New biologically active ionic liquids with benzethonium cation-efficient SAR inducers and antimicrobial agents
Patrycja Czerwoniec
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Faculty of Chemistry, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorRafal Kukawka
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Search for more papers by this authorMaciej Spychalski
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Search for more papers by this authorRyszard Koczura
Department of Microbiology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorJoanna Mokracka
Department of Microbiology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorCorresponding Author
Marcin Smiglak
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Innosil Sp. z o.o., Poznań, Poland
Correspondence to: M Smiglak, Poznan Science and Technology Park, Adam Mickiewicz University Foundation, ul. Rubiez 46, 61-612 Poznan, Poland. E-mail: [email protected]
Search for more papers by this authorPatrycja Czerwoniec
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Faculty of Chemistry, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorRafal Kukawka
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Search for more papers by this authorMaciej Spychalski
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Search for more papers by this authorRyszard Koczura
Department of Microbiology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorJoanna Mokracka
Department of Microbiology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poznań, Poland
Search for more papers by this authorCorresponding Author
Marcin Smiglak
Poznan Science and Technology Park, Adam Mickiewicz University Foundation, Poznań, Poland
Innosil Sp. z o.o., Poznań, Poland
Correspondence to: M Smiglak, Poznan Science and Technology Park, Adam Mickiewicz University Foundation, ul. Rubiez 46, 61-612 Poznan, Poland. E-mail: [email protected]
Search for more papers by this authorAbstract
BACKGROUND
An urgent need to find new methods for crop protection remains open due to the withdrawal from the market of the most toxic pesticides and increasing consumer awareness. One of the alternatives that can be used in modern agriculture is the use of bifunctional compounds whose actions towards plant protection are wider than those of conventional pesticides.
RESULTS
In this study, we present the investigation of the biological efficacy of nine dual-functional salts containing a systemic acquired resistance (SAR)-inducing anion and the benzethonium cation. A significant result of the presented study is the discovery of the SAR induction activity of benzethonium chloride, which was previously reported only as an antimicrobial agent. Moreover, the concept of dual functionality was proven, as the application of presented compounds in a given concentrations resulted both in the control of human and plant bacteria species and induction of SAR.
CONCLUSION
The strategy presented in this article shows the capabilities of derivatization of common biologically active compounds into their ionic derivatives to obtain bifunctional salts. This approach may be an example of the design of potential new compounds for modern agriculture. It provides plants with two complementary actions allowing to provide efficient protection to plants, if one mode of action is ineffective. © 2024 Society of Chemical Industry.
CONFLICT OF INTEREST STATEMENT
The authors declare no competing financial interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are openly available in Poznan Science and Technology Park Repository at https://ppnt.poznan.pl/repository.
Supporting Information
Filename | Description |
---|---|
ps8014-sup-0001-Supinfo.docxWord 2007 document , 26.7 KB | Data S1. Nuclear magnetic resonance analysis. Data S2. SAR induction activity. Data S3. Antimicrobial activity of tested substances containing benzethonium cation. Table S1. MIC and MBC values of new derivatives. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Curreri AM, Mitragotri S and Tanner EEL, Recent advances in ionic liquids in biomedicine. Adv Sci 8:2004819 (2021).
- 2Kowal D, Rola K, Cybinska J, Skorenski M, Zajac A, Szpecht A et al., Fluorescent ionic liquid micro reservoirs fabricated by dual-step E-beam patterning. Mater Res Bull 142:111434 (2021).
- 3Zielinski D, Szpecht A, Hinc P, Maciejewski H and Smiglak M, Mono N-Alkylated DABCO-Based Ionic Liquids and their Application as Latent Curing Agents for Epoxy Resins. ACS Appl Polym Mater 3: 5481–5493 (2021).
- 4Zhuang W, Hachem K, Bokov D, Javed Ansari M and Taghvaie Nakhjiri A, Ionic liquids in pharmaceutical industry: a systematic review on applications and future perspectives. J Mol Liq 349:118145 (2022).
- 5Zajac A, Kukawka R, Pawlowska-Zygarowicz A, Stolarska O and Smiglak M, Ionic liquids as bioactive chemical tools for use in agriculture and the preservation of agricultural products. Green Chem 20: 4764–4789 (2018).
