Skip to main content
SpringerLink
Log in

Synthesis and evaluation of indole derivatives as photosynthesis and plant growth inhibitors

  • PAPER
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Indole derivatives were synthetized based on the Fischer indole methodology using different phenyl hydrazine hydrochlorides and either cyclohexanone or 2-butanone. The pre- and post-emergent herbicidal activities were evaluated against Ipomoea grandifolia. A carbazole, 6-chloro-2,3,4,9-tetrahydro-1H-carbazole (3b), decreased the PIabs parameter by 32% and increased the cross-section related parameters, indicating the inactivation of the reaction center on photosystem II. Compound 3b acts as a post-emergent herbicide prototype since dry biomass was reduced by 50%, corroborating the fluorescence results. Comparing instead with a germination experiment, 2,3,4,9-tetrahydro-1H-carbazole (3a)was found to be the most effective agent, inhibiting seed germination by 22% and decreasing root length by 50%. The tetrahydrocarbazoles showed better results than indole derivatives potentially due to the presence of methylene groups at structures, which increase the compounds' lipophilicity and may facilitate their access to the plant. In addition, electron withdrawing groups on the aromatic ring were found to correlate with increased herbicide activity. Further optimization of this series towards the development of herbicides is ongoing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. J. R. Vyvyan, Allelochemicals as leads for new herbicides and agrochemicals, Tetrahedron, 2002, 58, 1631–1646.

    Article  CAS  Google Scholar 

  2. F. E. Dayan, C. L. Cantrell and S. O. Duke, Natural products in crop protection, Bioorg. Med. Chem., 2009, 17, 4022–4034.

    Article  CAS  PubMed  Google Scholar 

  3. I. Heap, Pest Manage. Sci., 2014, 70, 1306–1315.

    Article  CAS  Google Scholar 

  4. L. C. A. Barbosa, A. J. Demuner, E. S. De Alvarenga, A. Oliveira, B. King-Diaz and B. Lotina-Hennsen, Phytogrowth- and photosynthesis-inhibiting properties of nostoclide analogues, Pest Manage. Sci., 2006, 62, 214–222.

    Article  CAS  Google Scholar 

  5. M. I. Aguilar, M. G. Romero, M. I. Chávez, B. King-Díaz and B. Lotina-Hennsen, Biflavonoids isolated from Selaginella lepidophylla inhibit photosynthesis in spinach chloroplasts, J. Agric. Food Chem., 2008, 56, 6994–7000.

    Article  CAS  PubMed  Google Scholar 

  6. D. Torres-Romero, B. King-Díaz, I. A. Jiménez, B. Lotina-Hennsen and I. L. Bazzocchi, Sesquiterpenes from Celastrus vulcanicola as photosynthetic inhibitors, J. Nat. Prod., 2008, 71, 1331–1335.

    Article  CAS  PubMed  Google Scholar 

  7. T. A. M. Veiga, B. King-Díaz, A. S. F. Marques, O. M. Sampaio, P. C. Vieira, M. F. G. F. Da Silva and B. Lotina-Hennsen, Furoquinoline alkaloids isolated from Balfourodendron riedelianum as photosynthetic inhibitors in spinach chloroplasts, J. Photochem. Photobiol., B, 2013, 120, 36–43.

    Article  CAS  Google Scholar 

  8. J. O. S. Varejao, L. C. A. Barbosa, E. V. V. Varejao, C. R. A. Maltha, B. King-Díaz and B. Lotina-Hennsen, Cyclopent-4-ene-1,3-diones: A new class of herbicides acting as potent photosynthesis inhibitors, J. Agric. Food Chem., 2014, 62, 5772–5780.

