Abstract
Herbicides are used in agriculture to increase crop yield. However, their use often prompts concern about the consequences safety of crop production. Salicylic acid (SA) is a phenolic compound considered a phytohormone that confers plant resistance to different stresses. To determine the influence of SA on the reduction of herbicide-induced toxicity, we used young bean (Phaseolus vulgaris L.) seedlings treated with 1 mM of SA, 100 µM of prometryne or combined treatments. After 30 days of culture, prometryne treatment resulted in plant growth inhibition (shoot height, leaf area, fresh and dry weight) and decreased photosynthetic pigments content. It increased malondialdehyde (MDA) and hydrogen peroxide (H2O2) levels. Meanwhile, the activities of enzymatic antioxidants, catalase (CAT) and ascorbate peroxidase (APX), as well as herbicide detoxification enzyme glutathione S‑transferase (GST), were significantly improved. Furthermore, herbicide enhanced proline amount and decreased that of glutathione. These findings reflect the presence of stress status. An exogenous supply of SA seemed to reduce the deleterious effects caused by prometryne and appeared to overcome this stress status. Such positive effect was reflected by enhancement of growth and leaf pigments contents, regulating antioxidant enzyme activities (CAT, APX, GST), and decreasing oxidative stress indices. This study demonstrates that exogenous application of SA to young bean plants reversed and/or minimized the damage caused by prometryne through the protection and improvement of some morpho-biochemical characters.
Similar content being viewed by others
References
Ahmad F, Singh A, Kamal A (2017) Ameliorative effect of salicylic acid in salinity stressed Pisum sativum by improving growth parameters, activating photosynthesis and enhancing antioxidant defense system. Biosci Biotech Res Comm 10(3):481–489. https://doi.org/10.21786/bbrc/10.3/22
Ahmad F, Kamal A, Singh A, Ashfaque F, Alamri S, Siddiqui MH (2020) Salicylic acid modulates antioxidant system, defense metabolites, and expression of salt transporter genes in Pisum sativum under salinity stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10271-5
Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30:161–175. https://doi.org/10.3109/07388550903524243
Akbar N, Ehsanullah Jabran K, Ali MA (2011) Weed management improves yield and quality of direct seeded rice. Aust J Crop Sci 5(6):688–694
Akbulut GB, Yigit E, Bayram D (2015) Investigation of the effects of salicylic acid on some biochemical parameters in Zea mays to glyphosate herbicide. J Environ Anal Toxicol. https://doi.org/10.4172/2161-0525.1000271
Alia, Prasad KVSK, Pardha Saradhi P (1995) Effect of zinc on free radical and proline in Brassica juncea and Cajanus cajan. Phytochemistry 39:45–47. https://doi.org/10.1016/0031-9422(94)00919-K
Almeida AC, Gomes T, Langford K, Thomas KV, Tollefsen KE (2019) Oxidative stress potential of the herbicides bifenox and metribuzin in the microalgae Chlamydomonas reinhardtii. Aquat Toxicol 210:117–128. https://doi.org/10.1016/j.aquatox.2019.02.021
Ananieva EA, Alexieva VS, Popova LP (2002) Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J Plant Physiol 159(7):685–693. https://doi.org/10.1078/0176-1617-0706
Ananieva EA, Christov KN, Popova LP (2004) Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. J Plant Physiol 161(3):319–328. https://doi.org/10.1078/0176-1617-01022
Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82(10):1227–1238
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006
Azhir S, Abad HHS, Mobasser HR (2015) The effect of acetylsalicylic acid and calcium chloride on the vase life of cut flower Rose Samurai. Int J 7(1):668–672
Bayram D, Yigit E, Akbulut GB (2015) The effects of salicylic acid on Helianthus annuus L. exposed to quizalofop-P-ethyl. Am J Plant Sci 6:2412–2425. https://doi.org/10.4236/ajps.2015.614244
Belkhadi A, Hediji H, Abbes Z, Nouairi I, Barhoumi Z, Zarrouk M, Chaïbi W, Djebali W (2010) Effects of exogenous salicylic acid pre-treatment on cadmium toxicity and leaf lipid content in Linum usitatissimum L. Ecotoxicol Environ Saf 73:1004–1011. https://doi.org/10.1016/j.ecoenv.2010.03.009
