Abstract
Winter rye (Secale cereale L. cv. Rushnik) seeds were treated with thidiazuron (TDZ; 0.01–10 nmol/L), a plant growth regulator (PGR) with cytokinin-like activity, and grown hydroponically for 7 days. The aim of pretreatment with TDZ was to try and mitigate herbicide-induced stress in winter rye plants. The leaves of 7-days-old seedlings were sprayed with 100 μM of paraquat (PQ), a herbicide, and biochemical and physiological responses were assessed after 4 or 8 h in fully developed leaves. After 8 h, PQ treatment significantly increased H2O2 and lipid peroxidation levels (39% increase for both relative to 0 h) as well as APOX activity (35% increase), but significantly decreased total antioxidant activity (33% decrease) and photosynthetic apparatus activity (up to 38% decrease), as assessed by chlorophyll fluorescence parameters. Pretreatment with TDZ weakened the toxic effects of PQ on rye seedlings, especially 8 h after PQ treatment. This was most evident for low doses (0.01 to 1 nmol/L) of TDZ. An index of efficiency indicated that 0.1 nmol/L TDZ was the most effective concentration to reduce the toxic effect of PQ on winter rye seedlings. This research provides fundamental information about the practical use of TDZ as a means to diminish the toxic effects of a herbicide (PQ) on cultivated winter rye plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data supporting the results of this study are available from the authors, but the availability of these data is subject to restrictions that were used on the recommendation of the Mordovian State University (Saransk, Russia) for this study and therefore are not publicly available. However, the data are available from the authors upon reasonable request and with the permission of the Mordovian State University.
Abbreviations
- AOA:
-
Antioxidative activity
- APOX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- ChlF:
-
Chlorophyll fluorescence
- DPPH:
-
2,2-Diphenyl-1-picrylhydrazyl
- F0 :
-
Minimum chlorophyll a fluorescence
- Fm :
-
Maximum chlorophyll a fluorescence
- Fv/Fm :
-
Maximum quantum yield of photosystem 2
- IE:
-
Efficiency index of the PGR
- LPO:
-
Lipid peroxidation
- MDA:
-
Malondialdehyde
- O2ˉ:
-
Superoxide
- PGR:
-
Plant growth regulator
- POX:
-
Guaiacol peroxidase
- PQ:
-
Paraquat
- PSA:
-
Photosynthetic apparatus
- PSI:
-
Photosystem 1
- PSII:
-
Photosystem 2
- qP:
-
Coefficient of photochemical quenching of ChlF
- ROS:
-
Reactive oxygen species
- TBA:
-
Thiobarbituric acid
- TCA:
-
Trichloroacetic acid
- TDZ:
-
Thidiazuron
- Y(II):
-
The effective photochemical quantum yield of PSII
- Y(NPQ):
-
The non-photochemical light-induced quenching of ChlF
References
Abedi T, Pakniyat H (2010) Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J Genet Plant Breed 46:27–34. https://doi.org/10.17221/67/2009-CJGPB
Akter N, Islam MR, Karim MA, Hossain T (2014) Alleviation of drought stress in maize by exogenous application of gibberellic acid and cytokinins. J Crop Sci Biotech 17:41–48. https://doi.org/10.1007/s12892-013-0117-3
Ali A, Malangisha GK, Yang H, Li C, Wang C, Yang Y, Mahmoud A, Khan J, Yang J, Hu Z, Zhang M (2021) Strigolactone alleviates herbicide toxicity via maintaining antioxidant homeostasis in watermelon (Citrullus lanatus). Agriculture 11:419. https://doi.org/10.3390/agriculture11050419
Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159:685–693. https://doi.org/10.1078/017616102400375296
Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2015) Lipids and proteins – major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121. https://doi.org/10.1007/s11356-014-3917-1
