Abstract
Bauhinia holophylla is a woody plant found in the Brazilian Cerrado used in folk medicine to treat diabetes. Lectins are glycoproteins with several biotechnological applications and play important roles in plant defenses and in medicine. Lectins have been produced in vitro using plant tissue culture techniques. This study shows the production and characterization of lectin from B. holophylla by callus culture. Calli were obtained from leaf segments placed on woody plant and Murashige and Skoog media supplemented with 2,4-dichlorophenoxyacetic acid (0, 4.52, 9.05, 18.10 µM) or 6-benzylaminopurine (0, 4.44, 8.88, 17.75 µM), in the presence or absence of light. The highest concentrations of lectin expressed by hemagglutination activity were observed in green and compact callus induced in woody plant medium supplemented with 6-benzylaminopurine in the presence of light, which showed specificity by all types of erythrocytes tested. The highest concentrations of lectin (128 HU mg−1) and fresh weight of callus were observed in the stationary phase (41st–60th day). Lectin was not detected in subcultured calli. d-Galactose promoted the highest inhibitory effect on the lectin activity in human erythrocytes ABO system, especially B-type. Lectin has been shown to be a stable protein, maintaining its hemagglutination activity after incubation at a wide range of temperatures, pH values and ethylenediaminetetraacetic acid concentrations.
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Afolabi-Balogun NB, Inuwa HM, Ishiyaku MF, Bakare-Odunoola MT, Nok AJ (2012) Isolation and characterization of a mannose-binding insecticidal lectin gene from Allium sativum (garlic) and its putative role in insect resistance using bioinformatics tools. Infect Genet Evol 12:1508–1512. https://doi.org/10.1016/j.meegid.2012.05.008
Ahmed ABA, Pallela R, Rao AS, Rao MV, Mat Taha R (2011) Optimized conditions for callus induction, plant regeneration and alkaloids accumulation in stem and shoot tip explants of Phyla nodiflora. Span J Agric Res 9:1262–1270. https://doi.org/10.5424/sjar/20110904-453-10
Ali M, Abassi BH, Haq I-UL (2013) Production of commercially important secondary metabolites and antioxidant activity in cell suspension cultures of Artemisia absinthium L. Ind Crops Prod 49:400–406. https://doi.org/10.1016/j.indcrop.2013.05.033
Al-Khayri JM (2012) Determination of the date palm cell suspension growth curve, optimum plating efficiency, and influence of liquid medium on somatic embryogenesis. Emir J Food Agric 24:444–455
Arunyanart S, Chaitrayagun M (2005) Induction of somatic embryogenesis in lotus (Nelumbo nucifera Geartn.). Sci Hortic 105:411–420. https://doi.org/10.1016/j.scienta.2005.01.034
Ávila AL, Pereyra SM, Argüello J (1998) Nitrogen concentration and proportion of NH4-N affect potato cultivar response in solid and liquid media. HortScience 33:336–338
Bala M, Nag TN, Mathur K, Kumar S, Vyas M, Saini A, Tomar B (2010) In vitro callus induction for determination of lectin activity in pea (Pisum sativum L.) variety (AP-1). Rom Biotechnol Lett 15:5781–5787. https://doi.org/10.1080/11263509609438342
Bari AU, Silva HC, Silva MTL, Pereira Junior FNP, Cajazeiras JB, Sampaio AH, Leal RB, Teixeira EH, Rocha BAM, Nascimento KS, Nagano CS, Cavada BS (2013) Purification and partial characterization of a new mannose/glucose-specific lectin from Dialium guineense Willd seeds that exhibits toxic effect. J Mol Recognit 26:351–356. https://doi.org/10.1002/jmr.2279
Borrebaeck CAK, Linsefors L (1985) Hormonal regulation of the lectin biosynthesis in callus culture of the Phaseolus vulgaris plant. Plant Physiol 79:659–662. https://doi.org/10.1104/pp.79.3.659
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Braga KQ, Coimbra MC, Castro AHF (2015) In vitro germination, callus induction and phenolic compounds contents from Pyrostegia venusta (Ker Gawl.) Miers. Acta Sci Biol Sci 37:151–158. https://doi.org/10.4025/actascibiolsci.v37i2. 26067
Buul VJV, Brouns FJPH (2014) Health effects of wheat lectins: a review. J Cereal Sci 59:112–117. https://doi.org/10.1016/j.jcs.2014.01.010
