Investigation of the Molecular Mechanisms of Pesticide Action on the Photosynthetic Apparatus of Higher Plants and Algae

Abstract

This article presents an analysis of the mechanisms of action of the common pesticides thiamethoxam and its derivative clothianidin on the growth, morphology, and photosynthetic processes of plants and algae. A detailed analysis of the results of biophysical studies of the mechanism of changes in electron transport, transport, and morphology of chloroplasts in plants and algae under the influence of pesticides is presented. It is demonstrated for the first time that the local mechanism of action of thiamethoxam modifies the transfer of electrons from Q_Ā to the quinone pool (Ψ_Eo) and the functional activity of PSII (PI_ABS), while clothianidin modifies the rate of electron transfer between Q_A and Q_B, as well as the proportion of PSII centers that are unable to restore the quinone pool either by blocking electron transport or by reducing the rate of plastoquinone binding to Q_B. It has been established that clothianidin induces the formation of free radicals and alters the morphology, surface topography, and viscosity of chloroplast membranes. Changes in pigment content and properties under the influence of clothianidin on algae during a short incubation period (24 h) and a long (21 days) incubation period are different, but are accompanied by a cessation of cell growth, as well as a decrease in the F_V/F_M parameter and chlorophyll content. It has been shown that an increase in the number of cycles (the CL action--CL wash cycles) leads to a smaller decrease in the F_V/F_M value. According to the authors, the presence of chlorophyll in the cell is a key factor determining resistance

The work was carried out as part of the funding for Lomonosov MSU budget programs

Please cite this article in English as:

Maksimov G.V., Shutova V.V. Investigation of the molecular mechanisms of pesticide action on the photosynthetic apparatus of higher plants and algae. Herald of the Bauman Moscow State Technical University, Series Natural Sciences, 2026, no. 4 (127), pp. 74--96 (in Russ.). EDN: RJFLWU

References

[1] Gupta R. The oxygen-evolving complex: a super catalyst for life on earth, in response to abiotic stresses. Plant Signal Behav., 2020, vol. 15, no. 12, art. 1824721. DOI: https://doi.org/10.1080/15592324.2020.1824721

[2] Jeschke P., Nauen R., Schindler M., et al. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem., 2011, vol. 59, no. 7, pp. 2897--2908. DOI: https://doi.org/10.1021/jf101303g

[3] Radolinski J., Wu J., Xia K., et al. Plants mediate precipitation-driven transport of a neonicotinoid pesticide. Chemosphere, 2019, vol. 222, pp. 445--452. DOI: https://doi.org/10.1016/j.chemosphere.2019.01.150

[4] Macedo W.R., Araujo D.K., de Camargo e Castro P.R. Unravelling the physiologic and metabolic action of thiamethoxam on rice plants. Pestic. Biochem. Physiol., 2013, vol. 107, no. 2, pp. 244--249. DOI: https://doi.org/10.1016/j.pestbp.2013.08.001

[5] Larsen R.J., Falk D.E. Effects of a seed treatment with a neonicotinoid insecticide on germination and freezing tolerance of spring wheat seedlings. Can. J. Plant Sci., 2013, vol. 93, no. 3, pp. 535--540. DOI: https://doi.org/10.4141/CJPS2012-127

[6] Cataneo A.C., Ferreira L.C., Carvalho J.C., et al. Improved germination of soybean seed treated with thiamethoxam under drought conditions. Seed Sci. Technol., 2010, vol. 38, no. 1, pp. 248--251. DOI: https://doi.org/10.15258/sst.2010.38.1.27

[7] Preetha G., Stanley J. Influence of neonicotinoid insecticides on the plant growth attributes of cotton and okra. J. Plant Nutr., 2012, vol. 35, no. 8, pp. 1234--1245. DOI: https://doi.org/10.1080/01904167.2012.676134

[8] Xia X.J., Huang Y.Y., Wang L., et al. Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pestic. Biochem. Physiol., 2006, vol. 86, no. 1, pp. 42--48. DOI: https://doi.org/10.1016/j.pestbp.2006.01.005

[9] Aksoy O., Deveci A., Sibel K., et al. Phytotoxic effect of Quizalofop-P-Ethyl on Soybean (Glycine max L.). J. Biol. Environ. Sci., 2013, vol. 7, no. 19, pp. 49--55.

[10] Shakir S. K., Irfan S., Akhtar B., et al. Pesticide-induced oxidative stress and antioxidant responses in tomato (Solanum Lycopersicon) seedlings. Ecotoxicology, 2018, vol. 27, no. 7, pp. 919--935. DOI: https://doi.org/10.1007/S10646-018-1916-6

[11] Touzout N., Mehallah H., Moralent R., et al. Phytotoxic evaluation of neonicotinoid imidacloprid and cadmium alone and in combination on tomato (Solanum Lycopersicon L.). Ecotoxicology, 2021, vol. 30, no. 6, pp. 1126--1137. DOI: https://doi.org/10.1007/s10646-021-02421-6

[12] Todorenko D.A., Slatinskaya O.V., Hao J., et al. Photosynthetic pigments and phytochemical activity of photosynthetic apparatus of maize (Zea mays L.) leaves under the effect of thiamethoxam. Selskokhozyaystvennaya biologiya [Agricultural Biology], 2020, vol. 55, no. 1, pp. 66--76 (in Russ.). DOI: https://doi.org/10.15389/agrobiology.2020.1.66rus

[13] Todorenko D.A., Hao J., Slatinskaya O.V., et al. Effect of thiamethoxam on photosynthetic pigments and primary photosynthetic reactions in two maize genotypes (Zea mays). Funct. Plant Biol., 2021, vol. 48, no. 10, pp. 994--1004. DOI: https://doi.org/10.1071/FP21134

[14] Hao J. Issledovanie molekulyarnykh mekhanizmov deystviya pestitsidov na fotosinteticheskiy apparat vysshikh rasteniy. Dis. kand. biol. nauk [Study of the molecular mechanisms of pesticide action on the photosynthetic apparatus of higher plants. Cand. Sc. (Biol.) Diss.]. Moscow, MSU, 2025 (in Russ.).

