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Marija Marković
Department of Plant Physiology, Institute for Biological Research “Siniša Stanković“—National Institute of the Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, 11060 Belgrade, Serbia

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Review
Published: 30 April 2021 in Plants
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In ornamental geophytes, conventional vegetative propagation is not economically feasible due to very slow development and ineffective methods. It can take several years until a new plant is formed and commercial profitability is achieved. Therefore, micropropagation techniques have been developed to increase the multiplication rate and thus shorten the multiplication and regeneration period. The majority of these techniques rely on the formation of new bulbs and their sprouting. Dormancy is one of the main limiting factors to speed up multiplication in vitro. Bulbous species have a period of bulb dormancy which enables them to survive unfavorable natural conditions. Bulbs grown in vitro also exhibit dormancy, which has to be overcome in order to allow sprouting of bulbs in the next vegetation period. During the period of dormancy, numerous physiological processes occur, many of which have not been elucidated yet. Understanding the process of dormancy will allow us to speed up and improve breeding of geophytes and thereby achieve economic profitability, which is very important for horticulture. This review focuses on recent findings in the area of bulb dormancy initiation and release in fritillaries, with particular emphasis on the effect of plant growth regulators and low-temperature pretreatment on dormancy release in relation to induction of antioxidative enzymes’ activity in vitro.

ACS Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Slađana Jevremović; Angelina Subotić. Bulb Dormancy In Vitro—Fritillaria meleagris: Initiation, Release and Physiological Parameters. Plants 2021, 10, 902 .

AMA Style

Marija Marković, Milana Trifunović Momčilov, Branka Uzelac, Slađana Jevremović, Angelina Subotić. Bulb Dormancy In Vitro—Fritillaria meleagris: Initiation, Release and Physiological Parameters. Plants. 2021; 10 (5):902.

Chicago/Turabian Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Slađana Jevremović; Angelina Subotić. 2021. "Bulb Dormancy In Vitro—Fritillaria meleagris: Initiation, Release and Physiological Parameters." Plants 10, no. 5: 902.

Review
Published: 31 December 2020 in Plants
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Centaurium erythraea (centaury) is a traditionally used medicinal plant, with a spectrum of secondary metabolites with confirmed healing properties. Centaury is an emerging model in plant developmental biology due to its vigorous regenerative potential and great developmental plasticity when cultured in vitro. Hereby, we review nearly two decades of research on somatic embryogenesis (SE) in centaury. During SE, somatic cells are induced by suitable culture conditions to express their totipotency, acquire embryogenic characteristics, and eventually give rise to somatic embryos. When SE is initiated from centaury root explants, the process occurs spontaneously (on hormone-free medium), directly (without the callusing phase), and the somatic embryos are of unicellular origin. SE from leaf explants has to be induced by plant growth regulators and is indirect (preceded by callusing). Histological observations and culture conditions are compared in these two systems. The changes in antioxidative enzymes were followed during SE from the leaf explants. Special focus is given to the role of arabinogalactan proteins during SE, which were analyzed using a variety of approaches. The newest and preliminary results, including centaury transcriptome, novel potential SE markers, and novel types of arabinogalactan proteins, are discussed as perspectives of centaury research.

ACS Style

Ana D. Simonović; Milana M. Trifunović-Momčilov; Biljana K. Filipović; Marija P. Marković; Milica D. Bogdanović; Angelina R. Subotić. Somatic Embryogenesis in Centaurium erythraea Rafn—Current Status and Perspectives: A Review. Plants 2020, 10, 70 .

AMA Style

Ana D. Simonović, Milana M. Trifunović-Momčilov, Biljana K. Filipović, Marija P. Marković, Milica D. Bogdanović, Angelina R. Subotić. Somatic Embryogenesis in Centaurium erythraea Rafn—Current Status and Perspectives: A Review. Plants. 2020; 10 (1):70.

Chicago/Turabian Style

Ana D. Simonović; Milana M. Trifunović-Momčilov; Biljana K. Filipović; Marija P. Marković; Milica D. Bogdanović; Angelina R. Subotić. 2020. "Somatic Embryogenesis in Centaurium erythraea Rafn—Current Status and Perspectives: A Review." Plants 10, no. 1: 70.

