Abstract
Key message
Silicon enhances root water uptake in salt-stressed cucumber plants through up-regulating aquaporin gene expression. Osmotic adjustment is a genotype-dependent mechanism for silicon-enhanced water uptake in plants.
Abstract
Silicon can alleviate salt stress in plants. However, the mechanism is still not fully understood, and the possible role of silicon in alleviating salt-induced osmotic stress and the underlying mechanism still remain to be investigated. In this study, the effects of silicon (0.3 mM) on Na accumulation, water uptake, and transport were investigated in two cucumber (Cucumis sativus L.) cultivars (‘JinYou 1’ and ‘JinChun 5’) under salt stress (75 mM NaCl). Salt stress inhibited the plant growth and photosynthesis and decreased leaf transpiration and water content, while added silicon ameliorated these negative effects. Silicon addition only slightly decreased the shoot Na levels per dry weight in ‘JinYou 1’ but not in ‘JinChun 5’ after 10 days of stress. Silicon addition reduced stress-induced decreases in root hydraulic conductivity and/or leaf-specific conductivity. Expressions of main plasma membrane aquaporin genes in roots were increased by added silicon, and the involvement of aquaporins in water uptake was supported by application of aquaporin inhibitor and restorative. Besides, silicon application decreased the root xylem osmotic potential and increased root soluble sugar levels in ‘JinYou 1.’ Our results suggest that silicon can improve salt tolerance of cucumber plants through enhancing root water uptake, and silicon-mediated up-regulation of aquaporin gene expression may in part contribute to the increase in water uptake. In addition, osmotic adjustment may be a genotype-dependent mechanism for silicon-enhanced water uptake in plants.
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Abbreviations
- A leaf :
-
Supported leaf area
- DTT:
-
Dithiothreitol
- E :
-
Transpiration rate
- g s :
-
Stomatal conductance
- Lpr :
-
Root hydraulic conductance
- L sc :
-
Leaf-specific conductivity of the stem
- PIP:
-
Plasma membrane intrinsic protein
- P n :
-
Net CO2 assimilation rate
- SL:
-
Stem length
References
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164:1600–1618
Chen W, Yao X, Cai K, Chen J (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
Dannon EA, Wydra K (2004) Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes. Physiol Mol Plant 64:233–243
Dichio B, Montanaro G, Sofo A, Xiloyannis C (2013) Stem and whole-plant hydraulics in olive (Olea europaea) and kiwifruit (Actinidia deliciosa). Trees 27:183–191
Diogo RVC, Wydra K (2007) Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol Mol Plant 70:120–129
Dragisic Maksimovic J, Mojovic M, Maksimovic V, Romheld 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
Fuhrs H, Gotze S, Specht A, Erban A, Gallien S, Heintz D, Van Dorsselaer A, Kopka J, Braun HP, Horst WJ (2009) Characterization of leaf apoplastic peroxidases and metabolites in Vigna unguiculata in response to toxic manganese supply and silicon. J Exp Bot 60:1663–1667
Gao X, Zou C, Wang L, Zhang F (2004) Silicon improves water use efficiency in maize plants. J Plant Nutr 27:1457–1470
Gao X, Zou C, Wang L, Zhang F (2006) Silicon decreases transpiration rate and conductance from stomata of maize plants. J Plant Nutr 29:1637–1647
Ghareeb H, Bozsó Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant 75:83–89
Gong HJ, Randall DP, Flowers TJ (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant Cell Environ 29:1970–1979
Gunes A, Inal A, Bagci EG, Coban S (2007a) Silicon-mediated changes on some physiological and enzymatic parameters symptomatic of oxidative stress in barley grown in sodic-B toxic soil. J Plant Physiol 164:807–811
Gunes A, Inal A, Bagci EG, Pilbeam D (2007b) Silicon-mediated changes of some physiological and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in sodic-B toxic soil. Plant Soil 290:103–114
