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Silicon mitigates cold stress in barley plants via modifying the activity of apoplasmic enzymes and concentration of metabolites

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Abstract

Apoplasm is the first compartment encountering environmental stresses and is important for plant’s tolerance to low temperature. The effect of silicon (Si) on tolerance to low-temperature stress, e.g., chilling and freezing, has been shown in some plant species, while the involvement of leaf apoplasm in the Si-mediated amelioration of cold stress has not been investigated to date. In this work, one winter and one spring barley (Hordeum vulgare L.) cultivars were grown without or with Si (56 mg L−1 as Na2SiO3) and exposed to gradual temperature decrease from + 25 to + 5 °C for cold acclimation and then treated with freezing (− 5 °C) temperatures. Growth inhibition, photosynthesis reduction, and loss of membrane integrity under low-temperature conditions were higher in the spring than in the winter cultivars, but these parameters were similarly alleviated by Si in both cultivars. Cold acclimation decreased the lethal temperature (LT50) and increased survival (%) of plants exposed to freezing temperatures. The effect of acclimation treatment on reduction of LT50 was substituted completely by Si in both cultivars, while in the case of survival rate, Si substituted for acclimation treatment only in the winter cultivar. The activity of antioxidative enzymes and concentrations of soluble carbohydrates and proteins in the leaf apoplasm were increased upon cold acclimation and particularly on Si treatment; the highest values were observed in Si–cold-acclimated plants. Our data demonstrated an ameliorative effect of Si under both chilling and freezing stresses in barley via modification of biochemical properties in the leaf apoplasm.

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References

  • Adatia MH, Besford RT (1986) The effects of silicon on cucumber plants grown in recirculating nutrient solution. Ann Bot 58:343–351

    Article  CAS  Google Scholar 

  • Agarie S, Hanaoka N, Ueno O, Miyazaki A, Kubota F, Agata W, Kaufman PB (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 

  • Awasthi R, Bhandari K, Nayyar H (2015) Temperature stress and redox homeostasis in agricultural crops. Front Environ Sci 3:11

    Article  Google Scholar 

  • Azeem S, Li Z, Zheng H, Lin W, Arafat Y, Zhang Z, Lin X, Lin W (2016) Quantitative proteomics study on Lsi1 in regulation of rice (Oryza sativa L.) cold resistance. Plant Growth Regul 78:307–323

    Article  CAS  Google Scholar 

  • Baek SH, Kwon IS, Park TI, Yun SJ, Kim JK, Choi KG (2000) Activities and isozyme profiles of antioxidant enzymes in intercellular compartment of overwintering barley leaves. BMB Rep 33:385–390

    CAS  Google Scholar 

  • Benkherbache N, Tondelli A, Djekoune A, Francia E, Pecchioni N, Hassous L, Stanca AM (2016) Marker characterization of vernalization and low-temperature tolerance loci in barley genotypes adapted to semi-arid environments. Czech J Genet Plant Breed 52:157–162

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160:283–292

    Article  CAS  Google Scholar 

  • Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1009–1011

    Article  Google Scholar 

  • Clarkson DT (2007) The plant leaf apoplast. In: Sattelmacher B, Horst WJ (eds) The Apoplast of higher plants: Compartment of storage, transport and reactions. Springer, The Netherlands, pp 3–12

    Google Scholar 

  • Cooke J, Leishman MR (2016) Consistent alleviation of abiotic stress with silicon addition: a meta-analysis. Func Ecol 30:1340–1357

    Article  Google Scholar 

  • Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O, Ma JF, Kronzucker HJ, Bélanger RR (2019) The controversies of silicon’s role in plant biology. New Phytol 221:67–85

    Article  Google Scholar 

  • Cuesta-Marcos A, Muñoz-Amatriaín M, Filichkin T, Karsai I, Trevaskis B, Yasuda S, Hayes P, Sato K (2015) The relationships between development and low temperature tolerance in barley near isogenic lines differing for flowering behavior. Plant Cell Physiol 56:2312–2324

