Abstract
This study aimed to investigate using Stypopodium schimperi, brown alga extract, as a biofertilizer. Algae can be an essential bio-stimulant that increases plant growth and development. Brown algae especially have critical biological activities due to their high secondary metabolite content. This study also determined the biochemical and physicochemical composition and phenolic content of the S. schimperi, an alien brown alga in the Mediterranean Sea.
Dose-dependent effects of these extracts on seed germination, root-shoot growth, seedling vigor index, and genome stability of Solanum lycopersicum plant were studied. Inductively coupled plasma mass spectrometry (ICP-MS) analysis revealed the primary elemental composition of the effective extract (10%). Attenuated Total Reflectance-Fourier Transform Infrared (ATR-FTIR) spectroscopy showed phloroglucinol composition, the primary structural molecule of a phlorotannin, in the content of the extract. In addition, the phenolic content was determined by the Folin-Ciocalteu method, while the phenol-sulphuric acid method was used to determine carbohydrates by spectrophotometer. Genomic template analysis was conducted by calculating Inter Simple Sequence Repeats (ISSR) profile changes.
Na, Mg, K, Fe, Mo, and Se were determined as elemental compositions of the 10% extract according to ICP-MS analysis. The ATR-FTIR resulted in four different spectral bands at 3350 cm−1, 2936 cm−1, 1636 cm−1, and 1414 cm−1, which were attributed to the phloroglucinol components. Our results showed that the highest phloroglucinol concentration could inhibit root growth and decrease genomic template stability (GST). The GTS difference between the control and 0.5% extract-treated group was approximately 91.38%, as revealed by ISSR analysis. The lowest GTS value (39.66%) was observed in the roots of S. lycopersicum treated with 5% extract.
The present study demonstrated for the first time that a low concentration of S. schimperi extract could be used as a biofertilizer in agriculture. An alien macroalga that may be harmful to the ecosystem is being transformed into a beneficial one by being brought into the economy.
Similar content being viewed by others
Data availability
All data generated during this study are included in this published article. The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Agarwal P, Patel K, Das AK, Ghosh A, Agarwal PK (2016) Insights into the role of seaweed Kappaphycus alvarezii sap towards phytohormone signalling and regulating defence responsive genes in Lycopersicon esculentum. J Appl Phycol 28:2529–2537. https://doi.org/10.1007/s10811-015-0784-1
Ali O, Ramsubhag A, Jayaraman J (2021) Biostimulant properties of seaweed extracts in plants: implications towards sustainable crop production. Plants 10:531. https://doi.org/10.3390/plants10030531
Amlani M, Yetgin S (2022) Seaweeds: bioactive components and properties, potential risk factors, uses, extraction and purification methods. Mar Sci Technol Bull 11:9–31. https://doi.org/10.33714/masteb.1021121
Aydın B (2021) Antibacterial activities of methanolic extracts of different seaweeds from Iskenderun Bay, Turkey. IJSM 8:120–126. https://doi.org/10.21448/ijsm.894564
Baroud S, Tahrouch S, El Mehrach K, Sadki I, Fahmi F, Hatimi A (2021) Effects of brown algae on germination, growth and biochemical composition of tomato leaves (Solanum lycopersicum). J Saudi Soc Agric Sci 20:337–343. https://doi.org/10.1016/j.jssas.2021.03.005
Baroud S, Tahrouch S, Sadqi I, Hammou RA, Hati-mi A (2019) Effect of brown algae on germination, growth and biochemical composition of pepper leaves (Capsicum annuum). Atlas J Biol 611–618. https://doi.org/10.5147/ajb.v0i0.209
Booth E (1969) In: Blunden G (ed) The manufacture and properties of liquid seaweed extracts. Proceedings of the sixth international seaweed symposium, Tokyo, pp 655–662