Guntzer F, Keller C, Meunier J (2012) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32:201–213
Hattori T, Inanaga S, Araki H, An P, Morita S, Luxova M, Lux A (2005) Application of silicon enhanced drought tolerance in Sorghum bicolor. Physiol Plant 123:459–466
Hattori T, Sonobe K, Inanaga S, An P, Morita S (2008) Effects of silicon on photosynthesis of young cucumber seedlings under osmotic stress. J Plant Nutr 31:1046–1058
Heine G, Tikum G, Horst W (2006) The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd. J Exp Bot 58:569–577
Huang Y, Bie ZL, Liu ZX, Zhen A, Wang WJ (2009) Protective role of proline against salt stress is partially related to the improvement of water status and peroxidase enzyme activity in cucumber. Soil Sci Plant Nutr 55:698–704
Husain S, von Caemmerer S, Munns R (2004) Control of salt transport from roots to shoots of wheat in saline soil. Funct Plant Biol 31:1115–1126
Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–313
Kiirika LM, Stahl F, Wydra K (2013) Phenotypic and molecular characterization of resistance induction by single and combined application of chitosan and silicon in tomato against Ralstonia solanacearum. Physiol Mol Plant 81:1–12
Knipfer T, Besse M, Verdeil JL, Fricke W (2011) Aquaporin-facilitated water uptake in barley (Hordeum vulgare L.) roots. J Exp Bot 62:4115–4126
Kurabachew H, Wydra K (2014) Induction of systemic resistance and defense-related enzymes after elicitation of resistance by rhizobacteria and silicon application against Ralstonia solanacearum in tomato (Solanum lycopersicum). Crop Prot 57:1–7
Lee SK, Sohn EY, Hamayun M, Yoon JY, Lee IJ (2010) Effect of silicon on growth and salinity stress of soybean plant grown under hydroponic system. Agrofor Syst 80:333–340
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
Liang Y, Zhang W, Chen Q, Ding R (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 53:29–37
Liang Y, Zhu J, Li Z, Chu G, Ding Y, Zhang J, Sun W (2008) Role of silicon in enhancing resistance to freezing stress in two contrasting winter wheat cultivars. Environ Exp Bot 64:286–294
Liu P, Yin L, Deng X, Wang S, Tanaka K, Zhang S (2014) Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J Exp Bot 65:4747–4756
Liu P, Yin L, Wang S, Zhang M, Deng X, Zhang S, Tanaka K (2015) Enhanced root hydraulic conductance by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress in Sorghum bicolor L. Environ Exp Bot 111:42–51
Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65:3049–3057
Machado S, Paulsed GM (2001) Combined effects of drought and high temperature on water relations of wheat and sorghum. Plant Soil 233:179–187
Matoh T, Kairusmee P, Takahashi E (1986) Salt-induced damage to rice plants and alleviation effect of silicate. Soil Sci Plant Nutr 32:295–304
Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624
Ming DF, Pei ZF, Naeem MS, Gong HJ, Zhou WJ (2012) Silicon alleviates PEG-induced water-deficit stress in upland rice seedlings by enhancing osmotic adjustment. J Agron Crop Sci 198:14–26
Mišić D, Šiler B, Nestorović Živković J, Simonović A, Maksimović V, Budimir S, Janošević D, Đuričković M, Nikolić M (2012) Contribution of inorganic cations and organic compounds to osmotic adjustment in root cultures of two Centaurium species differing in tolerance to salt stress. Plant Cell Tiss Org (PCTOC) 108:389–400
Mitani N, Ma JF (2005) Uptake system of silicon in different plant species. J Exp Bot 56:1255–1261
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotox Environ Safe 60:324–349
Pfaffl M (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:203–207
Qian ZJ, Song JJ, Chaumont F, Ye Q (2014) Differential responses of plasma membrane aquaporins in mediating water transport of cucumber seedlings under osmotic and salt stresses. Plant Cell Environ 38:461–473
