Research Article
Synthesis of Esters Containing Cinnamoyl Motif with Potential Larvicide Action: A Computational, Ecotoxicity and in Vitro Cytotoxicity Assessments
Paulo Ricardo dos Santos Correia,
Cenira Monteiro de Carvalho,
Cristhyan Rychard da Silva Cunha,
Rafael Antonio Santos da Silva,
Monaly de Oliveira Lima,
Saraliny Bezerra França,
Emiliano de Oliveira Barreto,
Josealdo Tonholo,
Dimas José da Paz Lima,
Paulo Ricardo dos Santos Correia
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCenira Monteiro de Carvalho
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCristhyan Rychard da Silva Cunha
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorRafael Antonio Santos da Silva
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorMonaly de Oliveira Lima
Institute of Biological and Heath Science, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorSaraliny Bezerra França
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorEmiliano de Oliveira Barreto
Institute of Biological and Heath Science, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorJosealdo Tonholo
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCorresponding Author
Dimas José da Paz Lima
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorPaulo Ricardo dos Santos Correia,
Cenira Monteiro de Carvalho,
Cristhyan Rychard da Silva Cunha,
Rafael Antonio Santos da Silva,
Monaly de Oliveira Lima,
Saraliny Bezerra França,
Emiliano de Oliveira Barreto,
Josealdo Tonholo,
Dimas José da Paz Lima,
Paulo Ricardo dos Santos Correia
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCenira Monteiro de Carvalho
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCristhyan Rychard da Silva Cunha
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorRafael Antonio Santos da Silva
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorMonaly de Oliveira Lima
Institute of Biological and Heath Science, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorSaraliny Bezerra França
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorEmiliano de Oliveira Barreto
Institute of Biological and Heath Science, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorJosealdo Tonholo
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorCorresponding Author
Dimas José da Paz Lima
Institute of Chemistry and Biotechnology, Federal University of Alagoas, Avenida Lourival de Melo Mota, 57070-970 Maceio, AL, Brazil
Search for more papers by this authorAbstract
An increasing morbidity and mortality rate has been related to arboviruses transmitted by Aedes aegypti. Compounds with cinnamoyl moiety represent an alternative against mosquitos, considering their larvicidal activity. This study aimed to assess the larvicidal activity of cinnamic ester derivates against Aedes aegypti larvae, along with evaluating their toxicity effect to assess its safety as a larvicide. Ethyl cinnamate demonstrated larvicidal activity (LC50=48.59 μg/mL). Morphological changes in larvae were detected, as a degenerative response in the thorax. Through molecular docking, the molecular binding mode between 3b, 3c, and acetylcholinesterase showed strong hydrogen bond interactions. Preliminary in vitro cell viability revealed the non-cytotoxicity of 3c. Ecotoxicity results indicated a sensitivity of Artemia salina to cinnamic esters. The phytotoxicity bioassays show potential for cinnamic compounds to enhance germination and root development. These findings suggest that compound 3c is more suitable as a larvicide since it demonstrated low toxicity.
Graphical Abstract
Conflict of interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
Research data are not shared.
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References
- 1Pan American Health Organization, ‘Technical document for the implementation of interventions based on generic operational scenarios for Aedes aegypti control, 2016.
- 2V. C. Maniero, M. O. Santos, R. L. Ribeiro, P. A. C. de Oliveira, T. B. da Silva, A. B. Moleri, I. R. Martins, C. C. Lamas, S. V. Cardozo, ‘Dengue, Chikungunya E Zika Vírus No Brasil: Situação Epidemiológica, Aspectos Clínicos E Medidas Preventivas’, Alm. Multidiscip. Pesqui. 2016, 3, 118–145.
- 3S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, S. I. Hay, ‘The global distribution and burden of dengue’, Nature. 2013, 496, 504–507.
- 4World Health Organization. Dengue and severe dengue In: Fact Sheet 2021. http://www.who.int. Accessed June 24, 2020.
- 5A. Wilder-Smith, ‘Dengue vaccine development by the year 2020: challenges and prospects’, Curr. Opin. Virol. 2020, 43, 71–78.
- 6S. R. S. Hadinegoro, J. L. Arredondo-García, M. R. Capeding, S. Pallardy, F. Noriega, A. Bouckenooghe, ‘Controversy and debate on dengue vaccine series – article 2: response to review of a licensed dengue vaccine: inappropriate subgroup analyses and selective reporting may cause harm in mass vaccination programs’, J. Clin. Epidemiol. 2018, 95, 140–141.
