Effect of thiamethoxam on photosynthetic pigments and primary photosynthetic reactions in two maize genotypes (Zea mays)
Daria A. Todorenko A , Jingrao Hao A , Olga V. Slatinskaya A , Elvin S. Allakhverdiev A B , Venera V. Khabatova C , Aleksey D. Ivanov D , Cedomir N. Radenovic E F , Dmitry N. Matorin A , Saleh Alwasel G , Georgy V. Maksimov A D I and Suleyman I. Allakhverdiev C G H IA Lomonosov Moscow State University, Faculty of Biology, Leninskie Gory, Moscow 119991, Russian Federation.
B Russian National Medical Research Centre of Cardiology, 3rd Cherepkovskaya Street, 15A, Moscow 121552, Russian Federation.
C KA Timiryazev Institute of Plant Physiology RAS, Botanicheskaya Street, 35, Moscow 127276, Russian Federation.
D Federal State Autonomous Educational Institution of Higher Education ‘National Research Technological University ‘MISiS’, Leninskiy Avenue 4, Moscow 119049, Russian Federation.
E Maise Research Institute, Zemun Polje, Belgrade, Republic of Serbia.
F University of Belgrade, Faculty of Physical Chemistry, Belgrade, Republic of Serbia.
G Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia.
H Institute of Basic Biological Problems RAS, Pushchino, Moscow Region 142290, Russian Federation.
I Corresponding authors. Email: suleyman.allakhverdiev@gmail.com; gmaksimov@mail.ru
Functional Plant Biology 48(10) 994-1004 https://doi.org/10.1071/FP21134
Submitted: 30 April 2021 Accepted: 2 June 2021 Published: 2 July 2021
Abstract
Neonicotinoid insecticides are used against the wide range of pests to protect plants. The influence of neonicotinoids on target and non-target insects is well understood. Hence, there are controversial opinions about the effect of neonicotinoids on the plants. We investigated pigments and photosynthetic primary reactions in two maize genotypes (the inbred line zppl 225 and hybrid zp 341) under thiamethoxam (TMX) treatment by root irrigation. It was found that the effect of TMX depended on pesticide application techniques and selection of maize genotype. TMX was added to the soil by root irrigation on the 4th and 8th days after planting, and photosynthetic characteristics monitored on the 10th and 12th days after planting. The primary photochemical reactions in PSII (Fv/Fm) of both maize genotypes were not affected under two variants of TMX treatment during all growing period. The hybrid zp341 was shown to be more susceptible to both TMX treatments, demonstrating a decrease in photosynthetic characteristics (JIP-test parameters) as well as changes in the content of pigments and in the conformation of the carotenoid molecule. Our findings suggest that the combination of fluorescence method and Raman spectroscopy is a perspective tool for monitoring plant state under pesticide application.
Keywords: carotenoid, chlorophyll, chlorophyll fluorescence, maize, thiamethoxam, TMX, pesticide, Raman spectroscopy, neonicotinoid insecticides.
References
Aksoy Ö, Deveci A, Sibel K, Akdeniz GB (2013) Phytotoxic effect of Quizalofop-P-Ethyl on soybean (Glycine max L.). Journal of Biological & Environmental Sciences 7, 49–55.Aliyeva NK, Aliyeva DR, Suleymanov SY, Rzayev FH, Gasimov EK, Huseynova IM (2020) Biochemical properties and ultrastructure of mesophyll and bundle sheath thylakoids from maize (Zea mays) chloroplasts. Functional Plant Biology 47, 970–976.
| Biochemical properties and ultrastructure of mesophyll and bundle sheath thylakoids from maize (Zea mays) chloroplasts.Crossref | GoogleScholarGoogle Scholar | 32574552PubMed |
Allakhverdiev SI (2020) Optimising photosynthesis for environmental fitness. Functional Plant Biology 47, iii–vii.