Blair M, Gonzales LF, Kimani PM, Butare L (2010) Genetic diversity, inter-gene pool introgression and nutritional quality of common beans (Phaseolus vulgaris L.) from central africa. Theor Appl Genet 121(2):237–248. https://doi.org/10.1007/s00122-010-1305-x
Borsani O, Valpuesta V, Botella A (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126(3):1024–1030. https://doi.org/10.1104/pp.126.3.1024
Boulahia K, Carol P, Planchais S, Abrous-Belbachir O (2016) Phaseolus vulgaris L. seedlings exposed to prometryn herbicide contaminated soil trigger an oxidative stress response. J Agric Food Chem 64:3150–3160. https://doi.org/10.1021/acs.jafc.6b00328
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)-model food legumes. Plant Soil 252:55–128
Chandrakar V, Dubey A, Keshavkant S (2016) Modulation of antioxidant enzymes by salicylic acid in arsenic exposed Glycine max L. J Soil Sci Plant Nutr 16(3):662–676. https://doi.org/10.4067/S0718-95162016005000048
Clark SM, Mur LAJ, Wood JE, Scott IMIM (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermo tolerance in Arabidopsis thaliana. Plant J 38(3):432–437. https://doi.org/10.1111/j.1365-313X.2004.02054.x
Cui J, Zhang R, Wu GL, Zhu HM, Yang H (2010) Salicylic acid reduces napropamide toxicity by preventing its accumulation in rapeseed (Brassica napus L.). Arch Environ Contam Toxicol 59(1):100–108. https://doi.org/10.1007/s00244-009-9426-4
Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43(2):266–280. https://doi.org/10.3109/03602532.2011.552910
Damanik RI (2012) Response of antioxidant systems in oxygen deprived suspension cultures of rice (Oryza sativa L.). Plant Growth Regul 67:83–92. https://doi.org/10.1007/s10725-012-9668-4
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. https://doi.org/10.3389/fenvs.00053
Dasari S, Ganiavi MS, Yellanurkonda P, Basha S, Meriga B (2018) Role of glutathione S‑transferases in detoxification of a polycyclic aromatic hydrocarbon, methylcholanthrene. Chem Biol Interact 294:81–90. https://doi.org/10.1016/j.cbi.2018.08.023
Deef HE (2013) Salicylic acid and cytokinin protects maize plant against glyphosate action. Egypt J Agron 35(2):115–133. https://doi.org/10.21608/AGRO.2013.82
Delorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic microorganisms:a review. Environ Toxicol Chem 20(1):84–98. https://doi.org/10.1002/etc.5620200108
Dikić D (2014) Prometryn. In: Wexler P (ed) Encyclopedia of toxicology, 3rd edn. Academic Press, pp 1077–1081
Dorey S, Baillieul F, Saindrenan P, Fritige B, Kaufmann S (1998) Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Mol Plant Microbe Interact 11:1102–1109. https://doi.org/10.1094/MPMI.1998.11.11.1102
Edwards R, Dixon DP, Walbot V (2000) Plant glutathione S‑transferases:enzymes with multiple functions in sickness and health. Trends Plant Sci 5(5):193–198. https://doi.org/10.1016/s1360-1385(00)01601-0
Esperanza M, Seoane M, Rioboo C, Herrero C, Cid Á (2015) Chlamydomonas reinhardtii cells adjust themetabolismto maintain viability in response to atrazine stress. Aquat Toxicol 165:64–72. https://doi.org/10.1016/j.aquatox.2015.05.012
Esperanza M, Seoane M, Rioboo C, Herrero C, Cid A (2016) Early alterations on photosynthesis-related parameters in Chlamydomonas reinhardtii cells exposed to atrazine: A multiple approach study. Sci Total Environ 554:237–245. https://doi.org/10.1016/j.scitotenv.2016.02.175
Fai BP, Grant A, Reid B (2007) Chlorophyll a fluorescence as a biomarker for rapid toxicity assessment. Environ Toxicol Chem 26:1520–1531. https://doi.org/10.1897/06-394r1.1
Fayez KA, Radwan DEM, Mohamed AK, Abdelrahman AM (2011) Herbicides and salicylic acid applications caused alterations in total amino acids and proline contents of peanut cultivars. J Environ Sci Stud 6(1):55–61. https://doi.org/10.21608/JESJ.2011.188493
Fernandes B, Soares C, Braga C, Rebotim A, Rafael Ferreira R, Ferreira J, Fidalgo F, Pereira R, Cachada A (2020) Ecotoxicological assessment of a glyphosate-based herbicide in cover plants: Medicago sativa L. as a model species. Appl Sci 10(15):5098. https://doi.org/10.3390/app10155098
Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194(1):7–15. https://doi.org/10.1083/jcb.201102095
Follak S, Hurle K (2003) Effect of airborne bromoxynil-octanoate and metribuzin on non-target plants. Environ Pollut 126(2):139–146. https://doi.org/10.1016/s0269-7491(03)00228-8
Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis regulation and signaling. New Phytol 146(3):359–388. https://doi.org/10.1046/j.1469-8137.2000.00667.x
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 17(7):1866–1875. https://doi.org/10.1105/tpc.105.033589
Foyer CH, Theodoulou FL, Delrot S (2001) The functions of inter- and intracellular glutathione transport systems in plants. Trends Plant Sci 4(10):486–492. https://doi.org/10.1016/s1360-1385(01)02086-6
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
Gondim FA, Gomes-Filho E, Costa JH, Mendes Alencar NL, Prisco JT (2012) Catalase plays a key role in salt stress acclimation induced by hydrogen peroxide pretreatment in maize. Plant Physiol Biochem 56:62–71. https://doi.org/10.1016/j.plaphy.2012.04.012
González-Barreiro O, Rioboo C, Cid A, Herrero C (2004) Atrazine-induced chlorosis in Synechococcus elongatus cells. Arch Environ Contam Toxicol 46(3):301–307. https://doi.org/10.1007/s00244-003-2149-z
Goraya GK, Asthir B (2016) Magnificant role of intracellular reactive oxygen species production and its scavenging encompasses downstream processes. J Plant Biol 59:215–222
Gozzo F (2003) Systemic acquired resistance in crop protection: from nature to a chemical approach. J Agric Food Chem 51(16):4487–4503. https://doi.org/10.1021/jf030025s
Gülengül SC, Karabulut F (2021) Physiological and biochemical effects of 2.4‑D herbicide in wheat (Triticum aestivum L.) varieties. J Sci Technol 11(1):6–12. https://doi.org/10.17678/beuscitech.863405
Gullner G, Komives T, Kiraly L, Schroder P (2018) Glutathionne S‑transferase enzymes in plant-pathogen interactions. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01836
Habibi G (2012) Exogenous salicylic acid alleviates oxidative damage of barley plants under drought stress. Acta Biol Szeged 56(1):57–63
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S‑transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596. https://doi.org/10.1007/s10646-013-1050-4
Hasanuzzaman M, Alam Md M, Nahar K, Ahamed KU, Fujita M (2014) Exogenous salicylic acid alleviates salt stress-induced oxidative damage in Brassica napus by enhancing the antioxidant defense and glyoxalase systems. Aust J Crop Sci 8(4):631–639
Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants:biosynthesis and physiological role in environmen tal stress tolerance. Physiol Mol Biol Plants 23:249–268. https://doi.org/10.1007/s12298-017-0422-2
Hasanuzzaman M, Borhannuddin Bhuyan MHM, Zulfiqar F, Raza A, Mohsin SM, Al Mahmud J, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9(8):681. https://doi.org/10.3390/antiox9080681
Hassan NM, Nemat Alla MM (2005) Oxidative stress in herbicide-treated broad bean and maize plants. Acta Physiol Plant 27(4):429–438. https://doi.org/10.1007/s11738-005-0047-x
Hayat S, Fariduddin Q, Ali B, Ahmad A (2005) Effect of salicylic acid on growth and enzyme activities of wheat seedlings. Acta Agron Hung 53:433–437. https://doi.org/10.1556/AAgr.53.2005.4.9
Hussein MM, Balbaa LK, Gaballah MS (2007) Salicylic acid and salinity effects on growth of maize plants. Res J Agric Biol Sci 3(4):321–328
Idrees M, Khan MMA, Aftab T, Naeem M, Hashmi N (2010) Salicylic acid-induced physiological and biochemical changes in lemongrass varieties under water stress. J Plant Interact 5:293–303. https://doi.org/10.1080/17429145.2010.508566
Ivanov S, Shopova E, Kerchev P, Sergiev I, Miteva L, Polizoev D, Alexieva V (2013) Long-term impact of sublethal atrazine perturbs the redox homeostasis in pea (Pisum sativum L.) plants. Protoplasama 250(1):95–102. https://doi.org/10.1007/s00709-012-0378-6
Janda T, Gondor OK, Yordanova R, Szalai G, Pál M (2014) Salicylic acid and photosynthesis:signalling and effects. Acta Physiol Plant 36(10):2537–2546
Jangra M, Devi S, Satpal, Kumar N, Goyal V, Mehrota S (2022) Amelioration effect of salicylic acid under salt stress in Sorghum bicolor L. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-022-03853-4
Jiang L, Yang H (2009) Prometryne-induced oxidative stress and impact on antioxidant enzymes in wheat. Ecotoxicol Environ Saf 72(6):1687–1693. https://doi.org/10.1016/j.ecoenv.2009.04.025
Jiang L, Maa L, Sui Y, Han SQ, Wu ZY, Feng YX, Yang H (2010) Effect of manure compost on the herbicide prometryne bioavailability to wheat plants. J Hazard Mater 184:337–344. https://doi.org/10.1016/j.jhazmat.2010.08.041
