The effects of β-lactam antibiotics and hygromycin B on de novo shoot organogenesis in apple cv. Golden Delicious

Mariana Stanišić, Slavica Ninković, Jelena Savić, Tatjana Ćosić, Nevena Mitić

Abstract


Since the genetic transformation of the apple is strongly genotype-dependent and generally inefficient, the evaluation of factors affecting shoot regeneration are crucial for the establishment of a successful transformation process. In this report, we evaluated the effects of the β-lactam antibiotics meropenem and timentin on in vitro regeneration via de novo shoot organogenesis from leaf explants of apple cv. Golden Delicious, as well as on the growth of the Agrobacterium tumefaciens strain EHA 105, and compared them with the commonly used β-lactam cefotaxime. Also, we report for the first time the effect of hygromycin B as a selective agent in the domesticated apple, as regards shoot regeneration and shoot multiplication efficiency. We observed that cefotaxime and timentin at concentrations higher than 100 mg L-1 were sufficient to prevent Agrobacterium growth during a two-week period, while meropenem exhibited an inhibitory effect on bacterial growth at all tested concentrations (25-150 mg L-1). Cefotaxime at a concentration of 300 mg L-1 increased the number of regenerated shoots per explant (9.39) in comparison with the control (7.67). In contrast to cefotaxime, meropenem and timentin caused a decrease in shoot regeneration efficiency, but larger and more developed shoots were obtained on meropenem (25-125 mg L-1) after the same period of cultivation. Hygromycin B at a concentration of 5 mg L-1 or higher completely inhibited shoot regeneration and induced explant tissue necrosis. Therefore, the selection procedure with a final concentration of 4 mg L-1 throughout organogenesis and 10 mg L-1 for further shoot growth and multiplication is recommended for an efficient transformation process in apple cv. Golden Delicious.

https://doi.org/10.2298/ABS170731037S

Received: July 31, 2017; Revised: September 23, 2017; Accepted: September 25, 2017; Published online: October 11, 2017

How to cite this article: Stanišić M, Ninković S, Savić J, Ćosić T, Mitić N. The effects of β-lactam antibiotics and hygromycin B on de novo shoot organogenesis in apple cv. Golden Delicious. Arch Biol Sci. 2018;70(1):179-90.


Keywords


cefotaxime; meropenem; Malus × domestica Borkh.; regeneration; timentin

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Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova,V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan, A C, Bus V, Chagne D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouze P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R. The genome of the domesticated apple (Malus x domestica Borkh.). Nat Genet. 2010;42:833-9.

Keller DM, Lotspeich WDJBC-L. Effect of phlorizin on the osmotic behavior of mitochondria in isotonic sucrose. J Biol Chem.1959;234:991-4.

Vick HD, Deidrich DF. Reevaluation of renal tubular glucose transport inhibition by phlorizin analogs. Am J Physiol.1973;224:552-7.

Awad MA, de Jager A, van Westing LM. Flavonoid and chlorogenic acid levels in apple fruit: characterisation of variation. Sci Hort. 2000;83:249-63.

Puite KJ, Schaart JG. Genetic modification of the commercial Agrobacterium tumefaciens mediated transformation method. Plant Sci. 1996;119:125-33.

Maximova SN, Dandekar M, Guiltinan MJ. Investigation of Agrobacterium mediated transformation of apple using green fluorescent protein: high transient expression and low stable transformation suggest that factors other than T DNA transfer are rate limiting. Plant Mol Biol. 1998;37:549-59.

Dai H, Li W, Han G, Yang Y, Ma Y, Li H, Zhang Z. Development of a seedling clone with high regeneration capacity and susceptibility to Agrobacterium in apple. Sci Hort. 2013;16: 202-8.

James DJ, Passey AJ, Barbara DJ, Bevan M. Genetic transformation of apple (Malus pumila Mill.) using a disarmed Ti-binary vector. Plant Cell Rep. 1989;7:658-61.

Zhang Z, Jing S, Wang G, Fang H, Wu L. Genetic transformation of the commercial apple cultivars New Jonagold and regeneration of its transgenic plants. Acta Hortic Sinica. 1997;24:378-80.

Seong ES, Song KJ, Jegal S, Yu CY, Chung IM. Silver nitrate and aminoethoxyvinylglycine effect Agrobacterium-mediated apple transformation. Plant Growth Regul. 2005;45:75-82.

Wu Y, Li Y, Wua Y, Chenga H, Li Y, Zhaoa Y, Li Y. Transgenic plants from fragmented shoot tips of apple (Malus baccata (L.) Borkhausen) via agrobacterium-mediated transformation. Sci Hortic. 2011;128:450-56.

