Abstract
The root bark of Peritassa campestris (Cambess.) A.C. Sm. (Celastraceae) accumulates quinonemethide triterpenes (QMTs), an important class of bioactive compounds that shows potent antitumor activity. The production of these metabolites is difficult by both chemical synthesis, because of the complex molecular structure, and extraction from plant resources, because of the low yield. Thus, the aim of this work was to evaluate the influence of some important factors on the synthesis of QMTs to increase their production in adventitious roots grown in vitro. The effects of luminosity, mechanical damage to the tissue, source and concentration of carbon, auxins, macronutrient and micronutrient concentrations and the elicitation with its endophytic microorganism, Bacillus megaterium, isolated from roots grown in vitro were evaluated. Additionally, we compared the production of QMTs of roots in vitro with that of P. campestris roots bark in natura. Our results showed that all stimulating agents affected the biosynthesis of QMTs, with the exception of luminosity. The pattern of QMTs produced was different for the in vitro and in natura roots, including the accumulation of the majority QMTs: the in vitro roots accumulated maytenin (1) and 22β-hydroxy-maytenin (2), and the in natura roots showed the accumulation of maytenin (1), 22β-hydroxy-maytenin (2), 20α-hydroxy-maytenin (3), and maytenol (4). Therefore, we concluded that the biosynthesis of QMTs by P. campestris roots is affected by biotic and abiotic factors.
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Almeida MTR de, Ríos-Luci C, Padrón JM, Palermo JA (2010) Antiproliferative terpenoids and alkaloids from the roots of Maytenus vitis-idaea and Maytenus spinosa. Phytochemistry 71:1741–1748. doi:10.1016/j.phytochem.2010.06.023
Baenas N, García-Viguera C, Moreno D (2014) Elicitation: a tool for enriching the bioactive composition of foods. Molecules 19:13541–13563. doi:10.3390/molecules190913541
Barrow JR, Osuna-Avila P, Reyes-Vera I (2004) Fungal endophytes intrinsically associated with micropropagated plants regenerated from native Bouteloua eriopoda Torr. and Atriplex canescens (Pursh) Nutt. Vitr. Cell Dev Biol Plant 40:608–612. doi:10.1079/IVP2004584
Buffa Filho W, Corsino J, Bolzani V da S et al (2002) Quantitative determination of cytotoxic Friedo-nor -oleanane derivatives from five morphological types of Maytenus ilicifolia (celastraceae) by reverse-phase high-performance liquid chromatography. Phytochem Anal 13:75–78. doi:10.1002/pca.626
Carvalho PF, Silva DS, Bolzani V, Furlan M (2005) Antioxidant quinonemethide triterpenes from Salacia campestris. Chem Biodivers 2:367–372. doi:10.1002/cbdv.200590016
Cevatemre B, Botta B, Mori M et al (2016) The plant-derived triterpenoid tingenin B is a potent anticancer agent due to its cytotoxic activity on cancer stem cells of breast cancer in vitro. Chem Biol Interact 260:248–255. doi:10.1016/j.cbi.2016.10.001
Chaban C, Waller F, Furuya M, Nick P (2003) Auxin responsiveness of a novel cytochrome P450 in rice coleoptiles. Plant Physiol 133:2000–2009. doi:10.1104/pp.103.022202
Chmielowska J, Veloso J, Gutiérrez J et al (2010) Cross-protection of pepper plants stressed by copper against a vascular pathogen is accompanied by the induction of a defence response. Plant Sci 178:176–182. doi:10.1016/j.plantsci.2009.11.007
Coppede JS, Pina ES, Paz TA et al (2014) Cell cultures of Maytenus ilicifolia Mart. are richer sources of quinone-methide triterpenoids than plant roots in natura. Plant Cell Tissue Organ Cult 118:33–43. doi:10.1007/s11240-014-0459-7
Corsino J, Carvalho PRF de, Kato MJ et al (2000) Biosynthesis of friedelane and quinonemethide triterpenoids is compartmentalized in Maytenus aquifolium and Salacia campestris. Phytochemistry 55:741–748. doi:10.1016/S0031-9422(00)00285-5
Cruz CD (2013) GENES—a software package for analysis in experimental statistics and quantitative genetics. Acta Sci Agron 35:271–276. doi:10.4025/actasciagron.v35i3.21251
Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol 32:77–87. doi:10.1016/j.pbi.2016.06.019
Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102:180–196. doi:10.3732/ajb.1400285
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência e Agrotecnol 35:1039–1042. doi:10.1590/S1413-70542011000600001
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. doi:10.1016/0014-4827(68)90403-5
Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526. doi:10.1021/np058128n
