Enhanced production and identification of antioxidants in in vitro cultures of the cacti Mammillaria candida and Turbinicarpus laui
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Cacti are an important source of metabolites but present limitations for their commercial exploitation, like slow growth and a decrease of wild populations. An alternative to obtain their biocompounds without affecting the natural environment are the in vitro culture techniques. We established in vitro cultures from Mammillaria candida Scheidweiler and Turbinicarpus laui Glass and Foster and used different stresses to increase metabolites and antioxidant activity. The cultures were exposed to 1.25% polyethylene glycol to induce a moderate drought stress, 50 g L−1 sucrose to generate an osmotic stress, chitosan (1.25 to 5 mg mL−1) to simulate a biotic attack, or to UV light. Chitosan was the best elicitor improving 1.5 times the concentration of phenolics, 9 to 10 times the content of flavonoids and betalains, and 16% the antioxidant activity in M. candida suspensions. In T. laui suspensions, this elicitor duplicates the flavonoids content and antioxidant activity. The antioxidant levels in elicited suspensions increased 5 to 10 times in relation to plant tubercles. Eleven compounds were identified in M. candida suspensions being digalloyl rhamnoside and epicatequin gallate the most abundant; in the T. laui suspensions, 16 compounds were detected and the most abundant were 17-decarboxi neobetanin and derivatives of luteolin. Thus, cacti in vitro culture is an efficient system to obtain high level of metabolites of biological interest.
KeywordsAntioxidants Betalains Mammillaria candida Phenolics Turbinicarpus laui
We are grateful to CONACYT for the scholarship to ARM (no. 401860).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Antunes-Ricardo M, Moreno-García BE, Gutiérrez-Uribe JA, Aráiz-Hernández D, Alvarez MM, Serna-Saldivar SO (2014) Induction of apoptosis in colon cancer cells treated with isorhamnetin glycosides from Opuntia ficus-indica pads. Plant Foods Hum Nutr 69:331–336. https://doi.org/10.1007/s11130-014-0438-5 CrossRefGoogle Scholar
- Astello-García M, Cervantes I, Nair V, Santos-Díaz MS, Reyes-Agüero A, Guéraud F, Nègre-Salvayre A, Rossignol M, Cisneros-Zevallos L, Barba de la Rosa AP (2015) Chemical composition and phenolic compounds profile of cladodes from Opuntia spp. cultivars with different domestication gradient. J Food Compost Anal 43:119–130. https://doi.org/10.1016/j.jfca.2015.04.016 CrossRefGoogle Scholar
- Castellanos-Santiago E, Yahia EM (2008) Identification and quantification of betalains from the fruits of 10 mexican prickly pear cultivars by high-performance liquid chromatography and electrospray ionization mass spectrometry. J Agr Food Chem 56:5758–5764. https://doi.org/10.1021/jf800362t CrossRefGoogle Scholar
- Chappel J, Hahlbrock K (1984) Transcription of plant defence genes in response to UV light or fungal elicitor. Nature311:76–78. doi: https://doi.org/10.1038/311076a0
- Chiu FL, Lin JK (2005) HPLC analysis of naturally occurring methylated catechins, 3‘ ‘- and 4‘ ‘-methyl-epigallocatechin gallate, in various fresh tea leaves and commercial teas and their potent inhibitory effects on inducible nitric oxide synthase in macrophages. J Agr Food Chem 53:7035–7042. https://doi.org/10.1021/jf0507442 CrossRefGoogle Scholar
- Esmaeelpanah E, Razavi BM, Vahdati Hasani F, Hosseinzadeh H (2017) Evaluation of epigallocatechin gallate and epicatechin gallate effects on acrylamide-induced neurotoxicity in rats and cytotoxicity in PC 12 cells. Drug Chem Toxicol 26:1–8. https://doi.org/10.1080/01480545.2017.1381108 Google Scholar
