Influence of the flowering stage in the production of urechitol A in Agrobacterium rhizogenes-transformed plants of Pentalinon andrieuxii

  • Marlene Pires-Moreira Unidad de Biotecnología, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán https://orcid.org/0000-0001-8754-2918
  • Samuel Chan-Poot Unidad de Bioquímica y Biología Molecular de Plantas, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán
  • Elidé Avilés-Berzunza Unidad de Bioquímica y Biología Molecular de Plantas, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán https://orcid.org/0009-0009-5050-5326
  • Karlina Garcia-Sosa Unidad de Biotecnología, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán
  • Gregorio Godoy-Hernández Unidad de Bioquímica y Biología Molecular de Plantas, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán https://orcid.org/0000-0003-0225-3709
  • Luis Manuel Peña-Rodríguez Unidad de Biotecnología, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán https://orcid.org/0000-0001-6511-5122
keywords: ontogeny, root metabolites, secondary metabolism, terpenoid production

Abstract

Background: Pentalinon andrieuxii, is a medicinal plant used in Mayan folk medicine against leishmaniosis. It is an important source of terpenoids whose biosynthesis has been reported to be influenced by the ontogeny of the plant.

Hypotheses: Flowering positively influences the production of urechitol A in Pentalinon andrieuxii.

Studied species: Pentalinon andrieuxii (Müll. Arg.) B.F. Hansen & Wunderlin (Apocynaceae)

Study site and dates: Mérida, Yucatán, Mexico, 2019 and 2020.

Methods: Flowering was induced by exposing plants to temperatures above 32 °C. Plant tissue samples were collected before flowering induction and at full bloom and extracted with methanol. Analyses of the dichloromethane-soluble fraction of the crude extract by Gas Chromatography-Mass Spectrometry allowed the detection and quantification of urechitol A.

Results: Flowering stage of P. andrieuxii has a positive influence on the production of urechitol A in the root of the plant, with the contents of the tri-nor-sesquiterpene increasing from a minimum of 43 to a maximum of 91 times during the flowering stage of plants, both transformed and wild type.

Conclusions: P. andrieuxii perceives high temperatures as an important environmental cue to flower; flowering positively influences the production of urechitol A in the roots of the plant; production of the tri-nor-sesquiterpene is controlled by the plant.

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Author Biography

Luis Manuel Peña-Rodríguez, Unidad de Biotecnología, Centro de Investigación Científica de Yucatán, A.C., Mérida, Yucatán

Investigador Titular D
Unidad Académica: Biotecnología
SNI: Nivel II (2011-2015)

Educación

  • Doctorado, Doctor en Química. Universidad de Alberta-Canada. 1985
  • Postdoctorado, Profesor Visitante. Universidad Estatal de Carolina del Norte-EUA. 1988
  • Postdoctorado, Profesor Visitante. Universidad de New Brunswick-Canada. 1993
  • Estancia Sabática. Universidad Nacional Autónoma de México. 2000
  • Estancia Sabática. Universidad Técnica de Munich-Alemania. 2011

Línea Actual de Investigación

  • Química de Productos Naturales: Fitoquímica (detección, aislamiento e identificación de metabolitos bioactivos producidos por plantas medicinales); Ecología Química (estudio del papel de los metabolitos secundarios en interacciones planta-patógeno y planta-insecto; Metabolómica y Biosíntesis.

 

Influence of the flowering stage in the production of urechitol A in <em>Agrobacterium rhizogenes</em>-transformed plants of <em>Pentalinon andrieuxii</em>