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Budzałek G, Śliwińska-Wilczewska S, Wiśniewska K, Wochna A, Bubak I, Latała A, Wiktor JM (2021) Macroalgal defense against competitors and herbivores. Int J Mol Sci 22:7865. https://doi.org/10.3390/ijms22157865
Camargo JA, Alonso A (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Int 32:831–849. https://doi.org/10.1016/j.envint.2006.05.002
Cantarutti C, Dinu R, Mija A (2020) Biorefinery byproducts and epoxy biorenewable monomers: a structural elucidation of humins and triglycidyl ether of phloroglucinol cross-linking. Biomacromolecules 21:517–533. https://doi.org/10.1021/acs.biomac.9b01248
Carrasco-Gill S, Apaolaza LH, Lucena JJ (2018) Effect of several commercial seaweed extracts in the mitigation of iron chlorosis of tomato plants (Solanum lycopersicum L.). Plant Growth Regul 86:401–411. https://doi.org/10.1007/s10725-018-0438-9
Castellanos-Barriga LG, Santacruz-Ruvalcaba F, Hernández-Carmona G, Ramírez-Briones E, Hernández- Herrera RM (2017) Effect of seaweed liquid extracts from Ulva lactuca on seedling growth of mung bean (Vigna radiata). J Appl Phycol 29:2479–2488. https://doi.org/10.1007/s10811-017-1082-x
Çekiç FO, Ekinci S, Inal MS, Unal D (2017) Silver nanoparticles induced genotoxicity and oxidative stress in tomato plants. Turk J Biol 41:700–707. https://doi.org/10.3906/biy-1608-36
Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393. https://doi.org/10.1007/s10811-010-9560-4
D'Souza L, Devi P, Divya Shridhar MP, Naik CG (2008) Use of Fourier Transform Infrared (FTIR) spectroscopy to study cadmium-induced changes in Padina tetrastromatica (Hauck). Anal Chem Insights 3:135–143. https://doi.org/10.4137/117739010800300001
Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
Dumale JV, Ramosa GR, Divina CC (2016) Plant growth promoting effect, gibberellic acid and auxin like activity of liquid extract of Caulerpa racemosa on rice seed germination. Int J Agric Technol 12:2219–2226
Eef B, Marlies D, van Swam K, Veen A, Burger L (2018) Biostimulants. In: Identification of the seaweed biostimulant market (Phase 1). The North Sea Farm Foundation, A.D. Den Haag, The Netherlands
Feldscher B, Stammler A, Bögge H, Glaser T (2010) Synthesis and characterization of a trinuclear CuII3 complex bridged by an extended phloroglucinol-ligand: implications for a rational enhancement of ferromagnetic interactions. Dalton Trans 39:11675–11685. https://doi.org/10.1039/c0dt00961j
Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209. https://doi.org/10.1007/BF02670897
Galil B (2007) Seeing Red: alien species along the Mediterranean coast of Israel. Aquat Invasions 2:281–312. https://doi.org/10.3391/ai.2007.2.4.2
Garcia C, Furtado de Almeida AA, Costa M, Britto D, Valle R, Royaert S, Marelli JP (2019) Abnormalities in somatic embryogenesis caused by 2,4-D: an overview. Plant Cell, Tissue Organ Cult 137:193–212. https://doi.org/10.1007/s11240-019-01569-8
Górka B, Korzeniowska K, Lipok J, Wieczorek PP (2018) The biomass of algae and algal extracts in agricultural production. In: Gorka B (ed) Developments in applied phycology, 1st edn. Springer, Science and Business Media LLC, Berlin, Germany, pp 103–114
Gunupuru LR, Patel JS, Sumarah MW, Renaud JB, Mantin EG, Prithiviraj BA (2019) Plant biostimulant made from the marine brown algae Ascophyllum nodosum and chitosan reduce Fusarium head blight and mycotoxin contamination in wheat. PLoS One 11:1–19. https://doi.org/10.1371/journal.pone.0220562
Gupta S, Stirk WA, Plačková L, Kulkarni MG, Doležal K, Van Staden J (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
Hamouda MM, Saad-Allah KM, Gad D (2022) Potential of seaweed extract on growth, physiological, cytological and biochemical parameters of wheat (Triticum aestivum L.) Seedlings. J Soil Sci Plant Nutr 22:1818–1831. https://doi.org/10.1007/s42729-022-00774-3