Nauerby B, Billing K, Wyndaele R. Influence of the antibiotic timentin on plant regeneration compared to carbenicillin and cefotaxime in concentrations suitable for elimination of Agrobacterium tumefaciens. Plant Sci.1997;12:169-77.

da Silva Mendes AF, Cidale LC, de Oliveira MLP, Otoni WC, Soares-Filho WDS, Costa MGC. Evaluation of novel beta-lactam antibiotics in comparison to cefotaxime on plant regeneration of Citrus sinensis L. Osb. Plant Cell Tissue Organ Cult. 2009;97:331-6.

Qin YH, Teixeira da Silva JA, Bi JH, Zhang SL, Hu GB. Response of in vitro strawberry to antibiotics. Plant Growth Regul. 2011;65:183-93.

Costa MGC, Nogueira FTS, Figueira ML, Otoni WC, Brommonschenkel SH, Cecon, PR. Influence of the antibiotic timentin on plant regeneration of tomato (Lycopersicon esculentum Mill.) cultivars. Plant Cell Rep. 2000;19:327-32.

Tereso S, Miguel C, Maroco J, Oliveira MM. Susceptibility of embryogenic and organogenic tissues of maritime pine (Pinus pinaster) to antibiotics used in Agrobacterium-mediated genetic transformation. Plant Cell Tissue Organ Cult. 2006;87:33-40.

Bosela MJ. Effects of β-lactam antibiotics, auxins, and cytokinins on shoot regeneration from callus cultures of two hybrid aspens, Populus tremuloides x P. tremula and P. x canescens x P. gradidentata. Plant Cell Tissue Organ Cult. 2009;98:249-61.

Naderi D, Askari-Khorasgani O, Mahmoudi E. Cefotaxime and benzyladenine improve melon regeneration. Iran J Biotechnol. 2016;14:56-60.

Dai W, Castillo C. Factors affecting plant regeneration from leaf tissues of Buddleia species. HortScience. 2007;42:1509-17.

Mittal P, Gosal SS, Senger A, Kumar P. Impact of cefotaxime on somatic embryogenesis and shoot regeneration in sugarcane. Physiol Mol Biol Plants. 2009;15:257-65.

Padilla IMG, Burgos L. Aminoglycoside antibiotics: structure, functions and effects on in vitro plant culture and genetic transformation protocols. Plant Cell Rep. 2010; 29:1203-13.

Yepes LM, Aldwinckle HS. Factors that affect leaf regeneration in apple and effect of antibiotics in morphogenesis. Plant Cell Tissue Organ Cult. 1994;37:257-69.

Mann RL, Bromer WW. The isolation of a second antibiotic from Streptomyces hygroscopicus. J Am Chem Soc. 1958;80:2714-6.

Parrott WA, All JN, Adang MJ, Bailey MA, Boerma HR, Stewart CN. Recovery and evaluation of soybean plants transgenic for a Bacillus thuringiensis var. kurstaki insecticidal gene. In Vitro Cell Dev Biol Plant. 1994;30:144-9.

Nyaboga E, Tripathi JN, Manoharan R, Tripathi L. Agrobacterium-mediated genetic transformation of yam (Dioscorea rotundata): an important tool for functional study of genes and crop improvement. Front Plant Sci. 2014;5:1-12.

Phlaetita W, Chin DP, Otanga N, Nakamura I, Mii, M. High efficiency Agrobacterium-mediated transformation of Dendrobium orchid using protocorms as a target material. Plant Biotechnol 2015;32:323-7.

Eustice DC, Wilhelm JM. Fidelity of the eukaryotic codon–anticodon interaction: Interference by aminoglycoside antibiotics. Biochemistry. 1984;23:1462-7.

Peske F, Savelsbergh A, Katunin VI, Rodnina MV, Wintermeyer W. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J Mol Biol. 2004;34:1183-94

Angenon G, Dillen W, Montagu MV. Antibiotic resistance markers for plant transformation, In: Gelvin SB, Schilperoort RA, еditors. Plant Molecular Biology Manual II. Dordrecht: Klumer; 1994. p. 1-13.

Dolgov SV, Skryabin KG. Transgenic apple clonal rootstock resistant to Basta herbicide. Acta Hortic. 2004;663:499-502.

Modgil M, Sharma R. Effect of antibiotics on regeneration and elimination of bacteria during gene transfer in apple. Acta Hort. 2009;839:353-9.

Park YD, Ronis DH, Boe AA, Cheng ZM. Plant regeneration from leaf tissue of four North Dakota genotypes of potato (Solanum tuberosum L.). Am J Potato Res.1995;72:329-38.

Eady CC, Lister CE. A comparison of four selective agents for use with Allium cepa L. immature embryos and immature embryo-derived cultures. Plant Cell Rep. 1998;18:117-21.

Meng ZH, Liang AH, Yang WC. Effects of hygromycin on cotton cultures and its application in Agrobacterium-mediated cotton transformation. In Vitro Cell Dev Biol Plant. 2007;43:111-8.