Jiang L, Yang Y, Jia LX, Lin JL, Liu Y, Pan B, Lin Y (2016) Biological responses of wheat (Triticum aestivum) plants to the herbicide simetryne in soils. Ecotoxicol Environ Saf 127:87–94. https://doi.org/10.1016/j.ecoenv.2016.01.012
Jini D, Joseph B (2017) Physiological mechanism of salicylic acid for alleviation of salt stress in rice. Rice Sci 24(2):97–108. https://doi.org/10.1016/j.rsci.2016.07.007
Kahn MIR, Fatma M, Per TS, Anjum NA, Kahn NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. https://doi.org/10.3389/fpls.2015.00462
Kaur N, Kaur J, Grewal SK, Singh I (2019) Effect of heat stress on antioxidative defense system and its amelioration by heat acclimation and salicylic acid pre-treatments in three pigeonpea genotypes. Indian J Agric Biochem 32(1):106–110. https://doi.org/10.5958/0974-4479.2019.00014.5
Kavas M, Akça OE, Akçay UC, Peksel B, Eroğlu S, Öktem HA, Yücel M (2015) Antioxidant responses of peanut (Arachis hypogaea L.) Seedlings to prolonged salt-induced stress. Arch Biol Sci 67(4):1303–1312. https://doi.org/10.2298/abs150407107k
Kaya A, Doğanlar ZB (2016) Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicol Environ Saf 124:470–479. https://doi.org/10.1016/j.ecoenv.2015.11.026
Kaya A, Yigit E (2012) Interactions among glutathione S‑transferase, glutathione reductase activity and glutathione contents in leaves of Vicia faba L. subjected to flurochloridone. Fresenius Environ Bull 21:1635–1640
Khalvandi M, Siosemardeh A, Roohi E, Keramati S (2021) Salicylic acid alleviated the effect of drought stress on photosynthetic characteristics and leaf protein pattern in winter wheat. Heliyon 7:e5908. https://doi.org/10.1016/j.heliyon.2021.e05908
Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74. https://doi.org/10.1016/j.plaphy.2014.03.026
Khan MIR, Fatma M, Per TS, Naser A, Anjum NA, Khan NA (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462. https://doi.org/10.3389/fpls.2015.00462
Khan W, Prithviraj B, Smith DL (2003) Photosynthetic responses of corn and soybean to foliar application of salicylates. J Plant Physiol 160:485–492. https://doi.org/10.1078/0176-1617-00865
Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439–1458. https://doi.org/10.1007/BF00016484
Koo YM, Heo AY, Choi HW (2020) Salicylic acid as a safe plant protector and growth regulator. Plant Pathol J 36(1):1–10. https://doi.org/10.5423/PPJ.RW.12.2019.0295
Kovacik J, Grúz J, Backor M, Strnad M, Repcák M (2009) Salicylic acidinduced changes to growth and phenolic metabolism in Matricaria chamomilla plants. Plant Cell Rep 28(1):135–143. https://doi.org/10.1007/s00299-008-0627-5
Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanisms. Photosynth Res 98:551–564. https://doi.org/10.1007/s11120-008-9349-3
Kumar S, Ahanger MA, Alshaya H, Jan BL, Yerramilli V (2022) Salicylic acid mitigates salt induced toxicity through the modifications of biochemical attributes and some key antioxidants in Capsicum annuum. Saudi J Biol Sci 29(3):1337–1347. https://doi.org/10.1016/j.sjbs.2022.01.028
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331. https://doi.org/10.1016/s1369-5266(02)00275-3
Kurama EE, Fenille RC, Rosa VE Jr, Rosa DD, Ulian EC (2002) Mining the enzymes involved in the detoxification of reactive oxygen species (ROS) in sugarcane. Mol Plant Pathol 3:251–259. https://doi.org/10.1046/j.1364-3703.2002.00119.x
Li X, Riaz M, Song B, Liang X, Liu H (2022) Exogenous salicylic acid alleviates fomesafen toxicity by improving photosynthetic characteristics and antioxidant defense system in sugar beet. Ecotoxicol Environ Saf 238:113587. https://doi.org/10.1016/j.ecoenv.2022.113587
Liang L, Lu YL, Yang H (2012) Toxicology of isoproturon to the food crop wheat as affected by salicylic acid. Environ Sci Pollt Res Int 19(6):2044–2054. https://doi.org/10.1007/s11356-011-0698-7
Liang X, Zhang L, Natarajan SK, Becker DD (2013) Proline mechanisms of stress survival. Antioxid Redox Sign 19(9):998–1011. https://doi.org/10.1089/ars.2012.5074
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu J, Li L, Yuang F, Chen M (2019) Exogenous salicylic acid improves the germination of Limonium bicolor seeds under salt stress. Plant Signal Behav 14(9):1–8. https://doi.org/10.1080/15592324.2019.1644595
