Abstract
Soil degradation is a global environmental problem that puts at risk food security. Improving soil health is, therefore, a major challenge for sustainable agriculture. Biostimulants are products consisting of microorganisms or substances that stimulate plant metabolism, enhance crop performance, and increase plant resistance to biotic and abiotic stresses. A viable approach to reducing chemical inputs is using biostimulants to ensure improved production yield and quality. Humic substances, seaweed extracts, hydrolysed proteins and amino acids, plant extracts, inorganic compounds, beneficial microorganisms, chitosan and other biopolymers are the major categories of biostimulants discussed in this review. Through various mechanisms, such as nutrient absorption enhancement, root growth stimulation, antioxidant activity, and soil structure improvement, these biostimulants have an impact on the interface between soils and plants. Apart from soil degradation, soil and water pollution due to high concentrations of potentially toxic elements (PTEs) is also an important issue. Phytoremediation has the potential to be an effective and environmentally friendly approach for soil remediation and regeneration. Biostimulants have shown encouraging results in the field of phytoremediation by increasing plant biomass, enhancing metal accumulation in plant tissues, as well as improving the overall efficacy of removing PTEs from contaminated soils. The specific mechanisms through which biostimulants contribute to phytoremediation include metal complexion, stabilization and transport to non-vital plant compartments. However, those agro-environmental beneficial effects of biostimulants on degraded soils have not been thoroughly reviewed to date. Therefore, the aim of this review was to present a comprehensive study concerning the use of biostimulants and their interaction in the soil–plant interface under different conditions. This review presents the state of the art about the agricultural and environmental applications of biostimulants to soils as a sustainable agronomic tool to improve soil health and ameliorate PTE contaminated soils.
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References
Abbas SH, Ismail IM, Moustafa TM, Sulaymon AH (2014) Biosorption of heavy metals. J Chem Sci Technol 3(4):74–102
Abd El-Mageed TA, Semida WM, Mohamed GF, Rady MM (2016) Combined effect of foliar-applied salicylic acid and deficit irrigation on physiological-anatomical responses, and yield of squash plants under saline soil. S Afr J Bot 106:8–16. https://doi.org/10.1016/j.sajb.2016.05.005
Al-Ghamdi AA, Elansary HO (2018) Synergetic effects of 5-aminolevulinic acid and Ascophyllum nodosum seaweed extracts on Asparagus phenolics and stress related genes under saline irrigation. Plant Physiol Biochem 129:273–284. https://doi.org/10.1016/j.plaphy.2018.06.008
Alharby HF, Al-Zahrani HS, Hakeem KR, Alsamadany H, Desoky ESM, Rady MM (2021) Silymarin-enriched biostimulant foliar application minimizes the toxicity of cadmium in maize by suppressing oxidative stress and elevating antioxidant gene expression. Biomolecules 11:1–28. https://doi.org/10.3390/biom11030465
Almaroai YA, Usman ARA, Ahmad M, Kim KR, Vithanage M, Sikok Y (2013) Role of chelating agents on release kinetics of metals and their uptake by maize from chromated copper arsenate-contaminated soil. Environ Technol (UK) 34:747–755. https://doi.org/10.1080/09593330.2012.715757
Antoniadis V, Levizou E, Shaheen SM, Ok YS, Sebastian A, Baum C, Prasas MNV, Wenzel WW, Rinklebe J (2017) Trace elements in the soil–plant interface: phytoavailability, translocation, and phytoremediation—a review. Earth-Sci Rev 171:621–645. https://doi.org/10.1016/j.earscirev.2017.06.005
Antoniadis V, Shaheen SM, Levizou E, Shahid M, Niazi NK, Vithanage M, Ok YS, Bolan N, Rinklebe J (2019) A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: are they protective concerning health risk assessment? A review. Environ Int 127:819–847. https://doi.org/10.1016/j.envint.2019.03.039
Antoniadis V, Shaheen SM, Stärk H-J, Wennrich R, Levizou E, Merbach I, Rinklebe J (2021) Phytoremediation potential of twelve wild plant species for toxic elements in a contaminated soil. Environ Int 146:106233. https://doi.org/10.1016/j.envint.2020.106233
Antoniadis V, Thalassinos G, Levizou E, Wang X, Wang S-L, Shaheen SM, Rinklebe J (2022) Hazardous enrichment of toxic elements in soils and olives in the urban zone of Lavrio, Greece, a legacy, millennia-old silver/lead mining area and related health risk assessment. J Hazard Mater 434:128906. https://doi.org/10.1016/j.jhazmat.2022.128906
