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Silicon chelates from plant waste promote in vitro shoot production and physiological changes in strawberry plantlets

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Abstract

For the first time, the effect of mechanocomposite (MC) based on biogenic silica and green-tea catechins on axillary shoot formation, physiological and biochemical characteristics of two strawberry cultivars (‘Alpha’ and ‘Solnechnaya polyanka’) was studied. The shoots were cultured on Gamborg-Eveleg’s medium (B5) supplemented with 0.75 mg l−1 6-benzylaminopurine (BA) (control) and 0.0, 2.5, 5.0 or 10.0 mg l−1 MC for 60 days. The highest regeneration responses (100%) and axillary shoot proliferation (up to 15.06 ± 0.81) correlating with increasing fresh weight (FW), dry weight (DW) on the media supplemented with 5.0 mg l−1 MC for both genotypes were recorded. The improvement in shoot regeneration accompanied with enhancing some antioxidant enzymes activity (superoxide dismutase and peroxidase) on the media supplemented with 5.0 mg l−1 MC for both genotypes. The increase in endogenous H2O2 concentration displaying a high morphogenetic potential in the presence of 2.5 and 5.0 mg l−1 MC was only observed in cv. ‘Alpha’ shoots. Overall, a positive effect of MC on the quality of in vitro shoots was established. Concentrations of photosynthetic pigments (chlorophylls a and b, and carotenoids), and their ratios (chlorophyll a/b, chlorophyll (a + b)/carotenoids) indicated a high physiological state of the plantlets grown with 5.0 mg l−1 MC. The accumulation of endogenous cytokinin (iP) and indole-3-acetic acid (IAA) is associated with the effect of MC in various concentrations on the organogenic response of both cultivars. Thus, the outcomes of this study can be utilized for the development of new systems for a healthy planting material production using “green chemistry” approaches and recommended for commercial strawberry micropropagation.

Key message

Silicon chelates from plant waste are the useful component of plant tissue culture media for optimizing commercial strawberry micropropagation and preventing the occurrence of in vitro-derived disorders in plantlets.

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Availability of data and material

All data generated or analyzed during this study are included in this article. The data are available from the corresponding author on reasonable request.

Abbreviations

BA:

6-benzylaminopurine

B5 :

Gamborg-Eveleg’s basal salt medium

Car:

Carotenoid

CAT:

Catalase

Chl:

Chlorophyll

CK:

Cytokinin

DW:

Dry weight

FW:

Fresh weight

H2O2 :

Hydrogen peroxide

HPLC–DAD:

High-performance liquid chromatography coupled with diode-array detection

IAA:

Indole-3-acetic acid

IBA:

Indole-3-butyric acid

iP:

N6-isopentenyladenine

MC:

Mechanocomposite

POD:

Peroxidase

SOD:

Superoxide dismutase

References

  • Abdalla MM (2011) Beneficial effects of diatomite on the growth, the biochemical contents and polymorphic DNA in Lupinus albus plants grown under water stress. ABJNA 2:207–220

    CAS  Google Scholar 

  • Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5:369–374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aeby H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Google Scholar 

  • AL-Oqla FM, Omari MA (2017) Sustainable biocomposites: challenges, potential and barriers for development. In: Jawaid M, Sapuan SM, Alothman OY (eds) Green biocomposites. Springer, New York, pp 13–29

    Google Scholar 

  • Ambros EV, Toluzakova SY, Gorodova RA, Shapolova EG, Novikova TI (2015) The effect of the siliceous composites of rice husk and green tea on growth and development of Fragaria × ananassa Duch. Regenerants during the adaptation to ex vitro conditions. Turczaninowia 18:96–102

    Google Scholar 

  • Ambros EV, Zaytseva YG, Krasnikov AA, Novikova TI (2017) Optimization of microshoots regeneration systems of Fragaria × ananassa (Rosaceae) genotypes perspectived for Siberian region. Plant Life of Asian Russia 28:73–80

    Google Scholar 

  • Ambros E, Batrakova V, Krasnikov A, Zaytseva Y, Trofimova E, Novikova T (2018a) Effect of a biogenic silica and green-teaflavonoids-based mechanocomposite on Fragaria × ananassa Duch. leaf anatomy in in vitro conditions. BIO Web of Conferences. https://doi.org/10.1051/bioconf/20181100001

