Boosting crop productivity: The essential role of biostimulants under abiotic stress conditions

V Yogesh Kumar; Shanmugam Kavitha; Parasuraman Boominathan; Velusamy Manonmani; Arumugam Thanga  Hemavathy; Kulandaivel Malarkodi; Appusami Sudha; Chinnasamy Pradipa

doi:10.14719/pst.4428

Authors

V Yogesh Kumar Department of Seed Science and Technology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0009-0004-1565-651X
Shanmugam Kavitha Department of Seed Science and Technology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-7045-4062
Parasuraman Boominathan Department of Crop Physiology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-3287-4904
Velusamy Manonmani Department of Seed Science and Technology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-5982-8983
A Thanga Hemavathy Department of Pulses, Centre for Plant Breeding and Genetics, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-7312-3779
Kulandaivel Malarkodi Department of Seed Science and Technology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0002-8974-9389
Appusami Sudha Department of Plant Pathology, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0009-0006-0463-0765
Chinnasamy Pradipa Agro Climate Research Centre, Tamil Nadu Agricultural University, Coimbatore 641 003, India https://orcid.org/0000-0001-7623-6691

DOI:

https://doi.org/10.14719/pst.4428

Keywords:

abiotic stress tolerance, biostimulant, crop growth, seed germination, yield

Abstract

Climate change has witnessed detrimental effects on the environment that significantly contribute to the loss of agricultural production and productivity. With the growing population and limited or rather decreasing land for cultivation, food insecurity has become a major concern globally. Contamination of all sorts, including injudicious use of chemicals and anthropological interventions for all important reasons like ensuring food security and other short-term benefits have turned out to be the major contributors to ecosystem and soil health degradation. To balance the situation, we have credible alternatives like biostimulants- both a necessity and a sustainable option. Biostimulants are substances used or added to reduce the intensity of the harmful effects caused by abiotic stress factors like drought, salinity, temperature, heavy metal and nutritional imbalance, thereby ensuring enhanced seed germination, crop growth and development and yield. The paper discusses in detail the various potent biostimulant applications humic substances (humic and fulvic acid), chitosan, seaweed extract, protein hydrolysates and other N-containing compounds, inorganic compounds, beneficial fungi and beneficial bacteria that play important roles in increasing resilience and reducing the ill effects that plants face due to abiotic stress. Additionally, also briefing about the necessity of the current agricultural scenario to switch to such sustainable, reliable and eco-friendly options to create a healthy, habitable globe for us and future generations to thrive. Research should identify optimal biostimulant combinations for specific plants and conditions, focusing on application timing and interactions with fertilizers to enhance sustainable agriculture in the future.

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References

Organization WH. The state of food security and nutrition in the world 2019: safeguarding against economic slowdowns and downturns: Food and Agriculture Org. 2019.

Zandalinas SI, Fritschi FB, Mittler R. Global warming, climate change and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci. 2021;26(6):588?99. https://doi.org/10.1016/j.tplants.2021.02.011

Prasad B, Chakravorty S. Effects of climate change on vegetable cultivation-a review. Nat Environ Pollut Technol. 2015;14(4):923?29.

Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, et al. Crop production under drought and heat stress: plant responses and management options. Front Plant Sci. 2017;8(1147):1?17. https://doi.org/10.3389/fpls.2017.01147

Yang T, Siddique KH, Liu K. Cropping systems in agriculture and their impact on soil health-A review. Glob Ecol Conserv. 2020;23:1?13. https://doi.org/10.1016/j.gecco.2020.e01118

Rouphael Y, Colla G. Synergistic biostimulatory action: Designing the next generation of plant biostimulants for sustainable agriculture. Front Plant Sci. 2018;9:1?7. https://doi.org/10.3389/fpls.2018.01655

Hamza B, Suggars A. Biostimulants: myths and realities. TurfGrass Trends. 2001;8:6?10.