Journal article
Published: 13 November 2020 in Plants
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The bulb is the main propagation organ of snake’s head fritillary (Fritillaria meleagris L.), a horticulturally attractive and rare geophyte plant species. In this study, we investigated the effect of soaking bulbs in GA3 solution (1, 2, and 3 mg L−1) combined with low-temperature treatment (7 °C) on breaking the dormancy of in vitro bulbs. Sugar status (total soluble sugars, glucose, and fructose content) was analyzed in different parts of the sprouted bulbs. The results showed that the soluble sugar concentration was highest in bulbs soaked in GA3. The main sugar in fritillary bulbs was glucose, while fructose content was much lower. Glucose concentration dramatically increased after bulb chilling (7 °C), and its accumulation was predominantly detected in the lower sprout portion during the first weeks of sprouting. Sugar concentration was significantly lower in nonchilled bulbs, which indicates the importance of low temperature in bulb development and sprouting.

ACS Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Olga Radulović; Snežana Milošević; Slađana Jevremović; Angelina Subotić. Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 2: Effect of GA3 Soaking and Chilling on Sugar Status in Sprouted Bulbs. Plants 2020, 9, 1573 .

AMA Style

Marija Marković, Milana Trifunović Momčilov, Branka Uzelac, Olga Radulović, Snežana Milošević, Slađana Jevremović, Angelina Subotić. Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 2: Effect of GA3 Soaking and Chilling on Sugar Status in Sprouted Bulbs. Plants. 2020; 9 (11):1573.

Chicago/Turabian Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Olga Radulović; Snežana Milošević; Slađana Jevremović; Angelina Subotić. 2020. "Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 2: Effect of GA3 Soaking and Chilling on Sugar Status in Sprouted Bulbs." Plants 9, no. 11: 1573.

Journal article
Published: 27 October 2020 in Plants
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Bulbs are the main vegetative reproductive organs of Fritillaria meleagris L. In nature, as well as in vitro, they become dormant and require low temperatures for further growth during the next vegetative period. In the present study, using 10 μM of gibberellic acid (GA3), or gibberellin biosynthesis (GA) inhibitors—ancymidol (A) and paclobutrazol (P)—the dynamic changes in soluble sugars, fructose and glucose content, fresh weight and sprouting capacity were investigated. F. meleagris bulbs were cultured on medium with GA3 and GA inhibitors for 1, 2 and 5 weeks at two different temperatures (24 and 7 °C). GA3 improved bulb fresh weight, as well as sprouting percentage at both tested temperatures, compared to the control. The highest fresh weight increase (57.7%) and sprouting rate (29.02%) were achieved when bulbs were grown at 24 °C for 5 weeks. In addition, soluble sugar content was the highest in bulbs grown for 5 weeks on medium supplemented with GA3. The main sugar in fritillary bulbs was glucose, while fructose content was lower. The sensitivity of bulbs to GA inhibitors differed and significantly affected sugar content in bulbs. To our knowledge, this is the first study of the sugar composition in F. meleagris bulbs during breaking of the bulb’s dormancy and its sprouting.

ACS Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Aleksandar Cingel; Snežana Milošević; Slađana Jevremović; Angelina Subotić. Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 1: Effect of GA3, GA Inhibitors and Temperature on Fresh Weight, Sprouting and Sugar Content. Plants 2020, 9, 1449 .

AMA Style

Marija Marković, Milana Trifunović Momčilov, Branka Uzelac, Aleksandar Cingel, Snežana Milošević, Slađana Jevremović, Angelina Subotić. Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 1: Effect of GA3, GA Inhibitors and Temperature on Fresh Weight, Sprouting and Sugar Content. Plants. 2020; 9 (11):1449.

Chicago/Turabian Style

Marija Marković; Milana Trifunović Momčilov; Branka Uzelac; Aleksandar Cingel; Snežana Milošević; Slađana Jevremović; Angelina Subotić. 2020. "Breaking the Dormancy of Snake’s Head Fritillary (Fritillaria meleagris L.) In Vitro Bulbs—Part 1: Effect of GA3, GA Inhibitors and Temperature on Fresh Weight, Sprouting and Sugar Content." Plants 9, no. 11: 1449.