- Federspiel M, Fischer R, Hennig M, Mair MJ, Oberhauser T, Rimmler G, Albiez T, Bruhin J, Estermann H, Gandert C, Göckel V, Götzö S, Hoffmann U, Huber G, Janatsch G, Lauper S, Röckel-Stäbler O, Trussardi R, Zwahlen A (1999) Industrial synthesis of the key precursor in the synthesis of the anti-influenza drug oseltamivir phosphate (ro 64-0796/002, gs-4104-02): ethyl (3R,4S,5S)-4,5-epoxy-3-(1-ethyl-propoxy)-cyclohex-1-ene-1-carboxylate. OPR&D 3:266–274. https://doi.org/10.1021/op9900176 Google Scholar
- Ferrari S (2010) Biological elicitors of plant secondary metabolites: mode of action and use in the production of nutraceuticals. In: Giardi MT, Rea G, Berra B (ed.) Bio-farms for nutraceuticals, Springer-Landes Bioscience, pp 152–166Google Scholar
- Ferri M, Tassoni A (2011) Chitosan as elicitor of health beneficial secondary metabolites in in vitro plant cell cultures. In: Mackay RG, Tait JM (eds) Handbook of chitosan research and applications. Nova Science Publishers Inc, New York, pp 389–414Google Scholar
- González-Cabrera LD (2014) Efecto de reguladores del crecimiento exógenos sobre el desarrollo y la producción de metabolitos secundarios en cultivos de raíces transformadas de cactáceas. Dissertation University of Aguascalientes, MéxicoGoogle Scholar
- Inostroza-Blancheteau C, Reyes-Díaz M, Arellano A, Latsague M, Acevedo P, Loyola R, Arce-Johnson P, Alberdi M (2014) Effects of UV-B radiation on anatomical characteristics, phenolic compounds and gene expression of the phenylpropanoid pathway in highbush blueberry leaves. Plant Physiol Biochem 85:85–95. https://doi.org/10.1016/j.plaphy.2014.10.015 CrossRefGoogle Scholar
- Khan MI, Harsha PS, Giridhar P, Ravishankar GA (2012) Pigment identification, nutritional composition, bioactivity, and in vitro cancer cell cytotoxicity of Rivina humilis L. berries, potential source of betalains. LWT-Food Sci Technol 47:315–323. https://doi.org/10.1016/j.lwt.2012.01.025 CrossRefGoogle Scholar
- Lutty JM (2001) The cacti of CITES Appendix I. CITES Management Authority of Switzerland, BernGoogle Scholar
- Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
- Robles-Martínez M, Barba-de la Rosa AP, Guéraud F, Negre-Salvayre A, Rossignol M, Santos-Díaz MS (2016) Establishment of callus and cell suspensions of wild and domesticated Opuntia species: study on their potential as a source of metabolite production. Plant Cell Tissue Organ Cult 124:181–189. https://doi.org/10.1007/s11240-015-0886-0 CrossRefGoogle Scholar
- Santos-Díaz MS, Pérez-Molphe-Balch E, Ramírez-Malagón R, Núñez-Palenius HG, Ochoa-Alejo N (2010) Mexican threatened cacti: current status and strategies for their conservation. In: Tepper GH (ed), Species diversity and extinction, Hauppauge, NY:Nova Science Publishers, pp 1–60Google Scholar
- Santos-Díaz MS, Velásquez-García Y, González-Chávez MM (2005) Pigment production by callus of Mammillaria candida Scheidweiler (Cactaceae). Agrociencia 39:619–626Google Scholar
- Sotomayor JM, Arredondo-Gómez A, Sánchez-Barra FR, Méndez-Martínez M (2004) The genus Turbinicarpus in San Luis Potosí. Venogno, Italy: Cactus & CoGoogle Scholar
- Waterhouse AL (2002) Determination of total phenolics. In: Current protocols in food analytical chemistry, New York: John Wiley & Sons, Inc, pp 1–8Google Scholar
- Zaragoza-Martínez F, Lucho-Constantino GG, Ponce-Noyola T, Esparza-García F, Poggi-Varaldo H, Cerda-García C, Trejo-Tapia G, Ramos-Valdivia A (2016) Jasmonic acid stimulates the oxidative responses and triterpene production in Jatropha curcas cell suspension cultures through mevalonate as biosynthetic precursor. Plant Cell Tiss Organ Cult 127:47–56. https://doi.org/10.1007/s11240-016-1028-z CrossRefGoogle Scholar
- Zhao XM, She XP, Yu W, Liang XM, Du YG (2007) Effects of oligochitosans on tobacco cells and role of endogenous nitric oxide burst in resistance of tobacco to tobacco mosaic virus. J Plant Pathol 89:55–65Google Scholar