- 7J. E. Thames, C. D. Waters III, C. Valle, M. Bassetto, W. Aouadi, B. Martin, A. Falat, B. Coutard, A. Brancale, B. Canard, E. Decroly, K. L. Seley-Radtke, ‘Synthesis and Biological Evaluation of Novel Flexible Nucleoside Analogs that Inhibit Flavivirus Replication in vitro’ Bioorg. Med. Chem. 2020, 28, 115713.
- 8L. Eyer, R. Nencka, E. de Clercq, K. L. Seley-Radtke, D. Růžek, ‘Nucleoside analogs as a rich source of antiviral agents against arthropod-borne flaviviruses’, Antiviral Chem. Chemother. 2018, 26, 1–28.
10.1177/2040206618761299 Google Scholar
- 9R. A. G. B. Consoli, R. L. de Oliveira, ‘Principais mosquitos de importância sanitária no Brasil’, Fiocruz, Rio de Janeiro, 1994.
- 10K. R. Souza, M. L. R. Santos, I. C. S. Guimarães, G. D. S. Ribeiro, L. K. Silva, ‘Knowledge and practices in Aedes aegypti control among different social subjects in Salvador, Bahia State, Brazil’, Cad. Saude Publica. 2018, 34, 5.
- 11A. L. de S. A. Zara, S. M. Dos Santos, E. S. Fernandes-Oliveira, R. G. Carvalho, G. E. Coelho, ‘Estratégias de controle do Aedes aegypti: uma revisão’, Epidemiol. Serv. Saúde. 2016, 25, 391–404.
- 12R. D. S. Azevedo, K. V. G. Falcão, C. R. D. Assis, R. M. G. Martins, M. C. Araújo, G. T. Yogui, J. L. Neves, G. M. Seabra, M. B. S. Maia, I. P. G. Amaral, A. C. R. Leite, R. S. Bezerra, ‘Effects of pyriproxyfen on zebrafish brain mitochondria and acetylcholinesterase’, Chemosphere 2021, 28029, 263.
- 13M. M. C. de S. L. Diniz, A. D. da S Henriques, R. da S Leandro, D. L. Aguiar, E. B. Beserra, ‘Resistance of Aedes aegypti to temephos and adaptive disadvantages’, Rev. Saude Publica. 2014, 48, 775–782.
- 14S. Knutsson, C. Engdahl, R. Kumari, N. Forsgren, C. Lindgren, T. Kindahl, S. Kitur, L. Wachira, L. Kamau, F. Ekström, A. Linusson, ‘Noncovalent Inhibitors of Mosquito Acetylcholinesterase 1 with Resistance-Breaking Potency’, J. Med. Chem. 2018, 61, 10545–10557.
- 15P. Sharma, ‘Cinnamic acid derivatives: A new chapter of various pharmacological activities’, J. Chem. Pharm. Res. 2011, 3, 403–423.
- 16J. D. Guzman, ‘Natural cinnamic acids, synthetic derivatives and hybrids with antimicrobial activity’, Molecules 2014, 19, 19292–19349.
- 17S. B. França, P. R. dos S Correia, I. B. D. De Castro, E. D. da S Júnior, M. E. de S B Barros, D. J. da P Lima, ‘Synthesis, applications and Structure-activity Relationship (SAR) of cinnamic acid derivatives: a review’, Res. Soc. Dev. 2021, 1, 10.
- 18A. P. de A dos Santos, S. N. Fialho, D. S. S. de Medeiros, A. F. G. Garay, J. A. R. Diaz, M. C. V. Gómez, C. B. G. Teles, L. de A Calderon, ‘Antiprotozoal action of synthetic cinnamic acid analogs’, Rev. Soc. Bras. Med. Trop. 2018, 51, 849–853.
- 19N. Ruwizhi, B. A. Aderibigbe, ‘Cinnamic acid derivatives and their biological efficacy’, Int. J. Mol. Sci. 2020, 21, 1–36.
- 20M. E. Perez, M. Haramboure, L. Mirande, G. P. Romanelli, M. I. Schneider, J. C. Autino, ‘Biological activity of three alkyl cinnamates on young larvae of Tuta absoluta’, Commun. Agric. Appl. Biol. Sci. 2013, 78, 299–303.