Du Jardin P. Plant biostimulants: Definition, concept, main categories and regulation. Sci Hortic. 2015;196:3?14. https://doi.org/10.1016/j.scienta.2015.09.021

Kavipriya R, Boominathan P. Influence of biostimulants and plant growth regulators on physiological and biochemical traits in tomato (Lycopersicon esculentum Mill.). Madras Agri J. 2018;105(4?6):225?28. https://doi.org/10.29321/MAJ.2018.000135

Bulgari R, Franzoni G, Ferrante A. Biostimulants application in horticultural crops under abiotic stress conditions. Agron. 2019;9(306):1?30. https://doi.org/10.3390/agronomy9060306

Adamo ML, Yonny ME, Villalba GF, Nazareno MA. Natural biostimulants foliar application as sustainable mitigation strategy of drought stress damage on the melon crop (Cucumis melo L.). Sci Hortic. 2024;323:112471. https://doi.org/10.1016/j.scienta.2023.112471

Fageria NK, Baligar VC. Enhancing nitrogen use efficiency in crop plants. Adv Agron. 2005;88:97?185. https://doi.org/10.1016/S0065-2113(05)88004-6

Taiz L, Zeiger E. Plant physiology sinauer associates. Inc, Sunderland, MA. 2006.

Gupta S, Bhattacharyya P, Kulkarni MG, Doležal K. Growth regulators and biostimulants: upcoming opportunities. Front Plant Sci. 2023;14:1?4. https://doi.org/10.3389/978-2-8325-2678-1

Stevenson F. Humus chemistry: Genesis, composition, reactions. John Wiley and Sons; 1994.

Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH. Biostimulants in plant science: a global perspective. Front Plant Sci. 2017;7(2049):1?32. https://doi.org/10.3389/fpls.2016.02049

Li J, Gerrewey VT, Geelen D. A meta-analysis of biostimulant yield effectiveness in field trials. Front Plant Sci. 2022;13(836702):1?13. https://doi.org/10.3389/fpls.2022.836702

Shiade SR, Zand-Silakhoor A, Fathi A, Rahimi R, Minkina T, Rajput VD, et al. Plant metabolites and signaling pathways in response to biotic and abiotic stresses: Exploring bio stimulant applications. Plant Stress. 2024;100454. https://doi.org/10.1016/j.stress.2024.100454

Ali S, Akhtar MS, Siraj M, Zaman W. Molecular communication of microbial plant biostimulants in the rhizosphere under abiotic stress conditions. Int J Mol Sci. 2024;25(22):12424. https://doi.org/10.3390/ijms252212424

Cristofano F, El-Nakhel C, Rouphael Y. Biostimulant substances for sustainable agriculture: Origin, operating mechanisms and effects on cucurbits, leafy greens and nightshade vegetables species. Biomolecules. 2021;11(1103):1?36. https://doi.org/10.3390/biom11081103

Ma Y, Freitas H, Dias MC. Strategies and prospects for biostimulants to alleviate abiotic stress in plants. Front Plant Sci. 2022;13(1024243):1?13. https://doi.org/10.3389/fpls.2022.1024243

González-Morales S, Solís-Gaona S, Valdés-Caballero MV, Juárez-Maldonado A, Loredo-Treviño A, Benavides-Mendoza A. Transcriptomics of biostimulation of plants under abiotic stress. Front Genet. 2021;12(583888):1?24. https://doi.org/10.3389/fgene.2021.583888

Franzoni G, Cocetta G, Prinsi B, Ferrante A, Espen L. Biostimulants on crops: Their impact under abiotic stress conditions. Horticulturae. 2022;8(189):1?20. https://doi.org/10.3390/horticulturae8030189

Makrigianni EA, Papadaki ES, Chatzimitakos T, Athanasiadis V, Bozinou E, Lalas SI. Application of humic and fulvic acids as an alternative method of cleaning water from plant protection product residues. Separations. 2022;9(313):1?13. https://doi.org/10.3390/separations9100313

Ampong K, Thilakaranthna MS, Gorim LY. Understanding the role of humic acids on crop performance and soil health. Front Agron. 2022;4:848621. https://doi.org/10.3389/fagro.2022.848621

