Abstract
The sorption of the allelochemical scopoletin (7-hydroxy-6-methoxycoumarin) was studied in eight agricultural soils and different model sorbents. We also determined its degradation in selected soils and related sorption and degradation results to the expression of scopoletin phytotoxicity in soil towards two model plant species, Eruca vesicaria and Hordeum vulgaris. Scopoletin was sorbed to a greater extent in acid soils than in alkaline soils. Correlations with soil properties indicated that the soil pH and fine (silt/clay) fraction played a primary role in the sorption of scopoletin by soils. Weak interactions controlled its sorption in acid soils, whereas stronger interactions, probably with mineral clay constituents, became more relevant in alkaline clay soils. Dissipation of scopoletin in the soils was microbial-mediated and occurred more slowly in acid than alkaline soils. As a result, the phytotoxic activity of scopoletin was expressed in acid but not in alkaline soil. The results point to the influence that soil properties are expected to exert on the expression of the phytotoxicity of scopoletin in natural and agricultural ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmat AM, Thiebault T, Guégan R (2019) Phenolic acids interactions with clay minerals: a spotlight on the adsorption mechanisms of gallic acid onto montmorillonite. Appl Clay Sci 180:105188. https://doi.org/10.1016/j.clay.2019.105188
Baghestani A, Lemieux C, Leroux GD, Baziramakenga R, Simard RR (1999) Determination of allelochemicals in spring cereal cultivars of different competitiveness. Weed Sci 47:498–504. https://doi.org/10.1017/s0043174500092171
Benoit-Gnonlonfin GJ, Sanni A, Brimer L (2012) Review scopoletin - a coumarin phytoalexin with medicinal properties. Crit Rev Plant Sci 31:47–56. https://doi.org/10.1080/07352689.2011.616039
Blum U (1998) Effects of microbial utilization of phenolic acids and their phenolic acid breakdown products on allelopathic interactions. J Chem Ecol 24:685–708. https://doi.org/10.1023/A:1022394203540
Blum U, Shafer SR, Lehman ME (1999) Evidence for inhibitory allelopathic interactions involving phenolic acids in field soils: concepts vs. an experimental model. Crit Rev Plant Sci 18:673–693. https://doi.org/10.1080/07352689991309441
Boyd SA (1982) Adsorption of substituted phenols by soil. Soil Sci 134:337–343
Bravetti MMM, Carpinella MC, Palacios SM (2020) Phytotoxicity of Cortaderia speciosa extract, active principles, degradation in soil and effectiveness in field tests. Chemoecology 30:15–24. https://doi.org/10.1007/s00049-019-00294-0
Cecchi AM, Koskinen WC, Cheng HH, Haider K (2004) Sorption-desorption of phenolic acids as affected by soil properties. Biol Fertil Soils 39:235–242. https://doi.org/10.1007/s00374-003-0710-6
Celis R, Real M, Hermosin MC, Cornejo J (2005) Sorption and leaching behaviour of polar aromatic acids in agricultural soils by batch and column leaching tests. Eur J Soil Sci 56:287–297. https://doi.org/10.1111/j.1365-2389.2004.00676.x
Cheng F, Cheng Z (2015) Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Front Plant Sci 6:1020. https://doi.org/10.3389/fpls.2015.01020
Clausen L, Fabricius I, Madsen L (2001) Adsorption of pesticides onto quartz, calcite, kaolinite, and alpha-alumina. J Environ Qual 30:846–857
Clemens S, Weber M (2016) The essential role of coumarin secretion for Fe acquisition from alkaline soil. Plant Signal Behav 11:e114197. https://doi.org/10.1080/15592324.2015.1114197
Cruz-Guzmán M, Celis R, Hermosín MC, Leone P, Nègre M, Cornejo J (2003) Sorption-desorption of lead (II) and mercury (II) by model associations of soil colloids. Soil Sci Soc Am J 67:1378–1387. https://doi.org/10.2136/sssaj2003.1378
Dayan FE, Duke SO (2014) Natural compounds as next generation herbicides. Plant Physiol 166:1090–1105. https://doi.org/10.1104/pp.114.239061
Dubus IG, Barriuso E, Calvet R (2001) Sorption of weak organic acids in soils: clofencet, 2,4-D and salicylic acid. Chemosphere 45:767–774. https://doi.org/10.1016/S0045-6535(01)00108-4
Einhellig FA, Rice EL, Risser PG, Wender SH (1970) Effects of scopoletin on growth, CO2 exchange rates, and concentration of scopoletin, scopolin, and chlorogenic acids in tobacco, sunflower, and pigweed. Bull Torrey Bot Club 97:22–33