Arnao MB, Hernández-Ruiz J (2019) Melatonin as a chemical substance or as phytomelatonin rich-extracts for use as plant protector and/or biostimulant in accordance with EC legislation. Agronomy. https://doi.org/10.3390/agronomy9100570
Arockiam Jeyasundar PGS, Ali A, Azeem M, Li Y, Guo D, Sikdar A, Anbdelrahman H, Kwon E, Antoniadis V, Mani VM, Shaheen SM, Rinklebe J, Zhang Z (2021) Green remediation of toxic metals contaminated mining soil using bacterial consortium and Brassica juncea. Environ Pollut 277:116789. https://doi.org/10.1016/j.envpol.2021.116789
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. https://doi.org/10.1007/s005720100097
Babu SMOF, Hossain MB, Rahman MS, Rahman M, Ahmed ASS, Hasan MM, Rakib A, Emran T, Bin Xiao J, Simal-Gandara J (2021) Phytoremediation of toxic metals: a sustainable green solution for clean environment. Appl Sci 11:1–34. https://doi.org/10.3390/app112110348
Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473. https://doi.org/10.3389/fpls.2018.01473
Baglieri A, Cadili V, Mozzetti Monterumici C, Gennari M, Tabasso S, Montoneri E, Nardi S, Negre M (2014) Fertilization of bean plants with tomato plants hydrolysates. Effect on biomass production, chlorophyll content and N assimilation. Sci Hortic 176:194–199. https://doi.org/10.1016/j.scienta.2014.07.002
Bakhat HF, Bibi N, Hammad HM, Shah GM, Abbas S, Rafique HM, Mohamed AKSH, Maqbool MM (2023) Effect of silicon fertilization on eggplant growth and insect population dynamics. SILICON. https://doi.org/10.1007/s12633-022-02279-1
Behie SW, Bidochka MJ (2014) Nutrient transfer in plant-fungal symbioses. Trends Plant Sci 19:734–740. https://doi.org/10.1016/j.tplants.2014.06.007
Benjelloun I, Thami Alami I, El Khadir M, Douira A, Udupa SM (2021) Co-inoculation of Mesorhizobium ciceri with either Bacillus sp. or Enterobacter aerogenes on chickpea improves growth and productivity in phosphate-deficient soils in dry areas of a Mediterranean region. Plants 10(3):571. https://doi.org/10.3390/plants10030571
Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R, Rouphael Y, Colla G, Terzi V, Lucini L (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Biochem 137:203–212. https://doi.org/10.1016/j.plaphy.2019.02.007
Bhargava A, Carmona FF, Bhargava M, Srivastava S (2012) Approaches for enhanced phytoextraction of heavy metals. J Environ Manag 105:103–120. https://doi.org/10.1016/j.jenvman.2012.04.002
Bradáčová K, Weber NF, Morad-Talab N, Asim M, Imran M, Weinmann M, Neumann G (2016) Micronutrients (Zn/Mn), seaweed extracts, and plant growth-promoting bacteria as cold-stress protectants in maize. Chem Biol Technol Agric 3:1–10. https://doi.org/10.1186/s40538-016-0069-1
Bulgari R, Morgutti S, Cocetta G, Negrini N, Farris S, Calcante A, Spinardi A, Ferrari E, Mignani I, Oberti R et al (2017) Evaluation of borage extracts as potential biostimulant using a phenomic, agronomic, physiological, and biochemical approach. Front Plant Sci 8:1–16. https://doi.org/10.3389/fpls.2017.00935
Bulgari R, Franzoni G, Ferrante A (2019) Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 9(6):306. https://doi.org/10.3390/agronomy9060306
Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41. https://doi.org/10.1007/s11104-014-2131-8
Canal SB, Bozkurt MA, Yilmaz H (2022) Effects of humic acid and EDTA on phytoremediation, growth and antioxidant activity in rapeseed (Brassica napus L.) grown under heavy metal stress. Polish J Environ Stud 31:4051–4060. https://doi.org/10.15244/pjoes/148120
Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20. https://doi.org/10.1111/j.1365-3040.2010.02232.x
Chen D, Li Z, Yang J, Zhou W, Wu Q, Shen H, Ao J (2023) Seaweed extract enhances drought resistance in sugarcane via modulating root configuration and soil physicochemical properties. Ind Crops Prod 194:116321. https://doi.org/10.1016/j.indcrop.2023.116321
Chiaiese P, Corrado G, Colla G, Kyriacou MC, Rouphael Y (2018) Renewable sources of plant biostimulation: microalgae as a sustainable means to improve crop performance. Front Plant Sci 9:1782. https://doi.org/10.3389/fpls.2018.01782
Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, Rouphael Y (2015) Protein hydrolysates as biostimulants in horticulture. Sci Hortic 196:28–38. https://doi.org/10.1016/j.scienta.2015.08.037
Corte L, Dell’Abate MT, Magini A, Migliore M, Felici B, Roscini L, Sardella R, Tancini B, Emiliani C, Cardinali G et al (2014) Assessment of safety and efficiency of nitrogen organic fertilizers from animal-based protein hydrolysates-a laboratory multidisciplinary approach. J Sci Food Agric 94:235–245. https://doi.org/10.1002/jsfa.6239