Journal article
Published: 08 May 2020 in Plants
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The main topic of this study is the bioremediation potential of the common duckweed, Lemna minor L., and selected rhizospheric bacterial strains in removing phenol from aqueous environments at extremely high initial phenol concentrations. To that end, fluorescence microscopy, MIC tests, biofilm formation, the phenol removal test (4-AAP method), the Salkowski essay, and studies of multiplication rates of sterile and inoculated duckweed in MS medium with phenol (200, 500, 750, and 1000 mg L−1) were conducted. Out of seven bacterial strains, six were identified as epiphytes or endophytes that efficiently removed phenol. The phenol removal experiment showed that the bacteria/duckweed system was more efficient during the first 24 h compared to the sterile duckweed control group. At the end of this experiment, almost 90% of the initial phenol concentration was removed by both groups, respectively. The bacteria stimulated the duckweed multiplication even at a high bacterial population density (>105 CFU mL−1) over a prolonged period of time (14 days). All bacterial strains were sensitive to all the applied antibiotics and formed biofilms in vitro. The dual bacteria/duckweed system, especially the one containing strain 43-Hafnia paralvei C32-106/3, Accession No. MF526939, had a number of characteristics that are advantageous in bioremediation, such as high phenol removal efficiency, biofilm formation, safety (antibiotic sensitivity), and stimulation of duckweed multiplication.

ACS Style

Olga Radulović; Slaviša Stanković; Branka Uzelac; Vojin Tadić; Milana Trifunović-Momčilov; Jelena Lozo; Marija Marković. Phenol Removal Capacity of the Common Duckweed (Lemna minor L.) and Six Phenol-Resistant Bacterial Strains From Its Rhizosphere: In Vitro Evaluation at High Phenol Concentrations. Plants 2020, 9, 599 .

AMA Style

Olga Radulović, Slaviša Stanković, Branka Uzelac, Vojin Tadić, Milana Trifunović-Momčilov, Jelena Lozo, Marija Marković. Phenol Removal Capacity of the Common Duckweed (Lemna minor L.) and Six Phenol-Resistant Bacterial Strains From Its Rhizosphere: In Vitro Evaluation at High Phenol Concentrations. Plants. 2020; 9 (5):599.

Chicago/Turabian Style

Olga Radulović; Slaviša Stanković; Branka Uzelac; Vojin Tadić; Milana Trifunović-Momčilov; Jelena Lozo; Marija Marković. 2020. "Phenol Removal Capacity of the Common Duckweed (Lemna minor L.) and Six Phenol-Resistant Bacterial Strains From Its Rhizosphere: In Vitro Evaluation at High Phenol Concentrations." Plants 9, no. 5: 599.

Journal article
Published: 20 December 2018 in Polish Journal of Environmental Studies
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The aim of this work was to examine the multiplication of the common duckweed (Lemna minor), an aquatic plant species widespread in European stagnant waters, in two different media (Murashige – Skoog and Hoagland) with and without phenol supplementation. In order to quantify plant multiplication we have used relative growth rate and tolerance indices on both tested media and at five phenol concentrations (10, 15, 20, 30 and 100 mg/L). Furthermore, we examined the possibility of phenol removal from aqueous media containing different phenol concentrations, by using plant/bacteria system consisting of the duckweed and its naturally occurring microbial populations. After 7 days, number of newly formed fronds was approximately four times higher than at the beginning of the experiment on both tested media. The most important result in this study was removal of 70% of phenol from the highest initial concentration of 100 mg/L, in mixed cultures of duckweed and bacteria. By comparison, aseptic duckweed cultures removed approximately 50% of phenol at the same initial concentration. Our duckweed specimen showed a fast reproduction rate, high tolerance to phenol and a possible cooperation with rhizosphere-associated bacteria. All of these traits can be ultimately utilized for bioremediation purposes.