  • Ambros EV, Toluzakova SY, Shrainer LS, Trofimova EG, Novikova TI (2018b) An innovative approach to ex vitro rooting and acclimatization of Fragaria × ananassa Duch. Microshoots using а biogenic silica and green-tea-catechin-based mechanocomposite. In Vitro Cell Dev Biol Plant 54:436–443

    CAS  Google Scholar 

  • Ambros EV, Kotsupy OV, Karpova EA, Trofimova EG, Zaytseva YG, Novikova TI (2019) In vitro adaptive responses of Fragaria ananassa Duch. Plantlets induced by the mechanocomposite based on amorphous silica and flavonoids of green tea. Teor Prikl Ekol 4:116–122

    Google Scholar 

  • Asmar S, Castro E, Pasqual M, Pereira F, Soares J (2013a) Changes in leaf anatomy and photosynthesis of micropropagated banana plantlets under different silicon sources. Sci Hort 161:328–332

    CAS  Google Scholar 

  • Asmar SA, Pasqual M, de Araujo AG, Silva R, Rodrigues FA, Pio L (2013b) Morphophysiological characteristics of acclimatized ‘Grande Naine’ banana plants in response to in vitro use of silicon. Semin Cienc Agrar 34:73–81

    Google Scholar 

  • Barbosa LMP, de Paiva Neto VB, Carnevalli Dias LL, Festucci-Buselli RA, Alexandre SR, Iarema L, Finger FL, Otoni WC (2013) Biochemical and morpho-anatomical analyses of strawberry vitroplants hyperhydric tissues affected by BA and gelling agents. Rev Ceres 60:152–160

    CAS  Google Scholar 

  • Bellincampi D, Dipperro N, Salvi G, Cervcone F, De Lorenzo G (2000) Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol 122:1379–1385

    CAS  PubMed  PubMed Central  Google Scholar 

  • Borkowska B (2001) Morphological and physiological characteristics of micropropagated strawberry plants rooted in vitro or ex vitro. Sci Hort 89:195–206

    Google Scholar 

  • Braga FT, Nunes CF, Favero AC, Pasqual M, Carvalho JG, Castro EM (2009) Anatomical characteristics of the strawberry seedlings micropropagated using different sources of silicon. Pesqui Agropecu Bras 44:128–132

    Google Scholar 

  • Cappelletti R, Sabbadini S, Mezzetti B (2016) The use of TDZ for the efficient in vitro regeneration and organogenesis of strawberry and blueberry cultivars. Sci Hort 207:117–124

    CAS  Google Scholar 

  • Chen J, Ziv M (2001) The effect of ancymidol on hyperhydricity, regeneration, starch and antioxidant enzymatic activities in liquid-cultured narcissus. Plant Cell Rep 20:22–27

    PubMed  Google Scholar 

  • Chowdhury A, Sarkar S, Chowdhury A, Bardhan S, Mandal P, Chowdhury M (2016) Tea waste management: a case study from West Bengal, India. Indian J Sci Technol 9:1–6

    CAS  Google Scholar 

  • Christou A, Manganaris GA, Fotopoulos V (2014) Systemic mitigation of salt stress by hydrogen peroxide and sodium nitroprusside in strawberry plants via transcriptional regulation of enzymatic and non-enzymatic antioxidants. Environ Exp Bot 107:46–54

    CAS  Google Scholar 

  • Cosic T, Motyka V, Raspor M, Savic J, Cingel A, Vinterhalter B, Vinterhalter D (2015) In vitro shoot organogenesis and comparative analysis of endogenous phytohormones in kohlrabi (Brassica oleracea var. gongylodes): effects of genotype, explant type and applied cytokinins. Plant Cell Tissue Organ Cult 121:741–760

    CAS  Google Scholar 

  • Currie HA, Perry CC (2007) Silica in plants: biological, biochemical and chemical studies. Ann Bot 7:1383–1389

    Google Scholar 

  • Dutta Gupta S (2010) Role of free radicals and antioxidants in in vitro morphogenesis. In: Dutta Gupta S (ed) Reactive oxygen species and antioxidants in higher plants. CRC Press Inc and Science Pub, New York, pp 229–247