Critchley AT, Critchley JSC, Norrie J, Gupta S, Van Staden J (2021) Perspectives on the global biostimulant market: applications, volumes, and values, 2016 data and projections to 2022. Elsevier Inc
De Hita D, Fuentes M, García AC, Olaetxea M, Baigorri R, Zamarreño AM, Berbara R, Garcia-Mina JM (2019) Humic substances: a valuable agronomic tool for improving crop adaptation to saline water irrigation. Water Supply 19:1735–1740. https://doi.org/10.2166/ws.2019.047
Deliopoulos T, Kettlewell PS, Hare MC (2010) Fungal disease suppression by inorganic salts: a review. Crop Prot 9:1059–1075. https://doi.org/10.1016/j.cropro.2010.05.011
Desoky E-SM, Elrys AS, Rady MM (2019) Integrative moringa and licorice extracts application improves Capsicum annuum fruit yield and declines its contaminant contents on a heavy metals-contaminated saline soil. Ecotoxicol Environ Saf 169:50–60. https://doi.org/10.1016/j.ecoenv.2018.10.117
Desoky E-SM, Merwad A-RM, Semida WM, Ibrahim SA, El-Saadony MT, Rady MM (2020) Heavy metals-resistant bacteria (HM-RB): potential bioremediators of heavy metals-stressed Spinacia oleracea plant. Ecotoxicol Environ Saf 198:110685. https://doi.org/10.1016/j.ecoenv.2020.110685
Dobbss LB, dos Santos TC, Pittarello M, de Souza SB, Ramos AC, Busato JG (2018) Alleviation of iron toxicity in Schinus terebinthifolius Raddi (Anacardiaceae) by humic substances. Environ Sci Pollut Res 25:9416–9425. https://doi.org/10.1007/s11356-018-1193-1
Dogan M, Bolat I, Karakas S, Dikilitas M, Gutiérrez-Gamboa G, Kaya O (2022) Remediation of cadmium stress in strawberry plants using humic acid and silicon applications. Life. https://doi.org/10.3390/life12121962
du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14. https://doi.org/10.1016/j.scienta.2015.09.021
Dziugieł T, Wadas W (2020) Possibility of increasing early crop potato yield with foliar application of seaweed extracts and humic acids. J Cent Eur Agric 21:300–310. https://doi.org/10.5513/JCEA01/21.2.2576
El Khattabi O, El Hasnaoui S, Toura M, Henkrar F, Collin B, Levard C, Colin F, Merghoub N, Smouni A, Fahr M (2023) Seaweed extracts as promising biostimulants for enhancing lead tolerance and accumulation in tomato (Solanum lycopersicum). J Appl Phycol 35:459–469. https://doi.org/10.1007/s10811-022-02849-1
Elrys AS, Merwad ARMA, Abdo AIE, Abdel-Fatah MK, Desoky ESM (2018) Does the application of silicon and Moringa seed extract reduce heavy metals toxicity in potato tubers treated with phosphate fertilizers? Environ Sci Pollut Res 25:16776–16787. https://doi.org/10.1007/s11356-018-1823-7
Elzaawely AA, Ahmed ME, Maswada HF, Xuan TD (2017) Enhancing growth, yield, biochemical, and hormonal contents of snap bean (Phaseolus vulgaris L.) sprayed with moringa leaf extract. Arch Agron Soil Sci 63:687–699. https://doi.org/10.1080/03650340.2016.1234042
Etesami H, Jeong BR, Glick BR (2021) Contribution of arbuscular mycorrhizal fungi, phosphate-solubilizing bacteria, and silicon to P uptake by plant. Front Plant Sci 12:699618. https://doi.org/10.3389/fpls.2021.699618
European Parliament and Council Regulation (EU) 2019/1009 2019, 128
Evangelou MWH, Daghan H, Schaeffer A (2004) The influence of humic acids on the phytoextraction of cadmium from soil. Chemosphere 57:207–213. https://doi.org/10.1016/j.chemosphere.2004.06.017
Fitriatin BN, Suryatmana P, Yuniarti A, Istifadah N (2017) The application of phosphate solubilizing microbes biofertilizer to increase soil p and yield of maize on ultisols Jatinangor. KnE Life Cciences. https://doi.org/10.18502/kls.v2i6.1037
García-Martínez AM, Díaz A, Tejada M, Bautista J, Rodríguez B, Santa María C, Parrado J (2010) Enzymatic production of an organic soil biostimulant from wheat-condensed distiller solubles: effects on soil biochemistry and biodiversity. Process Biochem 45(7):1127–1133. https://doi.org/10.1016/j.procbio.2010.04.005
Gavrileskou M (2021) Enhancing phytoremediation of soils polluted with heavy metals. Curr Opin Biotechnol 74:21–31
Giordano M, Petropoulos SA, Cirillo C, Rouphael Y (2021a) Biochemical, physiological, and molecular aspects of ornamental plants adaptation to deficit irrigation. Horticulturae 7(5):107. https://doi.org/10.3390/horticulturae7050107
Giordano M, Petropoulos SA, Rouphael Y (2021b) Response and defence mechanisms of vegetable crops against drought, heat and salinity stress. Agriculture 11:1–30. https://doi.org/10.3390/agriculture11050463
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. https://doi.org/10.1016/j.micres.2013.09.009
Gómez-Merino FC, Trejo-Téllez LI (2015) Biostimulant activity of phosphite in horticulture. Sci Hortic 196:82–90. https://doi.org/10.1016/j.scienta.2015.09.035