Livingstone DR (2001) Contaminated-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666. https://doi.org/10.1016/s0025-326x(01)00060-1
Lu FF, Xu JY, Ma LY, Su XN, Wang XQ, Yang H (2018) Isoproturon-induced salicylic acid confers Arabidopsis resistance to isoproturon phytotoxicity and degradation in plants. J Agric Food Chem 66(50):13073–13083. https://doi.org/10.1021/acs.jafc.8b04281
Lu FF, Liu JT, Zhang N, Chen ZJ, Yang H (2020) OsPAL as a key salicylic acid synthetic component is a critical factor involved in mediation of isoproturon degradation in a paddy crop. J Cleaner Prod 262:121476. https://doi.org/10.1016/j.jclepro.2020.121476
Luo Y, Tang H, Zhang Y (2011) Production of reactive oxygen species and antioxidant metabolism about strawberry leaves to low temperatures. J Agric Sci 3:89–96. https://doi.org/10.5539/jas.v3n2p89
Magne C, Larher E (1992) Higher sugar content of extract interfere with colorimetric determination of amino acid and free proline. Anal Biochem 200(1):115–118. https://doi.org/10.1016/0003-2697(92)90285-f
Martinoia E, Grill E, Tommasini R, Kreuz K, Amrhein N (1993) ATP-dependent glutathione S‑conjugate ‘export’ pump in the vacuolar membrane of plants. Nature 364:247–249
May M, Vernoux T, Leaver C, Van Montagu M, Inze D (1998) Review article. Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49(321):649–667. https://doi.org/10.1093/jxb/49.321.649
Mengistu LW, Mueller-Warrant GW, Liston A, Barker RE (2000) psb mutation (valine 219 to isoleucine) in Poa annua resistant to metribuzin and diuron. Pest Manag Sci 56:209–217
Millar AH, Mittova V, Kiddle G (2003) Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol 133(2):443–447. https://doi.org/10.1104/pp.103.028399
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mittler R (2017) ROS are good. Trends Plant Sci 22(1):11–19. https://doi.org/10.1016/j.tplants.2016.08.002
Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4. https://doi.org/10.3389/fpls.2014.00004
Moharekar S, Lokhande S, Hara T, Tanaka R, Tanaka A, Chavan P (2003) Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings. Photosynthetica 41:315–317. https://doi.org/10.1023/B:PHOT.0000011970.62172.15
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nazar R, Iqbal N, Syeed S, Khan NA (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. J Plant Physiol 168(8):807–815. https://doi.org/10.1016/j.jplph.2010.11.001
Nazar R, Umar S, Khan NA, Sareer O (2015) Salicylic acid supplementation improves photosynthesis and growth in mustard through changes in proline accumulation and ethylene formation under drought stress. S Afr J Bot 98:84–94. https://doi.org/10.1016/j.sajb.2015.02
Negrisoli E, Velini ED, Tofoli GR, Cavenaghi AL, Martins D, Morelli JL, Costa AGF (2004) Selectivity of pre-emergence herbicides to sugarcane treated with nematicides. Planta Daninha 22(4):567–575. https://doi.org/10.1590/S0100-83582004000400011
Nemat Alla MM, Hassan NM, El Bastawisy ZM (2008) Changes in antioxidants and kinetics of glutathione-S-transferase of maize in response to isoproturon treatment. Plant Biosyst 142(1):5–16. https://doi.org/10.1080/11263500701872135
Nie W, Gong B, Chen Y, Wang J, Wei M, Shi Q (2018) Photosynthetic capacity, ion homeostasis and reactive oxygen metabolism were involved in exogenous salicylic acid increasing cucumber seedlings tolerance to alkaline stress. Sci Hortic 235:413–423. https://doi.org/10.1016/j.scienta.2018.13.011
Noreen Z, Ashraf M (2009) Change in antioxidant enzymes and some key metabolites in some genetically diverse cultivars of radish (Raphanus sativus L.). Environ Exp Bot 67(2):395–402. https://doi.org/10.1016/j.envexpbot.2009.05.011
Ould said C, Boulahia K, Eid MAM, Rady MM, Djebbar RR, Abrous-Belbachir O (2021) Exogenously used proline offers pPotent antioxidative and osmoprotective strategies to re-balance growth and physio-biochemical attributes in herbicide-stressed Trigonella foenum-graecum. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-021-00604-y
Parashar A, Yusuf M, Fariduddin QAhmad A (2014) Salicylic acid enhances antioxidant system in Brassica juncea grown under different levels of manganese. Int J Biol Macromol 70:551–558. https://doi.org/10.1016/j.ijbiomac.2014.07.014