- 6Badgujar KC, Badgujar VC and Bhanage BM, Recent update on use of ionic liquids for enzyme immobilization, activation, and catalysis: a partnership for sustainability. Curr Opin Green Sustainable Chem 36:100621 (2022).
- 7Welton T, Ionic liquids: a brief history. Biophys Rev 10: 691–706 (2018).
- 8Smiglak M, Metlen A and Rogers RD, The Second Evolution of Ionic Liquids: From Solvents and Separations to Advanced Materials—Energetic Examples from the Ionic Liquid Cookbook. Acc Chem Res 40: 1182–1192 (2007).
- 9Wang F, Ge C, Duan D, Lin H, Li L, Naumov P et al., Recent progress in ionic liquids for stability engineering of perovskite solar cells. Small Struct 3:2200048 (2022).
- 10Ferraz R, Branco LC, Prudêncio C, Noronha JP and Petrovski Ž, Ionic liquids as active pharmaceutical ingredients. ChemMedChem 6: 975–985 (2011).
- 11Singh SK and Savoy AW, Ionic liquids synthesis and applications: an overview. J Mol Liq 297:112038 (2020).
- 12Czerniak K, Gwiazdowski R, Marcinkowska K and Pernak J, Dicationic triazolium fungicidal ionic liquids with herbicidal properties. Chem Pap 74: 261–271 (2020).
- 13Smiglak M, Lewandowski P, Kukawka R, Budziszewska M, Krawczyk K, Obrępalska-Stęplowska A et al., Dual functional salts of benzo[1.2.3]thiadiazole-7-carboxylates as a highly efficient weapon against viral plant diseases. ACS Sustainable Chem Eng 5: 4197–4204 (2017).
- 14Kukawka R, Spychalski M, Stróżyk E, Byzia E, Zajac A, Kaczyński P et al., Synthesis, characterization and biological activity of bifunctional ionic liquids based on dodine ion. Pest Manag Sci 78: 446–455 (2022).
- 15Markiewicz M, Lewandowski P, Spychalski M, Kukawka R, Feder-Kubis J, Beil S et al., New bifunctional ionic liquid-based plant systemic acquired resistance (SAR) inducers with an improved environmental hazard profile. Green Chem 23: 5138–5149 (2021).
- 16Kianfar E and Mafi S, Ionic liquids: properties, application, and synthesis. Fine Chem Eng 2: 22–31 (2021).
- 17Fargnoli M, Lombardi M, Puri D, Casorri L, Masciarelli E, Mandić-Rajčević S et al., The safe use of pesticides: a risk assessment procedure for the enhancement of occupational health and safety (OHS) management. Int J Environ Res Public Health 16: 310 (2019).
- 18Hermoso V, Carvalho SB, Giakoumi S, Goldsborough D, Katsanevakis S, Leontiou S et al., The EU biodiversity strategy for 2030: opportunities and challenges on the path towards biodiversity recovery. Environ Sci Policy 127: 263–271 (2022).
- 19Vlot AC, Sales JH, Lenk M, Bauer K, Brambilla A, Sommer A et al., Systemic propagation of immunity in plants. New Phytol 229: 1234–1250 (2021).
- 20Wang D, Liu B, Ma Z, Feng J, Yan H and Reticine A, A new potent natural elicitor: isolation from the fruit peel of citrus reticulate and induction of systemic resistance against tobacco mosaic virus and other plant fungal diseases. Pest Manag Sci 77: 354–364 (2021).
- 21Kaur A, Sharma VK and Sharma S, Management of spot blotch of barley: an eco-friendly approach. Australas Plant Pathol 50: 389–401 (2021).
- 22Spychalski M, Kukawka R, Krzesiński W, Spiżewski T, Michalecka M, Poniatowska A et al., Use of new BTH derivative as supplement or substitute of standard fungicidal program in strawberry cultivation. Agronomy 11: 43 (2021).
10.3390/agronomy11061031 Google Scholar
- 23Spychalski M, Kukawka R, Prasad R, Borodynko-Filas N, Stępniewska-Jarosz S, Turczański K et al., A new benzothiadiazole derivative with systemic acquired resistance activity in the protection of zucchini (Cucurbita pepo convar. Giromontiina) against viral and fungal pathogens. Plants 12: 43 (2022).