Gu H, Qui H, Tian T, Zhan SS, Deng THB, Chaney RL, Wang SZ, Tang YT, Morel JL, Qiu RL (2011) Mitigation effects of silicon rich amendments on heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil. Chemosphere 83:1234–1240. https://doi.org/10.1016/j.chemosphere.2011.03.014
Guo JM, Lei M, Yang J, Yang J, Wan XM, Chen TB, Zhou XY, Gu SP, Guo GH (2017) Effect of fertilizers on the Cd uptake of two sedum species (Sedum spectabile Boreau and Sedum aizoon L.) as potential Cd accumulators. Ecol Eng 106:409–414. https://doi.org/10.1016/j.ecoleng.2017.04.069
Gupta S, Stirk W, Plačková L, Kulkarni MG, Doležal L, Staden JV (2021) Interactive effects of plant growth-promoting rhizobacteria and a seaweed extract on the growth and physiology of Allium cepa L. (onion). J Plant Physiol 262:153437. https://doi.org/10.1016/j.jplph.2021.153437
Halpern M, Bar-Tal A, Ofek M, Minz D, Muller T, Yermiyahu U (2015) The use of biostimulants for enhancing nutrient uptake. Adv Agron 130:141–174. https://doi.org/10.1016/bs.agron.2014.10.001
Hayes MHB, Mylotte R, Swift RS (2017) Chapter two-humin: its composition and importance in soil organic matter. Adv Agron 143:47–138. https://doi.org/10.1016/bs.agron.2017.01.001
Hedrich R (2012) Ion channels in plants. Physiol Rev 92:1777–1811. https://doi.org/10.1152/physrev.00038.2011
Howladar SM (2014) A novel Moringa oleifera leaf extract can mitigate the stress effects of salinity and cadmium in bean (Phaseolus vulgaris L.) plants. Ecotoxicol Environ Saf 100:69–75. https://doi.org/10.1016/j.ecoenv.2013.11.022
Hu R, Wang H, Liu Q, Lin L, Liao M, Deng H, Wang Z, Liang D, Wang X, Xia H et al (2020) An algal biostimulant promotes growth and decreases cadmium uptake in accumulator plant Nasturtium officinale. Int J Environ Anal Chem 102(16):1–9. https://doi.org/10.1080/03067319.2020.1784413
Ibrahim EA, Ramadan WA (2015) Effect of zinc foliar spray alone and combined with humic acid or/and chitosan on growth, nutrient elements content and yield of dry bean (Phaseolus vulgaris L.) plants sown at different dates. Sci Hortic 184:101–105. https://doi.org/10.1016/j.scienta.2014.11.010
Ijaz A, Imran A, Anwar ul Haq M, Khan QM, Afzal M (2016) Phytoremediation: recent advances in plant-endophytic synergistic interactions. Plant Soil 405:179–195. https://doi.org/10.1007/s11104-015-2606-2
Islam F, Yasmeen T, Ali Q, Ali S, Arif MS, Hussain S, Rizvi H (2014) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293. https://doi.org/10.1016/j.ecoenv.2014.03.008
du Jardin P (2012) The science of plant biostimulants—a bibliographic analysis. Dir. Enterp. Ind. (European Comm. 37)
Ji H, Wang J, Chen F, Fan N, Wang X, Xiao Z, Wang Z (2022) Meta-analysis of chitosan-mediated effects on plant defense against oxidative stress. Sci Total Environ 851:158212. https://doi.org/10.1016/j.scitotenv.2022.158212
Jorda H, Perelman A, Lazarovitch N, Vanderborght J (2018) Exploring osmotic stress and differences between soil-root interface and bulk salinities. Vadose Zone J 17:1–13. https://doi.org/10.2136/vzj2017.01.0029
Karapouloutidou S, Gasparatos D (2019) Effects of biostimulant and organic amendment on soil properties and nutrient status of Lactuca sativa in a calcareous saline-sodic soil. Agriculture 9:164. https://doi.org/10.3390/agriculture9080164
Khalofah A, Bokhari NA, Migdadi HM, Alwahibi MS (2020) Antioxidant responses and the role of Moringa oleifera leaf extract for mitigation of cadmium stressed Lepidium sativum L. S Afr J Bot 129:341–346. https://doi.org/10.1016/j.sajb.2019.08.041
Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Hodges DM, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386–399. https://doi.org/10.1007/s00344-009-9103-x
Koleška I, Hasanagić D, Todorović V, Murtić S, Klokić I, Paradiković N, Kukavica B (2017) Biostimulant prevents yield loss and reduces oxidative damage in tomato plants grown on reduced NPK nutrition. J Plant Interact 12:209–218. https://doi.org/10.1080/17429145.2017.1319503
Kuwada K, Wamocho LS, Utamura M, Matsushita I, Ishii T (2006) Effect of red and green algal extracts on hyphal growth of arbuscular mycorrhizal fungi, and on mycorrhizal development and growth of papaya and passionfruit. Agronomy J 98(5):1340–1344. https://doi.org/10.2134/agronj2005.0354
Li Y, Wang Y, Khan MA, Luo W, Xiang Z, Xu W, Zhong B, Ma J, Ye Z, Zhu Y et al (2021) Effect of plant extracts and citric acid on phytoremediation of metal-contaminated soil. Ecotoxicol Environ Saf 211:111902. https://doi.org/10.1016/j.ecoenv.2021.111902
Liu Z, Wang L, Ding S, Xiao H (2018) Enhancer assisted-phytoremediation of mercury contaminated soils by Oxalis corniculata L., and rhizosphere microorganism distribution of Oxalis corniculata L. Ecotoxicol Environ Saf 160:171–177. https://doi.org/10.1016/j.ecoenv.2018.05.041