Calafell F, Roubinet F, Ramirez-Soriano A, Bertranpetit J, Saitou N (2008) Evolutionary dynamics of the human ABO gene. Hum Genet 124:123–135. https://doi.org/10.1007/s00439-008-0530-8
Carvalho AS, Silva MV, Gomes FS, Paiva PMG, Malafaia CB, Silva TD, Vaz AFM, Arruda IRS, Napoleão TH, Carneiro-da-Cunha MG, Correia MTS (2015) Purification, characterization and antibacterial potential of a lectin isolated from Apuleia leiocarpa seeds. Int J Biol Macromol 75:402–408. https://doi.org/10.1016/j.ijbiomac.2015.02.001
Charungchitrak S, Petsom A, Sangvanich P, Karnchanatat A (2010) Antifungal and antibacterial activities of lectin from the seeds of Archidendron jiringa Nielsen. Food Chem 126:1025–1032. https://doi.org/10.1016/j.foodchem.2010.11.114
Coenen C, Lomax TL (1997) Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends Plant Sci 2:351–356. https://doi.org/10.1016/S1360-1385(97)84623-7
Del Sol FGD, Cavada BS, Calvete JJ (2007) Crystal structures of Cratylia xoribunda seed lectin at acidic and basic pHs. Insights into the structural basis of the pH-dependent dimer–tetramer transition. J Struct Biol 158:1–9. https://doi.org/10.1016/j.jsb.2006.08.014
Devi PR, Kombiah P, Sudhakar GLR, Babu C (2014) Purification and characterization of a novel lectin from Geotrupes stercorarius. Int J Adv Biotechnol Res 5:157–162
Eymar E, Alegre L, Toribio M, Vela-López D (2000) Effect of activated charcoal and 6-benzykadenine in vitro nitrogen upatake by Lagerstroemia indica. Plant Cell Tissue Organ Cult 63:57–65. https://doi.org/10.1023/A:1006471519609
Feitosa LS, Costa AS, Arrigoni-Blank MF, Dibax R, Botanico MP, Blank AF (2013) Indução e análise histológica de calos em explantes foliares de Jatropha curcas L. (Euphorbiaceae). Biosci J 29:370–377
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciênc Agrotec 35:1039–1042. https://doi.org/10.1590/S1413-70542011000600001
Fu LL, Zhou CC, Yao S, Yu JY, Liu B, Bao JK (2011) Plant lectins: targeting programmed cell death pathways as antitumor agents. Int J Biochem Cell Biol 43:1442–1449. https://doi.org/10.1016/j.biocel.2011.07.004
George EF, Michael AH, De Klerk GJ (2008) Plant propagation by tissue culture—the background. Springer, Dordrecht
Ghosh BN, Dasgupta B, Sircar PK (1985) Lectin distribution at different stages in the tissues of Cecropia obtusifolia. Curr Sci 54:80–82
Girão DKFB, Cavada BS, Pires AF, Martins TV, Franco AX, Morais CM, Nascimento KS, Delatorre P, Nagano CS (2015) The galactose-binding lectin isolated from Bauhinia bauhinioides Mart. seeds inhibits neutrophil rolling and adhesion via primary cytokines. J Mol Recognit 28:285–291. https://doi.org/10.1002/jmr.2441
Gueven A, Knorr D (2011) Isoflavonoid production by soy plant callus suspension culture. J Food Eng 103:237–243. https://doi.org/10.1016/j.jfoodeng.2010.10.019
Hartig K, Beck E (2006) Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biol 8:389–396. https://doi.org/10.1055/s-2006-923797
Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. https://doi.org/10.1105/tpc.113.116053
Inbar M, Sachs L (1969) Interaction of the carbohydrate-binding protein concanavalin A with normal and transformed cells. Proc Natl Acad Sci USA 63:1418–1425
James DW, Ghosh M, Etzler ME (1985) Production of a lectin in tissue cultures of Dolichos biflorus. Plant Physiol 77:630–634. https://doi.org/10.1104/pp.77.3.630
Jaskani MJ, Abbas H, Sultana R, Khan MM, Qasim M, Khan IA (2008) Effect of growth hormones on micropropagation of Vitis vinifera L. cv. Perlette. Pak J Bot 40:105–109
Jayavardhanan KK, Padikkala J, Panikkar KR (1996) Lectin biosynthesis in callus culture established from seeds of Canavalia virosa. Biol Plant 38:329–334. https://doi.org/10.1007/BF02896658
Joyce SM, Cassells AC, Jain M (2003) Stress and aberrant phenotypes in in vitro culture. Plant Cell Tissue Organ Cult 74:103–121. https://doi.org/10.1023/A:1023911927116
Lee KP, Lee DW (2013) The identification of in vitro production of lectin from callus cultures of Korean Mistletoe (Viscum album L. var. coloratum). Biosci Biotechnol Biochem 77:884–887. https://doi.org/10.1271/bbb.120962