    Article  CAS  Google Scholar 

  • Dahal K, Kane K, Sarhan F, Grodzinski B, Hüner NP (2012) Cold acclimation inhibits CO2-dependent stimulation of photosynthesis in spring wheat and spring rye. Botany 90:433–444

    Article  CAS  Google Scholar 

  • Detmann KC, Araújo WL, Martins SC, Sanglard LM, Reis JV, Detmann E, Rodrigues F, Nunes-Nesi A, Fernie AR, DaMatta FM (2012) Silicon nutrition increases grain yield, which, in turn, exerts a feed-forward stimulation of photosynthetic rates via enhanced mesophyll conductance and alters primary metabolism in rice. New Phytol 196:752–562

    Article  CAS  Google Scholar 

  • Dietz KJ (2000) The extracellular matrix of the plant cell: location of signal perception, transduction and response. In: Esser K, Lüttge U, Kadereit J, Beyschlag W (eds) Progress in Botany. Springer, Heidelberg, pp 215–237

    Google Scholar 

  • Elliott CL, Snyder GH (1991) Autoclave-induced digestion for the colorimetric determination of silicon in rice straw. J Agr Food Chem 39:1118–1119

    Article  CAS  Google Scholar 

  • Etesami H, Jeong BR (2018) Silicon (Si): review and future prospects on the action mechanisms in alleviating biotic and abiotic stresses in plants. Ecotoxicol Environ Safe e147:881–896

    Article  Google Scholar 

  • Fan Q, Sun W, Li Z, Liang Y (2009) Effects of silicon on photosynthesis and its major relevant enzyme activities in wheat leaves under short-term cold stress. Plant Nutr Fert Sci 15:544–550

    CAS  Google Scholar 

  • Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane-lipids - a mechanism of chilling tolerance. Proc Natl Acad Sci (USA) 91:8787–8791

    Article  CAS  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  CAS  Google Scholar 

  • Gururani MA, Venkatesh J, Tran LS (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320

    Article  CAS  Google Scholar 

  • Gusta LV, Wisniewski M (2013) Understanding plant cold hardiness: an opinion. Physiol Plant 147:4–14

    Article  CAS  Google Scholar 

  • Hajiboland R (2012) Effect of micronutrient deficiencies on plant stress responses. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants. Springer, New York, pp 283–329

    Chapter  Google Scholar 

  • Hajiboland R (2014) Reactive oxygen species and photosynthesis. In: Ahmad P (ed) Oxidative damage to plants, antioxidant networks and signaling. Elsevier, San Diego, pp 1–63

    Google Scholar 

  • Hajiboland R, Aliasgharzadeh N, Laiegh SF, Poschenrieder C (2010) Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331:313–327

    Article  CAS  Google Scholar 

  • Hajiboland R, Bahrami-Rad S, Poschenrieder C (2017a) Silicon modifies both a local response and a systemic response to mechanical stress in tobacco leaves. Biol Plant 61:187–191

    Article  CAS  Google Scholar 

  • Hajiboland R, Cheraghvareh L, Poschenrieder C (2017b) Improvement of drought tolerance in tobacco (Nicotiana rustica L.) plants by silicon. J Plant Nutr 40:1661–1676

    Article  CAS  Google Scholar 

  • He Y, Xiao H, Wang H, Chen Y, Yu M (2010) Effect of silicon on chilling-induced changes of solutes, antioxidants, and membrane stability in seashore paspalum turfgrass. Acta Physiol Plant 32:487–494

    Article  CAS  Google Scholar 

  • Huber SC, Huber JL (1996) Role and regulation of sucrose phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:431–444

    Article  CAS  Google Scholar 

  • Ishibashi M, Kobayashi F, Nakamura J, Murai K, Takumi S (2007) Variation of freezing tolerance, Cor/Lea gene expression and vernalization requirement in Japanese common wheat. Plant Breed 126:464–469