Wilmink A, Dons JJ. Selective agents and marker genes for use in transformation of monocotyledonous plants. Plant Mol Biol Rep. 1993;11:165-85.

Hood EE, Gelvin SB, Melchers LS, Hoekema A. New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res. 1993;2:208-18.

Mitić N, Stanišić M, Milojević J, Tubić Lj, Ćosić T, Nikolić R, Ninković S. Optimization of in vitro regeneration from leaf explants of apple cultivars Golden Delicious and Melrose. HortScience. 2012;47:1117-22.

Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant. 1962;15:473-97.

Linsmaier EM, Skoog F. Organic growth factor requirements of tobacco tissue cultures. Physiol Plant. 1965;18:100-27.

Zwietering MH, Jongenburger I, Rombouts FM, Van'Triet K. Modeling of the bacterial growth curve. Appl Environ Microbiol. 1990;56:1875-81.

Ogawa Y, Mii M. Meropenem and moxalactam: Novel β-lactam antibiotics for efficient Agrobacterium-mediated transformation. Plant Sci. 2007;172:564-72.

Calabrese EJ, Blain RB. Hormesis and plant biology. Environ Pollut. 2008;157:42-8.

Dragicević M, Platiša J, Nikolić R, Todorović S, Bogdanović M, Mitić N, Simonović A. Herbicide phosphinothricin causes direct stimulation hormesis. Dose-Response. 2013;11:344-60.

Grzebelus E, Skop L. Effect of β-lactam antibiotics on plant regeneration in carrot protoplast cultures. In Vitro Cell Dev Biol Plant. 2014;50:568-75.

Naing AH, Park KI, Lim SH, Kim CK. Appropriate choice of antibiotics for plant regeneration and optimization of selective agents to be used in genetic transformation of chrysanthemum. Plant Omics. 2014;7:237-43.

Bucourt R, Bormann D, Heymes R, Perronnet M. Chemistry of cefotaxime. J Antimicrob Chemother. 1980;6:63-7.

Mathias RJ, Boyd LA. Cefotaxime stimulates callus growth, embryogenesis and regeneration in hexaploid bread wheat (Triticum aestivum). Plant Sci. 1986;46:217-23.

Pius J, George L, Eapen S, Rao PS. Enhanced plant regeneration in pearl millet (Pennisetum americanum) by ethylene inhibitors and cefotaxime. Plant Cell Tissue Organ Cult.1993;32:91-6.

Grewal D, Gill R, Gosal SS. Influence of antibiotic cefotaxime on somatic embryogenesis and plant regeneration in indica rice. Biotechnol J. 2006;1:1158-62.

Demain AL, Elander RP. The β-lactam antibiotics: past, present, and future. Antonie Van Leeuwenhoek.1999;75:5-19.

De Bondt A, Eggermont K, Druart P, De Vil M, Goderis I, Vanderleyden J, Broekaert WF. Agrobacterium-mediated transformation of apple (Malus x domestica Borkh.): an assessment of factors affecting gene transfer efficiency during early transformation steps. Plant Cell Rep. 1994;13:587-93.

Szankowski I, Briviba K, Fleschhut J, Schönherr J, Jacobsen HJ, Kiesecker H. Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa). Plant Cell Rep. 2003;22:141-9.

Holford P, Newbury HJ. The effects of antibiotics and their breakdown products on the in vitro growth of Antirrhinum majus. Plant Cell Rep. 1992;11:93-6.

Mamidala P, Nanna RS. Efficient in vitro plant regeneration, flowering and fruiting of dwarf tomato cv. Micro-Msk. Plant Omics J. 2009;2:98-102.

Tang H, Ren Z, Krczal G. An evaluation of antibiotics for the elimination of Agrobacterium tumefaciens from walnut somatic embryos and for the effects on the proliferation of somatic embryos and regeneration of transgenic plants. Plant Cell Rep. 2000;19:881-7.

Silva TER, Cidade LC, Alvim FC, Cascardo JCM, Costa MGC. Studies on genetic transformation of Theobroma cacao L.: evaluation of different polyamines and antibiotics on somatic embryogenesis and the efficiency of uidA gene transfer by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult. 2009;99:287-98.

Norelli JL, Aldwinckle HS. The role of aminoglycoside antibiotics in the regeneration and selection of neomycin phosphotransferase transgenic apple tissue. J Am Soc Hortic Sci. 1993;118:311-6.

Bolar JP, Brown SK, Norelli JL, Aldwinckle HS. Factors affecting the transformation of Marshall McIntosh apple by Agrobacterium tumefaciens. Plant Cell Tissue Organ Cult. 1999;5:31-8.

Seong ES, Song KJ. Factors affecting the early gene transfer step in the development of transgenic ‘Fuji’ apple plants. Plant Growth Regul. 2008;54:89-95.


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