ACS Style

Olga Radulovic; Marija Petrić; Martin Raspor; Vojin Tadić; Petar Jovanović; Vladan Zečević. Assessment of in vitro Multiplication of Lemna minor in the Presence of Phenol: Plant/Bacteria System for Potential Bioremediation – Part I. Polish Journal of Environmental Studies 2018, 28, 803 -809.

AMA Style

Olga Radulovic, Marija Petrić, Martin Raspor, Vojin Tadić, Petar Jovanović, Vladan Zečević. Assessment of in vitro Multiplication of Lemna minor in the Presence of Phenol: Plant/Bacteria System for Potential Bioremediation – Part I. Polish Journal of Environmental Studies. 2018; 28 (2):803-809.

Chicago/Turabian Style

Olga Radulovic; Marija Petrić; Martin Raspor; Vojin Tadić; Petar Jovanović; Vladan Zečević. 2018. "Assessment of in vitro Multiplication of Lemna minor in the Presence of Phenol: Plant/Bacteria System for Potential Bioremediation – Part I." Polish Journal of Environmental Studies 28, no. 2: 803-809.

Journal article
Published: 20 December 2018 in Polish Journal of Environmental Studies
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In this work, we demonstrate that the rhizosphere of common duckweed (Lemna minor) is inhabited with various phenol-resistant bacterial strains. Based on 16S rRNA sequencing, we have identified 60 rhizosphere-associated bacterial isolates belonging to 10 different bacterial genera (Pseudomonas,...

ACS Style

Olga Radulovic; Marija Petrić; Martin Raspor; Olja Stanojević; Tamara Janakiev; Vojin Tadić; Slaviša Stanković. Culture-Dependent Analysis of 16S rRNA Sequences Associated with the Rhizosphere of Lemna minor and Assessment of Bacterial Phenol-Resistance: Plant/Bacteria System for Potential Bioremediation – Part II. Polish Journal of Environmental Studies 2018, 28, 811 -822.

AMA Style

Olga Radulovic, Marija Petrić, Martin Raspor, Olja Stanojević, Tamara Janakiev, Vojin Tadić, Slaviša Stanković. Culture-Dependent Analysis of 16S rRNA Sequences Associated with the Rhizosphere of Lemna minor and Assessment of Bacterial Phenol-Resistance: Plant/Bacteria System for Potential Bioremediation – Part II. Polish Journal of Environmental Studies. 2018; 28 (2):811-822.

Chicago/Turabian Style

Olga Radulovic; Marija Petrić; Martin Raspor; Olja Stanojević; Tamara Janakiev; Vojin Tadić; Slaviša Stanković. 2018. "Culture-Dependent Analysis of 16S rRNA Sequences Associated with the Rhizosphere of Lemna minor and Assessment of Bacterial Phenol-Resistance: Plant/Bacteria System for Potential Bioremediation – Part II." Polish Journal of Environmental Studies 28, no. 2: 811-822.

Journal article
Published: 01 January 2018 in Scientia Horticulturae
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We investigated the removal of phenol from water solutions (200 mg L−1) using two varieties of lettuce (Lactuca sativa L.) and their hairy roots. Experiments were done in a hydroponic system where adult plants were grown in phenol solutions for 10 days. The solution was refreshed every two days in order to maintain the constant concentration of phenol. Hairy roots were also cultivated in a solution containing phenol at concentrations varying from 25 to 125 mg L−1 in order to determine the maximum concentration of phenol that can be removed by hairy roots. Both varieties of lettuce reduced the concentration of phenol below the detection limit after six days at the initial phenol concentration of 200 mg L−1. Transformed roots completely removed phenol at the initial concentrations of 100 mg L−1, but were not able to remove phenol at constant concentration above 25 mg L−1. Lettuce plants and hairy roots are excellent candidates for the process of phenol removal from wastewaters. This plant is good choice for bioremediation of water and represents a potentially efficient and inexpensive system for water purification. The performance of lettuce plants and hairy roots to remove phenol from water solutions under real conditions, depleted nutrients or presence of other compounds should be examined further.