Anjum NA, Sharma P, Gill SS, Hasanuzzaman M, Khan EA, Mohamed AA, Kachhap K, Thangavel P, Devi GD, Vasudhevan P, Sofo A, Khan NA, Misra AN, Lukatkin AS, Singh HP, Pereira EA, Tuteja N (2016) Catalase and ascorbate peroxidase—representative H2O2-detoxifying haeme enzymes in plants. Environ Sci Pollut Res 23:19002–19029. https://doi.org/10.1007/s11356-016-7309-6
Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Asgher M, Khan MI, Anjum NA, Khan NA (2015) Minimising toxicity of cadmium in plants—role of plant growth regulators. Protoplasma 252:399–413. https://doi.org/10.1007/s00709-014-0710-4
Avalbaev A, Allagulova C, Maslennikova D, Fedorova K, Shakirova F (2021) Methyl jasmonate and cytokinin mitigate the salinity-induced oxidative injury in wheat seedlings. J Plant Growth Regul 40:1741–1752. https://doi.org/10.1007/s00344-020-10221-1
Bakshi P, Bali S, Kaur P, Khajuria A, Khanna K, Mir BA, Ohri P, Bhardwaj R (2020) Pesticide toxicity amelioration in plants by plant hormones. In: Singh VP, Singh A, Tripathi DK, Singh S, Prasad SM, Chauhan DK (eds) Pesticides in crop production Physiological and Biochemical Action. John Wiley & Sons Ltd, USA, pp 233–258. https://doi.org/10.1002/9781119432241
Bashmakov DI, Lukatkin AS, Miliauskienė J, Duchovskienė L, Duchovskis P (2021) The efficiency of pre-treatment of maize seeds with plant growth regulators for resistance of maize seedlings to zinc ions. Zemdirbyste-Agriculture 108:125–132. https://doi.org/10.13080/z-a.2021.108.016
Belkadhi A, Haro AD, Soengas P, Obregon S, Cartea ME, Djebali W, Chaïbi W (2013) Salicylic acid improves root antioxidant defense system and total antioxidant capacities of flax subjected to cadmium. Omics J Integr Biol 17:398–406. https://doi.org/10.1089/omi.2013.0030
Bhandari S, Nailwal TK (2020) Role of brassinosteroids in mitigating abiotic stresses in plants. Biologia 75:2203–2230. https://doi.org/10.2478/s11756-020-00587-8
Bhattacharjee S (2014) Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr Sci 107:1811–1823
Bindschler LV, Minibaeva F, Gardner SL, Gerrish C, Davies DR, Bolwell GP (2001) Early signaling events in the apoplastic oxidative burst in suspension cultured French bean cells involve cAMP and Ca2+. New Phytol 151:185–194. https://doi.org/10.1046/j.1469-8137.2001.00170.x
Boutin C, Strandberg B, Carpenter D, Mathiassen SK, Thomas PJ (2014) Herbicide impact on non-target plant reproduction: What are the toxicological and ecological implications? Env Pollut 185:295–306. https://doi.org/10.1016/j.envpol.2013.10.009
Chagas RM, Silveira JAG, Ribeiro RV, Vitorello VAI, Carrer H (2008) Photochemical damage and comparative performance of superoxide dismutase and ascorbate peroxidase in sugarcane leaves exposed to paraquat-induced oxidative stress. Pest Biochem Physiol 90:181–188. https://doi.org/10.1016/j.pestbp.2007.11.006
Chiang YJ, Wu YX, Chiang MY, Wang CY (2008) Role of antioxidative system in paraquat resistance of tall fleabane (Conyza sumatrensis). Weed Sci 56:350–355. https://doi.org/10.1614/WS-07-153.1
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Env Exp Bot 109:212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021
dos Santos CM, de Almeida SM (2015) Physiological and biochemical responses of sugarcane to oxidative stress induced by water deficit and paraquat. Acta Physiol Plant 37:172. https://doi.org/10.1007/s11738-015-1935-3
Dwivedi SK, Arora A, Singh VP, Singh GP (2018) Induction of water deficit tolerance in wheat due to exogenous application of plant growth regulators: membrane stability, water relations and photosynthesis. Photosynthetica 56:478–486. https://doi.org/10.1007/s11099-017-0695-2
Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388. https://doi.org/10.1046/j.1469-8137.2000.00667.x