References

Amasino R. 2010. Seasonal and developmental timing of flowering. Plant Journal. 61: 1001-1013. DOI: https://doi.org/10.1111/j.1365-313X.2010.04148.x
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. 2006. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLos Genetics. 2:106. DOI: https://doi.org/10.1371/journal.pgen.0020106
Banerjee S, Nau S, Hochwald SN, Xie H, Zhang J. 2022. Anticancer properties and mechanisms of botanical derivatives. Phytomedicine. 3: 10039. DOI: https://doi.org/10.1016/j.phyplu.2022.100396
Bogdanović MD, Todorović SI, Banjanac T, Dragićević MB, Verstappen FW, Bouwmeester HJ, Simonović AD. 2014. Production of guaianolides in Agrobacterium rhizogenes-transformed chicory regenerants flowering in vitro. Indutrial Crops and Products. 60: 52-59. DOI: https://doi.org/10.1016/j.indcrop.2014.05.054
Broun P, Liu Y, Queen E, Schwarz Y, Abenes ML, Leibman M. 2006. Importance of transcription factors in the regulation of plant secondary metabolism and their relevance to the control of terpenoid accumulation. Phytochemical Reviews. 5: 27-38. DOI:10.1007/s11101-006-9000-x
Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J. 2003. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry. 62: 471-481. DOI: https://doi.org/10.1016/S0031-9422(02)00549-6
Büntgen U, Piermattei A, Krusic PJ, Esper J, Sparks T, Crivellaro A. 2022. Plants in the UK flower a month earlier under recent warming. Proceedings of the Royal Society B. 289:20212456.
Cantrell CL, Dayan FE, Duke SO. 2012. Natural products as sources for new pesticides. Journal of Natural Products. 75: 1231-1242. DOI: https://doi.org/10.1021/np300024u
Capovilla G, Schmid M, Posé D. 2015. Control of flowering by ambient temperature. Journal of Experimental Botany. 66: 59-69. DOI: https://doi.org/10.1093/jxb/eru416
Cichewicz RH, Kouzi SA. 2004. Chemistry, biological activity, and chemotherapeutic potential of betulinic acid for the prevention and treatment of cancer and HIV infection. Medicinal Research Review. 24: 90-114. DOI: https://doi.org/10.1002/med.10053
Chan-Bacab MJ, Balanza E, Deharo E, Muñoz V, Garcı́a RD, Peña-Rodrı́guez LM. 2003. Variation of leishmanicidal activity in four populations of Urechites andrieuxii. Journal of Ethnopharmacology. 86: 243-247. DOI: https://doi.org/10.1016/S0378-8741(03)00011-4
Cho LH, Yoon J, An G. 2017. The control of flowering time by environmental factors. Plant. J. 90: 708-719. DOI: https://doi.org/10.1111/tpj.13461
Ferreira JF, Simon JE, Janick J. 1995. Developmental studies of Artemisia annua: flowering and artemisinin production under greenhouse and field conditions. Planta Medica. 61: 167-170. DOI: 10.1055/s-2006-958040
Gobbo-Neto L, Lopes NP. 2007. Medicinal plants: factors of influence on the content of secondary metabolites. Química Nova. 30: 374-381. DOI: https://doi.org/10.1590/S0100-40422007000200026
Guitton Y, Nicolè F, Moja S, Benabdelkader T, Valot N, Legrand S, Legendre L. 2010. Lavender inflorescence: a model to study regulation of terpenes synthesis. Plant Signalling & Behavior. 5: 749-751. DOI: https://doi.org/10.4161/psb.5.6.11704
Gupta G, Peine KJ, Abdelhamid D, Snider H, Shelton AB, Rao L. Satoskar, AR. 2015. A novel sterol isolated from a plant used by Mayan traditional healers is effective in treatment of visceral leishmaniasis caused by Leishmania donovani. ACS infectious diseases. 1: 497-506. DOI:https://doi.org/10.1021/acsinfecdis.5b00081