ACS Style

Vojin Tadić; Marija Petrić; Branka Uzelac; Snežana Milošević; Zoran Vujčić; Jasmina Stevanović; Jovan Tadić. Phenol removal from solution using different varieties of lettuce ( Lactuca sativa L.) – Part 1. Scientia Horticulturae 2018, 231, 210 -218.

AMA Style

Vojin Tadić, Marija Petrić, Branka Uzelac, Snežana Milošević, Zoran Vujčić, Jasmina Stevanović, Jovan Tadić. Phenol removal from solution using different varieties of lettuce ( Lactuca sativa L.) – Part 1. Scientia Horticulturae. 2018; 231 ():210-218.

Chicago/Turabian Style

Vojin Tadić; Marija Petrić; Branka Uzelac; Snežana Milošević; Zoran Vujčić; Jasmina Stevanović; Jovan Tadić. 2018. "Phenol removal from solution using different varieties of lettuce ( Lactuca sativa L.) – Part 1." Scientia Horticulturae 231, no. : 210-218.

Journal article
Published: 01 December 2015 in Comptes Rendus. Biologies
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Morphogenesis in vitro is a complex and still poorly defined process. We investigated esterase and peroxidase isoforms detected in bulb scale, during Fritillaria meleagris morphogenesis. Bulbs were grown either at 4 °C or on a medium with an increased concentration of sucrose (4.5%) for 30 days. After these pre-treatments, the bulb scales were further grown on nutrient media that contained different concentrations of 2,4-dichlorophenoxyacetic acid (2,4-D) and kinetin (KIN) or thidiazuron (TDZ). Regeneration of somatic embryos and bulblets occurred at the same explant. The highest numbers of somatic embryos and bulblets were regenerated on the medium containing 2,4-D and KIN (1mg/L each), while morphogenesis was most successful at a TDZ concentration between 0.5 and 1mg/L. Monitoring of esterases and peroxidases was performed by growing bulb scales on a medium enriched with 2,4-D and KIN or TDZ (1mg/L), and the number and activity of isoforms were followed every 7 days for 4 weeks. In control explants, six isoforms of esterase were observed. Three isoforms of peroxidase were not detected in the control bulb scale, which has not begun its morphogenesis process.

ACS Style

Marija Petrić; Angelina Subotić; Sladjana Jevremović; Milana Trifunović-Momčilov; Vojin Tadić; Marica Grujić; Zoran Vujčić. Esterase and peroxidase isoforms in different stages of morphogenesis in Fritillaria meleagris L. in bulb-scale culture. Comptes Rendus. Biologies 2015, 338, 793 -802.

AMA Style

Marija Petrić, Angelina Subotić, Sladjana Jevremović, Milana Trifunović-Momčilov, Vojin Tadić, Marica Grujić, Zoran Vujčić. Esterase and peroxidase isoforms in different stages of morphogenesis in Fritillaria meleagris L. in bulb-scale culture. Comptes Rendus. Biologies. 2015; 338 (12):793-802.

Chicago/Turabian Style

Marija Petrić; Angelina Subotić; Sladjana Jevremović; Milana Trifunović-Momčilov; Vojin Tadić; Marica Grujić; Zoran Vujčić. 2015. "Esterase and peroxidase isoforms in different stages of morphogenesis in Fritillaria meleagris L. in bulb-scale culture." Comptes Rendus. Biologies 338, no. 12: 793-802.

Book chapter
Published: 18 June 2015 in The Gentianaceae - Volume 2: Biotechnology and Applications
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Histochemical localization using the β-Glc Yariv reagent and immunolocalization with arabinogalactan protein (AGP) reactive antibodies (LM2, JIM13, JIM15, JIM16, MAC207) were performed during morphogenic induction in root cultures of Centaurium erythraea Rafn cultured on half-strength MS medium without plant growth regulators. The observations revealed that β-Glc Yariv reagent specifically bound to AGPs in cells of the root epidermis and central cylinder. Monoclonal antibodies recognizing AGPs were localized in epidermal cells and cells of the central cylinder (LM2 , JIM16), vascular tissue (JIM15), globular somatic embryos (LM2, MAC207), and de novo-formed meristematic centers in the root cortex (JIM16). The effect of β-Glc Yariv reagent was investigated after supplementation (0–75 μM) in the culture medium. The morphogenetic potential was increased at lower concentrations (15–25 μM) of treatment with β-Glc Yariv reagent but inhibited (40 %) at the highest concentration. These results implicate that AGPs play a significant role during the development of somatic embryos and adventitious shoots in root cultures of C. erythraea.