    Article  CAS  Google Scholar 

  • Jain R, Shrivastava A, Solomon S, Yadav R (2007) Low temperature stress-induced biochemical changes affect stubble bud sprouting in sugarcane (Saccharum spp. hybrid). Plant Growth Regul 53:17–23

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Rios-Gonzalez K, Veisz O, Páldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci 164:301–306

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Lesk´o K, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674–1682

    Article  CAS  Google Scholar 

  • Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation–what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  Google Scholar 

  • Johnson HS, Hatch MD (1970) Properties and regulation of leaf nicotinamide–adenine dinucleotide phosphate–malate dehydrogenase and ‘malic’enzyme in plants with the C4-dicarboxylic acid pathway of photosynthesis. Biochem J 119:273–280

    Article  CAS  Google Scholar 

  • Johnson CM, Stout PR, Broyer TC, Carlton AB (1957) Comparative chlorine requirements of different plant species. Plant Soil 8:337–353

    Article  CAS  Google Scholar 

  • Joudmand A, Hajiboland R, Habibi G (2019) Cold acclimation capacity and freezing tolerance in some Iranian barley cultivars. J Agric Sci Technol (in press)

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  Google Scholar 

  • Kanervo E, Tasaka Y, Murata N, Aro EM (1997) Membrane lipid unsaturation modulates processing of the photosystem II reaction-center protein D1 at low temperatures. Plant Physiol 114:841–849

    Article  CAS  Google Scholar 

  • Kim YH, Khan AL, Waqas M, Lee IJ (2017) Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: A review. Front Plant Sci 8:510

    PubMed  PubMed Central  Google Scholar 

  • Kosova K, Prášil IT, Vitamvas P (2008) The relationship between vernalization-and photoperiodically-regulated genes and the development of frost tolerance in wheat and barley. Biol Plant 52:601–615

    Article  CAS  Google Scholar 

  • Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4:112–166

    Article  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 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

    Article  CAS  Google Scholar 

  • Liang Y, Nikolic M, Bélanger R, Gong H, Song A (2015) Silicon-mediated tolerance to drought and low-temperature stress. In: Silicon in Agriculture. Springer, The Netherlands, pp 143–159

    Chapter  Google Scholar 

  • Liu J (2015) Temperature-mediated alterations of the plant apoplast as a mechanism of intracellular freezing stress avoidance. Dissertation, University of Saskatchewan, Canada

  • Liu JJ, Lin SH, Xu PL, Wang XJ, Bai JG (2009) Effects of exogenous silicon on the activities of antioxidant enzymes and lipid peroxidation in chilling-stressed cucumber leaves. Agric Sci China 8:1075–1086

    Article  CAS  Google Scholar 

  • Luyckx M, Hausman JF, Lutts S, Guerriero G (2017) Silicon and plants: current knowledge and technological perspectives. Front Plant Sci 8:411

    Article  Google Scholar 

  • Matteucci M, D’angeli S, Errico S, Lamanna R, Perrotta G, Altamura MM (2011) Cold affects the transcription of fatty acid desaturases and oil quality in the fruit of Olea europaea L. genotypes with different cold hardiness. J Exp Bot 62:3403–3420

    Article  CAS  Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337

    Article  CAS  Google Scholar 

  • Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228

    Article  CAS  Google Scholar 

  • Moradtalab N, Weinmann M, Walker F, Höglinger B, Ludewig U, Neumann G (2018) Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances. Front Plant Sci 9:420

    Article  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta (BBA-Bioenergetics) 1767:414–421

    Article  CAS  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  CAS  Google Scholar 

  • Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540

    Article  CAS  Google Scholar 

  • Prado K, Maurel C (2013) Regulation of leaf hydraulics: from molecular to whole plant levels. Front Plant Sci 4:255

    Article  Google Scholar 

  • Rizza F, Pagani D, Gut M, Prášil IT, Lago C, Tondelli A, Orrù L, Mazzucotelli E, Francia E, Badeck FW, Crosatti C (2011) Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci 51:2759–2779

