Silicon-mediated improvement in the salt resistance of wheat (Triticum aestivum) results from increased sodium exclusion and resistance to oxidative stress
Muhammad Saqib A B D E , Christian Zörb A C and Sven Schubert AA Institute of Plant Nutrition, Justus Liebig University, Heinrich-Buff-Ring 26-32, D-35392 Giessen, Germany.
B Institute of Soil and Environmental Sciences, University of Agriculture, Faisalabad-38040, Pakistan.
C Institute of Plant Nutrition and Soil Sciences, Christian-Albrechts-Universität Kiel, Hermann-Rodewald-Str. 2, D-24118 Kiel, Germany.
D Present address: Biotechnology Research Center, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, 113-8657 Tokyo, Japan.
E Corresponding author. Email: drhmsab@yahoo.com
Functional Plant Biology 35(7) 633-639 https://doi.org/10.1071/FP08100
Submitted: 28 March 2008 Accepted: 30 June 2008 Published: 21 August 2008
Abstract
Silicon (Si) is reported to reduce the effect of salinity on wheat (Triticum aestivum L.) and other crops. In the present study, Si decreased plant Na+ uptake and shoot : root Na+ distribution of a salt-resistant as well as a salt-sensitive wheat genotype. Reduced shoot Na+ concentration and increased shoot K+ : Na+ ratio led to improved plant growth. Silicon increased cell-wall Na+ binding from 49% in SARC-1 and 37% in 7-Cerros under salinity to 87% in SARC-1 and 79% in 7-Cerros under salinity + silicon. It may also have resulted in decreased potentially toxic leaf sap Na+ concentration. The concentration of glutathione, an important antioxidant in plants, was increased due to the addition of Si under saline conditions. The salt-resistant wheat genotype SARC-1 was less Si-responsive in terms of shoot fresh weight, having a 39% increase compared with a 49% increase in 7-Cerros, as well as root fresh weight, having a 12% increase compared with a 22% in 7-Cerros. It is concluded that Si may have improved shoot growth of the salt-resistant as well as the salt-sensitive wheat genotype by decreasing plant Na+ uptake and shoot : root Na+ distribution as well as by increasing glutathione concentration. Silicon may have also improved in-plant Na+ detoxification by increasing cell-wall Na+ binding.
Additional keywords: ascorbate, cell wall, glutathione, salinity.
Acknowledgements
M. Saqib gratefully acknowledges the support of DAAD (Deutscher Akademischer Austauschdienst) in the form of a fellowship that enabled him to carry out this work. The excellent technical assistance of Tina Volk, Anne Weber, Roland Pfanschilling and Christina Plachta is gratefully acknowledged.
Ahmad R,
Zaheer SH, Ismail S
(1992) Role of silicon in salt tolerance of wheat (Triticum aestivum L.). Plant Science 85, 43–50.
| Crossref | GoogleScholarGoogle Scholar |
Chen Z,
Zhou M,
Newman IA,
Mendham NJ,
Zhang G, Shabala S
(2007) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Functional Plant Biology 34, 150–162.
| Crossref | GoogleScholarGoogle Scholar |
Drew MC, Läuchli A
(1985) Oxygen dependent exclusion of sodium ions from shoots by roots of Zea mays (cv. Pioneer 3906) in relation to salinity damage. Plant Physiology 79, 171–176.
| PubMed |
Epstein E
(1999) Silicon. Annual Review of Plant Physiology and Plant Molecular Biology 50, 641–664.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 & Environment 29, 1970–1979.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gunes A,
Inal A,
Bagei EG, Pilbeam DJ
(2007) Silicon-mediated changes of some physiological and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in sodic-B toxic soil. Plant and Soil 290, 103–114.
| Crossref | GoogleScholarGoogle Scholar |
Hoagland DR, Arnon DI
(1950) The water culture method for growing plants without soil. California Agriculture Experimental Station Circular 347, 1–39.
Inanaga S, Okasaka A
(1996) Calcium and silicon binding compounds in cell walls of rice shoots. Soil Science and Plant Nutrition 41, 103–110.
Iwasaki K,
Maier P,
Fecht M, Horst WJ
(2002) Effects of silicon supply on apoplastic manganese concentrations in leaves and their relation to manganese tolerance in cowpea (Vigna unguiculata L. Walp). Plant and Soil 238, 281–288.
| Crossref | GoogleScholarGoogle Scholar |
James RA,
von Caemmerer S,
Condon AGT,
Zwart AB, Munns R
(2008) Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Functional Plant Biology 35, 111–123.
| Crossref | GoogleScholarGoogle Scholar |
Liang Y
(1999) Effects of silicon on enzyme activity and sodium, potassium and calcium concentration in barley under salt stress. Plant and Soil 209, 217–224.
| Crossref | GoogleScholarGoogle Scholar |
Liang Y,
Chen Q,
Liu Q,
Zhang W, Ding R
(2003) Exogenous silicon (Si) increases antioxidant enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum vulgare L.). Journal of Plant Physiology 160, 1157–1164.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.). Environmental and Experimental Botany 53, 29–37.
| Crossref | GoogleScholarGoogle Scholar |
Ma JF, Yamaji N
(2006) Silicon uptake and accumulation in higher plants. Trends in Plant Science 11, 392–397.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ma JF,
Tamai K,
Yamaji N,
Mitani N,
Konishi S,
Katsuhara M,
Ishiguro M,
Murata Y, Yano M
(2006) A silicon transporter in rice. Nature 440, 688–691.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ma JF,
Yamaji N,
Mitani N,
Tamai K,
Konishi S,
Fujiwara T,
Katsuhara M, Yano M
(2007) An efflux transporter of silicon in rice. Nature 448, 209–212.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Matoh T,
Kairusmee P, Takahashi E
(1986) Salt-induced damage to rice plants and alleviation effect of silicate. Soil Science and Plant Nutrition 32, 295–304.
