The biosynthesis of pharmacologically active compounds in Calophyllum brasiliense seedlings is influenced by calcium and potassium under hydroponic conditions

Jorge Ivan Castillo-Arellano, Helia Reyna Osuna-Fernández, Marius Mumbru-Massip, Rocío Gómez-Cancino, Ricardo Reyes-Chilpa

Abstract


Background: The influence of soil nutrients on biosynthesis of secondary metabolites from tropical trees has been poorly investigated.

Questions: Does the deprival of Ca2+ and K+ influence the production of pharmacologically active compounds in the seedling of Calophyllum brasiliense?

Species study: Calophyllum brasiliense Cambess.

Study site: Los Tuxtlas, Veracruz, Mexico; November 2005 to November 2009.

Methods: The seedlings were obtained from seeds and subjected to different hydroponic treatments: 1) modified Hoagland solution (MHS), 2) MHS-Ca2+, and 3) MHS-K+. Growth, height, foliar biomass, and HPLC analysis were performed after 7 months.

Results: Under hydroponic conditions Ca2+ and K+ deficiency induced the mortality of 53 % and 28 % of the seedlings, respectively. The foliar biomass, and plant height of the survivors were also drastically reduced. MHS-K+ treatment induced a 15, 4.2 and 4.3-fold decrease for calanolides B, C, and apetalic acid in the leaves, respectively. MHS-Ca2+ treatment induced a decrease of 4.3, and 2.4-fold for calanolide B, and C, respectively.

Conclusion: Ca2+ is essential for survival of C. brasiliense seedlings under hydroponic conditions, Ca2+ and K+ are critical for growth, foliar production, and biosynthesis of apetalic acid, and calanolide B.


Keywords


Apetalic acid; calanolides; Calophyllum brasiliense; hydroponic; soil nutrients

Full Text:

PDF

References


Ahmad P, Abdel A, Abd_Allah E, Hashem A, Sarwat M, Anjun N, Gucel S. 2016. Calcium and Potassium Supplementation Enhanced Growth, Osmolyte Secondary Metabolite Production, and Enzymatic Antioxidant Machinery in Cadmium-Exposed Chickpea (Cicer arietinum L.). Frontiers in Plant Science 7. DOI: http://doi.org/10.3389/fpls.2016.00513

Ajithabai M, Rameshkumar B, Jayakumar G, Luxmi V, Mangalam S, Ajaikumar, Gayathri P. 2012. Decipic acid and 12-acetyl apetalic acid from Calophyllum decipiens. Indian Journal Chemistry 51: 393-397

Alaoui C, Kasrati A, Bekkouche K, Hassani L, Wohlmuth H, Leach D, Abbad A. 2014. Cultivation and the application of inorganic fertilizer modifies essential oil composition in two Moroccan species of Thymus. Industrial Crops and Products 62: 113-118. DOI: http://doi.org/10.1016/j.indcrop.2014.08.017

Bernabé-Antonio A, Estrada-Zúñiga M, Buendía-González L, Reyes-Chilpa R, Chávez-Avila V, Cruz-Sosa F. 2010. Production of anti-HIV-1 calanolides in a callus culture of Calophyllum brasiliense (Cambes). Plant Cell Tissue Organ Culture 103: 33-40. DOI: http://doi.org/10.1007/s11240-010-9750-4

Boeger M, Wisniewski C. 2003. Comparação da morfologia foliar de espécies arbóreas de três estádios sucessionais distintos de floresta ombrófila densa (Floresta Atlântica) no Sul do Brasil. Brazilian Journal of Botany 26: 61-72. DOI: http://doi.org/10.1590/S0100-84042003000100007

Borges C, Minatel I, Gomez-Gomez H, Pereira L. 2017. Medicinal plants: Influence of environmental factors on the content of secondary metabolites. Medicinal Plants and Environmental Challenges. DOI: http://doi.org/10.1007/978-3-319-68717-9_15