Shah ZH, Rehman HM, Akhtar T, Alsamadany H, Hamooh BT, Mujtaba T, et al. Humic substances: Determining potential molecular regulatory processes in plants. Front Plant Sci. 2018;9:263.https://doi.org/10.3389/fpls.2018.00263

Nardi S, Schiavon M, Francioso O. Chemical structure and biological activity of humic substances define their role as plant growth promoters. Molecules. 2021;26(8):2256. https://doi.org/10.3390/molecules26082256

Jindo K, Martim SA, Navarro EC, Pérez-Alfocea F, Hernandez T, Garcia C, et al. Root growth promotion by humic acids from composted and non-composted urban organic wastes. Plant and Soil. 2012;353:209?20. https://doi.org/10.1007/s11104-011-1024-3

Olivares FL, Aguiar NO, Rosa RCC, Canellas LP. Substrate biofortification in combination with foliar sprays of plant growth promoting bacteria and humic substances boosts production of organic tomatoes. Sci Hortic. 2015;183:100?08. https://doi.org/10.1016/j.scienta.2014.11.012

Canellas LP, Olivares FL, Aguiar NO, Jones DL, Nebbioso A, Mazzei P, Piccolo A. Humic and fulvic acids as biostimulants in horticulture. Sci Hortic. 2015;196:15?27. https://doi.org/10.1016/j.scienta.2015.09.013

Hurtado AQ, Yunque DA, Tibubos K, Critchley AT. Use of Acadian marine plant extract powder from Ascophyllum nodosum in tissue culture of Kappaphycus varieties. J Appl Phycol. 2009;21:633?39. https://doi.org/10.1007/s10811-008-9395-4

Sathya B, Indu H, Seenivasan R, Geetha S. Influence of seaweed liquid fertilizer on the growth and biochemical composition of legume crop, Cajanus cajan (L.) Mill sp. J Phytol. 2010;2(5):50?63.

Chen D, Zhou W, Yang J, Ao J, Huang Y, Shen D, et al. Effects of seaweed extracts on the growth, physiological activity, cane yield and sucrose content of sugarcane in China. Front Plant Sci. 2021;12:659130. https://doi.org/10.3389/fpls.2021.659130

Ali O, Ramsubhag A, Jayaraman J. Biostimulant properties of seaweed extracts in plants: Implications towards sustainable crop production. Plants. 2021;10(531):1?27. https://doi.org/10.3390/plants10030531

Kularathne MN, Srikrishnah S, Sutharsan S. Effect of seaweed extracts on ornamental plants: Article review. Curr Agric Res J. 2021;9(3):149?60. https://doi.org/10.12944/CARJ.9.3.02

Nardi S, Pizzeghello D, Schiavon M, Ertani A. Plant biostimulants: physiological responses induced by protein hydrolyzed-based products and humic substances in plant metabolism. Sci Agric. 2016;73:18?23. https://doi.org/10.1590/0103-9016-2015-0006

Zhang X, Yin J, Ma Y, Peng Y, Fenton O, Wang W, et al. Unlocking the potential of biostimulants derived from organic waste and by-product sources: Improving plant growth and tolerance to abiotic stresses in agriculture. Environ Technol Innov. 2024;103571. https://doi.org/10.1016/j.eti.2024.103571

Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, Rouphael Y. Protein hydrolysates as biostimulants in horticulture. Sci Hortic. 2015;196:28?38. https://doi.org/10.1016/j.scienta.2015.08.037

Olsen RL, Toppe J, Karunasagar I. Challenges and realistic opportunities in the use of by-products from processing of fish and shellfish. Trends Food Sci Technol. 2014;36(2):144?51. https://doi.org/10.1016/j.tifs.2014.01.007

Katiyar D, Hemantaranjan A, Singh B. Chitosan as a promising natural compound to enhance potential physiological responses in plant: a review. Indian J Plant Physiol. 2015;20:1?9. https://doi.org/10.1007/s40502-015-0139-6