Liener IE, Hill EG (1953) The effect of heat treatment on the nutritive value and hemagglutinating activity of soybean oil meal. J Nutr 49:609–620
Liu B, Bian HJ, Bao JK (2010) Plant lectins: potential antineoplastic drugs from bench to clinic. Cancer Lett 287:1–12. https://doi.org/10.1016/j.canlet.2009.05.013
Lloyd G, Mc Cown NB (1980) Commercially-feasible micropropagation of Mountain laurel, Kalmia latifolia, by use of shoot tip culture. Int Plant Propag Soc Proc 30:421–426
Loris R, Hamelrick T, Bouckaert J, Wyns L (1998) Legume lectin structure. Biochim Biophys Acta 1383:9–36. https://doi.org/10.1016/S0167-4838(97)00182-9
Loris R, Van Walle I, De Greve H, Beeckmans S, Deboeck F, Wyns L, Bouckaert J (2004) Structural basis of oligomannose recognition by the Pterocarpus angolensis seed lectin. J Mol Biol 335:1227–1240. https://doi.org/10.1016/j.jmb.2003.11.043
Luz LA, Silva MCC, Ferreira RS, Santana LA, Silva-Lucca RA, Mentele R, Oliva MLV, Paiva PMG, Coelho LCBB (2013) Structural characterization of coagulant Moringa oleifera lectin and its effect on hemostatic parameters. Int J Biol Macromol 58:31–36. https://doi.org/10.1016/j.ijbiomac.2013.03.044
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nagano CS, Calvete JJ, Barenttino D, Pérez A, Cavada BS, Sanz L (2008) Insights in to the structural basis of the pH-dependent dimer–tetramer equilibrium through crystallographic analysis of recombinant Diocleinae lectins. Biochem J 409:417–428. https://doi.org/10.1042/BJ20070942
Nakagawa R, Yasokawa D, Ikeda T, Nagashima K (1996) Purification and characterization of two lectins from callus of Helianthus tuberosus. Biosci Biotechnol Biochem 60:259–262. https://doi.org/10.1271/bbb.60.259
Panda PK, Mukhopadhyay S, Behera B, Bhol CS, Dey S, Das DN, Sinha N, Bissoyi A, Pramanik K, Maiti TK, Bhutia SK (2014) Antitumor effect of soybean lectin mediated through reactive oxygen species-dependent pathway. Life Sci 111:27–35. https://doi.org/10.1016/j.lfs.2014.07.004
Parasharami V, Yadav P, Mandkulkar S, Gaikwad S (2014) Ficus religiosa L.: callus, suspension culture and lectin activity in fruits and in vitro regenerated tissues. Br Biotechnol J 4:215–227. https://doi.org/10.9734/BBJ/2014/7338
Pawar K, Thengane SR (2009) Influence of hormones and medium components on expression of dipyranocoumarins in cell suspension cultures of Calophyllum inophyllum L. Process Biochem 44:916–922. https://doi.org/10.1016/j.procbio.2009.03.005
Pinheiro MS, Rodrigues LS, Neto LS, Moraes-Souza RQ, Soares TS, Américo MF, Campos KE, Damasceno DC, Volpato GT (2017) Effect of Bauhinia holophylla treatment in Streptozotocin-induced diabetic rats. An Acad Bras Cienc 89:1–10. https://doi.org/10.1590/0001-3765201720160050
Raikhel NV, Palevitz BA, Haigler CH (1986) Abscisic acid control of lect accumulation in wheat seedlings and callus cutures. Plant Physiol 80:167–171. https://doi.org/10.1104/pp.80.1.167
Rao S, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153. https://doi.org/10.1016/S0734-9750(02)00007-1
Rodrigues VEG, Carvalho DA (2001) Levantamento etnobotânico de plantas medicinais no domínio Cerrado na região do Alto Rio Grande – Minas Gerais. Ciênc Agrotec 25:102–123
Rozza AL, Cesar DAS, Pieroni LG, Saldanha LL, Dokkedal AL, Faria FM, Souza-Brito ARM, Vilegas W, Takahira RK, Pellizzon CH (2015) Antiulcerogenic activity and toxicity of Bauhinia holophylla hydroalcoholic extract. Evid Based Complement Altern Med 2015:1–9. https://doi.org/10.1155/2015/439506
Sá RA, Santos NDL, Silva CSB, Napoleão TH, Gomes FS, Cavada BS, Coelho LCBB, Navarro DMAF, Bieber LW, Paiva PMG (2009) Larvicidal activity of lectins from Myracrodruon urundeuva on Aedes aegypti. Comp Biochem Physiol C Toxicol Pharmacol 149:300–306. https://doi.org/10.1016/j.cbpc.2008.08.004
Sahin G, Verma G, Gurel E (2013) Calcium and magnesium elimination enhances accumulation of cardenolides in callus cultures of endemic Digitalis species of Turkey. Plant Physiol Biochem 73:139–143. https://doi.org/10.1016/j.plaphy.2013.09.007