Burney O, Jacobs D. 2011. Ungulate herbivory of regenerating conifers in relation to foliar nutrition and terpenoid production. Forest Ecology Management 262: 1834-1845. DOI: http://doi.org/10.1016/j.foreco.2011.07.035

Butler M. 2008. Natural products to drugs: natural product-derived compounds in clinical trials. Natural Products Reports 25: 475. DOI: http://doi.org/10.1039/b514294f

Caretto S, Linsalata V, Colella G, Mita G, Lattanzio V. 2015. Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress. International Journal of Molecular Sciences 16: 26378-26394 DOI: http://doi.org/10.3390/ijms161125967

Churngchow N, Rattarasarn M. 2001. Biosynthesis of scopoletin in Hevea brasiliensis leaves inoculated with Phytophthora palmivora. Journal of Plant Physiology 158: 875-882. DOI: http://doi.org/10.1078/0176-1617-00230

Cornelissen T, Stiling P. 2006. Responses of different herbivore guilds to nutrient addition and natural enemy exclusion. Ecoscience 13: 66-74. DOI: http://doi.org/10.2980/1195-6860(2006)13[66:RODHGT]2.0.CO;2

Davies MJ, Atkinson CJ, Burns C, Woolley JG, Hips NA, Arroo RRJ, Dungey N, Robinson T, Brown P, Flockart I, Hill C, Smith L, Bentley S. 2009. Enhancement of artemisinin concentration and yield in response to optimization of nitrogen and potassium supply to Artemisia annua. Annals of Botany 104: 315-323. DOI: http://doi.org/10.1093/aob/mcp126

De Carvalho L, Amaral A, Davide A . 2006. Classificação de sementes florestais quanto ao comportamento no armazenamento. Revista Brasileira de Sementes 28: 15-25 DOI: http://doi.org/10.1590/S0101-31222006000200003

Desjardins A. 2008. Natural product chemistry meets genetics: When is a genotype a chemotype? Journal of Agricultural and Food Chemistry 56: 7587-7592 DOI: http://doi.org/10.1021/jf801239j

El Gendy A, El Gohary A, Omer E, Hendawy S, Hussein M, Petrova V, Stanchev I. 2015. Effect of nitrogen and potassium fertilizer on herbage and oil yield of chervil plant (Anthriscus cerefolium L.). Industrial Crops and Products 69: 167-174. DOI: 10.1016/j.indcrop.2015.02.023

Elwers S, Zambrano A, Rohsius C, Lieberei R. 2009. Differences between the content of phenolic compounds in Criollo, Forastero and Trinitario cocoa seed (Theobroma cacao L.). European Food Research and Technology 229: 937-948. DOI: http://doi.org/10.1007/s00217-009-1132-y

Fernández-Hinojosa G, Johnson-Barria M .1986. Fisiología vegetal experimental. San José, Costa Rica: Instituto Interamericano de Cooperación para la agricultura. ISBN: 9789290390664

Fischer E, Dos Santos F. 2001. Demography, phenology and sex of Calophyllum brasiliense (Clusiaceae) trees in the Atlantic forst. Journal of Tropical Ecology 17: 903-909. DOI: http://doi.org/10.1017/S0266467401001675

Forkner R, Hunter M. 2000. What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology 81: 1588-1600. DOI: http://doi.org/10.1890/0012-9658(2000)081[1588:WGUMCD]2.0.CO;2

García-Zebadúa J, Reyes-Chilpa R, Huerta-Reyes M, Castillo-Arellano J, Santillán-Hernández S, Vázquez-Astudillo B, Mendoza-Espinoza J. 2014. Vitae 21:126-145

Glynn C, Herms D, Orians C, Hansen R, Larsson S. 2007. Testing the growth-differentiation balance hypothesis: Dynamic responses of willows to nutrient availability. New Phytologist 176: 623-634. DOI: http://doi.org/10.1111/j.1469-8137.2007.02203.x