Harwanto D, Negara BFSP, Tirtawijaya G, Meinita MDN, Choi JS (2022) Evaluation of toxicity of crude phlorotannins and phloroglucinol using different model organisms. Toxins 14:312. https://doi.org/10.3390/toxins14050312
Henry EC (2005) Report of alkaline extraction of aquatic plants. Science Advisory Council, Aquatic Plant Extracts, p 6
Hernández-Herrera RM, Santacruz-Ruvalcaba F, Ruiz-López MA, Norrie J, Hernández-Carmona G (2014) Effect of liquid seaweed extracts on growth of tomato seedlings (Solanum lycopersicum L.). J Appl Phycol 26:619–628. https://doi.org/10.1007/s10811-013-0078-4
Hong DD, Hien HM, Son PN (2007) Seaweeds from Vietnam used for functional food, medicine and biofertilizer. J Appl Phycol 19:817–826. https://doi.org/10.1007/s10811-007-9228-x
Hussain HI, Kasinadhuni N, Arioli T (2021) The effect of seaweed extract on tomato plant growth, productivity and soil. J Appl Phycol 33:1305–1314. https://doi.org/10.1007/s10811-021-02387-2
Hussein MH, Eltanahy E, Al Bakry AF, Elsafty N, Elshamy MM (2021) Seaweed extracts as prospective plant growth bio-stimulant and salinity stress alleviator for Vigna sinensis and Zea mays. J Appl Phycol 33:1273–1291. https://doi.org/10.1007/s10811-020-02330-x
Isah T (2015) Adjustments to in vitro culture conditions and associated anomalies in plants. Acta Biol Crac Ser Bot 57:9–28. https://doi.org/10.1515/abcsb-2015-0026
Islam MT, Gan HM, Ziemann M, Hussain HI, Arioli T, Cahill D (2020) Phaeophyceaean (Brown algal) extracts activate plant defense systems in Arabidopsis thaliana challenged with Phytophthora cinnamomi. Front Plant Sci 11:852. https://doi.org/10.3389/fpls.2020.00852
Ito T, Nisa K, Rakainsa SK, Lallo S, Morita H (2017) New phloroglucinol derivatives from Indonesian Baeckea frutescens. Tetrahedron 73:1177–1181. https://doi.org/10.1016/j.tet.2017.01.016
Jagota S, Dani H (1982) A new colorimetric technique for the estimation of vitamin C using Folin phenol reagent. Anal Biochem 127:178–182
Jones JB Jr (2012) Plant nutrition and soil fertility manual, 2nd edn. CRC press, Florida
Julia I, Oscar M, Analía L, Guilherme JZ, Virginia L (2020) Biofertilization with Macrocystis pyrifera algae extracts combined with PGPR-enhanced growth in Lactuca sativa seedlings. J Appl Phycol 32:4361–4371. https://doi.org/10.1007/s10811-020-02202-4
Kalaivanan C, Venkatesalu V (2012) Utilization of seaweed Sargassum myriocystum extracts as a stimulant of seedlings of Vigna mungo (L.) Hepper. Span J Agric Res 10:466–470. https://doi.org/10.5424/sjar/2012102-507-10
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
Kocira S, Szparaga A, Kuboń M, Czerwińska E, Piskier T (2019) Morphological and biochemical responses of Glycine max (L.) Merr. to the use of seaweed extract. Agronomy 9:93. https://doi.org/10.3390/agronomy9020093
Kumar G, Sahoo D (2011) Effect of seaweed liquid extract on growth and yield of Triticum aestivum var. Pusa Gold. J Appl Phycol 23:251–255. https://doi.org/10.1007/s10811-011-9660-9
Kumari R, Kaur I, Bhatnagar AK (2011) Effect of aqueous extract of Sargassum johnstonii Setchell and Gardner on growth, yield and quality of Lycopersicon esculentum Mill. J Appl Phycol 23:623–633. https://doi.org/10.1007/s10811-011-9651-x
Layek J, Das A, Idapuganti RG, Sarkar S, Ghosh A (2018) Seaweed extract as organic biostimulant improves productivity and quality of rice in Eastern Himalayas. J Appl Phycol 30:547–558. https://doi.org/10.1007/s10811-017-1225-0
Leyton A, Pezoa-Conte R, Barriga A, Buschmann AH, Mäki-Arvela P, Mikkola JP, Lienqueo ME (2016) Identification and efficient extraction method of phlorotannins from the brown seaweed Macrocystis pyrifera using an orthogonal experimental design. Algal Res 16:201–208. https://doi.org/10.1016/j.algal.2016.03.019
Li Y, Fu X, Duan D, Liu X, Xu J, Gao X (2017) Extraction and identification of phlorotannins from the brown alga, Sargassum fusiforme (Harvey) Setchell. Mar Drugs 15:49. https://doi.org/10.3390/md15020049