    Google Scholar 

  • Epstein E (1994) The anomaly of silicon in plant biology. PNAS 91:11–17

    CAS  PubMed  Google Scholar 

  • Exley C (2009) Silicon in life: whither biological silicification? Prog Mol Subcell Biol 47:173–184

    CAS  PubMed  Google Scholar 

  • FAOSTAT (2017) Food and Agriculture organization of the United Nation Statistical Database. http://faostat.fao.org

  • Farmer VC, Delbos E, Miller JD (2005) The role of phytolith formation and dissolution in controlling concentrations of silica in soil solutions and streams. Geoderma 127:71–79

    CAS  Google Scholar 

  • Gamborg OL, Eveleigh DE (1968) Culture methods and detection of glucanases in suspension cultures of wheat and barley. Can J Biochem 46:417–421

    CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1972) Superoxide dismutase I. occurrence in higher plants. Plant Physiol 59:309–314

    Google Scholar 

  • Guerriero G, Hausman JF, Legay S (2016) Silicon and the plant extracellular matrix. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00463

  • Guo B, He W, Zhao Y, Wu Y, Fu Y, Guo J, Wei Y (2017) Changes in endogenous hormones and H2O2 burst during shoot organogenesis in TDZ-treated Saussurea involucrate explants. Plant Cell Tissue Organ Cult 128:1–8

    CAS  Google Scholar 

  • Haddadi F, Aziz MA, Kamaladini H, Ravanfar SA (2013) Thidiazuron- and zeatin-induced high-frequency shoot regeneration from leaf and shoot-tip explants of strawberry. HortTechnology 23:276–281

    CAS  Google Scholar 

  • Hazarika BN (2003) Acclimatization of tissue cultured plants. Curr Sci 85:1704–1712

    CAS  Google Scholar 

  • Hazarika BN (2006) Morpho-physiological disorders in in vitro culture of plants. Sci Hort 108:105–120

    CAS  Google Scholar 

  • Holm G (1954) Chlorophyll mutations in barley. Acta Agric Scand 4:457–471

    Google Scholar 

  • Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY, Burritt DJ, Fujita M, Tran LS (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00420

  • Islam MM, Ahmed M, Mahaldar D (2005) In vitro callus induction and plant regeneration in seed explants of rice (Oryza sativa L.). Res J Agric Biol Sci 1:72–75

    Google Scholar 

  • Kancheva R, Borisova D, Georgiev G (2014) Chlorophyll assessment and stress detection from vegetation optical properties. EEEP 1:34–43

    Google Scholar 

  • Kazuko T, Hidekatsu Y, Hiroyuki N, Yoshiaki Y (2010) Antioxidant capacity of lignin from green tea waste. J Food Biochem 34:192–206

    Google Scholar 

  • Lang DY, Fei PX, Cao GY, Jia XX, Li YT, Zhang XH (2018) Silicon promotes seedling growth and alters endogenous IAA, GA3 and ABA concentrations in Glycyrrhiza uralensis under 100 mM NaCl stress. J Hortic Sci Biotechnol 94:1–7

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Liang Y, Nicolic M, Bélanger R, Gong H, Song A (2015) Silicon uptake and transport in plants: physiological and molecular aspects. In: Liang Y, Nicolic M, Bélanger R, Gong H, Song A (eds) Silicon in agriculture. Springer, Dordrecht, pp 69–82

  • Lim MY, Lee EJ, Jana S, Sivanesan I, Jeong BR (2012) Effect of potassium silicate on growth and leaf epidermal characteristics of begonia and pansy grown in vitro. Korean J Hortic Sci 30:579–585

    CAS  Google Scholar 

  • Lomovsky OI, Lomovskiy IO, Orlov DV (2017) Mechanochemical solid acid/base reactions for obtaining biologically active preparations and extracting plant materials. Green Chem Lett Rev 10:171–185

    CAS  Google Scholar 

  • Lozhnikova VN, Slastya IV (2010) Growth of spring barley and activity of endogenous phytohormones under the influence of silicon compounds. Agric Biol 3:102–107