Ghahremani B, Hassannejad S, Alizadeh K, Eslam BP (2022) Salicylic acid alleviates oxidative stress and lipid peroxidation caused by clopyralid herbicide in Indian mustard plants. Acta Physiol Plant 44:49. https://doi.org/10.1007/s11738-022-03382-x
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
Goltsev VN, Kalaji HM, Paunov M, Bąba W, Horaczek T, Mojski J, Kociel H, Allakhverdiev SI (2016) Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus. Russian J Plant Physiol 63: 869–893. https://doi.org/10.1134/S1021443716050058
Gruznova KA, Bashmakov DI, Brazaitytė A, Duchovskis P, Lukatkin AS (2017) Efficiency index as the integral indicator of Triticum aestivum response to growth regulators. Zemdirbyste-Agriculture 104:299–304. https://doi.org/10.13080/z-a.2017.104.038
Haisel D, Pospíšilová J, Synková H, Schnablová R, Bat′kova P (2006) Effects of abscisic acid or benzyladenine on pigment contents, chlorophyll fluorescence, and chloroplast ultrastructure during water stress and after rehydration. Photosynthetica 44:606–614. https://doi.org/10.1007/s11099-006-0079-5
Hasanuzzaman M, Nahar K, Alam MM, Bhuyan MHMB, Oku H, Fujita M (2018) Exogenous nitric oxide pretreatment protects Brassica napus L. seedlings from paraquat toxicity through the modulation of antioxidant defense and glyoxalase systems. Plant Physiol Biochem 126:173–186. https://doi.org/10.1016/j.plaphy.2018.02.021
Hasanuzzaman M, Bhuyan MHMB, Parvin K, Bhuiyan TF, Anee TI, Nahar K, Hossen S, Zulfiqar F, Alam M, Fujita M (2020) Regulation of ROS metabolism in plants under environmental stress: a review of recent experimental evidence. Int J Mol Sci 21:8695. https://doi.org/10.3390/ijms21228695
Hassan NM, Alla MMN (2005) Oxidative stress in herbicide-treated broad bean and maize plants. Acta Phys Plant 27:429–438. https://doi.org/10.1007/s11738-005-0047-x
Huang J, Silva EN, Shen Z, Jiang B, Lu H (2012) Effects of glyphosate on photosynthesis, chlorophyll fluorescence and physicochemical properties of cogongrass (Imperata cylindrical L.). Plant Omics J 5:177–183
Juneau P, Qiu B, Deblois CP (2007) Use of chlorophyll fluorescence as a tool for determination of herbicide toxic effect: Review. Toxicol Env Chem 89:609–625. https://doi.org/10.1080/02772240701561569
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102. https://doi.org/10.1007/s11738-016-2113-y
Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, Losciale P, Mishra VK, Misra AN, Nebauer SG, Pancaldi S, Penella C, Pollastrini M, Suresh K, Tambussi E, Yanniccari M, Zivcak M, Cetner MD, Samborska IA, Stirbet A, Olsovska K, Kunderlikova K, Shelonzek H, Rusinowski S, Bąba W (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res 132:13–66. https://doi.org/10.1007/s11120-016-0318-y
Kour J, Kohli SK, Khanna K, Bakshi P, Sharma P, Singh AD, Ibrahim M, Devi K, Sharma N, Ohri P, Skalicky M, Brestic M, Bhardwaj R, Landi M, Sharma A (2021) Brassinosteroid signaling, crosstalk and physiological functions in plants under heavy metal stress. Front Plant Sci 12:608061. https://doi.org/10.3389/fpls.2021.608061
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218. https://doi.org/10.1023/B:PRES.0000015391.99477.0d
Lascano HR, Munoz N, Robert G, Rodríguez M, Melchiorre M, Trippi V, Quero G (2012) Paraquat: an oxidative stress inducer. In: Hasaneen MN (ed) Herbicides–properties, synthesis and control of weeds. InTech, UK, pp 135–148
Lukatkin AS (2002a) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 1. reactive oxygen species formation during plant chilling. Russ J Plant Physiol 49:622–627. https://doi.org/10.1023/A:1020232700648
Lukatkin AS (2002b) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 2. the activity of antioxidant enzymes during plant chilling. Russ J Plant Physiol 49:782–788. https://doi.org/10.1023/A:1020965629243