10.3390/plants12010043 Google Scholar
- 24Turczański K, Bełka M, Kukawka R, Spychalski M and Smiglak M, A novel plant resistance inducer for the protection of european ash (Fraxinus excelsior l.) against hymenoscyphus fraxineus—preliminary studies. Forests 12: 1–8 (2021).
- 25Turczański K, Bełka M, Spychalski M, Kukawka R, Prasad R and Smiglak M, Resistance inducers for the protection of pedunculate oak (Quercus robur L.) seedlings against powdery mildew Erysiphe alphitoides. Plants 12: 635 (2023).
- 26Jarecka-Boncela A, Spychalski M, Ptaszek M, Włodarek A, Smiglak M and Kukawka R, The effect of a new derivative of benzothiadiazole on the reduction of Fusariosis and increase in growth and development of tulips. Agriculture 13: 853 (2023).
- 27Yassin M, Ton J, Rolfe SA, Valentine TA, Cromey M, Holden N et al., The rise, fall and resurrection of chemical-induced resistance agents. Pest Manag Sci 77: 3900–3909 (2021).
- 28Conrath U, Systemic acquired resistance. Plant Signal Behav 1: 179–184 (2006).
- 29Salman EK, Ghoniem KE, Badr ES, Aboulila AA and Emeran AA, Identification of chlorpromazine hydrochloride role as a new systemic acquired resistance inducer against Magnaporthe oryzae in rice. Physiol Mol Plant Pathol 117:101770 (2022).
- 30Wani MY, Mehraj S, Rather RA, Rani S, Hajam OA, Ganie NA et al., Systemic acquired resistance (SAR): a novel strategy for plant protection with reference to mulberry. Int J Chem Stud 2: 1184–1192 (2018).
- 31Feder-Kubis J, Czerwoniec P, Lewandowski P, Pospieszny H and Smiglak M, Ionic liquids with natural origin component: a path to new plant protection products. ACS Sustainable Chem Eng 8: 842–852 (2020).
- 32Kukawka R, Czerwoniec P, Lewandowski P, Pospieszny H and Smiglak M, New ionic liquids based on systemic acquired resistance inducers combined with the phytotoxicity reducing cholinium cation. New J Chem 42: 11984–11990 (2018).
- 33Smiglak M, Kukawka R, Lewandowski P, Budziszewska M, Obrępalska-Stęplowska A, Krawczyk K et al., New dual functional salts based on cationic derivative of plant resistance inducer—benzo[1.2.3]thiadiazole-7-carbothioic acid, S-methyl Ester. ACS Sustainable Chem Eng 4: 3344–3351 (2016).
- 34Rub MA, Azum N, Kumar D, Alotaibi MM and Asiri AM, Impact of numerous media on association, interfacial, and thermodynamic properties of promethazine hydrochloride (PMT) + benzethonium chloride (BTC) mixture of various composition. J Mol Liq 346:118287 (2022).
- 35Fuchsman P, Fetters K, O'Connor A, Bock M, Henning M, Brown L et al., Ecological risk analysis for benzalkonium chloride, benzethonium chloride, and chloroxylenol in US disinfecting and sanitizing products. Environ Toxicol Chem 41: 3095–3115 (2022).
- 36Thacker M, Sahoo A, Reddy AA, Bokara KK, Singh S, Basu S et al., Benzalkonium chloride-induced dry eye disease animal models: current understanding and potential for translational research. Indian J Ophthalmol 71: 1256 (2023).
- 37Fredell DL, Biological properties and applications of cationic surfactants, in Cationic Surfactants. Taylor & Francis Group, CRC Press pp. 31–60 (2019).
10.1201/9780429270376-4 Google Scholar
- 38Carrijo-Carvalho LC, Sant'ana VP, Foronda AS, de Freitas D and de Souza Carvalho FR, Therapeutic agents and biocides for ocular infections by free-living amoebae of Acanthamoeba genus. Surv Ophthalmol 62: 203–218 (2017).
- 39Machado I, Coquet L, Jouenne T and Pereira MO, Proteomic approach to Pseudomonas aeruginosa adaptive resistance to benzalkonium chloride. J Proteomics 89: 273–279 (2013).
