Effects of different types of sugars and plant growth regulators on kohlrabi seedling growth and development in vitro
Keywords:kohlrabi tissue culture, sugars, plant growth regulators, morphogenesis, de novo shoot formation
- Kohlrabi (Brassica oleracea var. gongylodes) with its edible stem tuber formed at the base of plant stem, presents a valuable source of nutrients.
- The effects of plant growth regulators and different concentrations of various sugars on kohlrabi in vitro development and tuber formation were studied.
- Growth and development of treated kohlrabi seedlings was highly affected in a distinctive manner with altered morphological traits. Plant growth regulators stimulated callus formation and de novo organogenesis.
- Further investigation of the underlying mechanisms is necessary for understanding stem swelling in kohlrabi and involvement of the carbon source, plant hormones and/or other factors.
Abstract: Kohlrabi (Brassica oleracea var. gongylodes), with its edible stem tuber formed at the base of the plant stem, presents a valuable source of nutrients. The potential effects of plant growth regulators (PGRs), as well as various concentrations of different sugars on the in vitro development of kohlrabi were studied. Ten-day-old kohlrabi seedlings were cultivated in vitro for 5 weeks at 18±2°C on half-strength MS media containing different concentrations of carbon source such as sucrose, fructose, glucose, xylose and mannitol, combined with or without specific plant growth regulators (N6-benzyladenine (BA), gibberellic acid (GA3), 2,3,5-triiodobenzoic acid (TIBA)). Results showed no tuber formation in all treatments, but growth and development of treated kohlrabi seedlings was significantly affected in a distinctive manner, with a variety of morphological traits being altered in comparison to matching controls.
Received: June 22, 2020; Accepted: July 1, 2020; Published online: July 14, 2020
How to cite this article: Ćosić T, Savić J, Raspor M, Cingel A, Ghalawnji N, Vinterhalter B, Ninković S. Effects of different types of sugars and plant growth regulators on kohlrabi seedling growth and development in vitro. Arch Biol Sci. 2020;72(3):349-57.
Cardoza V, Stewart CN. Brassica biotechnology: progress in cellular and molecular biology. In Vitro Cell Dev Biol-Pl. 2004;40:542-51.
Selman IW, Kulasegaram S. Development of the stem tuber in kohlrabi. J Exp Bot. 1967;18(56):471-90.
Sobeih WY. The photoperiodic regulation of bulbing in onions (Allium cepa L.). IV. The translocation of 14C-assimilate during bulbing in response to light and hormonal factors. J Hortic Sci. 1988;63:109-18.
Turgeon R. The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol. 1989;40:119-38.
Farrar J. Regulation of shoot-root ratio is mediated by sucrose. Plant Soil. 1982;185:13-9.
Smeekens GSM. Sugar induced signal transduction in plants. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:49-81.
Ondo Ovono P, Claire Kevers C, Dommes J. Effects of reducing sugar concentration on in vitro tuber formation and sprouting in yam (Dioscorea cayenensis-D. rotundata complex) Plant Cell Tissue Organ Cult. 2009;99(1):55-9.
Gabryszewska E. The effects of glucose and growth regulators on the organogenesis of Paeonia lactiflora Pall. in vitro. J Fruit Ornam Plant Res. 2010;18(2):309-20.
De Paiva Neto VB, Campos Otoni W. Carbon sources and their osmotic potential in plant tissue culture: does it matter? Sci Hortic. 2003;97:193-202.
Gopal J, Chamail A, Sarkar D. In vitro production of microtubers for conservation of potato germplasm: effect of genotype, abscisic acid, and sucrose. In Vitro Cell Dev Biol-Pl. 2004;40:185-90.
Omokolo ND, Boudjeko T, Tsafack Takadong JJ. In vitro tuberization of Xanthosoma sagittifolium L. Schott: effect of phytohormones, sucrose, nitrogen and photoperiod. Sci Hortic. 2003;98:337-45.
Zheng Y, Liu Y, Ma M, Xu K. Increasing in vitro microrhizome production of ginger (Zingiber officinale Roscoe). Acta Physiol Plant. 2008;30:513-19.
Kästner U, Klahr A, Keller ERJ, Kahane R. Formation of onion bulblets in vitro and viability during medium-term storage. Plant Cell Rep. 2001;20:137-42.
Price J, Laxmi A, Martin SKS, Jang JC. Global transcription proﬁling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell. 2004;16:2128-50.
Rolland F, Baena-Gonzalez E, Sheen J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol. 2006;576(1):675-709.
Xu X, van Lammeren AAM, Vermeer E, Vreugdenhil D. The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiol. 1998;117:575-84.
Nishijima T, Sugii H, Fukino N, Mochizuki T. Aerial tubers induced in turnip (Brassica rapa var. rapa (L.) Hartm.) by gibberellin treatment. Sci Hortic. 2005;105:423-33.
Xu Z, Wang Q-M, Guo Y-P, Guo D-P, Shah G A, Liu H-L, Mao A. Stem-swelling and photosynthate partitioning in stem mustard are regulated by photoperiod and plant hormones. Environ Exp Bot. 2008;62:160-7.