    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

    CAS  Google Scholar 

  • Markovich O, Steiner E, Kouřil Š, Tarkowski P, Aharoni A, Elbaum R (2017) Silicon promotes cytokinin biosynthesis and delays senescence in Arabidopsis and sorghum. Plant Cell Environ 40:1189–1196

    CAS  PubMed  Google Scholar 

  • Mathe C, Mosolygo A, Suranyi G, Beke A, Demeter Z, Toth VR, Beyer D, Meszaros I, Marta M (2012) Genotype and explant-type dependent morphogenesis and silicon response of common reed (Phragmites australis) tissue cultures. Aquat Bot 97:57–63

    CAS  Google Scholar 

  • Matilla-Vázquez MA, Matilla AJ (2012) Role of H2O2 as signaling molecule in plants. In: Ahmad P, Prasad M (eds) Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 361–380

    Google Scholar 

  • Matychenkov IV, Khomyakov DM, Pakhnenko EP, Bocharnikova EA, Matychenkov VV (2016) Mobile Si-rich compounds in the soil–plant system and methods for their determination. Moscow University Soil Science Bulletin 71:120–128

    Google Scholar 

  • Mehl KA, Davis M, Berger FG, Carson JA (2005) Myofiber degeneration/regeneration is induced in the cachectic ApsMin/+ mouse. J Appl Physiol 99:2379–2387

    CAS  PubMed  Google Scholar 

  • Mercier H, Souza BM, Kraus JE, Hamasaki RM, Sotta B (2003) Endogenous auxin and cytokinin contents associated with shoot formation in leaves of pineapple cultured in vitro. Braz J Plant Physiol 15:107–112

    CAS  Google Scholar 

  • Montpetit J, Vivancos J, Mitani-Ueno N, Yamaji N, Rémus-Borel W, Belzile F, Ma JF, Belanger RR (2012) Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol Biol 79:35–46

    CAS  PubMed  Google Scholar 

  • Musial C (2020) Kuban-Jankowska A. Beneficial properties of green tea catechins. Int J Mol Sci, Gorska-Ponikowska M. https://doi.org/10.3390/ijms21051744

    Book  Google Scholar 

  • Nayar PK, Mishra AK, Patnik S (1982) Silica in rice and flooded rice soils. II. Uptake of silica in relation to growth of rice varieties of different durations grown on an Inceptisol. Oryza 19:88–92

    CAS  Google Scholar 

  • Passey AJ, Barrett KJ, James DJ (2003) Adventitious shoot regeneration from seven commercial strawberry cultivars (Fragaria x ananassa Duch.) using a range of explant types. Plant Cell Rep 21:397–401

    CAS  PubMed  Google Scholar 

  • Rani A, Kumar Vats S, Sharma M, Kumar S (2011) Catechin promotes growth of Arabidopsis thaliana with concomitant changes in vascular system, photosynthesis and hormone content. Biol Plant 55:779–782

  • Reed BM, Wada S, De Noma J, Niedz RP (2013) Mineral nutrition influences physiological responses of pear in vitro. In Vitro Cell Dev Biol Plant 49:699–709

    CAS  Google Scholar 

  • Rozhanskaya OA, Lomovsky OI, Trofimova EG, Lomova TG (2016) Products of mechanical treatment of plant waste material as a means of controlling the morphogenesis of chickpea (Cicer arietinum L.) in vitro and in agro. Success of Morden. Science and Education 8:31–37

    Google Scholar 

  • Sahebi M, Hanafi MM, Siti Nor Akmar A, Rafii MY, Azizi P, Tengoua F, Nurul Mayzaitul Azwa J, Shabanimofrad M (2015) Importance of silicon and mechanisms of biosilica formation in plants. Biomed Res Int. https://doi.org/10.1155/2015/396010

  • Shapolova EG, Lomovsky OI (2013) Mechanochemical solubilization of silicon dioxide with polyphenol compounds of plant origin. Russ J Bioorganic Chem 39:765–770

    CAS  Google Scholar 

  • Shapolova E, Lomovskii O, Kazachinskaya E, Loktev V, Teplyakova T (2016) Antiviral activity of SiO2–polyphenol composites prepared mechanochemically from plant raw materials. Pharm Chem J 50:595–599