    Article  CAS  PubMed  Google Scholar 

  9. L. Semelkova, K. Konecna, P. Paterova, V. Kubicek, J. Kunes, L. Novakova, J. Marek, L. Naesens, M. Pesko, K. Kralova, M. Dolezal and J. Zitko, Synthesis and biological evaluation of N-alkyl-3-(alkylamino)-pyrazine-2-carboxamides, Molecules, 2015, 20, 8687–8711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. O. M. Sampaio, M. M. C. de Lima, T. A. M. Veiga, B. King-Díaz, M. F. G. F. Da Silva and B. Lotina-Hennsen, Evaluation of antidesmone alkaloid as a photosynthesis inhibitor, Pestic. Biochem. Physiol., 2016, 134, 55–62.

    Article  CAS  PubMed  Google Scholar 

  11. D. Q. Yang, Y. L. Luo, W. H. Dong, Y. P. Yin, Y. Li and Z. L. Wang, Response of photosystem II performance and antioxidant enzyme activities in stay-green wheat to cytokinin, Photosynthetica, 2018, 56, 567–577.

    Article  CAS  Google Scholar 

  12. M. Franic, V. Galie, M. Mazur and D. Šimie, Effects of excess cadmium in soil on JIP-test parameters, hydrogen peroxide content and antioxidant activity in two maize inbreds and their hybrid, Photosynthetica, 2018, 56, 660–669.

    Article  CAS  Google Scholar 

  13. R. J. Strasser, M. Tsimilli-Michael and A. Srivastava, in Chlorophyll a Fluorescence, 2004, pp. 321–362.

    Book  Google Scholar 

  14. H. X. Ding, K. K.-C. Liu, S. M. Sakya, A. C. Flick and C. J. O'Donnell, Synthetic approaches to the 2011 new drugs, Bioorg. Med. Chem., 2013, 21, 2795–2825.

    Article  CAS  PubMed  Google Scholar 

  15. T. D. Penning, Small-molecule PARP modulators-current status and future therapeutic potential., Curr. Opin. Drug Discovery Dev., 2010, 13, 577–586.

    CAS  Google Scholar 

  16. N. Charrier, B. Clarke, L. Cutler, E. Demont, C. Dingwall, R. Dunsdon, P. East, J. Hawkins, C. Howes, I. Hussain, P. Jeffrey, G. Maile, R. Matico, J. Mosley, A. Naylor, A. O'Brien, S. Redshaw, P. Rowland, V. Soleil, K. J. Smith, S. Sweitzer, P. Theobald, D. Vesey, D. S. Walter and G. Wayne, Second generation of hydroxyethylamine BACE-1 inhibitors: Optimizing potency and oral bioavailability, J. Med. Chem., 2008, 51, 3313–3317.

    Article  CAS  PubMed  Google Scholar 

  17. V. Sharma, P. Kumar and D. Pathaka, Biological importance of the indole nucleus in recent years: A comprehensive review, J. Heterocycl. Chem., 2010, 47, 491–502.

    CAS  Google Scholar 

  18. T. V. Sravanthi and S. L. Manju, Eur. J. Pharm. Sci., 2016, 91, 1–10.

    Article  CAS  PubMed  Google Scholar 

  19. H. Zhang, Q. Wang, X. Ning, H. Hang, J. Ma, X. Yang, X. Lu, J. Zhang, Y. Li, C. Niu, H. Song, X. Wang and P. G. Wang, Synthesis and Biological Evaluations of a Series of Thaxtomin Analogues, J. Agric. Food Chem., 2015, 63, 3734–3741.

    Article  CAS  PubMed  Google Scholar 

  20. D. Sipaviciute, D. Tavgeniene, G. Krucaite, J. Grazulevicius, D. Volyniuk, B. Yao, Z. Xie, B. Zhang and S. Grigalevicius, Twin compounds of phenylethenyl substituted indole as efficient materials for electroluminescent devices, 2016, vol. 134.

  21. M. Zhang, G. Qin, J. Liu, Z. Zhen, A. A. Fedorchuk, G. Lakshminarayana, A. A. Albassam, A. M. El-Naggar, K. Ozga and I. V. Kityk, Modification of indole by electronrich atoms and their application in novel electron donor materials, Chem. Phys. Lett., 2017, 681, 105–109.