Chakraborty M, Hasanuzzaman M, Rahman M, Khan MA, Bhowmik P, Mahmud NU, et al. Mechanism of plant growth promotion and disease suppression by chitosan biopolymer. Agriculture. 2020;10(12):624. https://doi.org/10.3390/agriculture10120624

Hidangmayum A, Dwivedi P, Katiyar D, Hemantaranjan A. Application of chitosan on plant responses with special reference to abiotic stress. Physiol Mol Biol Plants. 2019;25:313?26. https://doi.org/10.1007/s12298-018-0633-1

Morganti P, Morganti G, Nunziata ML. Chitin nanofibrils, a natural polymer from fishery waste: Nanoparticle and nanocomposite characteristics. Bionanotech to Save the Environ. 2019;60.

Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M. Physiological functions of beneficial elements. Curr Opin Plant Biol. 2009;12(3):267?74. https://doi.org/10.1016/j.pbi.2009.04.009

Sarraf M, Janeeshma E, Arif N, QudratUllahFarooqi M, Kumar V, Ansari NA, et al. Understanding the role of beneficial elements in developing plant stress resilience: Signalling and crosstalk with phytohormones and microbes. Plant Stress. 2023;100224. https://doi.org/10.1016/j.stress.2023.100224

Azad MOK, Park BS, Adnan M, Germ M, Kreft I, Woo SH, Park CH. Silicon biostimulant enhances the growth characteristics and fortifies the bioactive compounds in common and Tartary buckwheat plant. J Crop Sci Biotechnol. 2021;24:51?59. https://doi.org/10.1007/s12892-020-00058-1

Broadley M, Brown P, Cakmak I, Ma JF, Rengel Z, Zhao F. Chapter 8 - Beneficial elements. In: Marschner P, editor. Marschner's mineral nutrition of higher plants (Third Edition). San Diego: Academic Press; 2012. p. 249?69. https://doi.org/10.1016/B978-0-12-384905-2.00008-X

Behie SW, Bidochka MJ. Nutrient transfer in plant–fungal symbioses. Trends Plant Sci. 2014;19(11):734?40. https://doi.org/10.1016/j.tplants.2014.06.007

Lugtenberg BJ, Caradus JR, Johnson LJ. Fungal endophytes for sustainable crop production. FEMS Microbiol Ecol. 2016;92(12):1?17. https://doi.org/10.1093/femsec/fiw194

Mohammadi K, Khalesro S, Sohrabi Y, Heidari G. A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci. 2011;1(9):310?19.

Goyal RK, Habtewold JZ. Evaluation of legume–Rhizobial symbiotic interactions beyond nitrogen fixation that help the host survival and diversification in hostile environments. Microorganisms. 2023;11(6):1454. https://doi.org/10.3390/microorganisms11061454

Rahimi S, Talebi M, Baninasab B, Gholami M, Zarei M, Shariatmadari H. The role of plant growth-promoting rhizobacteria (PGPR) in improving iron acquisition by altering physiological and molecular responses in quince seedlings. Plant Physiol Biochem. 2020;155:406?15. https://doi.org/10.1016/j.plaphy.2020.07.045

Hua LIN, Caixing LAI, Guo YU, Sunahara GI, Liheng LIU, Ullah H, Jie LI . Root exudate-driven rhizospheric recruitment of plant growth-promoting rhizobacteria. Pedosphere. 2024. https://doi.org/10.1016/j.pedsph.2024.03.005

Olivares FL, Busato JG, de Paula AM, da Silva Lima L, Aguiar NO, Canellas LP. Plant growth promoting bacteria and humic substances: crop promotion and mechanisms of action. Chem Biol Technol Agric. 2017;4(1):30. https://doi.org/10.1186/s40538-017-0112-x

Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11(1):15?19. https://doi.org/10.1016/j.tplants.2005.11.002

Ashraf M, Harris P. Abiotic stresses: plant resistance through breeding and molecular approaches. CRC Press; 2005.