Farooq M, Jabran K, Cheema ZA, Wahid A, Siddique KHM (2011) The role of allelopathy in agricultural pest management. Pest Manag Sci 67:493–506. https://doi.org/10.1002/ps.2091
Fay PK, Duke WB (1977) An assessment of allelopathic potential in Avena germ plasm. Weed Sci 25:224–228. https://doi.org/10.1017/s0043174500033348
Fernández-Aparicio M, Cimmino A, Evidente A, Rubiales D (2013) Inhibition of Orobanche crenata seed germination and radicle growth by allelochemicals identified in cereals. J Agric Food Chem 61:9797–9803. https://doi.org/10.1021/jf403738p
Gámiz B, Facenda G, Celis R (2019) Modulating the persistence and bioactivity of allelochemicals in the rhizosphere: salicylic acid, a case of study. Arch Agron Soil Sci 65:581–595. https://doi.org/10.1080/03650340.2018.1512102
Gámiz B, Hermosín MC, Celis R (2018) Appraising factors governing sorption and dissipation of the monoterpene carvone in agricultural soils. Geoderma 321:61–68. https://doi.org/10.1016/j.geoderma.2018.02.005
Gámiz B, López-Cabeza R, Velarde P, Spokas KA, Cox L (2021) Biochar changes the bioavailability and bioefficacy of the allelochemical coumarin in agricultural soils. Pest Manag Sci 77:834–843. https://doi.org/10.1002/ps.6086
Ghimire BK, Ghimire B, Yu CY, Chung IM (2019) Allelopathic and autotoxic effects of Medicago sativa—derived allelochemicals. Plants 8:233
Govea KP, Tomita Pereira RS, Oliveria de Assis MD, Alves PI, Brancaglion GA, Toyota AE, Cardoso Machado JV, Carvalho DT, de Souza TC, Beijo LA, De Oliveira Ribeiro Trindade L, Barbosa S (2020) Allelochemical activity of eugenol-derived coumarins on Lactuca sativa L. Plants 9:533. https://doi.org/10.3390/plants9040533
Graña E, Costas-Gil A, Longueira S, Celeiro M, Teijeira M, Reigosa MJ, Sánchez-Moreiras AM (2017) Auxin-like effects of the natural coumarin scopoletin on Arabidopsis cell structure and morphology. J Plant Physiol 218:45–55. https://doi.org/10.1016/j.jplph.2017.07.007
Hanna K, Lassabatere L, Bechet B (2012) Transport of two naphthoic acids and salicylic acid in soil: experimental study and empirical modeling. Water Res 46:4457–4467. https://doi.org/10.1016/j.watres.2012.04.037
Heap I, Duke SO (2018) Overview of glyphosate-resistant weeds worldwide. Pest Manag Sci 74:1040–1049. https://doi.org/10.1002/ps.4760
Inderjit (2005) Soil microorganisms: an important determinant of allelopathic activity. Plant Soil 274:227–236. https://doi.org/10.1007/s11104-004-0159-x
Jain PK, Joshi H (2012) Coumarin: chemical and pharmacological profile. J Appl Pharm Sci 2:236–240. https://doi.org/10.7324/JAPS.2012.2643
Jin X, Wu F, Zhou X (2020) Different toxic effects of ferulic and p-hydroxybenzoic acids on cucumber seedling growth were related to their different influences on rhizosphere microbial composition. Biol Fertil Soils 56:125–136. https://doi.org/10.1007/s00374-019-01408-0
Kah M, Brown CD (2006) Adsorption of ionisable pesticides in soils. Rev Environ Contam Toxicol 188:149–217. https://doi.org/10.1007/978-0-387-32964-2_5
Kaur H, Kaur R, Kaur S, Baldwin IT, Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One 4:e4700. https://doi.org/10.1371/journal.pone.0004700
Kelsey JW, Kottler BD, Alexander M (1997) Selective chemical extractants to predict bioavailability of soil-aged organic chemicals. Environ Sci Technol 31:214–217. https://doi.org/10.1021/es960354j
Ketai W, Huitao L, Xingguo C, Yunkun Z, Zhide H (2001) Identification and determination of active components in Angelica dahurica Benth and its medicinal preparation by capillary electrophoresis. Talanta 54:753–761. https://doi.org/10.1016/S0039-9140(01)00327-7
Khan MI, Cheema SA, Shen C, Zhang C, Tang X, Shi J, Chen X, Park J, Chen Y (2012) Assessment of phenanthrene bioavailability in aged and unaged soils by mild extraction. Environ Monit Assess 184:549–559. https://doi.org/10.1007/s10661-011-1987-9
Kim M, Han J, Hyun S (2013) Anion exchange of organic carboxylate by soils responsible for positive Km-fc relationship from methanol mixture. Chemosphere 93:133–139. https://doi.org/10.1016/j.chemosphere.2013.05.005