Guevara S, Laborde D, Sánchez-Ríos G. 2006. Los Tuxtlas: El paisaje de la sierra. México: Instituto de Ecología. ISBN: 970-709-043-X, 9789707090439

Hua J, Moon T, Hong T, Park K, Son J, Chang H. 2008. 5-Methoxy-8-(2-hydroxy-3-buthoxy-3-methylbutyloxy)-psoralen isolated from Angelica dahurica inhibits cyclooxygenase-2 and 5-lipoxygenase in mouse bone marrow-derived mast cells. Archives of Pharmacal Research 31: 617-621. DOI: http://doi.org/10.1007/s12272-001-1202-9

Huber M, Epping J, Schulze G, Fricke J. Aziz Z, Brillatz T, Swyers M, Köllner T, Vogel H, Hammerbacher A, Triebwasser-Freese D, Robert C, Verhoeven K, Preite V, Gershenzon J, Erb M. 2016. A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack. PLOS Biology 14. DOI: http://doi.org/10.1371/journal.pbio.1002332

Huerta-Reyes M, Basualdo M, Abe F, Jimenez-Estrada M, Soler C, Reyes-Chilpa R. 2004. HIV-1 inhibitory compounds from Calophyllum brasiliense leaves. Biological and Pharmaceutical Bulletin 27: 1471-1475. DOI: http://doi.org/10.1248/bpb.27.1471

INEGI. 2009. [Instituto Nacional de Geografía Estadística] México. (accessed 20 September, 2002)

Kashman Y, Gustafson K, Fuller R, Cardellina II J, McMahon J, Currens M, Buckheit Jr R, Hughues S, Cragg G, Boyd R. 1992. HIV inhibitory natural products. Part 7. The calanolides, a novel HIV-inhibitory class of coumarin derivatives from the tropical rainforest tree, Calophyllum lanigerum. Journal of Medicinal Chemistry 35: 2735-2743. DOI: http://doi.org/10.1021/jm00093a004

Kováčik J, Klejdus B. 2014. Induction of phenolic metabolites and physiological changes in chamomile plants in relation to nitrogen nutrition. Food Chemistry 142: 334-341. DOI: http://doi.org/10.1016/j.foodchem.2013.07.074

Kováčik J, Klejdus B, Babula P, Jarošová M. 2014. Variation of antioxidants and secondary metabolites in nitrogen-deficient barley plants. Journal of Plant Physiology 171: 260-268. DOI: http://doi.org/10.1016/j.jplph.2013.08.004

Lattanzio V, Cardinali A, Ruta C, Morone F, Lattanzio V, Linsalata V, Cicco N. 2009. Relationship of secondary metabolism to growth in oregano (Origanum vulgare L.) shoot cultures under nutritional stress. Environmental and Experimental Botany 65: 54-62. DOI: http://doi.org/10.1016/j.envexpbot.2008.09.002

Lauchert U, Wild A. 1995. Studies on the Correlation of Putrescine and Potassium Contents in the Needles of Spruce Trees. Journal of Plant Physiology 147: 267-269. DOI: http://doi.org/10.1016/S0176-1617(11)81516-6

Laure F, Raharivelomanana P, Butaud J, Bianchini J, Gaydou E. 2008. Screening of anti-HIV-1 inophyllums by HPLC-DAD of Calophyllum inophyllum leaf extracts from French Polynesia Islands. Analytica Chimica Acta 624:147-153. DOI: http://doi.org/10.1016/j.aca.2008.06.046

Lim T, Lim Y, Yule C. 2017. Distribution and caracterisation of phenolic compounds in Macaranga pruinosa and associated soils in a tropical peat swamp forest. Journal of Tropical Forest Science 29:509-518. DOI: http://doi.org/10.26525/jtfs2017.29.4.509518