| Optimising photosynthesis for environmental fitness.Crossref | GoogleScholarGoogle Scholar | 33046183PubMed |
Bialek-Bylka GE, Hiyama T, Yumoto K, Koyama Y (1996) 15-Cis-β-carotene found in the reaction center of spinach Photosystem I. Photosynthesis Research 49, 245–250.
| 15-Cis-β-carotene found in the reaction center of spinach Photosystem I.Crossref | GoogleScholarGoogle Scholar | 24271702PubMed |
Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EA, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research International 22, 35–67.
| Environmental fate and exposure; neonicotinoids and fipronil.Crossref | GoogleScholarGoogle Scholar | 25096486PubMed |
Calafiori MH, Barbieri AA (2001) Effects of seed treatment with insecticide on the germination, nutrients, nodulation, yield and pest control in bean (Phaseolus vulgaris L.) culture. Ecossistema 26, 97–104.
Cataneo AC, Ferreira LC, Carvalho JC, Andréo-Souza Y, Corniani N, Mischan MM, Nunes JC (2010) Improved germination of soybean seed treated with thiamethoxam under drought conditions. Seed Science and Technology 38, 248–251.
| Improved germination of soybean seed treated with thiamethoxam under drought conditions.Crossref | GoogleScholarGoogle Scholar |
DeLorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic microorganisms: A review. Environmental Toxicology and Chemistry 20, 84–98.
| Toxicity of pesticides to aquatic microorganisms: A review.Crossref | GoogleScholarGoogle Scholar | 11351418PubMed |
Denholm I, Devine G, Foster S, Gorman K, Nauen R (2002) Incidence and management of insecticide resistance to neonicotinoids. In ‘The Proceedings of the International Brighton Crop Protection Conference – Pests and Diseases 1, 161. (British Crop Protection Council: Brighton, UK)
El-Naggar JB, Zidan NA (2013) Field evaluation of imidacloprid and thiamethoxam against sucking insects and their side effects on soil fauna. Journal of Plant Protection Research 53,
| Field evaluation of imidacloprid and thiamethoxam against sucking insects and their side effects on soil fauna.Crossref | GoogleScholarGoogle Scholar |
Ford KA, Casida JE, Chandran D, Gulevich AG, Okrent RA, Durkin KA, Sarpong R, Bunnelle EM, Wildermuth MC (2010) Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proceedings of the National Academy of Sciences of the United States of America 107, 17527–17532.
| Neonicotinoid insecticides induce salicylate-associated plant defense responses.Crossref | GoogleScholarGoogle Scholar | 20876120PubMed |
Ge J, Cui K, Yan H, Li Y, Chai Y, Liu X, Cheng J, Yu X (2017) Uptake and translocation of imidacloprid, thiamethoxam and difenoconazole in rice plants. Environmental Pollution 226, 479–485.
| Uptake and translocation of imidacloprid, thiamethoxam and difenoconazole in rice plants.Crossref | GoogleScholarGoogle Scholar | 28454637PubMed |
Goltsev V, Chernev P, Zaharieva I, Lambrev P, Strasser RJ (2005) Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range. Photosynthesis Research 84, 209–215.
| Kinetics of delayed chlorophyll a fluorescence registered in milliseconds time range.Crossref | GoogleScholarGoogle Scholar | 16049776PubMed |
Goltsev V, Zaharieva I, Chernev P, Strasser RJ (2009) Delayed chlorophyll fluorescence as a monitor for physiological state of photosynthetic apparatus. Biotechnology & Biotechnological Equipment 23, 452–457.
| Delayed chlorophyll fluorescence as a monitor for physiological state of photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |
Goltsev VN, Kalaji HM, Paunov M, Baba V, Horaczek T, Moyski J, Kozel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 63, 869–893.
| Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus.Crossref | GoogleScholarGoogle Scholar |
Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology 50, 977–987.
| An overview of the environmental risks posed by neonicotinoid insecticides.Crossref | GoogleScholarGoogle Scholar |
Govindjee G, Papageorgiou G (2004) ‘Chlorophyll a fluorescence: a signature of photosynthesis. Vol. 1908.’ (Springer: Dordrecht)
Gupta S, Gajbhiye VT, Gupta RK (2008) Soil dissipation and leaching behavior of a neonicotinoid insecticide thiamethoxam. Bulletin of Environmental Contamination and Toxicology 80, 431–437.
