Abstract
The current research has been conceptualized to see the impact of Trichoderma harzianum synthesized siderophore in alleviation of heavy metal stress [lead (Pb), mercury (Hg) and cadmium (Cd)] first time for Solanum melongena under high concentration. Alongside, we reported impact of siderophore in form of product for S. melongena seed germination in presence of heavy metal stress under high and low concentration. Optimization of siderophore production was achieved using Response Surface Methodology (RSM) that resulted in an increment of siderophore production. Through RSM, 92.7% siderophore unit was obtained whereas without using RSM only 89.1% siderophore unit was obtained. The novelty of this work lies in the fact that T. harzianum synthesized metal chelators have not been used previously for S. melongena seed germination under different heavy metal stress (Pb, Hg and Cd). Based on obtained results, we have found that in case of siderophore treated seeds, germination percentage was increased such as in 400 mg/kg of Cd and Pb concentration (with siderophore) seeds germination % was 66.6 ± 3.4% and 62.5 ± 6.8% respectively, whereas non-siderophore treated seeds germination % was 30.5 ± 5.1% and 27.7 ± 5.1% respectively. In presence of 100 mg/kg of Hg with siderophore, seed germination % was 59.7 ± 7.8% whereas in Hg stressed seeds (non siderophore treated) germination was 19.2 ± 3.9% respectively. The cluster heat map was deployed to analyze the effect of siderophore treatment on S. melongena seedling under heavy metal stress. Obtained results suggested that we can deploy the use of RSM to enhance the siderophore production using different factors such as carbon, nitrogen, pH and FeCl3 etc. It is worthwhile approach to use siderophore as plant growth promotor in heavy metal stress due to its metal chelating activity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abd-Alla MH (1998) Growth and siderophore production in vitro of Bradyrhizobium (Lupin) strains under iron limitation. Eur J Soil Biol 34:99–104. https://doi.org/10.1016/S1164-5563(99)80007-7
Abo-Elyousr KAM, Marei Almasaudi N (2022) Application of Trichoderma harzianum strain KABOFT4 for management of tomato bacterial wilt under greenhouse conditions. Gesunde Pflanzen 74:413–421. https://doi.org/10.1007/s10343-021-00618-7
Argandoña M, Nieto JJ, Iglesias-Guerra F et al (2010) Interplay between iron homeostasis and the osmotic stress response in the halophilic bacterium Chromohalobacter salexigens. Appl Environ Microbiol 76:3575–3589. https://doi.org/10.1128/AEM.03136-09
Arnow LE (1937) Colorimetric determination of the components of 3,4-dihydroxyphenylalaninetyrosine mixtures. J Biol Chem 118:531–537. https://doi.org/10.1016/s0021-9258(18)74509-2
Arora NK, Verma M (2017) Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech. https://doi.org/10.1007/s13205-017-1008-y
Baakza A, Vala AK, Dave BP, Dube HC (2004) A comparative study of siderophore production by fungi from marine and terrestrial habitats. J Exp Mar Biol Ecol 311:1–9. https://doi.org/10.1016/J.JEMBE.2003.12.028
Baran A, Antonkiewicz J (2017) Phytotoxicity and extractability of heavy metals from industrial wastes. Environ Prot Eng 43:143–155. https://doi.org/10.5277/epe170212
Böttcher T, Clardy J (2014) A chimeric siderophore halts swarming vibrio. Angew Chem Int Ed 53:3510–3513. https://doi.org/10.1002/anie.201310729
Bueno P, Piqueras A (2002) Effect of transition metals on stress, lipid peroxidation and antioxidant enzyme activities in tobacco cell cultures. Plant Growth Regul 36:161–167. https://doi.org/10.1023/A:1015044705137
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468. https://doi.org/10.1111/j.1399-3054.1991.tb00121.x
Calvente V, De Orellano ME, Sansone G et al (2001) A simple agar plate assay for screening siderophore producer yeasts. J Microbiol Methods 47:273–279. https://doi.org/10.1016/S0167-7012(01)00333-5
Carroll CS, Amankwa LN, Pinto LJ et al (2016) Detection of a serum siderophore by LC-MS/MS as a potential biomarker of invasive aspergillosis. PLoS ONE 11:1–16. https://doi.org/10.1371/journal.pone.0151260