- 21G. M. Fujiwara, V. Annies, C. F. de Oliveira, R. A. Lara, M. M. Gabriel, F. C. Betim, J. M. Nadal, P. V. Farago, J. F. Dias, O. G. Miguel, M. D. Miguel, F. A. Marques, S. M. Zanin, ‘Evaluation of larvicidal activity and ecotoxicity of linalool, methyl cinnamate and methyl cinnamate/linalool in combination against Aedes aegypti’, Ecotoxicol. Environ. Saf. 2017, 139, 238–244.
- 22M. O. Araújo, Y. Pérez-Castillo, L. H. G. Oliveira, F. C. Nunes, D. P. d. Sousa, ‘Larvicidal Activity of Cinnamic Acid Derivatives: Investigating Alternative Products for Aedes aegypti L. Control’, Molecules. 2020, 26, 1–21.
- 23S. Bezerra França, L. Carine Barros de Lima, C. Rychard da Silva Cunha, D. Santos Anunciação, E. Ferreira da Silva-Júnior, M. Ester de Sá Barreto Barros, D. José da Paz Lima, ‘Larvicidal activity and in silico studies of cinnamic acid derivatives against Aedes aegypti (Diptera: Culicidae)’, Bioorg. Med. Chem. 2021, 44, 116299.
- 24J. Lyu, J. Park, L. Kumar Pandey, S. Choi, H. Lee, J. De Saeger, S. Depuydt, T. Han, ‘Testing the toxicity of metals, phenol, effluents, and receiving waters by root elongation in Lactuca sativa L., Ecotoxicol.’, Environ. Saf. 2018, 149, 225–232.
- 25A. Priac, P.-M. Badot, G. Crini, ‘Treated wastewater phytotoxicity assessment using Lactuca sativa: Focus on germination and root elongation test parameters’, C. R. Biol. 2017, 340, 188–194.
- 26T. Buxton, S. Takahashi, A. M. Eddy Doh, J. Baffoe-Ansah, E. O. Owusu, C. S. Kim, ‘Insecticidal activities of cinnamic acid esters isolated from Ocimum gratissimum L. and Vitellaria paradoxa Gaertn leaves against Tribolium castaneum Hebst (Coleoptera: Tenebrionidae)’, Pest Manage. Sci. 2020, 76, 257–267.
- 27N. J. Kim, S. G. Byun, J. E. Cho, K. Chung, Y. J. Ahn, ‘Larvicidal activity of Kaempferia galanga rhizome phenylpropanoids towards three mosquito species’, Pest Manage. Sci. 2008, 64, 857–62.
- 28<N. Ríos, E. E. Stashenko, J. E. Duque, ′Evaluation of the insecticidal activity of essential oils and their mixtures against Aedes aegypti (Diptera: Culicidae)′, Rev. Bras. Entomol. 2017, 4, 307-311.
- 29R. La Corte, V. A. D. Melo, S. S. Dolabella, L. S. Marteis, ‘Variation in temephos resistance in field populations of Aedes aegypti (Diptera: Culicidae) in the state of Sergipe, Northeast Brazil’, Rev. Soc. Bras. Med. Trop. 2018, 51, 284–290.
- 30A. Donini, M. J. O'Donnell, ‘Analysis of Na+, Cl−, K+, H+ and NH4+ concentration gradients adjacent to the surface of anal papillae of the mosquito Aedes aegypti: Application of self-referencing ion-selective microelectrodes’, J. Exp. Biol. 2005, 208, 603–610.
- 31Townson, ‘The biology of mosquitoes. Development, nutrition and reproduction. By A. N. Clements. (London: Chapman & Hall, 1992)’, Bull. Entomol. Res. 1993, 1.
- 32V. B. Wigglesworth, ‘The Storage of Protein, Fat, Glycogen and Uric Acid in the Fat Body and other Tissues of Mosquito Larvae’, J. Exp. Biol. 1942, 19, 56–77.
- 33J. T. Nishiura, C. Burgos, S. Aya, Y. Goryacheva, W. Lo, ‘Modulation of larval nutrition affects midgut neutral lipid storage and temporal pattern of transcription factor expression during mosquito metamorphosis’, J. Insect Physiol. 2007, 53, 47–58.
- 34T. F. Procópio, K. M. Fernandes, E. V. Pontual, R. M. Ximenes, A. R. C. de Oliveira, C. D. S. Souza, A. M. M. de A Melo, D. M. D. A. F. Navarro, P. M. G. Paiva, G. F. Martins, T. H. Napoleão, ‘Schinus terebinthifolius Leaf extract causes midgut damage, interfering with survival and development of Aedes aegypti larvae’, PLoS One. 2015, 10, 1–19.