Gupta A, Gupta R. K, Dhingra G. K., Kuriyal S, Lal S, Arya R. Variations in growth of tubers of field grown Coleus barbatus as affected by different hormonal treatments African J Plant Sci. 2010;4(12):467-73.
Ross SD, Bollmann MP, Pharis RP, Sweet GB. Gibberellin A4/7 and the promotion of flowering in Pinus radiata: effects on partitioning of photoassimilate within the bud during primordial differentiation. Plant Physiol. 1984;76:326-30.
Roitsch T. Source-sink regulation by sugars and stress. Curr Opin Plant Biol. 1999;2:198-206.
Sokolova SV, Balashina NO, Krasavina MS. Activation of soluble acid invertase accompanies the cytokinin-induced source-sink leaf transition. Russ J Plant Physiol. 2002;49:86-91.
Trouverie J, Thévenot C, Rocher JP, Sotta B, Prioul JL. The role of abscisic acid in the response of a specific vacuolar invertase to water stress in the adult maize leaf. J Exp Bot. 2003;54:2177-86.
Borisjuk L, Rolletschek H, Wobus U, Weber H. Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. J Exp Bot. 2003;54(382):503-12.
Roumeliotis E, Kloosterman B, Oortwijn M, Kohlen W, Bouwmeester HJ, Visser RGF, Bachem CWB. The effects of auxin and strigolactones on tuber initiation and stolon architecture in potato. J Exp Bot. 2012;63:4539-48.
Wang GL, Huang Y, Zhang XY, Xu ZS, Wang F, Xiong AS. Transcriptome-based identification of genes revealed differential expression profiles and lignin accumulation during root development in cultivated and wild carrots. Plant Cell. 2016;35:1743-55.
Li J, Ding Q, Wang F, Zhang Y, Li H, Gao J. Integrative analysis of mRNA and miRNA expression profiles of the tuberous root development at seedling stages in turnips. PLoS One. 2015;10(9): e0137983.
Mitsui Y, Shimomura M, Komatsu K, Namiki N, Shibata-Hatta M, Imai M, Katayose Y, Mukai Y, Kanamori H, Kurita K, Kagami T, Wakatsuki A, Ohyanagi H, Ikawa H, Minaka N, Nakagawa K, Shiwa Y, Sasaki T. The radish genome and comprehensive gene expression profile of tuberous root formation and development. Sci Rep. 2015;5:10835.
Hearn DJ, O'Brien P, Poulsen TM. Comparative transcriptomics reveals shared gene expression changes during independent evolutionary origins of stem and hypocotyl/root tubers in Brassica (Brassicaceae). PLoS One. 2018;13(6):e0197166.
Ćosić T, Motyka V, Raspor M, Savić J, Cingel A, Vinterhalter B, Vinterhalter D, Trávníčková A, Dobrev PI, Bohanec B, Ninković S. 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. 2015;121(3):741-60.
Ćosić T, Raspor M, Savić J, Cingel A, Matekalo D, Zdravković-Korać S, Ninković S. Expression profiles of organogenesis-related genes over the time course of one-step de novo shoot organogenesis from intact seedlings of kohlrabi. J Plant Physiol. 2019;232:257-69.
Glendening TM, Sjolund R. In vitro propagation of kohlrabi from leaf explants. HortScience. 1988;23:772.
Khan MR, Rashid H, Ansar M, Chaudry Z. High frequency shoot regeneration and Agrobacterium-mediated DNA transfer in Canola (Brassica napus). Plant Cell Tissue Organ Cult 2003;75:223-31.
Ghnaya AB, Charles G, Branchard M. Rapid shoot regeneration from thin cell layer explants excised from petioles and hypocotyls in four cultivars of Brassica napus L. Plant Cell Tissue Organ Cult. 2008;92:25-30.
Abbasi BH, Khan M, Guo B, Bokhari SA, Khan MA. Efficient regeneration and antioxidative enzyme activities in Brassica rapa var. turnip. Plant Cell Tissue Organ Cult 2011;105:337-44.
Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum. 1962;15:473-97.
Linsmaier EM, Skoog F. Organic growth factor requirements of tobacco tissue cultures. Physiol Plantarum. 1965;18(1):100-27.
Koch KE. Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:509-40.
Ramon M, Rolland F, Sheen J. Sugar sensing and signaling. Arabidopsis Book. 2008;6:e0117.
Eveland AL, Jackson DP. Sugars, signaling and plant development. J Exp Bot. 2012;63(9):3366-77.
Simko I. Sucrose application causes hormonal changes associated with potato tuber induction. J Plant Growth Reg. 1994;13:73-77.
Prat S. Hormonal and daylength control of potato tuberisation. In: Davies PJ, editor. Plant hormones: biosynthesis, signal transduction, action! 3rd ed. Dordecht: Kluwer Academic Publishers; 2004. p. 538-60.