Chandwani S, Dewala S, Chavan SM et al (2023) Complete genome sequencing of Bacillus subtilis (CWTS 5), a siderophore-producing bacterium triggers antagonistic potential against Ralstonia solanacearum. J Appl Microbiol. https://doi.org/10.1093/jambio/lxad066
Chowdappa S, Jagannath S, Konappa N et al (2020) Detection and characterization of antibacterial siderophores secreted by endophytic fungi from Cymbidium aloifolium. Biomolecules. https://doi.org/10.3390/biom10101412
Dabral S, Yashaswee VA et al (2019) Biopriming with Piriformospora indica ameliorates cadmium stress in rice by lowering oxidative stress and cell death in root cells. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2019.109741
Dhungana S, White PS, Crumbliss AL (2001) Crystal structure of ferrioxamine B: a comparative analysis and implications for molecular recognition. J Biol Inorg Chem 6:810–818. https://doi.org/10.1007/s007750100259
Di Francesco A, Sciubba L, Bencivenni M et al (2022) Application of Aureobasidium pullulans in iron-poor soil. Can the production of siderophores improve iron bioavailability and yeast antagonistic activity? Ann Appl Biol 180:398–406. https://doi.org/10.1111/aab.12742
Dimkpa C, Svatoš A, Merten D et al (2008) Hydroxamate siderophores produced by Streptomyces acidiscabies E13 bind nickel and promote growth in cowpea (Vigna unguiculata L.) under nickel stress. Can J Microbiol 54:163–172. https://doi.org/10.1139/W07-130
Dimkpa CO, Svatoš A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces spp. Chemosphere 74:19–25. https://doi.org/10.1016/J.CHEMOSPHERE.2008.09.079
Dimkpa CO, Merten D, Svatoš A et al (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162. https://doi.org/10.1016/j.soilbio.2008.10.010
Duffy BK, Genevieve G, Fago DÉ (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438
Filippone E, Tranchida-Lombardo V, Vitiello A et al (2022) Evaluation of cadmium effects on six Solanum melongena L. cultivars from the Mediterranean basin. Agriculture (switzerland) 12:1. https://doi.org/10.3390/agriculture12071059
Gaba S, Rai AK, Varma A et al (2022) Biocontrol potential of mycogenic copper oxide nanoparticles against Alternaria brassicae. Front Chem 10:1–18. https://doi.org/10.3389/fchem.2022.966396
Ghosh SK, Banerjee S, Sengupta C (2017) Siderophore production by antagonistic fungi (Coleoptera: Chrysomelidae: Bruchinae) © 527 Bioassay, characterization and estimation of siderophores from some important antagonistic fungi
Ghosh SK, Bera T, Chakrabarty AM (2020) Microbial siderophore—a boon to agricultural sciences. Biol Control 144:104214
Goodell B, Jellison J, Liu J et al (1997) Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood. J Biotechnol 53:133–162. https://doi.org/10.1016/S0168-1656(97)01681-7
Grobelak A, Hiller J (2017) Bacterial siderophores promote plant growth: screening of catechol and hydroxamate siderophores. Int J Phytoremediat 19:825–833. https://doi.org/10.1080/15226514.2017.1290581
Groppa MD, Ianuzzo MP, Rosales EP et al (2012) Cadmium modulates NADPH oxidase activity and expression in sunflower leaves. Biol Plant 56:167–171
Haselwandter K, Winkelmann G (2002) Ferricrocin—an ectomycorrhizal siderophore of Cenococcum geophilum. Biometals 15:73–77. https://doi.org/10.1023/A:1013188823076
Heyno E, Klose C, Krieger-Liszkay A (2008) Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol 179:687–699. https://doi.org/10.1111/j.1469-8137.2008.02512.x
Kalyan VSRK, Meena S, Karthikeyan S, Jawahar D (2022) Isolation, screening, characterization, and optimization of bacterium isolated from calcareous soils for siderophore production. Arch Microbiol 204:1–28. https://doi.org/10.21203/rs.3.rs-1365991/v1
Kang SM, Shahzad R, Khan MA et al (2021) Ameliorative effect of indole-3-acetic acid- and siderophore-producing Leclercia adecarboxylata MO1 on cucumber plants under zinc stress. J Plant Interact 16:30–41. https://doi.org/10.1080/17429145.2020.1864039