- 35L. Shao, M. Devenport, M. Jacobs-Lorena, ‘The peritrophic matrix of hematophagous insects’, Arch. Insect Biochem. Physiol. 2001, 47, 119–125.
- 36T. M. Clark, A. Koch, D. F. Moffett, ‘The anterior and posterior ′stomach′ regions of larval Aedes aegypti midgut: regional specialization of ion transport and stimulation by 5-hydroxytryptamine’, J. Exp. Biol. 1999, 202, 247–52.
- 37A. C. M. Leódido, M. Ramalho-Ortigão, G. F. Martins, ‘The ultrastructure of the Aedes aegypti heart’, Arthropod Struct. Dev. 2013, 42, 539–550.
- 38S. Suwanmanee, U. Chaisri, L. Wasinpiyamongkol, N. Luplertlop, ‘Peritrophic membrane structure of Aedes aegypti (Diptera: Culicidae) mosquitoes after infection with dengue virus type 2 (D2-16681)’, Appl. Entomol. Zool. 2009, 44, 257–265.
- 39S. R. Whiten, W. Keith Ray, R. F. Helm, Z. N. Adelman, ‘Characterization of the adult Aedes aegypti early midgut peritrophic matrix proteome using LC/MS’, PLoS One. 2018, 13, 1–17.
- 40K. M. Fernandes, C. A. Neves, J. E. Serrão, G. F. Martins, ‘Aedes aegypti midgut remodeling during metamorphosis’, Parasitol. Int. 2014, 63, 506–512.
- 41K. Buch, T. Peters, T. Nawroth, M. Sänger, H. Schmidberger, P. Langguth, ‘Determination of cell survival after irradiation via clonogenic assay versus multiple MTT Assay – A comparative study’, Radiat. Oncol. 2012, 7, 1–6.
- 42R. Z. Behar, W. Luo, K. J. McWhirter, J. F. Pankow, P. Talbot, ‘Analytical and toxicological evaluation of flavor chemicals in electronic cigarette refill fluids’, Sci. Rep. 2018, 8, 1–11.
- 43R. Apriani, F. F. Abdullah, ‘Cytotoxic Activity of Ethyl-para-methoxycinnamate from Kaempferia galanga L. on A549 Lung Cancer and B16 Melanoma Cancer Cells’, Jurnal Kimia Sains dan Aplikasi 2021, 1, 22–28.
10.14710/jksa.24.1.22-28 Google Scholar
- 44X.-Y. Meng, H.-X. Zhang, M. Mezei, M. Cui, ‘Molecular Docking: A Powerful Approach for Structure-Based Drug Discovery’, Curr. Comput.-Aided Drug Des. 2012, 7, 146–157.
- 45E. Mongin, C. Louis, R. A. Holt, E. Birney, F. H. Collins, ‘The Anopheles gambiae genome: An update’, Trends Parasitol. 2004, 20, 49–52.
- 46A. Mori, N. F. Lobo, B. deBruyn, D. W. Severson, ‘Molecular cloning and characterization of the complete acetylcholinesterase gene (Ace1) from the mosquito Aedes aegypti with implications for comparative genome analysis’, Insect Biochem. Mol. Biol. 2007, 37, 667–674.
- 47C. Camacho, G. Coulouris, V. Avagyan, et al., ‘BLAST+: architecture and applications’, BMC Bioinf. 2009, 10, 421.
- 48J. P. Salo, A. Yliniemelä, J. Taskinen, ‘Parameter refinement for molecular docking’, J. Chem. Inf. Comput. Sci. 1998, 38, 832–839.
- 49G. Madhavi Sastry, M. Adzhigirey, T. Day, R. Annabhimoju, W. Sherman, ‘Protein and ligand preparation: Parameters, protocols, and influence on virtual screening enrichments’, J. Comput.-Aided Mol. Des. 2013, 27, 221–234.
- 50J. Cheung, A. Mahmood, R. Kalathur, L. Liu, P. R. Carlier, ‘Structure of the G119S Mutant Acetylcholinesterase of the Malaria Vector Anopheles gambiae Reveals Basis of Insecticide Resistance’, Structure 2018, 26, 130–136.