Mera MU, Beveridge TJ
(1993) Mechanism of silicate binding to the bacterial cell wall in Bacillus subtilis. Journal of Bacteriology 175, 1936–1945.
| PubMed |
Munns R
(1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell & Environment 16, 15–24.
| Crossref | GoogleScholarGoogle Scholar |
Munns R
(2005) Genes and salt tolerance: bringing them together. New Phytologist 167, 645–663.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Noctor G, Foyer CH
(1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Okamura M
(1980) An improved method for determination of l-ascorbic acid and l-dehydroascorbic acid in blood plasma. Clinica Chimica Acta 103, 259–268.
| Crossref | l-ascorbic acid and l-dehydroascorbic acid in blood plasma.&journal=Clinica Chimica Acta&volume=103&pages=259-268&publication_year=1980&author=M%20Okamura&hl=en&doi=10.1016/0009-8981(80)90144-8" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar |
Rogalla H, Römheld V
(2002) Role of leaf apoplast in silicon-mediated manganese tolerance of Cucumis sativus L. Plant, Cell & Environment 25, 549–555.
| Crossref | GoogleScholarGoogle Scholar |
Sairam RK,
Srivastava GC,
Agarwal S, Meena RC
(2005) Differences in antioxidant activity in response to salinity stress in tolerant and susceptible wheat genotypes. Biologia Plantarum 49, 85–91.
| Crossref | GoogleScholarGoogle Scholar |
Sangster AG
(1978) Silicon in the roots of higher plants. American Journal of Botany 65, 929–935.
| Crossref | GoogleScholarGoogle Scholar |
Saqib M,
Akhtar J, Qureshi RH
(2004) Pot study on wheat growth in saline and waterlogged compacted soil. II. Root growth and leaf ionic relations. Soil & Tillage Research 77, 179–187.
| Crossref | GoogleScholarGoogle Scholar |
Saqib M,
Zörb C,
Rengel Z, Schubert S
(2005) The expression of the endogenous vacuolar Na+/H+ antiporters in roots and shoots correlates positively with the salt resistance of wheat (Triticum aestivum L.). Plant Science 169, 959–965.
| Crossref | GoogleScholarGoogle Scholar |
Saqib M,
Zörb C, Schubert S
(2006) Salt-resistant and salt-sensitive wheat genotypes show similar biochemical reaction at protein level in the first phase of salt stress. Journal of Plant Nutrition and Soil Science 169, 542–548.
| Crossref | GoogleScholarGoogle Scholar |
Schubert S, Läuchli A
(1990) Sodium exclusion mechanisms at the root surface of two maize cultivars. Plant and Soil 123, 205–209.
| Crossref | GoogleScholarGoogle Scholar |
Sümer A,
Zörb C,
Yan F, Schubert S
(2004) Evidence of sodium toxicity for the vegetative growth of maize (Zea mays L.) during the first phase of salt stress. Journal of Applied Botany 78, 135–139.
Tester M, Davenport R
(2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tietze F
(1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione – applications to mammalian blood and other tissues. Analytical Biochemistry 27, 502–522.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tsai YC,
Hong CY,
Liu LF, Kao CH
(2004) Relative importance of Na+ and Cl− in NaCl-induced antioxidative systems in roots of rice seedlings. Physiologia Plantarum 122, 86–94.
| Crossref | GoogleScholarGoogle Scholar |
Tuna AL,
Kaya C,
Higgs D,
Murillo-Amador B,
Aydemir S, Girgin AR
(2008) Silicon improves salinity tolerance in wheat plants. Environmental and Experimental Botany 62, 10–16.
| Crossref | GoogleScholarGoogle Scholar |
Vaidyanathan H,
Sivakumar P,
Chakrabarty R, Thomas G
(2003) Scavenging of reactive oxygen species in NaCl-stressed rice (Oryza sativa L.) – differential response in salt-tolerant and sensitive varieties. Plant Science 165, 1411–1418.
| Crossref | GoogleScholarGoogle Scholar |
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 Science and Plant Nutrition 53, 278–285.
| Crossref | GoogleScholarGoogle Scholar |
Wang Y,
Stass A, Horst WJ
(2004) Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiology 136, 3762–3770.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yeo AR,
Flowers SA,
Rao G,
Welfare K,
Senanayake N, Flowers TJ
(1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant, Cell & Environment 22, 559–565.
| Crossref | GoogleScholarGoogle Scholar |
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 Science 167, 527–533.
| Crossref | GoogleScholarGoogle Scholar |