Gunatilaka AAL (1996) Triterpenoid Quinonemethides and related compounds (Celastroloids). In: Herz W, Kirby GW, Moore RE et al (eds) Fortschritte der chemie organischer naturstoffe/progress in the chemistry of organic natural products. Springer, Vienna, pp 1–123
Hernandes C, Pereira A, Severino P (2017) Compounds from Celastraceae targeting cancer pathways and their potential application in head and neck squamous cell carcinoma: a review. Curr Genomics 18:60–74. doi:10.2174/1389202917666160803160934
Jeller AH, Silva DHS, Lião LM et al (2004) Antioxidant phenolic and quinonemethide triterpenes from Cheiloclinium cognatum. Phytochemistry 65:1977–1982. doi:10.1016/j.phytochem.2004.03.039
Kusari S, Pandey SP, Spiteller M (2013) Untapped mutualistic paradigms linking host plant and endophytic fungal production of similar bioactive secondary metabolites. Phytochemistry 91:81–87. doi:10.1016/j.phytochem.2012.07.021
Liao P, Hemmerlin A, Bach TJ, Chye M-L (2016) The potential of the mevalonate pathway for enhanced isoprenoid production. Biotechnol Adv 34:697–713. doi:10.1016/j.biotechadv.2016.03.005
Lião LM, Silva GA, Monteiro MR, Rgio Albuquerque S (2008) Trypanocidal activity of quinonemethide triterpenoids from Cheiloclinium cognatum (Hippocrateaceae). Z Naturforsch 63:207–210. doi:10.1515/znc-2008-3-408
Ling APK, Ong SL, Sobri H (2011) Strategies in enhancing secondary metabolites production in plant cell cultures. Med Aromat Plant Sci Biotechnol 5:94–101
Lipko A, Swiezewska E (2016) Isoprenoid generating systems in plants—a handy toolbox how to assess contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthetic process. Prog Lipid Res 63:70–92. doi:10.1016/j.plipres.2016.04.002
Lloyd G, McCown B (1980) Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Int Plant Propag Soc Proc 30:421–427
Mano H, Morisaki H (2008) Endophytic Bacteria in the Rice Plant. Microbes Environ 23:109–117. doi:10.1264/jsme2.23.109
Migas P, Luczkiewicz M, Cisowski W (2006) The influence of auxins on the biosynthesis of isoprene derivatives in callus cultures of Vaccinium corymbosum var. bluecrop. Z Naturforsch C 61:565–570. doi:10.1515/znc-2006-7-816
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. doi:10.1111/j.1399-3054.1962.tb08052.x
Ngassapa O, Soejarto DD, Pezzuto JM, Farnsworth NR (1994) Quinone-methide triterpenes and salaspermic acid from Kokoona ochracea. J Nat Prod 57:1–8. doi:10.1021/np50103a001
Nosov AM (2012) Application of cell technologies for production of plant-derived bioactive substances of plant origin. Appl Biochem Microbiol 48:609–624. doi:10.1134/S000368381107009X
Oramas-Royo SM, Chávez H, Martín-Rodríguez P et al (2010) Cytotoxic triterpenoids from Maytenus retusa. J Nat Prod 73:2029–2034. doi:10.1021/np100517u
Paz TA, dos Santos VAFFM, Inácio MC et al (2013) Production of the quinone-methide triterpene Maytenin by in vitro Adventitious Roots of Peritassa campestris (Cambess.) A.C. Sm. (Celastraceae) and rapid detection and identification by APCI-IT-MS/MS. Biomed Res Int 2013:1–7. doi:10.1155/2013/485837
Pina ES, Coppede JS, Contini SHT, et al (2016a) Improved production of quinone-methide triterpenoids by Cheiloclinium cognatum root cultures: possibilities for a non-destructive biotechnological process. Plant Cell, Tissue Organ Cult 128:705–714. doi:10.1007/s11240-016-1151-x
Pina ES, Silva DB, Teixeira SP et al (2016b) Mevalonate-derived quinonemethide triterpenoid from in vitro roots of Peritassa laevigata and their localization in root tissue by MALDI imaging. Sci Rep 6:22627. doi:10.1038/srep22627
Qin S, Xing K, Jiang J-H et al (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol 89:457–473. doi:10.1007/s00253-010-2923-6
Ramirez-Estrada K, Vidal-Limon H, Hidalgo D et al (2016) Elicitation, an effective strategy for the biotechnological production of bioactive high-added value compounds in plant cell factories. Molecules 21:182. doi:10.3390/molecules21020182
Rasool S, Mohamed R (2016) Plant cytochrome P450s: nomenclature and involvement in natural product biosynthesis. Protoplasma 253:1197–1209. doi:10.1007/s00709-015-0884-4
Rodrigues-Filho E, Barros FAP, Fernandes JB, Braz-Filho R (2002) Detection and identification of quinonemethide triterpenes in Peritassa campestris by mass spectrometry. Rapid Commun Mass Spectrom 16:627–633. doi:10.1002/rcm.615
Rodriguez-Concepcion M, Forés O, Martinez-García JF, et al (2004) Distinct light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell Online 16:144–156. doi:10.1105/tpc.016204