Singh J, Thakur JK. Photosynthesis and abiotic stress in plants. Biotic and Abiotic Stress Tolerance in Plants. 2018;27?46. https://doi.org/10.1007/978-981-10-9029-5_2

Da Cunha Leme Filho JF, Chim BK, Bermand C, Diatta AA, Thomason WE. Effect of organic biostimulants on cannabis productivity and soil microbial activity under outdoor conditions. J Cannabis Res. 2024;6(1):16. https://doi.org/10.1186/s42238-024-00214-2

Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SM. Plant drought stress: effects, mechanisms and management. Sustain Agric. 2009;153?88. https://doi.org/10.1007/978-90-481-2666-8_12

Lephatsi M, Nephali L, Meyer V, Piater LA, Buthelezi N, Dubery IA, et al. Molecular mechanisms associated with microbial biostimulant-mediated growth enhancement, priming and drought stress tolerance in maize plants. Sci Rep. 2022;12(1):10450. https://doi.org/10.1038/s41598-022-14570-7

Etesami H. Potential advantage of rhizosheath microbiome, in contrast to rhizosphere microbiome, to improve drought tolerance in crops. Rhizosphere. 2021;20:100439. https://doi.org/10.1016/j.rhisph.2021.100439

Lastochkina O, Garshina D, Ivanov S, Yuldashev R, Khafizova R, Allagulova C, et al. Seed priming with endophytic Bacillus subtilis modulates physiological responses of two different Triticum aestivum L. cultivars under drought stress. Plants. 2020;9(12):1810. https://doi.org/10.3390/plants9121810

Alharby HF, Alzahrani YM, Rady MM. Seeds pretreatment with zeatins or maize grain-derived organic biostimulant improved hormonal contents, polyamine gene expression and salinity and drought tolerance of wheat. Intl J Agric Biol. 2020; 24(4):714?24.

Etesami H, Jeong BR, Glick BR. Potential use of Bacillus spp. as an effective biostimulant against abiotic stresses in crops—A review. Curr Res Biotechnol. 2023;100128. https://doi.org/10.1016/j.crbiot.2023.100128

Demehin O, Attjioui M, Goñi O, O’Connell S. Chitosan from mushroom improves drought stress tolerance in tomatoes. Plants. 2024;13(7):1038. https://doi.org/10.3390/plants13071038

Navarro-Morillo I, Navarro-León E, Atero-Calvo S, Rios JJ, Ruiz JM, Blasco B. Biostimulant-induced mitigation of cold and drought stresses in zucchini plants. Sci Hortic. 2024;331:113114. https://doi.org/10.1016/j.scienta.2024.113114

Khorasani H, Rajabzadeh F, Mozafari H, Pirbalouti AG. Water deficit stress impairment of morphophysiological and phytochemical traits of Stevia (Stevia rebaudiana Bertoni) buffered by humic acid application. S Afr J Bot. 2023;154:365?71. https://doi.org/10.1016/j.sajb.2023.01.030

Shabala S, Pottosin I. Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant. 2014;151(3):257?79. https://doi.org/10.1111/ppl.12165

Supraja K, Behera B, Balasubramanian P. Efficacy of microalgal extracts as biostimulants through seed treatment and foliar spray for tomato cultivation. Ind Crops Prod. 2020;151:112453. https://doi.org/10.1016/j.indcrop.2020.112453

Etesami H, Glick BR. Halotolerant plant growth–promoting bacteria: Prospects for alleviating salinity stress in plants. Environ Exp Bot. 2020;178:104124. https://doi.org/10.1016/j.envexpbot.2020.104124

Masrahi AS, Alasmari A, Shahin MG, Qumsani AT, Oraby HF, Awad-Allah MM. Role of arbuscular mycorrhizal fungi and phosphate solubilizing bacteria in improving yield, yield components and nutrients uptake of barley under salinity soil. Agriculture. 2023;13(3):537. https://doi.org/10.3390/agriculture13030537

Lastochkina O, Pusenkova L, Yuldashev R, Babaev M, Garipova S, Blagova Dy, et al. Effects of Bacillus subtilis on some physiological and biochemical parameters of Triticum aestivum L. (wheat) under salinity. Plant Physiol Biochem. 2017;121:80?88. https://doi.org/10.1016/j.plaphy.2017.10.020