    Article  CAS  Google Scholar 

  22. S. Kotha, M. Saifuddin and V. R. Aswar, A diversity-oriented approach to indolocarbazoles via Fischer indolization and olefin metathesis: total synthesis of tjipanazole D and I, Org. Biomol. Chem., 2016, 14, 9868–9873.

    Article  CAS  PubMed  Google Scholar 

  23. T. Heinrich and H. Böttcher, A new synthesis of indole 5-car-boxylic acids and 6-hydroxy-indole-5- carboxylic acids in the preparation of an o-hydroxylated metabolite of vilazodone, Bioorg. Med. Chem. Lett., 2004, 14, 2681–2684.

    Article  CAS  PubMed  Google Scholar 

  24. D.-Q. Xu, J. Wu, S.-P. Luo, J.-X. Zhang, J.-Y. Wu, X.-H. Du and Z.-Y. Xu, Fischer indole synthesis catalyzed by novel SO3H-functionalized ionic liquids in water, Green Chem., 2009, 11, 1239.

    Article  CAS  Google Scholar 

  25. S. Gore, S. Baskaran and B. König, Fischer indole synthesis in low melting mixtures, Org. Lett., 2012, 14, 4568–4571.

    Article  CAS  PubMed  Google Scholar 

  26. Z. G. Zhang, B. A. Haag, J. S. Li and P. Knochel, Efficient preparation of polyfunctional indoles via a zinc organometallic variation of the Fischer indole synthesis, Synthesis, 2011, 23–29.

    Google Scholar 

  27. A. R. Katritzky, G. W. Rewcastle and L. M. Vazquez de Miguel, Improved Syntheses of Substituted Carbazoles and Benzocarbazoles Via Lithiation of the (Dialkylamino) Methyl (Aminal) Derivatives, J. Org. Chem., 1988, 53, 794–799.

    Article  CAS  Google Scholar 

  28. D. Deorha and S. Joshi, Notes- Cyclic Products from Hydrazines. I. Nitroindoles, Nitrotetrahydrocarbazoles, Nitroindolenines and Nitrotetrahydrocarbazolenines, J. Org. Chem., 1961, 26, 3527–3530.

    Article  CAS  Google Scholar 

  29. Y. Li, T. Yan, K. Junge and M. Beller, Catalytic methylation of C-H bonds using CO2 and H2, Angew. Chem., Int. Ed., 2014, 53, 10476–10480.

    Article  CAS  Google Scholar 

  30. M. Tursky, L. L. R. Lorentz-Petersen, L. B. Olsen and R. Madsen, Iridium- and ruthenium-catalysed synthesis of 2,3-disubstituted indoles from anilines and vicinal diols, Org. Biomol. Chem., 2010, 8, 5576.

    Article  CAS  PubMed  Google Scholar 

  31. M. Takemoto, Y. Iwakiri and K. Tanaka, Oxidative Cleavage Reaction of Substituted Indoles Catalyzed by Plant Cell Cultures, 2007, vol. 72.

  32. T. Barf, F. Lehmann, K. Hammer, S. Haile, E. Axen, C. Medina, J. Uppenberg, S. Svensson, L. Rondahl and T. Lundbäck, N-Benzyl-indolo carboxylic acids: Design and synthesis of potent and selective adipocyte fatty-acid binding protein (A-FABP) inhibitors, Bioorg. Med. Chem. Lett., 2009, 19, 1745–1748.

    Article  CAS  PubMed  Google Scholar 

  33. P. E. Verkade and J. Lieste, Untersuchungen über indolderivate. X. Einige von 2,3-Dimethylindol abgeleitete Bz-Carbonsäuren, Recl. Trav. Chim. Pays-Bas, 1946, 65, 912–918.