Peixoto F, Alves-Fernandes D, Santos D, Fontainhas-Fernandes A (2006) Toxicological effects of oxyfluorfen on oxidative stress enzymes in tilapia Oreochromis niloticus. Pestic Biochem Physiol 85(2):91–96. https://doi.org/10.1016/j.pestbp.2005.10.007
Popova L, Pancheva T, Uzunova A (1997) Salicylic acid:properties, biosynthesis and physiological role. Bulg J Plant Physiol 23:85–93
Quan L, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: A versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50(1):2–18. https://doi.org/10.1111/j.1744-7909.2007.00599.x
Radwan DEM (2012) Salicylic acid induced alleviation of oxidative stress caused by clethodim in maize (Zea mays L.) leaves. Pestic Biochem Phys 102(2):182–188. https://doi.org/10.1016/j.pestbp.2012.01.002
Radwan DEM, Mohamed AK, Fayez KA, Abdelrahman AM (2019) Oxidative stress caused by Basagran® herbicide is altered by salicylic acid treatments in peanut plants. Heliyon 5(5):e1791. https://doi.org/10.1016/j.heliyon.2019.e01791
Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: Interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157. https://doi.org/10.1016/j.envexpbot.2017.02.010
Ramel F, Sulmon C, Bograd M, Couée I, Goueset G (2009) Differential patterns of reactive oxygen species and antioxidative mechanisms during atrazine injury and sucrose-induced tolerance in Arabidopsis thaliana plantlets. BMC Plant Biol. https://doi.org/10.1186/1471-2229-9-28
Raskin I (1992) Role of salicylic acid in plants. Annu Rev Plant Physiol Plant Mol Biol 43:439–463. https://doi.org/10.1146/annurev.pp.43.060192.002255
Raskin I, Skubatz H, Tang W, Meeuse BJD (1990) Salicylic acid levels in thermogenic and non-thermogenic plants. Ann Bot 66:376–373
Razzaq A, Cheema ZA, Jabran K, Farooq M, Khaliq A, Haider G, Basra SMA (2010) Weed management in wheat through combination of allelopathic water extracts with reduced doses of herbicides. Pak J Weed Sci Res 16(3):247–256
Reddy PS, Veeranjaneyulu K (1991) Proline metabolism in senescing leaves of horsgram (Macrotyloma uniflorum Lam.). J Plant Physiol 137(3):381–383. https://doi.org/10.1016/S0176-1617(11)80150-1
Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62(10):3321–3338. https://doi.org/10.1093/jxb/err031
Rutherford AW, Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26(11):648–653. https://doi.org/10.1016/s0968-0004(01)01953-3
Ryter SW, Tyrrell RM (1998) Singlet molecular oxygen (1O2): a possible effector of eukaryotic gene expression. Free Radic Biol Med 24(9):1520–1534. https://doi.org/10.1016/s0891-5849(97)00461-9
Sandmann G, Clarke I, Bramley P, Böger P (1984) Inhibition of phytoene desaturase the mode of action of certain bleaching herbicides. Z Naturforsch C 39(5):443–449
Sandoval-Carrasco CA, Ahuatzi-Chacón D, Galmdez-Mayer J, Ruiz-Ordaz N, Juárez-Ramírez C, Martínez-Jerónimo F (2013) Biodegradation of a mixture of the herbicides ametryn, and 2,4-dichlorophenoxyacetic biofilm reactor. Bioresour Technol 145:33–36. https://doi.org/10.1016/j.biortech.2013.02.068
Sharma A, Sidhu GPS, Araniti F, Bali AS, Shahzad B, Tripathi DK, Brestic M, Skalicky M, Landi M (2020) The role of salicylic acid in plants exposed to heavy metals. Molecules 25(3):540. https://doi.org/10.3390/molecules25030540
Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157(1):292–304. https://doi.org/10.1104/pp.111.183210
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(372):1305–1319. https://doi.org/10.1093/jexbot/53.372.1305
Shopova E, Brankova L, Katerova Z, Dimitrova L, Todorova D, Sergiev I, Talaat NB (2021) Salicylic acid pretreatment modulates wheat responses to glyphosate. Crops 1(2):88–96. https://doi.org/10.3390/crops1020009
Sies H (1985) Oxidative stress. Academic Press, London, p 507 https://doi.org/10.1016/B978-0-12-642760-8.50005-3
Simaei M, Khavari-Nejad RA, Bernard F (2012) Exogenous application of salicylic acid and nitric oxide on the ionic contents and enzymatic activities in NaCl-stressed soybean plants. Am J Plant Sci 3(10):1495–1503. https://doi.org/10.4236/ajps.2012.310180
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39(2):137–141. https://doi.org/10.1023/A:1022556103536
Singh G, Wright D (1999) Effects of herbicides on nodulation, symbiotic nitrogen fixation, growth and yield of pea (Pisum sativum). J Agric Sci 133(1):21–30. https://doi.org/10.1017/S0021859699006735