Rodríguez-Concepción M (2006) Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem Rev 5:1–15. doi:10.1007/s11101-005-3130-4
Rodríguez-Concepción M, Boronat A (2015) Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis. Curr Opin Plant Biol 25:17–22. doi:10.1016/j.pbi.2015.04.001
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. doi:10.1146/annurev.arplant.57.032905.105441
Ruan Y-L (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67. doi:10.1146/annurev-arplant-050213-040251
Salvador JAR, Santos RC, Figueiredo SAC, Jing Y (2014) Antitumor effects of celastrol and semi-synthetic derivatives. Mini Rev Org Chem 11:400–407. doi:10.2174/1570193X1103140915113701
Savitha BC, Thimmaraju R, Bhagyalakshmi N, Ravishankar GA (2006) Different biotic and abiotic elicitors influence betalain production in hairy root cultures of Beta vulgaris in shake-flask and bioreactor. Process Biochem 41:50–60. doi:10.1016/j.procbio.2005.03.071
Seo HR, Seo WD, Pyun B-J et al (2011) Radiosensitization by celastrol is mediated by modification of antioxidant thiol molecules. Chem Biol Interact 193:34–42. doi:10.1016/j.cbi.2011.04.009
Singh J, Sabir F, Sangwan RS et al (2015) Enhanced secondary metabolite production and pathway gene expression by leaf explants-induced direct root morphotypes are regulated by combination of growth regulators and culture conditions in Centella asiatica (L.) urban. Plant Growth Regul 75:55–66. doi:10.1007/s10725-014-9931-y
Smolenskaya IN, Reshetnyak OV, Smirnova YN et al (2007) Opposite effects of synthetic auxins, 2,4-dichlorophenoxyacetic acid and 1-naphthalene acetic acid on growth of true ginseng cell culture and synthesis of ginsenosides. Russ J Plant Physiol 54:215–223. doi:10.1134/S1021443707020094
Srivastava S, Sangwan RS, Tripathi S et al (2015) Light and auxin responsive cytochrome P450s from Withania somnifera Dunal: cloning, expression and molecular modelling of two pairs of homologue genes with differential regulation. Protoplasma 252:1421–1437. doi:10.1007/s00709-015-0766-9
Sung B, Park B, Yadav VR, Aggarwal BB (2010) Celastrol, a triterpene, enhances TRAIL-induced apoptosis through the down-regulation of cell survival proteins and up-regulation of death receptors. J Biol Chem 285:11498–11507. doi:10.1074/jbc.M109.090209
Wang H, Teriete P, Hu A et al (2015) Direct inhibition of c-Myc-Max heterodimers by celastrol and celastrol-inspired triterpenoids. Oncotarget 6:32380–32395. doi:10.18632/oncotarget.6116
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16 S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. doi:10.1128/jb.173.2.697-703.1991
Zhi-lin Y, Chuan-chao D, Lian-qing C (2007) Review: regulation and accumulation of secondary metabolites in plant-fungus symbiotic system. African J Biotechnol 6:1266–1271. doi:10.5897/AJB2007.000-2174
Acknowledgements
The authors thank the São Paulo Research Foundation (FAPESP) for the CIBFar-2013/07600-3 Grant and Dr. José Carlos Tavares Carvalho (Biological Sciences and Health Department, Federal University of Amapá, Brazil) for the electron microscopy analysis. M. C. Inácio thanks FAPESP for her fellowship (2014/19362-2). T. A. Paz thanks CAPES for the provision of a scholarship. A. M. S. Pereira and M. Furlan would also like to thank the National Council for Scientific and Technological Development (CNPq) for their research fellowships.
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MCI was responsible for the conception and design of all experiments, data analysis, and drafting and editing of the manuscript. TAP contributed with HPLC and MS analyses and revision of the manuscript. AMSP supervised the experiments and contributed to data interpretation and final revision of the manuscript. MF contributed to data interpretation, drafting and final revision of the manuscript and supervised all experiments.
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Communicated by Ali R. Alan.
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Inácio, M.C., Paz, T.A., Pereira, A.M.S. et al. Endophytic Bacillus megaterium and exogenous stimuli affect the quinonemethide triterpenes production in adventitious roots of Peritassa campestris (Celastraceae). Plant Cell Tiss Organ Cult 131, 15–26 (2017). https://doi.org/10.1007/s11240-017-1257-9
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DOI: https://doi.org/10.1007/s11240-017-1257-9