    CAS  Google Scholar 

  • Sivanesan I, Jeong BR (2014) Silicon promotes adventitious shoot regeneration and enhances salinity tolerance of Ajuga multiflora Bunge by altering activity of antioxidant enzyme. Sci World J. https://doi.org/10.1155/2014/521703

  • Soundararajan P, Manivannan A, Cho YS, Jeong BR (2017) Exogenous supplementation of silicon improved the recovery of hyperhydric shoots in Dianthus caryophyllus L. by stabilizing the physiology and protein expression. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00738

  • Streit MN, Canterle LP, Canto MW, LHH H (2005) As clorofilas. Ciênc Rural 35:748–755

    CAS  Google Scholar 

  • Tian M, Gu Q, Zhu M (2003) The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus. Plant Sci 165:701–707

    CAS  Google Scholar 

  • Trofimova EG, Podgorbunskikh EM, Skripkina TS, Bychkov AL, Lomovsky OI (2018) Scaling of the mechano-chemical process of production of silicon chelates from plant raw materials. Bulg Che. Commun 50:45–48

    Google Scholar 

  • Van Bockhaven J, De Vleesschauwer D, Hofte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J Exp Bot 64:1281–1293

    PubMed  Google Scholar 

  • Wang H, Li M, Yang Y, Maofu L, Dong J (2015) Histological and endogenous plant growth regulators changes associated with adventitious shoot regeneration from in vitro leaf explants of strawberry (Fragaria × ananassa cv. ‘Honeoye’). Plant Cell Tissue Organ Cult 123:479–488

    CAS  Google Scholar 

  • Wettstein D (1957) Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden. Exp Cell Res 12:427–434

    Google Scholar 

  • Wolff SP (1994) Ferrous ion oxidation in presence of ferric iron indicator xylenol orange for measurement of hydroperoxide. Methods Enzymol 233:182–189

    CAS  Google Scholar 

  • Zhanaeva TA, Lobanova IE, Kukushkina TA (1999) Flavonols and flavonol-oxidizing enzymes during buckwheat ontogenesis. Biol Bull Russ Acad Sci 26:105–108

    Google Scholar 

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Acknowledgements

In vitro propagation of F. × ananassa microplants was carried out with the financial support of the budgetary project of the Central Siberian Botanical Garden, SB RAS No АААА-А17-117012610051-5 within the framework of the State Assignment. Physiological and biochemical parameters of strawberry plantlets experiments were supported by the Russian Foundation for Basic Research and the Government of Novosibirsk Region as research project No. 19-44-540004. In our study, in vitro material from the collection of the Central Siberian Botanical Garden SB RAS – USU 440534 “Collection of living plants indoors and outdoors” was used.

Funding

In vitro propagation of F. × ananassa microplants was carried out with the financial support of the budgetary project of the Central Siberian Botanical Garden, SB RAS No АААА-А17-117012610051-5 within the framework of the State Assignment. Physiological and biochemical parameters of strawberry plantlets experiments were supported by the Russian Foundation for Basic Research and the Government of Novosibirsk Region as research project No. 19-44-540004

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Authors and Affiliations

  1. Central Siberian Botanical Garden, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russian Federation

    Elena Ambros, Evgeniya Karpova, Olga Kotsupiy, Yulianna Zaytseva & Tatyana Novikova

  2. Institute of Solid State Chemistry and Mechanochemistry, Siberian Branch of the Russian Academy of Science, Novosibirsk, Russian Federation

    Elena Trofimova

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  1. Elena Ambros
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  2. Evgeniya Karpova
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  3. Olga Kotsupiy
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  6. Tatyana Novikova
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Contributions

EVA, EAK, and TIN conceived and designed the experiments; EVA, EAK, OVK, and EGT conducted the experiment, collected, and analyzed the data; EVA and EAK wrote the draft of the manuscript; YGZ assisted in conducting the experiment, sample collection for the analysis; TIN proofread and finalized the manuscript.

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Correspondence to Elena Ambros.

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Ambros, E., Karpova, E., Kotsupiy, O. et al. Silicon chelates from plant waste promote in vitro shoot production and physiological changes in strawberry plantlets. Plant Cell Tiss Organ Cult 145, 209–221 (2021). https://doi.org/10.1007/s11240-020-02003-0

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