    Article  Google Scholar 

  34. M. R. Schmer, Q. Xue and J. R. Hendrickson, Salinity effects on perennial, warm-season (C 4) grass germination adapted to the northern Great Plains, Can. J. Plant Sci., 2012, 92, 873–881.

    Article  Google Scholar 

  35. S. J. Steinmaus, T. S. Prather and J. S. Holt, Estimation of base temperatures for nine weed species, J. Exp. Bot., 2000, 51, 275–286.

    Article  CAS  PubMed  Google Scholar 

  36. R. J. Strasser, A. Srivastava and M. Tsimilli-Michael, The fluorescence transient as a tool to characterize and screen photosynthetic samples, Probing Photosynth. Mech. Regul. Adapt., 2000, 443–480.

    Google Scholar 

  37. O. M. Sampaio, M. F. das G. F. da Silva, T. A. M. Veiga, B. King-Díaz and B. Lotina-Hennsen, Química Nov., 2012, 35, 2115–2118.

    Article  CAS  Google Scholar 

  38. L.-L. Meng, J.-F. Song, J. Wen, J. Zhang and J.-H. Wei, Effects of drought stress on fluorescence characteristics of photosystem II in leaves of Plectranthus scutellarioides, Photosynthetica, 2016, 54, 414–421.

    Article  CAS  Google Scholar 

  39. A. Digrado, L. G. de la Motte, A. Bachy, A. Mozaffar, N. Schoon, F. Bussotti, C. Amelynck, A.-C. Dalcq, M.-L. Fauconnier, M. Aubinet, B. Heinesch, P. du Jardin and P. Delaplace, Decrease in the Photosynthetic Performance of Temperate Grassland Species Does Not Lead to a Decline in the Gross Primary Production of the Ecosystem, Front. Plant Sci., 2018, 9, 67.

    Article  PubMed  PubMed Central  Google Scholar 

  40. E. G. Martinazzo, A. T. Perboni, P. V. De Oliveira, V. J. Bianchi and M. A. Bacarin, Photosynthetic activity in japanese plum under water deficit and flooding, Cienc. Rural, 2013, 43, 35–41.

    Article  CAS  Google Scholar 

  41. V. D. Kreslavski, M. Brestic, S. K. Zharmukhamedov, V. Yu. Lyubimov, A. V. Lankin, A. Jajoo and S. I. Allakhverdiev, Mechanisms of inhibitory effects of polycyclic aromatic hydrocarbons in photosynthetic primary processes in pea leaves and thylakoid preparations, Plant Biol., 2017, 19, 683–688.

    Article  CAS  PubMed  Google Scholar 

  42. K. Zushi, S. Kajiwara and N. Matsuzoe, Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit, Sci. Hortic., 2012, 148, 39–46.

    Article  CAS  Google Scholar 

  43. D. Pazuch, M. M. Trezzi, A. C. D. Guimaraes, M. V. J. Barancelli, R. Pasini and R. A. Vidal, Evolution of Natural Resistance to Glyphosate in Morning Glory Populations, Planta Daninha, 2017, 35,1–9.

    Article  Google Scholar 

  44. P. J. Christoffoleti, A. Borges, M. Nicolai, S. J. P. Carvalho, R. F. López-Ovejero and P. A. Monquero, Planta Daninha, 2006, 24, 83–90.

    Article  Google Scholar 

  45. A. G. Ferreira and M. E. A. Aquila, Alelopatia: uma área emergente da ecofisiologia, Rev. Bras. Fisiol. Veg., 2000, 12, 175–204.

    Google Scholar 

  46. C. M. Tice, Selecting the right compounds for screening: Does Lipinski’s rule of 5 for pharmaceuticals apply to agrochemicals?, Pest Manage. Sci., 2001, 57, 3–16.