Luo ZB, He J, Polle A, Rennenberg H (2016) Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv 34(6):1131–1148. https://doi.org/10.1016/j.biotechadv.2016.07.003
Luziatelli F, Ficca AG, Colla G, Švecová EB, Ruzzi M (2019) Foliar application of vegetal-derived bioactive compounds stimulates the growth of beneficial bacteria and enhances microbiome biodiversity in lettuce. Front Plant Sci 10:1–16. https://doi.org/10.3389/fpls.2019.00060
Menhas S, Yang X, Hayat K, Ali A, Ali EF, Shahid M, Shaheen SM, Rinklebe J, Hayat S, Zhou P (2022) Melatonin enhanced oilseed rape growth and mitigated Cd stress risk: a novel trial for reducing Cd accumulation by bioenergy crops. Environ Pollut 308:119642. https://doi.org/10.1016/j.envpol.2022.119642
Merwad AMA, Desoky EM, Rady MM (2018) Response of water deficit-stressed Vigna unguiculata performances to silicon, proline or methionine foliar application. Sci Hortic 228:132–144. https://doi.org/10.1016/j.scienta.2017.10.008
Mishra B, Chandra M, Pant D (2021) Genome-mining for stress-responsive genes, profiling of antioxidants and radical scavenging metabolism in hyperaccumulator medicinal and aromatic plants. Ind Crops Prod 173:114107. https://doi.org/10.1016/j.indcrop.2021.114107
Mohamed HM, Almaroai YA (2017) Effect of phosphate solubilizing bacteria on the uptake of heavy metals by corn plants in a long-term sewage wastewater treated soil. Int J Environ Sci Dev 8(5):366. https://doi.org/10.18178/ijesd.2017.8.5.979
Moor U, Põldma P, Tõnutare T, Karp K, Starast M, Vool E (2009) Effect of phosphite fertilization on growth, yield and fruit composition of strawberries. Sci Hortic 119:264–269. https://doi.org/10.1016/j.scienta.2008.08.005
Navarro-León E, López-Moreno FJ, Rios JJ, Blasco B, Ruiz JM (2020) Assaying the use of sodium thiosulphate as a biostimulant and its effect on cadmium accumulation and tolerance in Brassica oleracea plants. Ecotoxicol Environ Saf 200:110760. https://doi.org/10.1016/j.ecoenv.2020.110760
Nazir A, Shafiq M, Bareen FE (2022) Fungal biostimulant-driven phytoextraction of heavy metals from tannery solid waste contaminated soils. Int J Phytoremediat 24:47–58. https://doi.org/10.1080/15226514.2021.1924115
Nephali L, Piater LA, Dubery IA, Patterson V, Huyser J, Burgess K, Tugizimana F (2020) Biostimulants for plant growth and mitigation of abiotic stresses: a metabolomics perspective. Metabolites 10(12):505. https://doi.org/10.3390/metabo10120505
Nong H, Liu J, Chen J, Zhao Y, Wu L, Tang Y, Xu Z (2023) Woody plants have the advantages in the phytoremediation process of manganese ore with the help of microorganisms. Sci Total Environ 863:160995. https://doi.org/10.1016/j.scitotenv.2022.160995
Nunes da Silva M, Santos CS, Cruz A, López-Villamor A, Vasconcelos MW (2021) Chitosan increases Pinus pinaster tolerance to the pinewood nematode (Bursaphelenchus xylophilus) by promoting plant antioxidative metabolism. Sci Rep 11:1–10. https://doi.org/10.1038/s41598-021-83445-0
Olaetxea M, De Hita D, Garcia CA, Fuentes M, Baigorri R, Mora V, Garnica M, Urrutia O, Erro J, Zamarreño A et al (2018) Hypothetical framework integrating the main mechanisms involved in the promoting action of rhizospheric humic substances on plant root- and shoot- growth. Appl Soil Ecol 123:521–537. https://doi.org/10.1016/j.apsoil.2017.06.007
Ondrasek G, Romic D, Rengel Z (2020) Interactions of humates and chlorides with cadmium drive soil cadmium chemistry and uptake by radish cultivars. Sci Total Environ 702:134887. https://doi.org/10.1016/j.scitotenv.2019.134887
Pacheco D, Cotas J, Rocha C, Araujo GS, Figueirihna A, Concalves AMM, Bahcevandziev K, Pereira L (2021) Seaweeds’ carbohydrate polymers as plants growth promoters. Carbohydr Polym Technol Appl 2:100097. https://doi.org/10.1016/j.carpta.2021.100097
Panhwar QA, Radziah O, Rahman AZ, Sariah M, Razi IM, Naher UA (2011) Contribution of phosphate-solubilizing bacteria in phosphorus bioavailability and growth enhancement of aerobic rice. Span J Agric Res 9(3):810–820. https://doi.org/10.5424/sjar/20110903-330-10
Parađiković N, Teklić T, Zeljković S, Lisjak M, Špoljarević M (2019) Biostimulants research in some horticultural plant species—a review. Food Energy Secur 8:1–17. https://doi.org/10.1002/fes3.162
Petropoulos SA (2020) Practical applications of plant biostimulants in greenhouse vegetable crop production. Agronomy 10:10–13. https://doi.org/10.3390/agronomy10101569