Singh A, Kumar A, Yadav S, Singh IK (2019) Reactive oxygen species-mediated signaling during abiotic stress. Plant Gene 18:100173. https://doi.org/10.1016/j.plgene.2019.100173
Singh H, Singh NB, Singh A, Hussain I (2017) Exogenous application of salicylic acid to alleviate glyphosate stress in Solanum lycopersicum. Int J Veg Sci 23(6):552–566. https://doi.org/10.1080/19315260.2017.1347845
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16(6):13561–13578. https://doi.org/10.3390/ijms160613561
Song NH, Yang ZM, Zhou LX, Wu X, Yang H (2006) Effect of dissolved organic matter on the toxicity of chlorotoluron to Triticum aestivum. J Environ Sci 18(1):101–108
Song NH, Yin XL, Chen GF, Yang H (2007) Biological responses of wheat (Triticum aestivum) plants to the herbicide chlorotoluron in soils. Chemosphere 68(9):1779–1787. https://doi.org/10.1016/j.chemosphere.2007.03.023
Spormann S, Soares C, Fidalgo F (2019) Salicylic acid alleviates glyphosate-induced oxidative stress in Hordeum vulgare L. J Environ Manage 241:226–234. https://doi.org/10.1016/j.jenvman.2019.04.035
Stroch M, Lenk S, Navrátil M, Spunda V, Buschmann C (2008) Epidermal UVshielding and photosystem II adjustment in wild type and chlorina f2 mutant of barley during exposure to increased PAR and UV radiation. Environ Exp Bot 64(3):271–278. https://doi.org/10.1016/j.envexpbot.2008.05.007
Su YH, Zhu YG, Lin AJ, Zhang XH (2005) Interaction between cadmium and atrazine during uptake by rice seedlings (Oryza sativa l.). Chemosphere 60:802–809. https://doi.org/10.1016/j.chemosphere.2005.04.022
Sun C, Dudley S, McGinnis M, Trumble J, Gan J (2019) Acetaminophen detoxification in cucumber plants via induction of glutathione S‑transferases. Sci Total Environ 649:431–439. https://doi.org/10.1016/j.scitotenv.2018.08.346
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Tahjib-Ul-Arif M, Siddiqui MN, Sohag AM, Sakil MA, Rahman MM, Polash MAS, Mostofa MG, Tran LSP (2018) Salicylic acid-mediated enhancement of photosynthesis attributes and antioxidant capacity contributes to yield improvement of maize plants under salt stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-018-9867-y
Tang YP, Sun X, Wen T, Liu MJ, Yang MY, Chen XF (2017) Implications of terminal oxidase function in regulation of salicylic acid on soybean seedling photosynthetic performance under water stress. Plant Physiol Biochem 112:19–28. https://doi.org/10.1016/j.plaphy.2016.11.016
Tani E, Perraki A, Gerakari M, Chachalis D, Kanatas P, Goufa M, Papadakis IE (2020) How is glyphosate resistance modified by exogenous salicylic acid application on Conyza bonariensis biotypes. Phytoparasitica 48:305–315. https://doi.org/10.1007/s12600-020-00790-y
Tanner JJ (2008) Structural biology of proline catabolism. Amino Acids 35(4):719–730. https://doi.org/10.1007/s00726-008-0062-5
Troll W, Lindsey J (1955) A photometric method for the determination of proline. J Biol Chem 215(2):655–660. https://doi.org/10.1016/s0021-9258(18)65988-5
Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei 19(4):325–346. https://doi.org/10.1007/s12210-008-0022-8
Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143(4):606–616. https://doi.org/10.1016/j.cell.2010.10.020
Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35(4):753–759. https://doi.org/10.1007/s00726-008-0061-6
Vlot AC, Dempsey DMA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206. https://doi.org/10.1146/annurev.phyto.050908.135202
Vos IA, Pieterse CMJ, Wees SCM (2013) Costs and benefits of hormone-regulated plant defences. Plant Pathol 62(1):43–55. https://doi.org/10.1111/ppa.12105
Wang J, Ly M, Islam F, Gill RF, Yang C, Ali B, Yan G, Zhou W (2016) Salicylic acid mediates antioxidant defense system and ABA pathway related gene expression in Oryza sativa against quinclorac toxicity. Ecotoxicol Environ Saf 133:146–156. https://doi.org/10.1016/j.ecoenv.2016.07.002
Wang LJ, Fan L, Loescher W, Duan W, Liu GJ, Cheng JS (2010) Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol 10:34–40. https://doi.org/10.1186/1471-2229-10-34
Wang Q, Que X, Zheng R, Pang Z, Li C, Xiao B (2015) Phytotoxicity assessment of atrazine on growth and physiology of three emergent plants. Environ Sci Pollut Res 22:9646–9657. https://doi.org/10.1007/s11356-015-4104-8
Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4(3):162–176. https://doi.org/10.1016/j.cj.2016.01.010