Ranganathan S, Suvarchala V, Rajesh YBRD, Srinivasa Prasad M, Padmakumari AP, Voleti SR (2006) Effects of silicon sources on its deposition, chlorophyll content, and disease and pest resistance in rice. Biol Plant 50:713–716
Romero-Aranda MR, Jurado O, Cuartero J (2006) Silicon alleviates the deleterious salt effect on tomato plant growth by improving plant water status. J Plant Physiol 163:847–855
Rubio-Asensio JS, López-Berenguer C, Garma JG, Burger M, Bloom AJ (2014) Root strategies for nitrate assimilation. In: Morte A, Varma A (eds) Root Engineering: basic and applied concepts. Springer, Heidelberg, pp 251–267
Savant NK, Korndörfer GH, Datnoff LE, Snyder GH (1999) Silicon nutrition and sugarcane production: a review. J Plant Nutr 22:1853–1903
Shahzad M, Zörb C, Geilfus CM, Mühling KH (2013) Apoplastic Na+ in Vicia faba leaves rises after short-term salt stress and is remedied by silicon. J Agron Crop Sci 199:161–170
Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ exchanger. Proc Natl Acad Sci USA 97:6896–6901
Shi Y, Wang YC, Flowers TJ, Gong HJ (2013) Silicon decreases chloride transport in rice (Oryza sativa L.) in saline conditions. J Plant Physiol 170:847–853
Sonobe K, Hattori T, An P, Tsuji W, Eneji AE, Kobayashi S, Kawamura Y, Tanaka K, Inanaga S (2010) Effect of silicon application on sorghum root responses to water stress. J Plant Nutr 34:71–82
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 Amst 123:240–246
Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542
Trubat R, Cortina J, Vilagrosa A (2012) Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings. Oecologia 170:899–908
Tuna AL, Kaya C, Higgs D, Murillo-Amador B, Aydemir S, Girgin AR (2008) Silicon improves salinity tolerance in wheat plants. Environ Exp Bot 62:10–16
Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460
Wan H, Zhao Z, Qian C, Sui Y, Malik AA, Chen J (2010) Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber. Anal Biochem 399:257–261
Wang XS, Han JG (2007) Effects of NaCl and silicon on ion distribution in the roots, shoots and leaves of two alfalfa cultivars with different salt tolerance. Soil Sci Plant Nutr 53:278–285
Wu GQ, Liang N, Feng RJ, Zhang JJ (2013) Evaluation of salinity tolerance in seedlings of sugar beet (Beta vulgaris L.) cultivars using proline, soluble sugars and cation accumulation criteria. Acta Physiol Plant 35:2665–2674
Yin LN, Wang SW, Li JY, Tanaka K, Oka M (2013) Application of silicon improves salt tolerance through ameliorating osmotic and ionic stresses in the seedling of Sorghum bicolor. Acta Physiol Plant 35:3099–3107
Zhang JY, Wu FZ (2009) Effects of salt stress on chlorophyll content and chloroplast ultrastructure of different salt-tolerant cucumber varieties. China Vegetables 10:13–16 (in Chinese with English abstract)
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Zhu YX, Gong HJ (2014) Beneficial effects of silicon on salt and drought tolerance in plants. Agron Sustain Dev 34:455–472
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
Acknowledgments
This study is supported by the National Natural Science Foundation of China (31272152, 31471866), Program for New Century Excellent Talents in University of China (NCET-11-0441), and Research Fund for the Doctoral Program of Higher Education of China (20120204110020).
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This work has not been accepted or published in any other journal. It is not being considered for publication in any other journal. The authors declare that they have no conflict of interest.
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Communicated by L. Tripathi.
Y.-X. Zhu and X.-B. Xu contributed equally to this work.
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Zhu, YX., Xu, XB., Hu, YH. et al. Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus L.. Plant Cell Rep 34, 1629–1646 (2015). https://doi.org/10.1007/s00299-015-1814-9
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DOI: https://doi.org/10.1007/s00299-015-1814-9