    Article  CAS  Google Scholar 

  47. A. D. Gribble, R. J. Ife, A. Shaw, D. McNair, C. E. Novelli, S. Bakewell, V. P. Shah, R. E. Dolle, P. H. Groot, N. Pearce, J. Yates, D. Tew, H. Boyd, S. Ashman, D. S. Eggleston, R. Curtis Haltiwanger and G. Okafo, ATP-citrate lyase as a target for hypolipidemic intervention. 2. Synthesis and evaluation of (3R*,5S*)-rn-substituted-3-carboxy-3,5-di-hydroxyalkanoic acids and their y-lactone prodrugs as inhibitors of the enzyme in vitro and in vivo, J. Med. Chem., 1998, 41, 3582–3595.

    Article  CAS  PubMed  Google Scholar 

  48. M. Roche, J. Bignon, J. D. Brion, A. Hamze and M. Alami, Tandem one-pot palladium-catalyzed coupling of hydrazones, haloindoles, and amines: Synthesis of amino-N-vinylindoles and their effect on human colon carcinoma cells, J. Org. Chem., 2014, 79, 7583–7592.

    Article  CAS  PubMed  Google Scholar 

  49. A. Walser, T. Flynn, C. Mason, H. Crowley, C. Maresca, B. Yaremko and M. O’Donnell, Triazolobenzo- and Triazolothienodiazepines as Potent Antagonists of Platelet Activating Factor, J. Med. Chem., 1991, 34, 1209–1221.

    Article  CAS  PubMed  Google Scholar 

  50. J. Timothy, M. Ibanez, A. C. Rijnbrand, A. J. Jackson, G. P. Mittapalli, F. Zhao, J. E. MacDonald and F. Wong-Staal, Hepatitis c virus entry inhibitors, WO 2008021745A3, 2008.

    Google Scholar 

  51. M. Ohashi, T. Shudo, K. Nishijima, T. Notsu, A. Kikuchi, K. Yanagibashi and H. Nishida, Pyridocarbazol derivate die einen cGMP-PDE inhibilierenden effekt haben, EP 0985671, 2001.

    Google Scholar 

  52. M. Ohashi, T. Shudo, K. Nishijima, T. Notsu, A. Kikuchi, K. Yanagibashi and H. Nishida, Pyridocarbazole derivatives having cgmp-pde inhibitory activity, US 6197768, 2001.

Download references

Acknowledgements

We gratefully acknowledge the FAPEMAT (grants 0217830/2017 and 0250685/2017), CNPq (grant 430089/2016-3) and UFMT for financial support and fellowships. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Author information

Authors and Affiliations

  1. Forest Engineering Faculty, Federal University of Mato Grosso, Cuiabá-MT, Brazil

    Mylla Cristie da Silva Mendes

  2. Chemistry Department, Federal University of Mato Grosso, Cuiabá-MT, Brazil

    Bruno Rodrigues Fazolo, Jéssica Maria de Souza, Leonardo Gomes de Vasconcelos, Paulo Teixeira de Sousa Junior, Evandro Luiz Dall'Oglio & Olívia Moreira Sampaio

  3. Botany and Ecology Department, Bioscience Institute, Federal University of Mato Grosso, Cuiabá, Mato Grosso, Brazil

    Marcos Antônio Soares

  4. Engineering Institute/Chemistry, Federal University of Mato Grosso, Várzea Grande-MT, Brazil

    Lucas Campos Curcino Vieira

Authors
  1. Mylla Cristie da Silva Mendes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Rodrigues Fazolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jéssica Maria de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonardo Gomes de Vasconcelos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paulo Teixeira de Sousa Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Evandro Luiz Dall'Oglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcos Antônio Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olívia Moreira Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lucas Campos Curcino Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucas Campos Curcino Vieira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

da Silva Mendes, M.C., Fazolo, B.R., de Souza, J.M. et al. Synthesis and evaluation of indole derivatives as photosynthesis and plant growth inhibitors. Photochem Photobiol Sci 18, 1350–1358 (2019). https://doi.org/10.1039/c8pp00506k

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c8pp00506k

Search

Navigation