Khan A, Singh P, Srivastava A (2018) Synthesis, nature and utility of universal iron chelator—siderophore: a review. Microbiol Res 212–213:103–111. https://doi.org/10.1016/j.micres.2017.10.012
Kiran Kalyan R (2022) Isolation, screening, characterization, and optimization of bacterium isolated from calcareous soils for siderophore production. Arch Microbiol. https://doi.org/10.21203/rs.3.rs-1365991/v1
Kumari S, Vaishnav A, Jain S et al (2015) Bacterial-mediated induction of systemic tolerance to salinity with expression of stress alleviating enzymes in soybean (Glycine max L. Merrill). J Plant Growth Regul 34:558–573. https://doi.org/10.1007/s00344-015-9490-0
Kumari S, Khan A, Singh P et al (2019) Mitigation of As toxicity in wheat by exogenous application of hydroxamate siderophore of Aspergillus origin. Acta Physiol Plant. https://doi.org/10.1007/s11738-019-2902-1
Kumari S, Kumar P, Kiran S et al (2022) Optimization of siderophore production by Bacillus subtilis DR2 and its effect on growth promotion of Coriandrum sativum. Russ Agric Sci 48:467–475
Milagres AMF, Machuca A, Napoleão D (1999) Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J Microbiol Methods 37:1–6. https://doi.org/10.1016/S0167-7012(99)00028-7
Murugappan RM, Aravinth A, Karthikeyan M (2011) Chemical and structural characterization of hydroxamate siderophore produced by marine Vibrio harveyi. J Ind Microbiol Biotechnol 38:265–273. https://doi.org/10.1007/s10295-010-0769-7
Murugappan RM, Aravinth A, Rajaroobia R et al (2012) Optimization of MM9 medium constituents for enhancement of siderophoregenesis in marine pseudomonas putida using response surface methodology. Indian J Microbiol 52:433–441. https://doi.org/10.1007/s12088-012-0258-y
Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414. https://doi.org/10.1007/s00284-010-9722-2
Neilands JB (1954) Methodology of siderophores. Siderophores from microorganisms and plants. Springer, Berlin, pp 1–24
Nimbalkar RUR, Barge NS, Marathe RJ et al (2021) Application of response surface methodology for optimization of siderophore production. Indian J Agric Res. https://doi.org/10.18805/ijare.a-5663
Nithyapriya S, Lalitha S, Sayyed RZ et al (2021) Production, purification, and characterization of Bacillibactin siderophore of Bacillus subtilis and its application for improvement in plant growth and oil content in sesame. Sustainability. https://doi.org/10.3390/su13105394
Osman Y, Gebreil A, Mowafy AM et al (2019) Characterization of Aspergillus niger siderophore that mediates bioleaching of rare earth elements from phosphorites. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-019-2666-1
Pahari A, Mishra BB (2017) Characterization of siderophore producing rhizobacteria and its effect on growth performance of different vegetables. Int J Curr Microbiol Appl Sci 6:1398–1405. https://doi.org/10.20546/ijcmas.2017.605.152
Patel AK, Deshattiwar MK, Chaudhari BL, Chincholkar SB (2009) Production, purification and chemical characterization of the catecholate siderophore from potent probiotic strains of Bacillus spp. Bioresour Technol 100:368–373. https://doi.org/10.1016/J.BIORTECH.2008.05.008
Plackett RL, Burman JP (1946) The design of optimum multifactorial experiments author (s): R. L. Plackett , and J. P. Burman. published by: Biometrika stable URL : http://www.jstor.org/stable/2. Biometrika 33:305–325
Pluháček T, Lemr K, Ghosh D et al (2016) Characterization of microbial siderophores by mass spectrometry. Mass Spectrom Rev 35:35–47. https://doi.org/10.1002/mas.21461
Pourrut B, Shahid M, Dumat C et al (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136. https://doi.org/10.1007/978-1-4419-9860-6_4ï
Qi W, Zhao L (2013) Study of the siderophore-producing Trichoderma asperellum Q1 on cucumber growth promotion under salt stress. J Basic Microbiol 53:355–364. https://doi.org/10.1002/jobm.201200031
Rahoui S, Chaoui A, El Ferjani E (2010) Membrane damage and solute leakage from germinating pea seed under cadmium stress. J Hazard Mater 178:1128–1131. https://doi.org/10.1016/J.JHAZMAT.2010.01.115