Petropoulos SA, Taofiq O, Fernandes Â, Tzortzakis N, Ciric A, Sokovic M, Barros L, Ferreira ICFR (2019) Bioactive properties of greenhouse-cultivated green beans (Phaseolus vulgaris L.) under biostimulants and water-stress effect. J Sci Food Agric. https://doi.org/10.1002/jsfa.9881
Petropoulos SA, Fernandes Â, Plexida S, Chrysargyris A, Tzortzakis N, Barreira JCM, Barros L, Ferreira ICFR (2020) Biostimulants application alleviates water stress effects on yield and chemical composition of greenhouse green bean (Phaseolus vulgaris L.). Agronomy 10:1–26. https://doi.org/10.3390/agronomy10020181
Piccolo A, Pietramellara G, Mbagwu JSC (1997) Use of humic substances as soil conditioners to increase aggregate stability. Geoderma 75(3–4):267–277. https://doi.org/10.1016/S0016-7061(96)00092-4
Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274. https://doi.org/10.1016/j.pbi.2009.04.009
Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology—a charging concept. Plant Physiol Biochem 48:292–300. https://doi.org/10.1016/j.plaphy.2009.12.007
Qadir M, Hussain A, Hamayun M, Shah M, Iqbal A, Husna MW (2020) Phytohormones producing rhizobacterium alleviates chromium toxicity in Helianthus annuus L. by reducing chromate uptake and strengthening antioxidant. Chemosphere 258:127386. https://doi.org/10.1016/j.chemosphere.2020.127386
Qiu Z, Tan H, Zhou S, Cao L (2014) Enhanced phytoremediation of toxic metals by inoculating endophytic Enterobacter sp. CBSB1 expressing bifunctional glutathione synthase. J Hazard Mater 267:17–20. https://doi.org/10.1016/j.jhazmat.2013.12.043
Rady MM, Elrys AS, Selem E, Mohsen AAA, Arnaout SMAI, El-Sappah AH, El-Tarabily KA, Desoky E-SM (2023) Spirulina platensis extract improves the production and defenses of the common bean grown in a heavy metals-contaminated saline soil. J Environ Sci 129:240–257. https://doi.org/10.1016/j.jes.2022.09.011
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci 180:169–181. https://doi.org/10.1016/j.plantsci.2010.08.016
Rauser WE (1999) Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochem Biophys 31:19–48. https://doi.org/10.1007/BF02738153
Rehman S, Abbas G, Shahid M, Saqib M, Farooq ABU, Hussain M, Murtaza B, Amjad M, Naeem MA, Farooq A (2019) Effect of salinity on cadmium tolerance, ionic homeostasis and oxidative stress responses in conocarpus exposed to cadmium stress: implications for phytoremediation. Ecotoxicol Environ Saf 171:146–153. https://doi.org/10.1016/j.ecoenv.2018.12.077
Ren XM, Guo SJ, Tian W, Chen Y, Han H, Chen E, Li BL, Li YY, Chen ZJ (2019) Effects of plant growth-promoting bacteria (PGPB) inoculation on the growth, antioxidant activity, Cu uptake, and bacterial community structure of rape (Brassica napus L.) grown in cu-contaminated agricultural soil. Front Microbiol 10:1–12. https://doi.org/10.3389/fmicb.2019.01455
Reyes-Pérez JJ, Enríquez-Acosta EA, Ramírez-Arrebato MÁ, Rodríguez-Pedroso AT, Falcón-Rodríguez A (2020) Effect of humic acids, mycorrhiza, and chitosan on growth indicators of two tomato cultivars (Solanum lycopersicum L.). Terra Latinoam 38:653–666. https://doi.org/10.28940/terra.v38i3.671
Ricci M, Tilbury L, Daridon B, Sukalac K (2019) General principles to justify plant biostimulant claims. Front Plant Sci 10:1–8. https://doi.org/10.3389/fpls.2019.00494
Rinklebe J, Shaheen SM (2015) Miscellaneous additives can enhance plant uptake and affect geochemical fractions of copper in a heavily polluted riparian grassland soil. Ecotoxicol Environ Saf 119:58–65. https://doi.org/10.1016/j.ecoenv.2015.04.04
Riseh RS, Hassanisaadi M, Vatankhah M, Babaki SA, Barka EA (2022) Chitosan as a potential natural compound to manage plant diseases. Int J Biol Macromol 220:998–1009. https://doi.org/10.1016/j.ijbiomac.2022.08.109
Rose MT, Patti A, Little K, Brown AL, Jackson W, Cavagnaro TR (2014) A meta-analysis and review of plant-growth response to humic substances: practical implications for agriculture. In: Sparks DL (ed) Advances in agronomy, vol 124. Elsevier, pp 37–89
Rouphael Y, Colla G (2018) Synergistic biostimulatory action: designing the next generation of plant biostimulants for sustainable agriculture. Front Plant Sci 9:1655. https://doi.org/10.3389/fpls.2018.01655
Roussi Z, Ben Mrid R, Ennoury A, Nhhala N, Zouaoui Z, El Omari R, Nhiri M (2022) Insight into Cistus salviifolius extract for potential biostimulant effects in modulating cadmium-induced stress in sorghum plant. Physiol Mol Biol Plants 28:1323–1334. https://doi.org/10.1007/s12298-022-01202-7
Sánchez AS, Juárez M, Sánchez-Andreu J, Jordá J, Bermúdez D (2005) Use of humic substances and amino acids to enhance iron availability for tomato plants from applications of the chelate FeEDDHA. J Plant Nutr 28:1877–1886. https://doi.org/10.1080/01904160500306359