Hashimoto T, Hayashi A, Amano Y, Kohno J, Iwanari H, Usuda S, Yamada Y. 1991. Hyoscyamine 6β-hydroxylase, an enzyme involved in tropane alkaloid biosynthesis, is localized at the pericycle of the root. J. Biol. Chem. 266: 4648-4653. DOI: https://doi.org/10.1016/S0021-9258(20)64371-X
Hiebert-Giesbrecht M.R, Avilés-Berzunza E, Godoy-Hernández G, Peña-Rodríguez L.M. 2020. Genetic transformation of the tropical vine Pentalinon andrieuxii (Apocynaceae) via Agrobacterium rhizogenes produces plants with an increased capacity of terpenoid production. In Vitro Cell & Developmental Biology- Plant. 57: 21-29. DOI: 10.1007/s11627-020-10101-z
Hiebert‐Giesbrecht MR., Escalante‐Erosa F, García‐Sosa K, Dzib GR, Calvo‐Irabien LM, Peña‐Rodríguez LM. 2016. Spatio‐Temporal Variation of Terpenoids in Wild Plants of Pentalinon andrieuxii. Chemical Biodiversity. 13: 1521-1526. DOI: 10.1002/cbdv.201600085
Huang W, Gfeller V, Erb M. 2019. Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant-herbivore interactions of neighboring plants. Plant Cell Environment. 42: 1964-1973. DOI: 10.1111/pce.13534
Isah T. 2019. Stress and defense responses in plant secondary metabolites production. Biological Research. 52: 39. DOI: 10.1186/s40659-019-0246-3
Jagadish SK, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PV, Craufurd PQ. 2016. Implications of high temperature and elevated CO2 on flowering time in plants. Frontiers in Plant Science. 7:913. DOI: https://doi.org/10.3389/fpls.2016.0091
Jochum GM, Mudge KW, Thomas RB. 2007. Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herb Panax quinquefolius (Araliaceae). American Journal of Botany. 94: 819-826. DOI: 10.3732/ajb.94.5.819
Laitinen J, Julkunen-Tiitto R, Rousi M, Heinonen J, Tahvanainen J. 2005. Ontogeny and environment as determinants of the secondary chemistry of three species of white birch. Journal of Chemical Ecology. 31: 2243-2262. DOI: 10.1007/s10886-005-7100-5
Lee J, Hyun CG. 2023. Natural Products for Cosmetic Applications. Molecules. 28: 534. DOI: 10.3390/molecules28020534
Lezama‐Dávila CM, Pan L, Isaac‐Márquez AP, Terrazas C, Oghumu S, Isaac‐Márquez R, Pech-Dizib MY, Barbi J, Calomeni E, Parinandi N, Kinghorn AD, Satoskar AR. 2014. Pentalinon andrieuxii root extract is effective in the topical treatment of cutaneous leishmaniasis caused by Leishmania mexicana. Phytotherapy Research. 28: 909-916. DOI: 10.1002/ptr.5079
Li J, Goto M, Yang X, Morris-Natschke SL, Huang L, Chen CH, Lee KH. 2016. Fluorinated betulinic acid derivatives and evaluation of their anti-HIV activity. Bioorganic & Medicinal Chemistry Letters. 26: 68-71. DOI: 10.1016/j.bmcl.2015.11.029
Li Y, Kong D, Fu Y, Sussman MR, Wu H. 2020. The effect of developmental and environmental factors on secondary metabolites in medicinal plants. Plant Physiology and Biochemistry. 148: 80-89. DOI: 10.1016/j.plaphy.2020.01.006
Mannan A, Ahmed I, Arshad W, Hussain I, Mirza B. 2011. Effects of vegetative and flowering stages on the biosynthesis of artemisinin in Artemisia species. Archives of Pharmacal Research. 34: 1657- 61. DOI:10.1007/s12272-011-1010-6
McClung CR, Lou P, Hermand V, Kim JA. 2016. The importance of ambient temperature to growth and the induction of flowering. Frontiers in Plant Science. 7: 1266. DOI: 10.3389/fpls.2016.01266
Meira CS, Barbosa-Filho JM, Lanfredi-Rangel A, Guimarães ET, Moreira DR, Soares M.B. 2016. Antiparasitic evaluation of betulinic acid derivatives reveals effective and selective anti-Trypanosoma cruzi inhibitors. Experimental Parasitol. 166:108-15. DOI: 10.1016/j.exppara.2016.04.007