Liu W, Zhu D, Liu DW, Liu DH, Geng M, Zhou W, Mi W, Yang T, Hamilton D. 2010. Influence of nitrogen on the primary and secondary metabolism and synthesis of flavonoids in Chrysanthemum morifolium Ramat. Journal of Plant Nutrition 33: 240-254. DOI: http://doi.org/10.1080/01904160903434287

Martinez-Sanchez J. 2006. Pasture trees in tropical Mexico: the effect of soil nutrients on seedling growth. Revista de Biología Tropical 54: 363-370

Marx E, Hart J. 1996. Soil test interpretation guide. No. 1478. Oregon: Oregon State University Extension Service. https://ir.library.oregonstate.edu/downloads/00000020g (Acceced 12-29-2018)

McKee T, Covington C, Fuller R, Bokesch H, Young S, Cardellina J, Kadushin M, Soejarto D, Stevens P, Cragg G, Boyd M. 1998. Pyranocoumarins from tropical species of the genus Calophyllum: A chemotaxonomic study of extracts in the National Cancer Institute Collection. Journal of Natural Products 61: 1252-1256. DOI: http://doi.org/10.1021/np980140a

Mendonça-Freitas M, Monnerat P, Curcino-Vieira J. 2008. Mineral deficiency in Passiflora alata curtis: Vitexin bioproduction. Journal of Plant Nutrition 31: 1844-1854. DOI: http://doi.org/10.1080/01904160802325552

Milošević T, Milošević N, Glišić I, Bošković-Rakocević L, Milivojević J. 2013. Fertilization effect on trees and fruits characteristics and leaf nutrient status of apricots which are grown at Cacak region (Serbia). Scientia Horticulturae (Amsterdam) 164: 112-123. DOI: http://doi.org/10.1016/j.scienta.2013.09.028

Muzika R, Pregitzer K, Hanover J. 1989. Changes in terpene production following nitrogen fertilization of grand fir (Abies grandis (Dougl.) Lindl.) seedlings. Oecologia 80: 485-489. DOI: http://doi.org/10.1007/BF00380070

Nerg A, Kainulainen P, Vuorinen M, Hanso M, Holopainen J, Turkela T. 1994. Seasonal and geographical variation of terpenes, resin acids and total phenolics in nursery grown seedlings of Scots pine (Pinus sylvestris L.). New Phytologist 128:703-713. DOI: http://doi.org/10.1111/j.1469-8137.1994.tb04034.x

Pal P, Kumar R, Guleria V, Mahajan M, Prasad R, Pathania V, Gill B, Singh D, Chand G, Singh B, Singh R and Singh P. 2015. Crop-ecology and nutritional variability influence growth and secondary metabolites of Stevia rebaudiana Bertoni. BMC Plant Biology 15. DOI: http://doi.org/10.1186/s12870-015-0457-x

Pavarini DP, Pavarini SP, Niehues M, Lopes NP. 2012. Exogenous influences on plant secondary metabolite levels. Animal Feed Science and Technology 176: 5-16. DOI: http://doi.org/10.1016/j.anifeedsci.2012.07.002

Akula R, Ravishankar G. 2011. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signaling & Behavior 6: 1720-1731 DOI: http://doi.org/10.4161/psb.6.11.17613

Resende A, Furtini-Neto A, Curi N, Muniz J, Faria M. 2000. Accumulation and nutritional efficiency of macronutrients in forest species of different successional groups in response to phosphorus fertilizer application. Ciência e Agrotecnologia 24: 160-173

Reyes-Chilpa R, Estrada-Muñiz E, Ramírez-Apan T, Amekraz B, Aumelas A, Jankowski C, Vázquez-Torres M. 2004. Cytotoxic effects of mammea type coumarins from Calophyllum brasiliense. Life Sciences 75:1635-1647. DOI: http://doi.org/10.1016/j.lfs.2004.03.017