Santacruz-García AC, Senilliani MG, Gómez AT, Ewens M, Yonny ME, Villalba GF, Nazareno MA (2022) Biostimulants as forest protection agents: Do these products have an effect against abiotic stress on a forest native species? Aspects to elucidate their action mechanisms. For Ecol Manag 522:120446. https://doi.org/10.1016/j.foreco.2022.120446
Sathiyabama M, Manikandan A (2021) Foliar application of chitosan nanoparticle improves yield, mineral content and boost innate immunity in finger millet plants. Carbohydr Polym. https://doi.org/10.1016/j.carbpol.2021.117691
Shaheen SM, Rinklebe J (2015) Impact of emerging and low cost alternative amendments on the (im)mobilization and phytoavailability of Cd and Pb in a contaminated floodplain soil. Ecol Eng 74:319–326. https://doi.org/10.1016/j.ecoleng.2014.10.024
Shaheen SM, Rinklebe J, Selim MH (2015) Impact of various amendments on immobilization and phytoavailability of nickel and zinc in a contaminated floodplain soil. Int J Environ Sci Technol 12:2765–2776. https://doi.org/10.1007/s13762-014-0713-x
Shaheen SM, Mosa A, Natasha Jeyasundar PGSA, Hassan NEE, Yang X et al (2023) Pros and cons of biochar to soil potentially toxic element mobilization and phytoavailability: environmental implications. Earth Syst Environ 7:321–345. https://doi.org/10.1007/s41748-022-00336-8
Shahrajabian MH, Chaski C, Polyzos N, Petropoulos SA (2021a) Biostimulants application: a low input cropping management tool for sustainable farming of vegetables. Biomolecules 11:1–26. https://doi.org/10.3390/biom11050698
Shahrajabian MH, Chaski C, Polyzos N, Tzortzakis N, Petropoulos SA (2021b) Sustainable agriculture systems in vegetable production using chitin and chitosan as plant biostimulants. Biomolecules 11:1–18. https://doi.org/10.3390/biom11060819
Shahrajabian MH, Petropoulos SA, Sun W (2023) Survey of the influences of microbial biostimulants on horticultural crops: case studies and successful paradigms. Horticulturae 9:1–24. https://doi.org/10.3390/horticulturae9020193
Sharma G, Sharma P (2021) Chitosan nanofertilizer boost source activity in plant. J Plant Nutr 44:2486–2499. https://doi.org/10.1080/01904167.2021.1918159
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 2012:1–26. https://doi.org/10.1155/2012/217037
Sharon JA, Hathwaik LT, Glenn GM, Imam SH, Lee CC (2016) Isolation of efficient phosphate solubilizing bacteria capable of enhancing tomato plant growth. J Soil Sci Plant Nutr 16(2):525–536. https://doi.org/10.4067/S0718-95162016005000043
Shirkhani Z, Chehregani Rad A, Mohsenzadeh F (2021) Improving Cd-phytoremediation ability of Datura stramonium L. by Chitosan and Chitosan nanoparticles. Biologia (bratisl) 76:2161–2171. https://doi.org/10.1007/s11756-021-00758-1
Spann TM, Little HA (2011) Applications of a commercial extract of the brown seaweed Ascophyllum nodosum increases drought tolerance in container-grown “hamlin” sweet orange nursery trees. Hort Sci 46:577–582. https://doi.org/10.21273/hortsci.46.4.577
Srivastava S, Bist V, Srivastava S, Singh PC, Trivedi PK, Asif MH, Nautiyal CS (2016) Unraveling aspects of Bacillus amyloliquefaciens mediated enhanced production of rice under biotic stress of Rhizoctonia solani. Front Plant Sci 7:587. https://doi.org/10.3389/fpls.2016.00587
Strullu-Derrien C, Strullu DG (2007) Mycorrhization of fossil and living plants. C R Palevol 6:483–494. https://doi.org/10.1016/j.crpv.2007.09.006
Tarafdar JC (2022) Biostimulants for sustainable crop production. New Futur Dev Microb Biotechnol Bioeng Sustain Agric Revital Org Prod. https://doi.org/10.1016/B978-0-323-85579-2.00004-6
Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl- ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61:4449–4459. https://doi.org/10.1093/jxb/erq251
Técher D, Laval-Gilly P, Henry S, Bennasroune A, Formanek P, Martinez-Choice C, D’Innocenzo M, Muanda F, Dicko A, Rejšek K, Falla J (2011) Contribution of Miscanthus × giganteus root exudates to the biostimulation of PAH degradation: an in vitro study. Sci Total Environ 409:4489–4495. https://doi.org/10.1016/j.scitotenv.2011.06.049
Teng Z, Shao W, Zhang K, Huo Y, Zhu J, Li M (2019) Pb biosorption by Leclercia adecarboxylata: protective and immobilized mechanisms of extracellular polymeric substances. Chem Eng J 375:122113. https://doi.org/10.1016/j.cej.2019.122113
Tripathi R, Tewari R, Singh KP, Keswani C, Minkina T, Srivastava AK, De Corato U, Sansinenea E (2022) Plant mineral nutrition and disease resistance: a significant linkage for sustainable crop protection. Front Plant Sci 13:1–12. https://doi.org/10.3389/fpls.2022.883970