| Soil dissipation and leaching behavior of a neonicotinoid insecticide thiamethoxam.Crossref | GoogleScholarGoogle Scholar | 18431522PubMed |
Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry 59, 2897–2908.
| Overview of the status and global strategy for neonicotinoids.Crossref | GoogleScholarGoogle Scholar | 20565065PubMed |
Kalaji HM, Goltsev VN, Żuk-Gołaszewska K, Zivcak M, Brestic M (2017) ‘Chlorophyll fluorescence: understanding crop performance – basics and applications.’ (CRC Press: Boca Raton)
Kanne DB, Dick RA, Tomizawa M, Casida JE (2005) Neonicotinoid nitroguanidine insecticide metabolites: Synthesis and nicotinic receptor potency of guanidines, aminoguanidines, and their derivatives. Chemical Research in Toxicology 18, 1479–1484.
| Neonicotinoid nitroguanidine insecticide metabolites: Synthesis and nicotinic receptor potency of guanidines, aminoguanidines, and their derivatives.Crossref | GoogleScholarGoogle Scholar | 16167841PubMed |
Kilic S, Duran RE, Coskun Y (2015) Morphological and physiological responses of maize (Zea mays L.) seeds grown under increasing concentrations of chlorantraniliprole insecticide. Polish Journal of Environmental Studies 24, 1069–1075.
| Morphological and physiological responses of maize (Zea mays L.) seeds grown under increasing concentrations of chlorantraniliprole insecticide.Crossref | GoogleScholarGoogle Scholar |
Kish E, Wang K, Llansola-Portoles MJ, Ilioaia C, Pascal AA, Robert B, Yang C (2016) Probing the pigment binding sites in LHCII with resonance Raman spectroscopy: The effect of mutations at S123. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 1490–1496.
| Probing the pigment binding sites in LHCII with resonance Raman spectroscopy: The effect of mutations at S123.Crossref | GoogleScholarGoogle Scholar |
Koyama Y, Takatsuka I, Nakata M, Tasumi M (1988) Raman and infrared spectra of the all‐trans, 7‐cis, 9‐cis, 13‐cis and 15‐cis isomers of β‐carotene: Key bands distinguishing stretched or terminal‐bent configurations form central‐bent configurations. Journal of Raman Spectroscopy : JRS 19, 37–49.
| Raman and infrared spectra of the all‐trans, 7‐cis, 9‐cis, 13‐cis and 15‐cis isomers of β‐carotene: Key bands distinguishing stretched or terminal‐bent configurations form central‐bent configurations.Crossref | GoogleScholarGoogle Scholar |
Larsen RJ, Falk DE (2013) Effects of a seed treatment with a neonicotinoid insecticide on germination and freezing tolerance of spring wheat seedlings. Canadian Journal of Plant Science 93, 535–540.
| Effects of a seed treatment with a neonicotinoid insecticide on germination and freezing tolerance of spring wheat seedlings.Crossref | GoogleScholarGoogle Scholar |
Macedo WR, de Camargo e Castro PR (2011) Thiamethoxam: Molecule moderator of growth, metabolism and production of spring wheat. Pesticide Biochemistry and Physiology 100, 299–304.
| Thiamethoxam: Molecule moderator of growth, metabolism and production of spring wheat.Crossref | GoogleScholarGoogle Scholar |
Macedo WR, Araújo DK, de Camargo e Castro PR (2013) Unravelling the physiologic and metabolic action of thiamethoxam on rice plants. Pesticide Biochemistry and Physiology 107, 244–249.
| Unravelling the physiologic and metabolic action of thiamethoxam on rice plants.Crossref | GoogleScholarGoogle Scholar |
Macernis M, Galzerano D, Sulskus J, Kish E, Kim YH, Koo S, Valkunas L, Robert B (2015) Resonance Raman spectra of carotenoid molecules: Influence of methyl substitutions. The Journal of Physical Chemistry A 119, 56–66.