Rajenimbalkar RU, Barge NS, Marathe RJ et al (2022) Application of response surface methodology for optimization of siderophore production. Indian J Agric Res 56:230–237
Roy N, Bhattacharyya P, Chakrabartty PK (1994) Iron acquisition during growth in an iron-deficient medium by Rhizobium sp. isolated from Cicer arietinum. Microbiology (n Y) 140:2811–2820. https://doi.org/10.1099/00221287-140-10-2811
Sadeghi A, Karimi E, Dahaji PA et al (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28:1503–1509. https://doi.org/10.1007/s11274-011-0952-7
Sah S, Singh R (2015) Siderophore: structural and functional characterisation—a comprehensive review. Agriculture 61:97–114
Sahu S, Prakash A (2021) Siderophore from Talaromyces trachyspermus: augmentation and characterization. bioRxiv. https://doi.org/10.1101/2021.04.13.439607
Santos S, Neto IFF, Machado MD et al (2014) Siderophore production by Bacillus megaterium: effect of growth phase and cultural conditions. Appl Biochem Biotechnol 172:549–560. https://doi.org/10.1007/s12010-013-0562-y
Sasirekha B, Srividya S (2016) Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agric Nat Resour 50:250–256. https://doi.org/10.1016/J.ANRES.2016.02.003
Saxena R, Singh R (2010) Statistical optimization of conditions for protease production from Bacillus sp. Acta Biologica Szegediensis 54:135–141
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56. https://doi.org/10.1016/0003-2697(87)90612-9
Seneviratne M, Vithanage M (2015) The role of siderophores on plants under heavy meal stress: a view from the rhizosphere. Res Rev 4:23–29
Sepehri M, Khatabi B (2021) Combination of siderophore-producing bacteria and Piriformospora indica provides an efficient approach to improve cadmium tolerance in alfalfa. Microbe Ecol 81:717–730. https://doi.org/10.1007/s00248-020-01629-z/Published
Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272–275
Shaikh SS, Wani SJ, Sayyed RZ (2016) Statistical-based optimization and scale-up of siderophore production process on laboratory bioreactor. 3 Biotech. https://doi.org/10.1007/s13205-016-0365-2
Sharaff MM, Subrahmanyam G, Kumar A, Yadav AN (2020) Mechanistic understanding of the root microbiome interaction for sustainable agriculture in polluted soils. Elsevier, Amsterdam
Sharma C, Salem GEM, Sharma N et al (2020) Thrombolytic potential of novel thiol-dependent fibrinolytic protease from Bacillus cereus RSA1. Biomolecules 10:1–23. https://doi.org/10.3390/biom10010003
Sharma N, Dabral S, Tyagi J et al (2023) Interaction studies of Serendipita indica and Zhihengliuella sp. ISTPL4 and their synergistic role in growth promotion in rice. Front Plant Sci 14:1. https://doi.org/10.3389/fpls.2023.1155715
Sierra MJ, Millán R, Esteban E (2008) Potential use of Solanum melongena in agricultural areas with high mercury background concentrations. Food Chem Toxicol 46:2143–2149. https://doi.org/10.1016/j.fct.2008.02.009
Singh S, Prasad SM (2014) Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci Hortic 176:1–10. https://doi.org/10.1016/j.scienta.2014.06.022
Singh M, Singh P, Prasad SM (2022) α-Ketoglutarate enhanced Solanum melongena L. growth: acceleration of nitrogen assimilating enzymes and antioxidant system under arsenate toxicity. J Plant Growth Regul 41:1699–1713. https://doi.org/10.1007/s00344-021-10405-3
Sinha S, Mukherjee SK (2008) Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr Microbiol 56:55–60. https://doi.org/10.1007/s00284-007-9038-z
Sistrom DE, Machlis L (1954) Diploid, produced sporophytic. pp 50–55
Sultana S, Alam S, Karim MM (2021) Screening of siderophore-producing salt-tolerant rhizobacteria suitable for supporting plant growth in saline soils with iron limitation. J Agric Food Res 4:100150. https://doi.org/10.1016/J.JAFR.2021.100150
Sun Y, Juanli W, Shang X et al (2022) Screening of siderophore-producing bacteria and their effects on promoting the growth of plants. Curr Microbiol. https://doi.org/10.1007/s00284-022-02777-w