Reyes-Chilpa R, Estrada-Muñiz E, Vega-Ávila E, Abe F, Kinjo J, Hernández-Ortega S. 2008. Trypanocidal constituents in plants. 7. Mammea-type coumarins. Memórias do Instituto Oswaldo Cruz 103: 431-436. DOI: http://doi.org/10.1590/S0074-02762008000500004

Sampaio B, Edrada-Ebel R, Da Costa F. 2016. Effect of the environment on the secondary metabolic profile of Tithonia diversifolia: A model for environmental metabolomics of plants. Scientific Reports 6: 29265 DOI: http://doi.org/10.1038/srep29265

Sánchez-Sampedro M, Fernández-Tárrago J, Corchete P. 2005. Enhanced Silymarin accumulation is related to calcium deprivation in cell suspension cultures of Silybum marianum (L.) Gaertn. Journal of Plant Physiology 162: 1177-1182. DOI: http://doi.org/10.1016/j.jplph.2005.01.012

Shaw T, Moore J, Marshall J. 1998. Root chemistry of Douglas-fir seedlings grown under different nitrogen and potassium regimes. Canadian Journal of Forest Research 28: 1566-1573. DOI: http://doi.org/10.1139/cjfr-28-10-1566

Shen Y, Wang L, Khalil A, Kuo Y. 2004. Chromanones and dihydrocoumarins from Calophyllum blancoi. Chemical and Pharmaceutical Bulletin (Tokyo) 52: 402-405. DOI: http://doi.org/10.1248/cpb.52.402

Silveira S, Cordeiro-Silva R, Degenhardt-Goldbach J, Quoirin M. 2016. Micropropagation of Calophyllum brasiliense (Cambess.) from nodal segment. Brazilian Journal of Biology 76: 656-663. DOI: http://doi.org/10.1590/1519-6984.23714

Taiz L, Zeiger E . 2010. Plant Physiology. Sinauer Associates Inc. ISBN: 978-0-87893-866-7.

Verma N, Shukla S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. Journal of Applied Research on Medicinal and Aromatic Plants 2: 105-113: http://doi.org/10.1016/j.jarmap.2015.09.002

Vozzo J. 2002. Tropical Tree Seed Manual. Native Plants (Vol. 5). DOI: http://doi.org/10.1353/npj.2004.0004

Zangerl A, Berenbaum M .1987. Furanocoumarins in wild parsnip: effects of photosynthetically active radiation, ultraviolet light, and nutrients. Ecology 68: 516-520. DOI: http://doi.org/10.2307/1938456

Zavaleta-Mancera H. 2011. Leaf structure of two chemotypes of Calophyllum brasiliense from Mexico. Microscopy and Microanalysis 17: 340-341 DOI: http://doi.org/10.1017/S1431927611002571




DOI: http://dx.doi.org/10.17129/botsci.2018

Article Metrics

Abstract Views.
Total number of Abstract Views for this article.
a description of the source 112
This journal








Metrics Loading ...

Metrics powered by PLOS ALM

Refbacks

  • There are currently no refbacks.


 

Botanical Sciences is an international peer-reviewed journal that publishes scientific papers in plant sciences. The arguments, figures / schemes / photographs, quality and the general contents of this publication are full responsibility of the authors, and not commit the Editor- in-Chief or the Sociedad Botánica de México.

Botanical Sciences year 8, Vol. 97, No. 1, January-March 2019. Quarterly publication edited and published by Sociedad Botánica de México A.C. (www.socbot.mx). Editor in Chief Salvador Arias, Jardín Botánico, Instituto de Biología, 3er Circuito s/n, Ciudad Universitaria, Delegación Coyoacán, C.P. 04510. Reserves of Rights to the Exclusive Use No. 04-2017-040716054100-203, digital-ISSN 2007-4476, both granted by the Instituto Nacional del Derecho de Autor. Responsible for updating the page Pedro López, email: plopez@escire.mx, eScire. Last update March 11, 2019.

Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

 

 

website counter