- 40Marchetti V, Mancianti F, Cardini G and Luchetti E, Evaluation of fungicidal efficacy of benzalkonium chloride (Steramina G uv) and Virkon-S against Microsporum canis for environmental disinfection. Vet Res Commun 30: 255–261 (2006).
- 41Sola EA, Bourilhón P, Manzo RM and Frisón LN, Antifungal action of quaternary ammonium compounds against environmental molds isolated from food industries. J Food Saf 43: e13017 (2023).
- 42Smiglak M, Kukawka R, Lewandowski P and Pospieszny H, Cationic derivatives of the plant resistance inducer benzo[1,2,3] thiadiazole-7-carbothioic acid S-methyl ester (BTH) as bifunctional ionic liquids. Tetrahedron Lett 55: 3565–3568 (2014).
- 43Bica K, Rijksen C, Nieuwenhuyzen M and Rogers RD, In search of pure liquid salt forms of aspirin: ionic liquid approaches with acetylsalicylic acid and salicylic acid. Phys Chem Chem Phys 12: 2011–2017 (2010).
- 44Dean PM, Turanjanin J, Yoshizawa-Fujita M, MacFarlane DR and Scott JL, Exploring an anti-crystal engineering approach to the preparation of pharmaceutically active ionic liquids. Cryst Growth Des 9: 1137–1145 (2009).
- 45Arellano IHJ, Guarino JG, Paredes FU and Arco SD, Thermal stability and moisture uptake of 1-alkyl-3-methylimidazolium bromide. J Therm Anal Calorim 103: 725–730 (2011).
- 46Song Y, Xia Y and Liu Z, Influence of cation structure on physicochemical and antiwear properties of hydroxyl-functionalized imidazolium bis (trifluoromethylsulfonyl) imide ionic liquids. Tribol Trans 55: 738–746 (2012).
- 47Montanino M, Carewska M, Alessandrini F, Passerini S and Appetecchi GB, The role of the cation aliphatic side chain length in piperidinium bis(trifluoromethansulfonyl)imide ionic liquids. Electrochim Acta 57: 153–159 (2011).
- 48Cao Y and Mu T, Comprehensive investigation on the thermal stability of 66 ionic liquids by thermogravimetric analysis. Ind Eng Chem Res 53: 8651–8664 (2014).
- 49Czerwoniec P, Szymkowiak J and Smiglak M, Simple modifications of nicotinic, isonicotinic, and 2,6-dichloroisonicotinic acids toward new weapons against plant diseases. Open Chem 19: 1108–1115 (2021).
- 50Lozano-Durán R and Zipfel C, Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci 20: 12–19 (2015).
- 51Albrecht T and Argueso CT, Should I fight or should I grow now? The role of cytokinins in plant growth and immunity and in the growth–defence trade-off. Ann Bot 119: 725–735 (2017).
- 52Yu M-H, Zhao Z-Z and He J-X, Brassinosteroid signaling in plant–microbe interactions. Int J Mol Sci 19: 4091 (2018).
- 53van Butselaar T and Van den Ackerveken G, Salicylic acid steers the growth-immunity tradeoff. Trends Plant Sci 25: 566–576 (2020).
- 54 ThermoFischer Scientific Safety Data Sheet (2015) https://www.fishersci.com/store/msds?partNumber=AC105381000&countryCode=US&language=en [available on 31.12.2023]
- 55 European Medicine Agency, Questions and answers on benzalkonium chloride used as an excipient in medicinal products for human use. (2017). https://www.ema.europa.eu/en/documents/scientific-guideline/questions-and-answers-benzalkonium-chloride-used-excipient-medicinal-products-human-use_en.pdf [available on 31.12.2023]
- 56Frackowiak˛ P, Pospieszny H, Smiglak M and Obrępalska-Stęplowska A, Assessment of the efficacy and mode of action of benzo(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) and its derivatives in plant protection against viral disease. Int J Mol Sci 20: 1598 (2019).
- 57Smiglak M, Pospieszny H, Kukawka R, Lewandowski P, Stolarska O and Maciejewski H, Application of 7-Carboxybenzo(1,2,3)Thiadiazole Amides as Plant. Stimulants. Patent Application No. WO/2017/017626, 2 February 2017.