- 51J. Dutta, D. K. Sahoo, S. Jena, K. D. Tulsiyan, H. S. Biswal, ‘Non-covalent interactions with inverted carbon: a carbo-hydrogen bond or a new type of hydrogen bond?’, Phys. Chem. Chem. Phys. 2020, 22, 8988–8997.
- 52A. Basiri, M. Xiao, A. McCarthy, D. Dutta, S. N. Byrareddy, M. Conda-Sheridan, ‘Design and synthesis of new piperidone grafted acetylcholinesterase inhibitors’, Bioorg. Med. Chem. Lett. 2017, 27, 228–231.
- 53B. R. de Lima, J. M. Lima, J. B. Maciel, C. Q. Valentim, R. de C. S. Nunomura, E. S. Lima, H. H. F. Koolen, A. D. L. de Souza, M. L. B. Pinheiro, Q. B. Cass, F. M. A. da Silva, ‘Synthesis and Inhibition Evaluation of New Benzyltetrahydroprotoberberine Alkaloids Designed as Acetylcholinesterase Inhibitors’, Front. Chem. 2019, 7, 1–12.
- 54C. Y. Jia, F. Wang, G. F. Hao, G. F. Yang, ‘InsectiPAD: A Web Tool Dedicated to Exploring Physicochemical Properties and Evaluating Insecticide-Likeness of Small Molecules’, J. Chem. Inf. Model. 2019, 59 630–635.
- 55J. E. Webb, R. A. Green, ‘On the penetration of insecticides through the insect cuticle’, J. Exp. Biol. 1945, 22, 8–20.
- 56G. Hao, Q. Dong, G. Yang, ‘A comparative study on the constitutive properties of marketed pesticides’, Mol. Inf. 2011, 30, 614–622.
- 57D. Belsito, D. Bickers, M. Bruze, P. Calow, H. Greim, J. M. Hanifin, A. E. Rogers, J. H. Saurat, I. G. Sipes, H. Tagami, ‘A toxicologic and dermatologic assessment of related esters and alcohols of cinnamic acid and cinnamyl alcohol when used as fragrance ingredients’, Food Chem. Toxicol. 2007, 45, s21–s23.
- 58P. Lorenzo, J. Reboredo-Durán, L. Muñoz, H. Freitas, L. González, ‘Herbicidal properties of the commercial formulation of methyl cinnamate, a natural compound in the invasive silver wattle (Acacia dealbata)’, Weed Sci. 2019, 68, 69–78.
- 59B. C. Smale, N. J. Lasater, B. T. Hunter, ‘Fate and Metabolism of Dimethyl Sulfoxide in Agricultural Crops’, Ann. N. Y. Acad. Sci. 1975, 243, 228–236.
- 60H. Ratsch, ‘Interlaboratory Root Elongation Testing Of Toxic Substances On Selected Plant Species’, United States Environmental Protection Agency 1983, EPA-600/S3-83-051.
- 61A. Al-Maskri, L. Al-Kharusi, H. Al-Miqbali, M. M. Khan, ‘Effects of salinity stress on growth of lettuce (Lactuca sativa) under closed-recycle nutrient film technique’, Int. J. Agric. Biol. 2010, 12, 377–380.
- 62M. Sova, L. Saso, ‘Natural sources, pharmacokinetics, biological activities and health benefits of hydroxycinnamic acids and their metabolites’, Nutrients 2020, 12, 1–30.
- 63H. R. El-Seedi, A. M. A. El-Said, S. A. M. Khalifa, U. Göransson, L. Bohlin, A. K. Borg-Karlson, R. Verpoorte, ‘Biosynthesis, natural sources, dietary intake, pharmacokinetic properties, and biological activities of hydroxycinnamic acids’, J. Agric. Food Chem. 2012, 60, 10877–10895.
- 64M. Narukawa, K. Kanbara, Y. Tominaga, Y. Aitani, K. Fukuda, T. Kodama, N. Murayama, Y. Nara, T. Arai, M. Konno, S. Kamisuki, F. Sugawara, M. Iwai, Y. Inoue, ‘Chlorogenic acid facilitates root hair formation in lettuce seedlings’, Plant Cell Physiol. 2009, 50, 504–514.
- 65C. Ozcan, ‘Determination of organochlorine pesticides in some vegetable samples using GC/MS’, Polish J. Environ. Stud. 2016, 25, 1141–1147.