Sharma A, Ng TB, Wong JH, Lin P (2009) Characterization of a lectin from Phaseolus vulgaris cv. (Anasazi Beans). J Biomed Biotechnol 2009:92–95. https://doi.org/10.1155/2009/929568
Silva KLS, Cechinel-Filho VC (2002) Plantas do gênero Bauhinia: composição química e potencial farmacológico. Quim Nova 25:449–454. https://doi.org/10.1590/S0100-0422002000300018
Silva FMB, Moreira RA, Horta ACG, Silva ALC (2005) The lectin content of cotiledonary callus from Canavalia brasiliensis (Mart. ex. Benth). Asian J Plant Sci 4:214–219. https://doi.org/10.3923/ajps.2005.214.219
Silva JA, Damico DCS, Baldasso PA, Mattioli MAP, Winck FV, Fraceto LF, Novello JC, Maragoni S (2007) Isolation and biochemical characterization of a galactoside binding lectin from Bauhinia variegata Candida (BvcL) seeds. Protein J 26:193–201. https://doi.org/10.1007/s10930-006-9061-0
Silva HC, Pereira-Júnior FN, Simões RC, Barroso Neto IL, Nobre CB, Pereira MG, Nascimento KS, Rocha BS, Delatorre P, Nagano SC, Assreuyh AM, Cavada BS (2011) Purification and partial characterization of a new proinflammatory lectin from Bauhinia bauhinioides Mart. (Caesalpinoideae) seeds. Protein Pept Lett 18:396–402. https://doi.org/10.2174/092986611794653987
Silva HC, Pinto LS, Teixeira EH, Nascimento KS, Cavada BS, Silva ALC (2014) BUL: a novel lectin from Bauhinia ungulata L. seeds with fungistatic and antiproliferative activities. Process Biochem 49:203–209. https://doi.org/10.1016/j.procbio.2013.10.020 2014.
Sircar PK, Dagupta B, Gosh BN (1985) Lectin concanavalin a distribution at different stages in the tissues of Canavalia gladiata. Curr Sci 54:80–82
Sivakamavalli J, Vaseeharan B (2014) Purification, characterization and functional role of lectin from green tiger shrimp Penaeus semisulcatus. Int J Biol Macromol 67:64–70. https://doi.org/10.1016/j.ijbiomac.2014.03.008
Smith RH (2012) Plant tissue culture: techniques and experiments. Academic Press, San Diego
Szopa A, Ekiert H, Muszyn´ska B (2013) Accumulation of hydroxybenzoic acids and other biologically active phenolic acids in shoot and callus cultures of Aronia melanocarpa (Michx.) Elliott (black chokeberry). Plant Cell Tissue Organ Cult 113:323–329. https://doi.org/10.1007/s11240-012-0272-0
Van Damme EJM, Peumans WJ, Barre A, Rougé P (1998) Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Plant Sci 17:575–692. https://doi.org/10.1080/07352689891304276
Vaz AMSF (2013) Bauhinia in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB111840. Accessed 22 Nov 2013
Werner ET, Cuzzuol GRF, Pessotti CV, Lopes FP, Roger JA (2009) In vitro calogenesis control of pau-brasil. Rev Árvore 33:987–996. https://doi.org/10.1590/S0100-67622009000600001
Wong JH, Ng TB, Zhang KYB, Sze SCW, Wang HX (2010) Isolation of a mitogenic agglutinin with relatively high thermostability from seeds of the variegated shell ginger. Protein Pept Lett 17:38–43. https://doi.org/10.2174/092986610789909539
Wu J, Lin L (2002) Ultrasound-induced stress responses of Panax ginseng cells: enzymatic browning and phenolics productions. Biotechnol Prog 18:862–866. https://doi.org/10.1021/bp0255210
Acknowledgements
We thank Dr. Andreia Fonseca Silva for the botanical identification of this plant and Dávia Guimarães Pompeu and the staff member Donizetti Joel Vilas Boas for help in hemagglutination test and assistance in the field, respectively. The authors also wish to thank to Foundation for Research Support of Minas Gerais (FAPEMIG) (CRA APQ 01347-14) and National Council for Scientific and Technological Development (CNPq) (Process 444907/2014-9) for financial support.
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Communicated by Sergio J. Ochatt.
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Castro, A.H.F., da Silva Tavares, H., Pereira, S.R.F. et al. Production and characterization of lectin from Bauhinia holophylla (Fabaceae:Cercideae) calli. Plant Cell Tiss Organ Cult 134, 423–432 (2018). https://doi.org/10.1007/s11240-018-1432-7
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DOI: https://doi.org/10.1007/s11240-018-1432-7