Kim M, Kim J, Hyun S (2012) Solubility of organic acids in various methanol and salt concentrations: the implication on organic acid sorption in a cosolvent system. Chemosphere 89:262–268. https://doi.org/10.1016/j.chemosphere.2012.04.031
Kong CH, Xuan TD, Khanh TD, Tran HD, Trung NT (2019) Allelochemicals and signaling chemicals in plants. Molecules 24:2737. https://doi.org/10.3390/molecules24152737
Lebecque S, Lins L, Dayan FE, Fauconnier ML, Deleu M (2019) Interactions between natural herbicides and lipid bilayers mimicking the plant plasma membrane. Front Plant Sci 10:329. https://doi.org/10.3389/fpls.2019.00329
Lees K, Fitzsimons M, Snape J, Tappin A, Comber S (2018) Soil sterilisation methods for use in OECD 106: how effective are they? Chemosphere 209:61–67. https://doi.org/10.1016/j.chemosphere.2018.06.073
Levy L, Gurov A, Radian A (2020) The effect of gallic acid interactions with iron-coated clay on surface redox reactivity. Water Res 184:116190. https://doi.org/10.1016/j.watres.2020.116190
Li XJ, Xia ZC, Kong CH, Xu XH (2013) Mobility and microbial activity of allelochemicals in soil. J Agric Food Chem 61:5072–5079. https://doi.org/10.1021/jf400949m
Li ZR, Amist N, Bai LY (2019) Allelopathy in sustainable weeds management. Allelopath J 48:109–138
Liu J, Xie M, Li X, Jin H, Yang X, Yan Z, Su A, Qin B (2018) Main allelochemicals from the rhizosphere soil of Saussurea lappa (Decne.) Sch. Bip. and their effects on plants’ antioxidase systems. Molecules 23:2506. https://doi.org/10.3390/molecules23102506
Lotrario JB, Stuart BJ, Lam T, Arands RR, O'Connor OA, Kosson DS (1995) Effects of sterilization methods on the physical characteristics of soil: implications for sorption isotherm analyses. Bull Environ Contam Toxicol 54:668–675. https://doi.org/10.1007/BF00206097
Macías FA, Mejías FJR, Molinillo JMG (2019) Recent advances in allelopathy for weed control: from knowledge to applications. Pest Manag Sci 75:2413–2436. https://doi.org/10.1002/ps.5355
Martinez CO, de Souza Silva CMM, Fay EF, Abakerli RB, Maia AHN, Durrant LR (2008) The effects of moisture and temperature on the degradation of sulfentrazone. Geoderma 147:56–62. https://doi.org/10.1016/j.geoderma.2008.07.005
McBride MB, Kung KH (1991) Adsorption of phenol and substituted phenols by iron oxides. Environ Toxicol Chem 10:441–448. https://doi.org/10.1002/etc.5620100403
McSteen P (2010) Auxin and monocot development. Cold Spring Harb Perspect Biol 2:a001479. https://doi.org/10.1101/cshperspect.a001479
Michel A, Johnson RD, Duke SO, Scheffler BE (2004) Dose-response relationships between herbicides with different modes of action and growth of Lemna paucicostata: an improved ecotoxicological method. Environ Toxicol Chem 23:1074–1079. https://doi.org/10.1897/03-256
Niro E, Marzaioli R, De Crescenzo S, Castaldi S, Esposito A, Fiorentino A, Rutigliano FA (2016) Effects of the allelochemical coumarin on plants and soil microbial community. Soil Biol Biochem 95:30–39. https://doi.org/10.1016/j.soilbio.2015.11.028
Pan L, Li X, Jin H, Yang X, Qin B (2017) Antifungal activity of umbelliferone derivatives: synthesis and structure-activity relationships. Microb Pathog 104:110–115. https://doi.org/10.1016/j.micpath.2017.01.024
Pan L, Li X, Yan Z, Guo H, Qin B (2015) Phytotoxicity of umbelliferone and its analogs: structure-activity relationships and action mechanisms. Plant Physiol Biochem 97:272–277. https://doi.org/10.1016/j.plaphy.2015.10.020
Polubesova T, Eldad S, Chefetz B (2010) Adsorption and oxidative transformation of phenolic acids by Fe(III)-montmorillonite. Environ Sci Technol 44:4203–4209. https://doi.org/10.1021/es1007593
Puig CG, Revilla P, Barreal ME, Reigosa MJ, Pedrol N (2019) On the suitability of Eucalyptus globulus green manure for field weed control. Crop Prot 121:57–65. https://doi.org/10.1016/j.cropro.2019.03.016
Razavi SM (2011) Plant coumarins as allelopathic agents. Int J Biol Chem 5:86–90
Real M, Gámiz B, López-Cabeza R, Celis R (2019) Sorption, persistence, and leaching of the allelochemical umbelliferone in soils treated with nanoengineered sorbents. Sci Rep 9:9764. https://doi.org/10.1038/s41598-019-46031-z