- 66H. Bacha, M. Tekaya, S. Drine, F. Guasmi, L. Touil, H. Enneb, T. Triki, F. Cheour, A. Ferchichi, ‘Impact of salt stress on morpho-physiological and biochemical parameters of Solanum lycopersicum cv. Microtom leaves’, South African J. Bot. 2017, 108, 364–369.
- 67B. J. Young, N. I. Riera, M. E. Beily, P. A. Bres, D. C. Crespo, A. E. Ronco, ‘Toxicity of the effluent from an anaerobic bioreactor treating cereal residues on Lactuca sativa’, Ecotoxicol. Environ. Saf. 2012, 76, 182–186.
- 68Z. W. Yu, P. J. Quinn, ‘Dimethyl sulphoxide: A review of its applications in cell biology’, Biosci. Rep. 1994, 14, 259–281.
- 69S. W. Jacob, M. Bischel, R. J. Herschler, ‘Dimethyl Sulfoxide: Effects on the Permeability of Biologic Membranes (preliminary report)’, Curr Ther Res Clin Exp. 1964, 6, 193–8.
- 70J. J. Kocsis, S. Harkaway, R. Snyder, ‘Biological Effects of the Metabolites of Dimethyl Sulfoxide’, Ann. N. Y. Acad. Sci. 1975, 243, 104–109.
- 71L. A. Sciuchett, R. C. Iturrian, ‘Effects of dimethylsulfoxide (DMSO) and B995 on growth and metabolic products of Datura innoxia’, J. Pharm. Sci. 1965, 54, 1477–1480.
- 72J. P. Martínez, A. Antúnez, R. Pertuzé, M. D. P. Acosta, X. Palma, L. Fuentes, A. Ayala, H. Araya, S. Lutts, ‘Effects of saline water on water status, yield and fruit quality of wild (solanum chilense) and domesticated (solanum lycopersicum var. cerasiforme) tomatoes’, Exp. Agric. 2012, 48, 573–586.
- 73M. Al Hassan, M. Martínez Fuertes, F. J. Ramos Sánchez, O. Vicente, M. Boscaiu, ‘Effects of salt and water stress on plant growth and on accumulation of osmolytes and antioxidant compounds in cherry tomato’, Not. Bot. Horti Agrobot. Cluj-Napoca. 2015, 43, 1–11.
- 74M. Friedman, C. C. Tam, J. H. Kim, S. Escobar, S. Gong, M. Liu, X. Y. Mao, C. Do, I. Kuang, K. Boateng, J. Ha, M. Tran, S. Alluri, T. Le, R. Leong, L. W. Cheng, K. M. Land, ‘Anti-parasitic activity of cherry tomato peel powders’, Food 2021, 10, 1–15.
- 75F. Delgado-Vargas, L. Y. Sicairos-Medina, A. G. Luna-Mandujan, G. López-Angulo, N. Y. Salazar-Salas, M. O. Vega-García, J. B. Heredia, J. Á. López-Valenzuela, ‘Phenolic profiles, antioxidant and antimutagenic activities of Solanum lycopersicum var. Cerasiforme accessions from Mexico’, CyTA – J. Food. 2018, 16, 715–722.
- 76R. Kostka-Rick, W. J. Manning, ‘Radish (Raphanus sativus L.): A model for studying plant responses to air pollutants and other environmental stresses’, Environmental Pollution, 1993, 82, 107–138.
- 77K. M. Pirdosti, Z. Movahedi, M. Rostami, ‘Effect of cadmium stress on morpho-physiological traits in garden cress and radish in an aeroponic system’, Iran. J. Plant Physiol. 2019, 9, 2591–2599.
- 78R. Hjorth, C. Coutris, N. H. A. Nguyen, A. Sevcu, J. Alberto, A. Baun, E. J. Joner, ‘Ecotoxicity testing and environmental risk assessment of iron nanomaterials for subsurface remediation – Recommendations from the FP7 project NanoRem’, Chemosphere 2017, 182, 525–531.
- 79N. Zuverza-Mena, R. Armendariz, J. R. Peralta-Videa, J. L. Gardea-Torresdey, ‘Effects of silver nanoparticles on radish sprouts: Root growth reduction and modifications in the nutritional value’, Front. Plant Sci. 2016, 7, 1–11.
- 80C. Létondor, S. Pascal-Lorber, F. Laurent, ‘Uptake and distribution of chlordecone in radish: Different contamination routes in edible roots’, Chemosphere 2015, 118, 20–28.