| Resonance Raman spectra of carotenoid molecules: Influence of methyl substitutions.Crossref | GoogleScholarGoogle Scholar | 25476500PubMed |
Maienfisch P, Angst M, Brandl F, Fischer W, Hofer D, Kayser H, Kobel W, Rindlisbacher A, Senn R, Steinemann A, Widmer H (2001a) Chemistry and biology of thiamethoxam: A second generation neonicotinoid. Pest Management Science 57, 906–913.
| Chemistry and biology of thiamethoxam: A second generation neonicotinoid.Crossref | GoogleScholarGoogle Scholar | 11695183PubMed |
Maienfisch P, Huerlimann H, Rindlisbacher A, Gsell L, Dettwiler H, Haettenschwiler J, Sieger E, Walti M (2001b) The discovery of thiamethoxam: a second-generation neonicotinoid. Pest Management Science 57, 165–176.
| The discovery of thiamethoxam: a second-generation neonicotinoid.Crossref | GoogleScholarGoogle Scholar | 11455647PubMed |
Natalia TG, Robert MH (2016) Lifecycle assessment of neonicotinoid pesticides. Journal of Fertilizers & Pesticides 7, 165
| Lifecycle assessment of neonicotinoid pesticides.Crossref | GoogleScholarGoogle Scholar |
Preetha G, Stanley J (2012) Influence of neonicotinoid insecticides on the plant growth attributes of cotton and okra. Journal of Plant Nutrition 35, 1234–1245.
| Influence of neonicotinoid insecticides on the plant growth attributes of cotton and okra.Crossref | GoogleScholarGoogle Scholar |
Radenović ČN, Maksimov GV, Tyutyaev EV, Stanković GJ, Jovanović ŽV, Beljanski MV (2014) Detecting the phase transition in thylakoid membranes of maize inbred lines by means of delayed fluorescence. Plant Physiology and Biochemistry 81, 208–211.
| Detecting the phase transition in thylakoid membranes of maize inbred lines by means of delayed fluorescence.Crossref | GoogleScholarGoogle Scholar | 24836446PubMed |
Radolinski J, Wu J, Xia K, Stewart R (2018) Transport of a neonicotinoid pesticide, thiamethoxam, from artificial seed coatings. The Science of the Total Environment 618, 561–568.
| Transport of a neonicotinoid pesticide, thiamethoxam, from artificial seed coatings.Crossref | GoogleScholarGoogle Scholar | 29156230PubMed |
Robert B (2009) Resonance Raman spectroscopy. Photosynthesis Research 101, 147–155.
| Resonance Raman spectroscopy.Crossref | GoogleScholarGoogle Scholar | 19568956PubMed |
Saito S, Mitsuo T (1983) Normal coordinate analysis of p‐nitrobenzaldehyde and assignments of infrared and Raman bands. Journal of Raman Spectroscopy : JRS 20, 263–266.
Salares VR, Young NM, Carey PR, Bernstein HJ (1977) Excited state (excitation) interactions in polyene aggregates. Resonance Raman and absorption spectroscopic evidence. Journal of Raman Spectroscopy : JRS 6, 282–288.
| Excited state (excitation) interactions in polyene aggregates. Resonance Raman and absorption spectroscopic evidence.Crossref | GoogleScholarGoogle Scholar |
Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1706, 250–261.
| Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.Crossref | GoogleScholarGoogle Scholar |
Shakir SK, Kanwal M, Murad W, ur Rehman Z, ur Rehman S, Daud MK, Azizullah A (2016) Effect of some commonly used pesticides on seed germination, biomass production and photosynthetic pigments in tomato (Lycopersicon esculentum). Ecotoxicology (London, England) 25, 329–341.