Weckberker G, Cory JG (1988) Ribonucléotide reductase activity and growth of glutathione depleted mouse leukemia L1210 cells in vitro. Cancer Lett 40(3):257–264. https://doi.org/10.1016/0304-3835(88)90084-5
Wei YY, Zheng Q, Liu ZP, Yang ZM (2011) Regulation of tolerance of Chlamydomonas reinhardtii to heavy metal toxicity by heme oxygenase‑1 and carbon monoxide. Plant Cell Physiol 52(9):1665–1675. https://doi.org/10.1093/pcp/pcr102
Wen Y, Guo P, Yin M, Yan H, Wang Y (2012) Effect of prometryne on root activity and oxidative stress of Polygala tenuifolia Willd. seedling roots. Acta Ecol Sin 32(8):2506–2514. https://doi.org/10.5846/STXB201109281427
Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26(5):2007–2023. https://doi.org/10.1105/tpc.114.125427
Yin XL, Jiang L, Song NH, Yang H (2008) Toxic reactivity of wheat (Triticum aestivum) plants to herbicide isoproturon. J Agric Food Chem 56(12):4825–4831. https://doi.org/10.1021/jf800795v
Yousefvand P, Sohrabi Y, Heidari G, Weisany W, Mastinu A (2022) Salicylic acid stimulates defense systems in Allium hirtifolium grown under water deficit stress. Molecules. https://doi.org/10.3390/molecules27103083
Yu QQ, Lu FF, Ma LY, Yang H, Song NH (2021) Residues of reduced herbicides terbuthylazine, ametryn, and atrazine and Ttoxicology to maize and the environment through salicylic acid. ACS Omega 6:27396–27404. https://doi.org/10.1021/ascomega.1c04315
Zeb A, Fazal Ullah F, Gul SL, Khan M, Zainub B, Khan MN, Amin N (2017) Influence of salicylic acid on growth and flowering of zinnia cultivars. Sci Int (Lahre) 29(6):1329–1335
Zhang JJ, Lu YC, Zhang JJ, Tan LR, Yang H (2014) Accumulation and toxicological response of atrazine in rice crops. Ecotoxicol Environ Saf 102:105–112. https://doi.org/10.1016/j.ecoenv.2013.12.034
Zhang JJ, Lu YC, Zhang SH, Lu FF, Yang H (2016) Identification of transcriptome involved in atrazine detoxification and degradation in alfalfa (Medicago sativa) exposed to realistic environmental contamination. Ecotoxicol Environ Saf 130:103–112. https://doi.org/10.1016/j.ecoenv.2016.04.009
Zhang JJ, Wang YK, Zhou JH, Xie F, Guo QN, Lu FF, Jin SF, Zhu HM, Yang H (2018) Reduced phytotoxicity of propazine on wheat, maize and rapeseed by salicylic acid. Ecotoxicol Environ Saf 162:42–50. https://doi.org/10.1016/j.ecoenv.2018.06.068
Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252(3):911–924. https://doi.org/10.1007/s00709-014-0732-y
Zhou F, Last RL, Pichersky EE (2021) Degradation of salicylic acid to catechol in solanaceae by SA 1‑hydroxylase. Plant Physiol 185(3):876–891. https://doi.org/10.1093/plphs/kiaa096
Zhuge XL, Xu H, Xiul ZJ, Yang HL (2020) Biochemical functions of glutathione S‑transferase family of Salix babylonica. Front Plant Sci 11:364. https://doi.org/10.3389/fpls.2020.00364
Author information
Authors and Affiliations
Contributions
KB and OA planned and supervised the study. KB and CO carried out the experiments and created figures and tables. Wrote the paper: KB. Revised the paper:OA. All authors participated in data evaluation and preparation of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
K. Boulahia, C. Ould said and O. Abrous Belbachir declare that they have no competing interests.
Ethical standards
For this article no studies with human participants or animals were performed by any of the authors. All studies mentioned were in accordance with the ethical standards indicated in each case.
Rights and permissions
Springer Nature oder sein Lizenzgeber (z.B. eine Gesellschaft oder ein*e andere*r Vertragspartner*in) hält die ausschließlichen Nutzungsrechte an diesem Artikel kraft eines Verlagsvertrags mit dem/den Autor*in(nen) oder anderen Rechteinhaber*in(nen); die Selbstarchivierung der akzeptierten Manuskriptversion dieses Artikels durch Autor*in(nen) unterliegt ausschließlich den Bedingungen dieses Verlagsvertrags und dem geltenden Recht.
About this article
Cite this article
Boulahia, K., Ould said, C. & Abrous-Belbachir, O. Exogenous Application of Salicylic Acid Improve Growth and Some Physio-Biochemical Parameters in Herbicide Stressed Phaseolus vulgaris L.. Gesunde Pflanzen 75, 2301–2318 (2023). https://doi.org/10.1007/s10343-023-00878-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10343-023-00878-5