Reigosa MJ, Sánchez-Moreiras A, González L (1999) Ecophysiological approach in allelopathy. Crit Rev Plant Sci 18:577–608. https://doi.org/10.1080/07352689991309405
Robison T (1963) The organic constituents of higher plants: their chemistry and interrelationships. Burgess Publishing Company, Minneapolis
Sawhney BL, Kozloski RK, Isaacson PJ, Gent MPN (1984) Polymerization of 2,6-dimethylphenol on smectite surfaces. Clay Clay Miner 32:108–114. https://doi.org/10.1346/ccmn.1984.0320204
Seefeldt SS, Jensen JE, Fuerst EP (1995) Log-logistic analysis of herbicide dose-response relationship. Weed Technol 9:218–227
Serghini K, Pérez De Luque A, Castejón-Muñoz M, García-Torres L, Jorrín JV (2001) Sunflower (Helianthus annuus L.) response to broomrape (Orobanche cernua Loefl.) parasitism: induced synthesis and excretion of 7-hydroxylated simple coumarins. J Exp Bot 52:2227–2234. https://doi.org/10.1093/jexbot/52.364.2227
Shindo H, Huang PM (1984) Catalytic effects of manganese (IV), iron (III), aluminum, and silicon oxides on the formation of phenolic polymers. Soil Sci Soc Am J 48:927–934. https://doi.org/10.2136/sssaj1984.03615995004800040045x
Song Y (2014) Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. J Integr Plant Biol 56:106–113. https://doi.org/10.1111/jipb.12131
Stringlis IA, De Jonge R, Pieterse CMJ (2019) The age of coumarins in plant-microbe interactions. Plant Cell Physiol 60:1405–1419. https://doi.org/10.1093/pcp/pcz076
Tharayil N, Bhowmik PC, Xing B (2006) Preferential sorption of phenolic phytotoxins to soil: implications for altering the availability of allelochemicals. J Agric Food Chem 54:3033–3040. https://doi.org/10.1021/jf053167q
The Clay Minerals Society, CMS (2021). https://www.clays.org/
Trezzi MM, Vidal RA, Balbinot Junior AA, von Hertwig BH, da Silva Souza Filho AP (2016) Allelopathy: driving mechanisms governing its activity in agriculture. J Plant Interact 11:53–60. https://doi.org/10.1080/17429145.2016.1159342
Tülp HC, Fenner K, Schwarzenbach RP, Goss KU (2009) pH-dependent sorption of acidic organic chemicals to soil organic matter. Environ Sci Technol 43:9189–9195. https://doi.org/10.1021/es902272j
Wang TSC, Li SW, Ferng YL (1978) Catalytic polymerization of phenolic compounds by clay minerals. Soil Sci 126:15–21
Wang X, Peter S, Liu Z, Armstrong R, Rochfort S, Tang C (2019) Allelopathic effects account for the inhibitory effect of field-pea (Pisum sativum L.) shoots on wheat growth in dense clay subsoils. Biol Fertil Soils 55:649–659. https://doi.org/10.1007/s00374-019-01384-5
Winkler BC (1967) Quantitative analysis of coumarins by thin layer chromatography, related chromatographic studies, and the partial identification of scopoletin glycoside present in tobacco tissue culture. Ph.D. Dissertation. University of Oklahoma, Norman
Wolf DC, Dao TH, Scott HD, Lavy TL (1989) Influence of sterilization methods on selected soil microbiological, physical, and chemical properties. J Environ Qual 18:39–44. https://doi.org/10.2134/jeq1989.00472425001800010007x
Xiao Z, Le C, Xu Z, Gu Z, Lv J, Shamsi IH (2017) Vertical leaching of allelochemicals affecting their bioactivity and the microbial community of soil. J Agric Food Chem 65:7847–7853. https://doi.org/10.1021/acs.jafc.7b01581
Funding
This work was supported by the Spanish Ministry of Science, Innovation, and Universities (MCIU/AEI) with FEDER-FSE funds (grant AGL2017-82141-R). J.A. Galán-Pérez also thanks MCIU/AEI for a pre-doctoral contract (grant PRE2018-083293) linked to project AGL2017-82141-R.
Author information
Authors and Affiliations
Contributions
BG, RC: Conceptualization
BG, RC: Methodology
JAG, BG, RC: Formal analysis
JAG : Investigation
JAG: Writing—original draft preparation
BG, RC: Writing—review and editing
RC: Funding acquisition
BG, RC: Supervision
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 5307 kb)
Rights and permissions
About this article
Cite this article
Galán-Pérez, J.A., Gámiz, B. & Celis, R. Determining the effect of soil properties on the stability of scopoletin and its toxicity to target plants. Biol Fertil Soils 57, 643–655 (2021). https://doi.org/10.1007/s00374-021-01556-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-021-01556-2