| Effect of some commonly used pesticides on seed germination, biomass production and photosynthetic pigments in tomato (Lycopersicon esculentum).Crossref | GoogleScholarGoogle Scholar |
Shakir SK, Irfan S, Akhtar B, ur Rehman S, Daud MK, Taimur N, Azizullah A (2018) Pesticide-induced oxidative stress and antioxidant responses in tomato (Solanum lycopersicum) seedlings. Ecotoxicology (London, England) 27, 919–935.
| Pesticide-induced oxidative stress and antioxidant responses in tomato (Solanum lycopersicum) seedlings.Crossref | GoogleScholarGoogle Scholar |
Shutova VV, Tyutyaev EV, Veselova TV, Choob VV, Maksimov GV (2017) Dark adaptation and conformations of carotenoids in the cells of Cladophora aegagropila (L). Rabenh. Biophysics 62, 728–733.
| Dark adaptation and conformations of carotenoids in the cells of Cladophora aegagropila (L). Rabenh.Crossref | GoogleScholarGoogle Scholar |
Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, Mcfield M, Mineau P, Mitchell EA, Morrissey CA, Noome DA, Pisa L, Settele J, Stark JD, Tapparo A, Van Dyck H, Van Praagh J, Van Der Sluijs JP, Whitehorn PR, Wiemers M (2015) Systemic insecticides (Neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Environmental Science and Pollution Research International 22, 5–34.
| Systemic insecticides (Neonicotinoids and fipronil): Trends, uses, mode of action and metabolites.Crossref | GoogleScholarGoogle Scholar | 25233913PubMed |
Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology 104, 236–257.
| On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient.Crossref | GoogleScholarGoogle Scholar |
Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: A personal perspective of the thermal phase, the J-I-P rise. Photosynthesis Research 113, 15–61.
| Chlorophyll a fluorescence induction: A personal perspective of the thermal phase, the J-I-P rise.Crossref | GoogleScholarGoogle Scholar | 22810945PubMed |
Strasser RJ, Govindjee (1992) The F0 and the O-J-I-P fluorescence rise in higher plants and algae. In ‘Regulation of chloroplast biogenesis. Nato ASI Series (Series A: Life Sciences). Vol. 226’. (Ed. JH Argyroudi-Akoyunoglou) pp. 423–426. (Springer: Boston, MA)
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 321–362. (Springer: New York, USA)
Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1797, 1313–1326.
| Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis.Crossref | GoogleScholarGoogle Scholar |
Sur R, Stork A (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bulletin of Insectology 56, 35–40.
Tyutyaev EV, Shutova VV, Maksimov GV, Radenovich ChN, Grodzinskii DM (2015) State of photosynthetic pigments in hybrids and inbred lines of maize leaves. Fiziologiya rastenii i genetika 47, 147–159. [in Russian]
Vlasov AV, Maliar NL, Bazhenov SV, Nikelshparg EI, Brazhe NA, Vlasova AD, Osipov SD, Sudarev VV, Ryzhykau YL, Bogorodskiy AO, Zinovev EV, Rogachev AV, Manukhov IV, Borshchevskiy VI, Kuklin AI, Pokorn J, Sosnovtseva O, Maksimov GV, Gordeliy VI (2020) Raman scattering: from structural biology to medical applications. Crystals 10,
| Raman scattering: from structural biology to medical applications.Crossref | GoogleScholarGoogle Scholar |
von Wettstein D (1957) Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden (Chlorophyll lethals & submicroscopic morphological changes in plastids). Experimental Cell Research 12, 427–506.
| Chlorophyll-letale und der submikroskopische Formwechsel der Plastiden (Chlorophyll lethals & submicroscopic morphological changes in plastids).Crossref | GoogleScholarGoogle Scholar | 13437976PubMed | [in German]
Xia XJ, Huang YY, Wang L, Huang LF, Yu YL, Zhou YH, Yu JQ (2006) Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L. Pesticide Biochemistry and Physiology 86, 42–48.
| Pesticides-induced depression of photosynthesis was alleviated by 24-epibrassinolide pretreatment in Cucumis sativus L.Crossref | GoogleScholarGoogle Scholar |