Saadat H, Sedghi M. The effect of seed priming with chitosan on the improvement of physiological and biochemical traits of soybean (Glycine max (L.) Merrill) under salinity stress. Russ J Plant Physiol. 2024;71(6):187. https://doi.org/10.1134/S1021443724605858

Gul S, Nawaz MF, Yousaf MT, Rashid MH, Adnan MY, Tausif S, et al. Brown macro-seaweeds derived agro-biostimulant for Zea mays farming in saline conditions: Growth enhancement and optimum biochemical and ion feedback. Biocatal Agric Biotechnol. 2024;57:103105.https://doi.org/10.1016/j.bcab.2024.103105

Ennab HA, Mohamed AH, El-Hoseiny HM, Omar AA, Hassan IF, Gaballah MS, et al. Humic acid improves the resilience to salinity stress of drip-irrigated Mexican lime trees in saline clay soils. Agron. 2023 Jun 22;13(7):1680. https://doi.org/10.3390/agronomy13071680

Zamljen T, Medic A, Hudina M, Veberic R, Slatnar A. Biostimulative effect of amino acids on the enzymatic and metabolic response of two Capsicum annuum L. cultivars grown under salt stress. Sci Hortic. 2023;309:111713. https://doi.org/10.1016/j.scienta.2022.111713

Salehi S, Rezayatmand Z. The effect of foliar application of chitosan on yield and essential oil of savory (Satureja isophylla L.) under salt stress. J Med Herbs. 2017;8(2):101?08. https://doi.org/10.18869/JHD.2017.101

Szyma?ska R, ?lesak I, Orzechowska A, Kruk J. Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot. 2017;139:165?77. https://doi.org/10.1016/j.envexpbot.2017.05.002

Chinnusamy V, Zhu J, Zhu J-K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12(10):444?51. https://doi.org/10.1016/j.tplants.2007.07.002

Campobenedetto C, Grange E, Mannino G, Arkel VJ, Beekwilder J, Karlova R, et al. A biostimulant seed treatment improved heat stress tolerance during cucumber seed germination by acting on the antioxidant system and glyoxylate cycle. Front Plant Sci. 2020;11(836):1?12. https://doi.org/10.3389/fpls.2020.00836

Rayirath P, Benkel B, Hodges MD, Allan-Wojtas P, MacKinnon S, Critchley AT, Prithiviraj B. Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta. 2009;230:135?47. https://doi.org/10.1007/s00425-009-0920-8

Moradtalab N, Weinmann M, Walker F, Höglinger B, Ludewig U, Neumann G. Silicon improves chilling tolerance during early growth of maize by effects on micronutrient homeostasis and hormonal balances. Front Plant Sci. 2018;9(420):1?17. https://doi.org/10.3389/fpls.2018.00420

Jayaweera DP, Dambire C, Angelopoulou D, Munné-Bosch S, Swarup R, Ray RV. Physiological, molecular and genetic mechanism of action of the biostimulant Quantis™ for increased thermotolerance of potato (Solanum tuberosum L.). Chem Biol Technol Agric. 2024;11(9):1?19. https://doi.org/10.1186/s40538-023-00531-3

Li H, Kong F, Tang T, Luo Y, Gao H, Xu J, et al. Physiological and transcriptomic analyses revealed that humic acids improve low-temperature stress tolerance in zucchini (Cucurbita pepo L.) seedlings. Plants. 2023;12(3):548. https://doi.org/10.3390/plants12030548

Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, et al. Heavy metal stress and crop productivity. Crop Prod and Global Environ Issues. 2015;1?25. https://doi.org/10.1007/978-3-319-23162-4_1

Etesami H. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicol Environ Saf. 2018;147:175?91. https://doi.org/10.1016/j.ecoenv.2017.08.032

Desoky ESM, Merwad ARM, Semida WM, Ibrahim SA, El-Saadony MT, Rady MM. Heavy metals-resistant bacteria (HM-RB): Potential bioremediators of heavy metals-stressed Spinacia oleracea plant. Ecotoxicol Environ Saf. 2020;198:110685. https://doi.org/10.1016/j.ecoenv.2020.110685

