    Article  CAS  Google Scholar 

  • Xie ZX, Duan LS, Tian XL, Wang BM, Eneji AE, Li ZH (2008) Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J Plant Physiol 165:375–384

    Article  CAS  PubMed  Google Scholar 

  • Ye SF, Zhou YH, Sun Y, Zou LY, Yu JQ (2006) Cinnamic acid causes oxidative stress in cucumber roots, and promotes incidence of Fusarium wilt. Environ Exp Bot 56:255–262

    Article  CAS  Google Scholar 

  • Yu JQ, Matsui Y (1997) Effects of root exudates of cucumber (Cucumis sativus) and allelochemicals on ion uptake by cucumber seedlings. J Chem Ecol 23:817–827

    Article  CAS  Google Scholar 

  • Yu JQ, Matsui Y (1994) Phytotoxic substances in root exudates of cucumber (Cucumis sativus L.). J Chem Ecol 20:21–31

    Article  CAS  PubMed  Google Scholar 

  • Yu JQ, Shou SY, Qian YR, Zhu ZJ, Hu WH (2000) Autotoxic potential of cucurbit crops. Plant Soil 223:149–153

    Article  Google Scholar 

  • Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139

    Article  CAS  Google Scholar 

  • Zhang PY, Gao RG, Yang FJ, Wang XF, Wei M, Shi QH, Li Y (2014) Effects of silicon on photosynthetic characteristics and activity of antioxidant enzymes in continuous-cropped cucumber seedlings. Chinese Journal of Applied Ecology 25:1733–1738

    CAS  PubMed  Google Scholar 

  • Zhang Y, Gu M, Xia XJ, Shi K, Zhou YH, Yu JQ (2009) Effects of phenylcarboxylic acids on mitosis, endoreduplication and expression of cell cycle-related genes in roots of cucumber (Cucumis sativus L.). J Chem Ecol 35:679–688

    Article  CAS  PubMed  Google Scholar 

  • Zhu ZJ, Wei GQ, Li J, Qian QQ, Yu JQ (2004) Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci 167:527–533

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jianming Xie.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bu, R., Xie, J., Yu, J. et al. Autotoxicity in cucumber (Cucumis sativus L.) seedlings is alleviated by silicon through an increase in the activity of antioxidant enzymes and by mitigating lipid peroxidation. J. Plant Biol. 59, 247–259 (2016). https://doi.org/10.1007/s12374-016-0526-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0526-1

Keywords

Navigation