Morales JF. 2009. Estudios en las Apocinaceae neotropicales XXXIX: revisión de las Apocynoideae y Rauvolfioideae de Honduras. Anales del Jardín Botánico de Madrid. 66: 217- 262. DOI: 10.3989/ajbm.2205
Pan L, Lezama-Dávila CM, Isaac-Marquez A, Calomeni E, Fuchs J, Satoskar A, Kinghorn A. 2012. Sterols with antileishmanial activity isolated from the roots of Pentalinon andrieuxii. Phytochemistry. 82: 128-135. DOI: 10.1016/j.phytochem.2012.06.012
Pasquali G, Porto DD, Fett-Neto AG. 2006. Metabolic engineering of cell cultures versus whole plant complexity in production of bioactive monoterpene indole alkaloids: recent progress related to old dilemma. Journal of Bioscience and Bioengineering. 101: 287- 96. DOI: 10.1263/jbb.101.287
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://dx.doi.org/10.1016/j.anifeedsci.2012.07.002
Terletskaya NV, Korbozova NK, Grazhdannikov AE, Seitimova GA, Meduntseva ND, Kudrina NO. 2022. Accumulation of Secondary Metabolites of Rhodiola semenovii Boriss. In Situ in the Dynamics of Growth and Development. Metabolites. 6: 622. DOI: 10.3390/metabo12070622
Towler MJ, Weathers PJ. 2015. Variations in key artemisinic and other metabolites throughout plant development in Artemisia annua L. for potential therapeutic use. Industrial Crops and Products. 67:185-191. DOI: 10.1016/j.indcrop.2015.01.007
Tremlová B, Mikulášková HK, Hajduchová K, Jancikova S, Kaczorová D, Zeljković S, Dordevic D. 2021. Influence of technological maturity on the secondary metabolites of hemp concentrate (Cannabis sativa L.). Foods. 10: 1418. DOI: 10.3390/foods10061418
Yam-Puc A, Escalante-Erosa F, Pech-Lopez M, Chan-Bacab MJ, Arunachalampillai A, Wendt OF, Sterner O, Peña-Rodríguez LM. 2009. Trinorsesquiterpenoids from the root extract of Pentalinon andrieuxii. Journal of Natural Products. 72: 745 -748. DOI: 10.1021/np800554n
Yam-Puc A, Chee-González L, Escalante-Erosa F, Arunachalampillai A, Wendt O, Sterner O, Godoy-Hernández G, Peña-Rodríguez LM. 2012. Steroids from the root extract of Pentalinon andrieuxii. Phytochemical Letters. 5: 45-48. DOI: https://doi.org/10.1016/j.phytol.2011.09.004
Yang L, Wen KS, Ruan X, Zhao YX, Wei F, Wang Q. 2018. Response of plant secondary metabolites to environmental factors. Molecules. 23: 762. DOI:10.3390/molecules23040762
Wigge PA. 2013. Ambient temperature signaling in plants. Current Opinion in Plants Biology. 16: 661-666. DOI: 10.1016/j.pbi.2013.08.004
Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, Tantillo, DJ, Coates RM, O´Donnel C, Tokuhisa JG, Tholl D. 2013. Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell. 25: 1108-25. DOI: 10.1105/tpc.112.100057
Varikuti S, Shelton AB, Kotha SR, Gurney T, Gupta G, Hund TJ, Parinandi NL. 2022. Pentalinonsterol, a phytosterol from Pentalinon andrieuxii, is immunomodulatory through phospholipase A2 in macrophages toward its antileishmanial action. Cell Biochemistry and Biophysics. 80: 45 - 61. DOI:10.1007/s12013-021-01030-8
Verma N, Shukla S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. Journal of applied research in medicinal and aromatic plants. 2: 105-113. DOI: https://doi.org/10.1016/j.jarmap.2015.09.002
Published
2024-02-13
How to Cite
Pires-Moreira, M., Chan-Poot, S., Avilés-Berzunza, E., Garcia-Sosa, K., Godoy-HernándezG., & Peña-RodríguezL. M. (2024). Influence of the flowering stage in the production of urechitol A in Agrobacterium rhizogenes-transformed plants of Pentalinon andrieuxii. Botanical Sciences, 102(2), 438-446. https://doi.org/10.17129/botsci.3399
Section
PHYTOCHEMISTRY / FITOQUÍMICA