Vranova V, Rejsek K, Skene KR, Formanek P (2011) Non-protein amino acids: plant, soil and ecosystem interactions. Plant Soil 342:31–48. https://doi.org/10.1007/s11104-010-0673-y
Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol 47(8):1045–1057. https://doi.org/10.1093/pcp/pcj075
Wani PA, Khan MS, Zaidi A (2008) Impact of zinc-tolerant plant growth-promoting rhizobacteria on lentil grown in zinc-amended soil. Agron Sustain Dev 28:449–455. https://doi.org/10.1051/agro:2007048
Weil RR, Brady NC (2017) The nature and properties of soils. In: Weil RR, Brady NC (eds) Pearson ISBN 9780521885799
White JF, Kingsley KL, Zhang Q, Verma R, Obi N, Dvinskikh S, Elmore MT, Verma SK, Gond SK, Kowalski KP (2019) Review: endophytic microbes and their potential applications in crop management. Pest Manag Sci 75:2558–2565. https://doi.org/10.1002/ps.5527
Xu L, Geelen D (2018) Developing biostimulants from agro-food and industrial by-products. Front Plant Sci 871:1–13. https://doi.org/10.3389/fpls.2018.01567
Xu JC, Huang LM, Chen C, Wang J, Long XX (2019) Effective lead immobilization by phosphate rock solubilization mediated by phosphate rock amendment and phosphate solubilizing bacteria. Chemosphere 237:124540. https://doi.org/10.1016/j.chemosphere.2019.124540
Xu C, Mou B (2018) Chitosan as soil amendment affects lettuce growth, photochemical efficiency, and gas exchange. Horttechnology 28:476–480. https://doi.org/10.21273/HORTTECH04032-18
Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017) Biostimulants in plant science: a global perspective. Front Plant Sci 7:2049. https://doi.org/10.3389/fpls.2016.02049
Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:1–15. https://doi.org/10.3389/fpls.2020.00359
Yao Z, Li J, Xie H, Yu C (2012) Review on remediation technologies of soil contaminated by heavy metals. Proc Environ Sci 16:722–729
Younes NA, Anik TR, Rahman MM, Wardany AA, Dawood MFA, Tran L-SP, Abdel Latef AAH, Mostofa FG (2023) Effects of microbial biostimulants (Trichoderma album and Bacillus megaterium) on growth, quality attributes, and yield of onion under field conditions. Heliyon 9:e14203. https://doi.org/10.1016/j.heliyon.2023.e14203
Yu X, Shoaib M, Cheng X, Cui Y, Hussain S, Yan J, Zhou Z, Chen Q, Gu Y, Zou L et al (2022) Role of rhizobia in promoting non-enzymatic antioxidants to mitigate nitrogen-deficiency and nickel stresses in Pongamia pinnata. Ecotoxicol Environ Saf 241:113789. https://doi.org/10.1016/j.ecoenv.2022.113789
Yuan JL, Yue JJ, Gu XP, Lin CS (2017) Flowering of woody bamboo in tissue culture systems. Front Plant Sci 8:1589. https://doi.org/10.3389/fpls.2017.01589
Zhao Y, Naeth MA (2023) Soil amendment with a humic substance and arbuscular mycorrhizal fungi enhance coal mine reclamation. Sci Total Environ 823:153696. https://doi.org/10.1016/j.scitotenv.2022.153696
Zhao FG, Tang Z, Song JJ, Huang XY, Wang P (2022) Toxic metals and metalloids: uptake, transport, detoxification, phytoremediation, and crop improvement for safer food. Mol Plant 15:27–44. https://doi.org/10.1016/j.molp.2021.09.016
Zheng BX, Ibrahim M, Zhang DP, Bi QF, Li HZ, Zhou GW, Yang XR (2018) Identification and characterization of inorganic-phosphate-solubilizing bacteria from agricultural fields with a rapid isolation method. AMB Express 8:1–12. https://doi.org/10.1186/s13568-018-0575-6
Zou P, Lu X, Zhao H, Yuan Y, Meng L, Zhang C, Li Y (2019) Polysaccharides derived from the brown algae Lessonia nigrescens enhance salt stress tolerance to wheat seedlings by enhancing the antioxidant system and modulating intracellular ion concentration. Front Plant Sci 10:1–15. https://doi.org/10.3389/fpls.2019.00048
Zulfiqar F, Casadesús A, Brockman H, Munné-Bosch S (2020) An overview of plant-based natural biostimulants for sustainable horticulture with a particular focus on moringa leaf extracts. Plant Sci 295:110194. https://doi.org/10.1016/j.plantsci.2019.110194
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This work was funded by the General Secretariat for Research and Technology of Greece (project VAL-UEFARM PRIMA2019-11) and PRIMA foundation under the project VALUEFARM (PRI-MA/0009/2019). The fourth and fifth author also acknowledges the German Federal Ministry of Education and Research (BMBF) who funded their contribution (Project ID: 01DH20006) in the frame of the same PRIMA project (PRI-MA/0009/2019).
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Grammenou, A., Petropoulos, S.A., Thalassinos, G. et al. Biostimulants in the Soil–Plant Interface: Agro-environmental Implications—A Review. Earth Syst Environ 7, 583–600 (2023). https://doi.org/10.1007/s41748-023-00349-x
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DOI: https://doi.org/10.1007/s41748-023-00349-x