Lukatkin AS, Bashmakov DI, Kipaikina NV (2003) Protective role of thidiazuron treatment on cucumber seedlings exposed to heavy metals and chilling. Russ J Plant Physiol 50:305–307. https://doi.org/10.1023/A:1023857817284
Lukatkin AS, Gracheva NV, Grishenkova NN, Dukhovskis PV, Brazaitite AA (2007) Cytokinin-like growth regulators mitigate toxic action of zinc and nickel ions on maize seedlings. Russ J Plant Physiol 54:381–387. https://doi.org/10.1134/S1021443707030132
Lukatkin AS, Naraikina NV (2011) Assessing the effect of temperature stressors on maize plants from the change in antioxidative activity. Russ Agric Sci 37:364–366. https://doi.org/10.3103/S1068367411050168
Lukatkin AS, Garkova AN, Bochkarjova AS, Nushtaeva OV, Teixeira da Silva JA (2013) Treatment with the herbicide TOPIК induces oxidative stress in cereal leaves. Pest Biochem Physiol 105:44–49. https://doi.org/10.1016/j.pestbp.2012.11.006
Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: More than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386. https://doi.org/10.1093/pcp/pcv203
Mika A, Minibayeva F, Beckett R, Lüthje S (2004) Possible functions of extracellular peroxidases in stress-induced generation and detoxification of active oxygen species. Phytochem Rev 3:173–193. https://doi.org/10.1023/B:PHYT.0000047806.21626.49
Miyagawa Y, Tamoi M, Shigeoka S (2000) Evaluation of the defense system in chloroplasts to photooxidative stress caused by paraquat using transgenic tobacco plants expressing catalase from Escherichia coli. Plant Cell Physiol 41:311–320. https://doi.org/10.1093/pcp/41.3.311
Mohammadi H, Janmohammadi M, Sabaghnia N (2015) Chlorophyll fluorescence response of wheat to exogenous application of growth regulators under terminal drought stress. Ann Biol 70:13–27. https://doi.org/10.17951/c.2015.70.1.13
Mok MC, Mok DWS, Armstrong DJ, Shudo K, Isogai Y, Okamoto T (1982) Cytokinin activity of N-phenyl-N’-1,2,3-thiadiazol-5-ylurea (thidiazuron). Phytochemistry 21:1509–1511. https://doi.org/10.1016/S0031-9422(82)85007-3
Moustaka J, Moustakas M (2014) Photoprotective mechanism of the non-target organism Arabidopsis thaliana to paraquat exposure. Pest Biochem Physiol 111:1–6. https://doi.org/10.1016/j.pestbp.2014.04.006
Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953. https://doi.org/10.1111/j.1365-313X.2004.02092.x
Murthy BNS, Murch SJ, Saxena PK (1998) Thidiazuron: a potent regulator of in vitro plant morphogenesis. Vitro Cell Dev Biol Plant 34:267–275. https://doi.org/10.1007/BF02822732
Naeem M, Traub JR, Athar HR, Loescher W (2020) Exogenous calcium mitigates heat stress effects in common bean: A coordinated impact of photoprotection of PSII, up-regulating antioxidants, and carbohydrate metabolism. Acta Physiol Plant 42:180. https://doi.org/10.1007/s11738-020-03171-4
Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160. https://doi.org/10.1111/pce.12726
Preece JE, Huetteman CA, Ashby WC, Roth PL (1991) Micro- and cutting propagation of silver maple. I. results with adult and juvenile propagules. J Amer Soc Hort Sci 116:142–148. https://doi.org/10.2127/JASHS.116.1.142
Pütter J (1974) Peroxidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic Press, New York, pp 685–690
Semenova AS, Lukatkin AS (2015) Dual action of cytodef on stress effect of paraquat in winter rye plants. Russ J Plant Physiol 62:797–807. https://doi.org/10.1134/S102144371506014X
Sergiev IG, Alexieva VS, Ivanov SV, Moskova II, Karanov EN (2006) The phenylurea cytokinin 4PU-30 protects maize plants against glyphosate action. Pest Biochem Physiol 85:139–146. https://doi.org/10.1016/j.pestbp.2006.01.001