Kumar CN, Jadhav SK, Tiwari KL, Afaque Q. In vitro tuberization and colchicine content analysis of Gloriosa superba L. biotechnology. 2015;14(3):142-7.
Zel J, Debeljak N, Ucman R, Ravnikar M. The effect of jasmonic acid, sucrose and darkness on garlic (Allium sativum L. cv. Ptujski jesenski) bulb formation in vitro. In Vitro Cell Dev Biol-Pl. 1997;33:231-5.
Le Guen-Le Saos F, Hourmant A, Esnault F, Chauvin JE. In vitro bulb development in shallot (Allium cepa L. Aggregatum Group): Effects of anti-gibberellins, sucrose and light. Ann Bot. 2002;89:419-25.
Guo DP, Jiang YT, Zeng GW, Shah GA. Stem swelling of stem mustard, as affected by temperature and growth regulators. Sci Hortic. 1994;60:153-60.
Ewing EE. The role of hormones in potato (Solanum tuberosum L.) tuberization. In: Davies PG, editor. Plant Hormones: Physiology, biochemistry and molecular biology. Dordrecht: Kluwer; 1995. p. 698-724.
Xue T, Guo L, Xue J-p, Song Y-x, Lu H-d, Zhang A-m, Sheng W. Study of the system of tuberous root induction in vitro from Rehmannia glutinosa. Afr J Biotechnol. 2012;11(28):7202-7.
Brenner ML, Cheikh N. The role of hormones in photosynthate partitioning and seed filling. In: Davies PJ, editor. Plant hormones, physiology, biochemistry, and molecular biology. 2nd ed. Dordecht: Kluwer Academic Publishers; 1995. p. 649-70.
Gibson SI. Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol. 2005;8:93-102.
Asmono SL, Sari VK, Djenal A. The effects of different concentration of sucrose and various auxin on in vitro shoot and microtuber formation of red potato (Solanum tuberosum, L. var Desiree). 1st International Conference on Food and Agriculture 2018, ICoFA 2018; 20148 Oct 20-21; Nusa DuaBali, Indonesia. Institute of Physics Publishing; 2018. 012002. (IOP Conference Series: Earth and Environmental Science; Vol. 207).
Hannson J, Smeekens S. Sugar perception and signaling - an update. Curr Opin Plant Biol. 2009;12:562-7.
Dutt S, Manjul AS, Raigond P, Singh B, Siddappa S, Bhardwaj V. Key players associated with tuberization in potato: potential candidates for genetic engineering. Crit Rev Biotechnol. 2017;37(7):942-57.
Saniewski M, Węgrzynowicz-Lesiak E, Góraj-Koniarska J, Gabryszewska E. Effect of benzyladenine (BA) on auxin-induced stem elongation and thickening in tulip (Tulipa gesneriana L.). Acta Agrobot. 2016;69(1):1650.
Hannapel DJ, Sharma P, Lin T, Banerjee AK. The multiple signals that control tuber formation. Plant Physiol. 2017;174:845-56.
Albert NW, Davies KM, Schwinn KE. Gene regulation networks generate diverse pigmentation patterns in plants. Plant Signal Behav. 2014;9:e29526.
Bhjowani SS, Razdan MK. Plant Tissue Culture: Theory and Practice. Rev. edition. Elsevier; 1996. 766 p.
Patel TK, Williamson JD. Mannitol in Plants, Fungi, and Plant-Fungal Interactions. Trends Plant Sci. 2016;21(6):486-97.
Smirnoff N, Cumbes QJ. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry. 1989;28:1057-60.
Zhang Y, Hu Z, Zhu M, Zhu Z, Wang Z, Tian S, Chen G. Anthocyanin accumulation and molecular analysis of correlated genes in purple kohlrabi (Brassica oleracea var. gongylodes L.). J Agric Food Chem. 2015;63(16):4160-9.
Tholakalabavi A, Zwiazek JJ, Thorpe TA. Effect of mannitol and glucose-induced osmotic stress on growth, water relations, and solute composition of cell suspension cultures of poplar (Populus deltoides var. Occidentalis) in relation to anthocyanin accumulation. In Vitro Cell Dev Biol-Pl. 1994;30P:164-70.
Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 2006;140(2):637-46.
Song X, Guo H, Liu Y, Wan F, Zhang J, Chang X. Eﬀects of salicylic acid and sucrose on pigment content in Pistacia chinensis leaves. Sci Hortic. 2020;259:108783.
Hara M, Oki K, Hoshino K, Kuboi T. Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus) hypocotyl. Plant Sci. 2003;164:259-265.
Yuan T-T, Xu H-H, Zhang K-X, Guo T-T, Lu Y-T. Glucose inhibits root meristem growth via ABA INSENSITIVE 5, which represses PIN1 accumulation and auxin activity in Arabidopsis. Plant, Cell Environment. 2014;37:1338-50.
Zhang RX, Li S, He J, Liang YK. BIG regulates sugar response and C/N balance in Arabidopsis. Plant Signal Behav. 2019;14(11):1669418.