El Khattabi O, El Hasnaoui S, Toura M, Henkrar F, Collin B, Levard C, et al. Seaweed extracts as promising biostimulants for enhancing lead tolerance and accumulation in tomato (Solanum lycopersicum). J Appl Phycol. 2023 Feb;35(1):459?69. https://doi.org/10.1007/s10811-022-02849-1

Ghadbane M, Medjekal S, Benderradji L, Belhadj H, Daoud H. Assessment of arbuscular mycorrhizal fungi status and Rhizobium on date palm (Phoenix dactylifera L.) cultivated in a Pb contaminated soil. In: Recent advances in environmental science from the Euro-Mediterranean and surrounding regions (2nd Edition). Proceedings of 2nd Euro-Mediterranean Conference for Environmental Integration (EMCEI-2), Tunisia 2019. Springer International Publishing; 2021. pp. 703?07. https://doi.org/10.1007/978-3-030-51210-1_111

Francis B, Aravindakumar CT, Brewer PB, Simon S. Plant nutrient stress adaptation: A prospect for fertilizer limited agriculture. Environ Exp Bot. 2023;105431. https://doi.org/10.1016/j.envexpbot.2023.105431

Pandey R, Vengavasi K, Hawkesford MJ. Plant adaptation to nutrient stress. Plant Physiol Rep. 2021;26(4):583?86. https://doi.org/10.1007/s40502-021-00636-7

Halpern M, Bar-Tal A, Ofek M, Minz D, Muller T, Yermiyahu U. The use of biostimulants for enhancing nutrient uptake. Adv Agron. 2015;130:141?74. https://doi.org/10.1016/bs.agron.2014.10.001

Corona BEL, Ocampo AG, Juárez DR, García JO, Fernández IM, Puente EOR. Biostimulant effect of chitosan and phenolic extracts on the phenological development of the halophyte Salicornia bigelovii (Torr.). J Saudi Soc Agric Sci. 2023;22(8):584?90. https://doi.org/10.1016/j.jssas.2023.08.001

Al-Barakat HNK, Naser MA, Habeeb KH. Humic and fulvic fertilizers and zinc spray impact on the availability of zinc and phosphorous in soil and maize crop yield. Biopestic Int. 2023;19(1):75. https://doi.org/10.59467/BI.2023.19.75

Zhang Q, Kong Y, Masabni J, Niu G. Onion peel waste has the potential to be converted into a useful agricultural product to improve vegetable crop growth. HortSci. 2024;59(5):578?86. https://doi.org/10.21273/HORTSCI17694-24

Herrmann MN, Griffin LG, John R, Mosquera-Rodríguez SF, Nkebiwe PM, Chen X, et al. Limitations of soil-applied non-microbial and microbial biostimulants in enhancing soil P turnover and recycled P fertilizer utilization-a study with and without plants. Front Plant Sci. 2024;15:1?13. https://doi.org/10.3389/fpls.2024.1465537

Bhupenchandra I, Chongtham SK, Devi EL, Choudhary AK, Salam MD, Sahoo MR, et al. Role of biostimulants in mitigating the effects of climate change on crop performance. Front Plant Sci. 2022;13:1?19. https://doi.org/10.3389/fpls.2022.967665

Hamedani RS, Rouphael Y, Colla G, Colantoni A, Cardarelli M. Biostimulants as a tool for improving environmental sustainability of greenhouse vegetable crops. Sustain. 2020;12(12):5101. https://doi.org/10.3390/su12125101

O'Callaghan M, Ballard RA, Wright D. Soil microbial inoculants for sustainable agriculture: Limitations and opportunities. Soil Use Manag. 2022;38(3):1340?69. https://doi.org/10.1111/sum.12811

Rouphael Y, Colla G. Biostimulants in agriculture. Front Plant Sci. 2020;11(40):1?7. https://doi.org/10.3389/fpls.2020.00040