ACS Style

Milana Trifunović; Angelina Subotić; Marija Petrić; Sladjana Jevremović. The Role of Arabinogalactan Proteins in Morphogenesis of Centaurium erythraea Rafn In Vitro. The Gentianaceae - Volume 2: Biotechnology and Applications 2015, 113 -138.

AMA Style

Milana Trifunović, Angelina Subotić, Marija Petrić, Sladjana Jevremović. The Role of Arabinogalactan Proteins in Morphogenesis of Centaurium erythraea Rafn In Vitro. The Gentianaceae - Volume 2: Biotechnology and Applications. 2015; ():113-138.

Chicago/Turabian Style

Milana Trifunović; Angelina Subotić; Marija Petrić; Sladjana Jevremović. 2015. "The Role of Arabinogalactan Proteins in Morphogenesis of Centaurium erythraea Rafn In Vitro." The Gentianaceae - Volume 2: Biotechnology and Applications , no. : 113-138.

Journal article
Published: 29 August 2013 in Acta Physiologiae Plantarum
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We investigated the effect of low temperature and gibberellic acid (GA3) treatment on dormancy in Fritillaria meleagris L. bulbs. Also, we studied the effect of dormancy breaking on the antioxidant enzymes activity. To overcome dormancy, bulbs require a period (4–8 weeks) of exposure to low temperature. Bulbs regenerated in vitro were grown in the dark on medium without growth regulators at the standard (24 °C) or at low temperatures (4 and 15 °C) for 4, 6, 8 and 10 weeks. Bulbs were collected after 3, 4 and 5 weeks of cooling at 4 °C. To investigate the influence of GA3 on dormancy, bulbs were treated for 24 h with GA3 solutions with 1, 2 and 3 mg l−1 concentrations. During the period of growth of bulbs at 4 °C, regeneration of bulbs was very weak, while at 15 °C the number of regenerated bulbs increased significantly. Improved bulb sprouting was achieved by a short treatment with gibberellin. Low temperature also represents a kind of oxidative stress for the plant. The activity of superoxide dismutase, catalase (CAT) and peroxidase (POX) in bulbs of F. meleagris L. grown in vitro and ex vitro increased with decreasing temperature in contrast to glutathione reductase. POX showed generally lower activity than CAT which indicates that major role in the breaking dormancy and preparing bulbs for sprouting have catalases.

ACS Style

Marija Petrić; Sladjana Jevremović; Milana Trifunović-Momčilov; Vojin Tadić; Snežana Milošević; Milan Dragićević; Angelina Subotić. The effect of low temperature and GA3 treatments on dormancy breaking and activity of antioxidant enzymes in Fritillaria meleagris bulblets cultured in vitro. Acta Physiologiae Plantarum 2013, 35, 3223 -3236.

AMA Style

Marija Petrić, Sladjana Jevremović, Milana Trifunović-Momčilov, Vojin Tadić, Snežana Milošević, Milan Dragićević, Angelina Subotić. The effect of low temperature and GA3 treatments on dormancy breaking and activity of antioxidant enzymes in Fritillaria meleagris bulblets cultured in vitro. Acta Physiologiae Plantarum. 2013; 35 (11):3223-3236.

Chicago/Turabian Style

Marija Petrić; Sladjana Jevremović; Milana Trifunović-Momčilov; Vojin Tadić; Snežana Milošević; Milan Dragićević; Angelina Subotić. 2013. "The effect of low temperature and GA3 treatments on dormancy breaking and activity of antioxidant enzymes in Fritillaria meleagris bulblets cultured in vitro." Acta Physiologiae Plantarum 35, no. 11: 3223-3236.