[15] Volgusheva A.A., Hao J., He Y., et al. Effect of the insecticide clothianidin on the photosynthetic electron transport chain in pea. Photochem Photobiol., 2024, vol. 101, no. 3, pp. 580--591. DOI: https://doi.org/10.1111/php.14018

[16] Radenovich C.N., Maksimov G.V., Shutova V.V., et al. Using infrared spectroscopy and raman spectroscopy to evaluate the conformation of biomolecules in maize (Zea mays L.) lines. Selskokhozyaystvennaya biologiya [Agricultural Biology], 2021, vol. 56, no. 5, pp. 948--957 (in Russ.). DOI: https://doi.org/10.15389/agrobiology.2021.5.948rus

[17] Strasser R. J., Tsimilli-Michael M., Srivastava A. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G.C., Govindjee (eds). Chlorophyll a Fluorescence. Advances in Photosynthesis and Respiration, vol. 19. Dordrecht, Springer, 2004, pp. 321--362. DOI: https://doi.org/10.1007/978-1-4020-3218-9_12

[18] Volgusheva A.A., Petrova E.V., Kukarskikh G.P., et al. Influence of fermentation reactions on continuous hydrogen photoproduction by microalga Chlamydomonas reinhardtii under sulfur deficiency. Moscow Univ. Biol. Sci. Bull., 2022, vol. 77, no. 1, pp. 25--31. DOI: https://doi.org/10.3103/S0096392522010060/FIGURES/2

[19] Curtis V.A., Brand J.J., Togasaki R.K. Partial reactions of photosynthesis in briefly sonicated Chlamydomonas: I. Cell breakage and electron transport activities. Plant Physiol., 1975, vol. 55, no. 2, pp. 183--196. DOI: https://doi.org/10.1104/PP.55.2.183

[20] Lovyagina E.R., Davletshina L.N., Semin B.K. Peculiarities of Mn(II) cation oxidation in the photosystem II without an oxygen-evolving complex:evolutionary aspect. Moscow Univ. Biol. Sci. Bull., 2022, vol. 77, no. 2, pp. 92--97. DOI: https://doi.org/10.3103/S0096392522020055

[21] Schreier-Muccillo S., Marsh D., Smith I.C.P. Monitoring the permeability profile of lipid membranes with spin probes. Arch. Biochem. Biophys., 1976, vol. 172, no. 1, pp. 1--11. DOI: https://doi.org/10.1016/0003-9861(76)90041-2

[22] Radenovic C.N., Maksimov G.V., Kuramshina G.M., et al. Use of internal reflection spectroscopy for maize (Zea mays L.) Grain diagnosis. Selskokhozyaystvennaya biologiya [Agricultural Biology], 2022, vol. 57, no. 5, pp. 933--944 (in Russ.). DOI: https://doi.org/10.15389/agrobiology.2022.5.933rus

[23] Liu W., Shutova V.V., Maksimov G.V., et al. Use of nanostructured silver substrates (coatings) to study the content and conformation of β-carotene. Herald of the Bauman Moscow State Technical University, Series Natural Sciences, 2022, no. 2 (101), pp. 112--124. DOI: https://doi.org/10.18698/1812-3368-2022-2-112-124

[24] Parshina E.Yu., Samoylenko A.A., Maksimov G.V., et al. Integrated approach to studying pigment morphology and distribution in the algae cell. Herald of the Bauman Moscow State Technical University, Series Natural Sciences, 2024, no. 2 (113), pp. 129--148 (in Russ.). EDN: NBOFMH

[25] Volgusheva A.A., He Y., Maksimov G.V., et al. The resistance of Chlamydomonas reinhardtii cells to the neonicotinoid clothianidin. Ecotoxicology, 2025, vol. 34, no. 6, pp. 1105--1115. DOI: https://doi.org/10.1007/s10646-025-02899-4

[26] Henrysson T., Sundby C. Characterization of photosystem II in stroma thylakoid membranes. Photosynth. Res., 1990, vol. 25, no. 2, pp. 107--117. DOI: https://doi.org/10.1007/BF00035459/METRICS

[27] Kalaji H.M., Jajoo A., Oukarroum A., et al. The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. In: Emerging Technologies and Management of Crop Stress Tolerance, vol. 2. Academic Press, 2014, pp. 347--384. DOI: https://doi.org/10.1016/B978-0-12-800875-1.00015-6

[28] Pinnola A., Bassi R. Molecular mechanisms involved in plant photoprotection. Biochem. Soc. Trans., 2018, vol. 46, no. 2, pp. 467--482. DOI: https://doi.org/10.1042/BST20170307

[29] Chuartzman S.G., Nevo R., Shimoni E., et al. Thylakoid membrane remodeling during state transitions in Arabidopsis. The Plant Cell, 2008, vol. 20, no. 4, pp. 1029--1039. DOI: https://doi.org/10.1105/TPC.107.055830