    Article  CAS  Google Scholar 

  • Schoelynck J, Bal K, Backx H, Okruszko T, Meire P, Struyf E (2010) Silica uptake in aquatic and wetland macrophytes: a strategic choice between silica, lignin and cellulose? New Phytol 186:385–391

    Article  CAS  Google Scholar 

  • Sin’kevich MS, Sabel’nikova EP, Deryabin AN, Astakhova NV, Dubinina IM, Burakhanova EA, Trunova TI (2008) The changes in invertase activity and the content of sugars in the course of adaptation of potato plants to hypothermia. Russ J Plant Physiol 55:449–454

    Article  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  CAS  Google Scholar 

  • Tarkowski ŁP, Van den Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci 6:203

    Article  Google Scholar 

  • Tasgin E, Aticib O, Nalbantoglua B, Popovac LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  CAS  Google Scholar 

  • Tenhaken R (2015) Cell wall remodeling under abiotic stress. Front Plant Sci 7:771

    Google Scholar 

  • Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    Article  CAS  Google Scholar 

  • Turhan E, Aydogan C, Baykul A, Akoglu A, Evrenosäžlu Y, Ergin S (2012) Apoplastic antioxidant enzymes in the leaves of two strawberry cultivars and their relationship to cold-hardiness. Not Bot Horti Agrobot Cluj Napoca 40:114–122

    Article  CAS  Google Scholar 

  • Uemura M, Steponkus PL (1999) Cold acclimation in plants: relationship between the lipid composition and the cryostability of the plasma membrane. J Plant Res 112:245–254

    Article  Google Scholar 

  • Vanacker H, Harbinson J, Ruisch J, Carver TL, Foyer CH (1998) Antioxidant defences of the apoplast. Protoplasma 205:129–140

    Article  CAS  Google Scholar 

  • Vogg G, Heim R, Gotschy B, Beck E (1998) Hansen J. Frost hardening and photosynthetic performance of Scots pine (Pinus sylvestris L.). II. Seasonal changes in the fluidity of thylakoid membranes. Planta 204:201–206

    Article  CAS  Google Scholar 

  • Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236

    Article  Google Scholar 

  • Wang SY, Galletta GJ (1998) Foliar application of potassium silicate induces metabolic changes in strawberry plants. J Plant Nutr 21:157–167

    Article  CAS  Google Scholar 

  • Witzel K, Shahzad M, Matros A, Mock HP, Mühling KH (2011) Comparative evaluation of extraction methods for apoplastic proteins from maize leaves. Plant Methods 7:48

    Article  CAS  Google Scholar 

  • Wu G, Wilen RW, Robertson AJ, Gusta LV (1999) Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120:513–520

    Article  CAS  Google Scholar 

  • Yamada T, Kuroda K, Jitsuyama Y, Takezawa D, Arakawa K, Fujikawa S (2002) Roles of the plasma membrane and the cell wall in the responses of plant cells to freezing. Planta 215:770–778

    Article  CAS  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates extracts by anthrone. Biochem J 57:508–514

    Article  CAS  Google Scholar 

  • Zhao M, Liu W, Xia X, Wang T, Zhang WH (2014) Cold acclimation-induced freezing tolerance of Medicago truncatula seedlings is negatively regulated by ethylene. Physiol Plant 152:115–129

    Article  CAS  Google Scholar 

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Acknowledgements

This research was financially supported by the University of Tabriz.

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  1. Department of Plant Science, University of Tabriz, Tabriz, 51666-14779, Iran

    Arshad Joudmand & Roghieh Hajiboland

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Joudmand, A., Hajiboland, R. Silicon mitigates cold stress in barley plants via modifying the activity of apoplasmic enzymes and concentration of metabolites. Acta Physiol Plant 41, 29 (2019). https://doi.org/10.1007/s11738-019-2817-x

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