Tailor AJ, Joshi BH (2012) Characterization and optimization of siderophore production from Pseudomonas fluorescens strain isolated from sugarcane rhizosphere. J Environ Res Dev 6:688–694
Teta R, Esposito G, Kundu K et al (2022) A glimpse at siderophores production by anabaena flos-aquae UTEX 1444. Mar Drugs. https://doi.org/10.3390/md20040256
Tsutsumi M (1980) Intensification of arsenic toxicity to paddy rice by hydrogen sulfide and ferrous iron I induction of bronzing and iron accumulation in rice by arsenic. Soil Sci Plant Nutr 26:561–569. https://doi.org/10.1080/00380768.1980.10431243
Vaishnav A, Kumar R, Singh HB, Sarma BK (2022) Extending the benefits of PGPR to bioremediation of nitrile pollution in crop lands for enhancing crop productivity. Sci Total Environ 826:154170. https://doi.org/10.1016/J.SCITOTENV.2022.154170
Vinale F, Nigro M, Sivasithamparam K et al (2013) Harzianic acid: a novel siderophore from Trichoderma harzianum. FEMS Microbiol Lett 347:123–129
Völker C, Wolf-Gladrow DA (1999) Physical limits on iron uptake mediated by siderophores or surface reductases. Mar Chem 65:227–244. https://doi.org/10.1016/S0304-4203(99)00004-3
Waldron KJ, Tottey S, Yanagisawa S et al (2007) A periplasmic iron-binding protein contributes toward inward copper supply. J Biol Chem 282:3837–3846. https://doi.org/10.1074/jbc.M609916200
Wang YH, Feng JT, Zhang Q, Zhang X (2008) Optimization of fermentation condition for antibiotic production by Xenorhabdus nematophila with response surface methodology. J Appl Microbiol 104:735–744. https://doi.org/10.1111/j.1365-2672.2007.03599.x
Wang Y-J, Huang W, Li Y-Q et al (2021) Isolation, characterization and evaluation of a high-siderophore-yielding bacterium from heavy metal contaminated soil. Environ Sci Pollut Res. https://doi.org/10.21203/rs.3.rs-468448/v1
Wang Y, Huang W, Ali SW et al (2022) Isolation, identification, and characterization of an efficient siderophore producing bacterium from heavy metal contaminated soil. Curr Microbiol 7:9. https://doi.org/10.1007/s00284-022-02922-5
Winkelmann G, Schmid DG, Nicholson G et al (2002) Bisucaberin—a dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar). Biometals 15:153–160. https://doi.org/10.1023/A:1015206419613
Yadav G, Srivastva R, Gupta P (2021) Endophytes and their applications as biofertilizers. In: Microbial technology for sustainable environment. Springer, Singapore pp 95–123
Yadav G, Sharma N, Dabral S et al (2023) Functional insight of siderophore in reducing cadmium stress and inducing growth promotion in Solanum melongena. S Afr J Bot 158:479–494. https://doi.org/10.1016/J.SAJB.2023.05.032
Yilmaz K, Akinci İE, Akinci S (2009) Effect of lead accumulation on growth and mineral composition of eggplant seedlings (Solarium melongena). N Z J Crop Hortic Sci 37:189–199. https://doi.org/10.1080/01140670909510264
Yu S, Teng C, Bai X et al (2017) Optimization of siderophore production by Bacillus sp. PZ-1 and its potential enhancement of phytoextration of PB from soil. J Microbiol Biotechnol 27:1500. https://doi.org/10.4014/jmb.1705.05021
Acknowledgements
Authors would like to thanks Amity Institute of Microbial Technology for providing facilities.
Funding
None.
Author information
Authors and Affiliations
Contributions
GY: data collection, formal evaluation, conception, research, methodology, and software, NS: writing, and experiment, AG: conceptualization, AV: review, SLK: conceptualization and review, AM: methodology and software, DKC: Direction, Writing—review & editing, validation, representation, first draft.
Corresponding author
Ethics declarations
Conflict of interest
No author is involved in any conflict of interest.
Additional information
Handling Editor: Anket Sharma.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yadav, G., Sharma, N., Goel, A. et al. Trichoderma Mediated Metal Chelator and Its Role in Solanum melongena Growth Under Heavy Metals. J Plant Growth Regul 43, 178–200 (2024). https://doi.org/10.1007/s00344-023-11072-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11072-2