Sergiev I, Todorova D, Shopova E, Brankova L, Jankauskienė J, Jurkonienė S, Gavelienė V, Mockevičiūtė R (2020) Assessment of synthetic auxin type compounds as potential modulators of herbicide action in Pisum sativum L. Biologia 75:1845–1853. https://doi.org/10.2478/s11756-020-00557-0
Shahrtash M, Mohsenzadeh S, Mohabatkar H (2011) Salicylic acid alleviates paraquat oxidative damage in maize seedling. Asian J Exp Biol Sci 2:377–382
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037. https://doi.org/10.1155/2012/217037
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319. https://doi.org/10.1093/jexbot/53.372.1305
Strandberg B, Mathiassen SK, Bruus M, Kjaer C, Damgaard C, Andersen HV, Bossi R, Lofstrom P, Larsen SE, Bak J, Kudsk P (2012) Effects of herbicides on non-target plants: how do effects in standard plant tests relate to effects in natural habitats? Pesticide Research, Danish Ministry of the Environment, EPA, p 137
Todorova D, Sergiev I, Katerova Z, Shopova E, Dimitrova L, Brankova L (2021) Assessment of the biochemical responses of wheat seedlings to soil drought after application of selective herbicide. Plants 10:733. https://doi.org/10.3390/plants10040733
Varadi G, Darko E, Lehoczki E (2000) Changes in the xanthophyll cycle and fluorescence quenching indicate light-dependent early events in the action of paraquat and the mechanism of resistance to paraquat in Erigeron canadensis (L.) Cronq. Plant Physiol 123:1459–1470. https://doi.org/10.1104/pp.123.4.1459
Varshney S, Khan MIR, Masood A, Per TS, Rasheed F, Khan NA (2015) Contribution of plant growth regulators in mitigation of herbicidal stress. J Plant Biochem Physiol 3:4. https://doi.org/10.4172/2329-9029.1000160
Vineeth TV, Kumar P, Krishna GK (2016) Bioregulators protected photosynthetic machinery by inducing expression of photorespiratory genes under water stress in chickpea. Photosynthetica 54:234–242. https://doi.org/10.1007/s11099-016-0073-5
Wu D, Zhu J, Shu Z, Wang W, Yan C, Xu S, Wu D, Wang C, Dong Z, Sun G (2020) Physiological and transcriptional response to heat stress in heat-resistant and heat-sensitive maize (Zea mays L.) inbred lines at seedling stage. Protoplasma 257:1615–1637. https://doi.org/10.1007/s00709-020-01538-5
Yang D, Li Y, Shi Y, Cui Z, Luo Y, Zheng M, Chen J, Li Y, Yin Y, Wang Z (2016) Exogenous cytokinins increase grain yield of winter wheat cultivars by improving stay-green characteristics under heat stress. PLOS ONE 11:e0155437. https://doi.org/10.1371/journal.pone.0155437
Yonova P (2010) Design, synthesis and properties of synthetic cytokinins. recent advances on their application. General Appl Plant Physiol 36:124–147
Yonova P, Gateva S, Mincheva N, Jovchev G, Stergious M, Kapchina-Toteva V (2009) Improvement of tolerance to paraquat in barley (Hordeum vulgare L.) by a synthetic thiourea compound: Effects on growth and biochemical responses. General Appl Plant Physiol 35:162–171
Zhang L, Chen J, Zhang H, Ren Z, Luo P (2013) Effects of paraquat-induced oxidative stress on antioxidants and chlorophyll fluorescence in stay-green wheat (Triticum aestivum L.) flag leaves. Bangladesh J Bot 42:239–245. https://doi.org/10.3329/bjb.v42i2.18025
Acknowledgements
The authors thank Ms. Anastasija Sokolova for technical assistance during the preparation of this manuscript.
Funding
No funding was received to assist with the preparation of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by F. Araniti.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lukatkin, A.S., Semenova, A.S. & Teixeira da Silva, J.A. Treatment of winter rye (Secale cereale L.) seeds with thidiazuron mitigates the toxic response of seedlings to short-term treatment with a herbicide, paraquat. Acta Physiol Plant 45, 78 (2023). https://doi.org/10.1007/s11738-023-03565-0
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-023-03565-0