López A, Rico M, Rivero A, Suárez de Tangil M (2011) The effects of solvents on the phenolic contents and antioxidant activity of Stypocaulon scoparium algae extracts. Food Chem 125:1104–1109. https://doi.org/10.1016/j.foodchem.2010.09.101
Ma YF, Yuan F, Zhang XH, Zhou YL, Zhang XX (2017) Highly efficient enrichment of N-linked glycopeptides using a hydrophilic covalent-organic framework. Analyst 142:3212–3218. https://doi.org/10.1039/C7AN01027C
Michalak I, Chojnacka K (2015) Production of seaweed extracts by biological and chemical methods. In: Kim SK, Chojnacka K (eds) Marine algae extracts: processes, products, and applications. Wiley, Weinheim, Germany, pp 121–144
Michalak I, Tuhy Ł, Chojnacka K (2015) Seaweed extract by microwave-assisted extraction as plant growth biostimulant. Open Chem 13:1183–1195. https://doi.org/10.1515/chem-2015-0132
Mzibra A, Aasfar A, Mehdi K, Farrie Y, Boulif R, Kadmiri IM, Bamouh A, Allal D (2021) Improving growth, yield, and quality of tomato plants (Solanum lycopersicum L.) by the application of Moroccan seaweed-based biostimulants under greenhouse conditions. Agronomy 11:1373. https://doi.org/10.3390/agronomy11071373
Nagorskaya VP, Reunov AV, Lapshina LA, Ermak IM, Barabanova AO (2010) Inhibitor effect of k/b carrageenan from red alga Tichocarpus crinitus on the development of a potato virus X infection in leaves of Datura stramonium L. Biol Bull 37:653–658
Peng X, Tan Q, Zhou H, Xu J, Gu Q (2021) Discovery of phloroglucinols from Hypericum japonicum as ferroptosis inhibitors. Fitoterapia 153:104984. https://doi.org/10.1016/j.fitote.2021.104984
Puglisi I, La Bella E, Rovetto EI, Lo Piero AR, Baglieri A (2020) Biostimulant effect and biochemical response in lettuce seedlings treated with a Scenedesmus quadricauda extract. Plants 9:123. https://doi.org/10.3390/plants9010123
Rao GMN, Chatterjee R (2014) Effect of seaweed liquid fertilizer from Gracilaria textorii and Hypnea musciformis on seed germination and productivity of some vegetables crops. Univers J Plant Sci 2:115–120. https://doi.org/10.13189/ujps.2014.020701
Rengasamy KRR, Kulkarni MG, Stirk WA, Van Staden J (2015a) Eckol improves growth, enzyme activities, and secondary metabolite content in maize (Zea mays cv. Border King). J Plant Growth Regul 34:410–416. https://doi.org/10.1007/s00344-015-9479-8
Rengasamy KRR, Kulkarni MG, Stirk WA, Van Staden J (2015b) Eckol—a new plant growth stimulant from the brown seaweed Ecklonia maxima. J Appl Phycol 27:581–587. https://doi.org/10.1007/s10811-014-0337-z
Rengasamy KRR, Kulkarni MG, Pendota SC, Van Staden J (2016) Enhancing growth, phytochemical constituents and aphid resistance capacity in cabbage with foliar application of eckol—a biologically active phenolic molecule from brown seaweed. New Biotechnol 33:273–279. https://doi.org/10.1016/j.nbt.2015.11.002
Sampli P, Tsitsimpikou C, Vagias C, Harvala C, Roussis V (2000) Schimperiol, A new meroterpenoid from the brown alga Stypopodium schimperi. Nat Prod Lett 14:365–372. https://doi.org/10.1080/10575630008043769
Saravana PS, Choi JH, Park YB, Woo HC, Chun BS (2016) Evaluation of the chemical composition of brown seaweed (Saccharina japonica) hydrolysate by pressurized hot water extraction. Algal Res 13:246–254. https://doi.org/10.1016/j.algal.2015.12.004
Selvam GG, Sivakumar K (2013) Effect of foliar spray from seaweed liquid fertilizer of Ulva reticulata (Forsk.) on Vigna mungo L. and their elemental composition using SEM- energy dispersive spectroscopic analysis. Asian Pac J Reprod 2:119–125. https://doi.org/10.1016/S2305-0500(13)60131-1
Selvaraj S, Rajkumar P, Thirunavukkarasu K, Gunasekaran S, Kumaresan S (2018) Vibrational (FT-IR and FT-Raman), electronic (U.V.–vis) and quantum chemical investigations on pyrogallol: a study on benzenetriol dimers. Vib Spectrosc 95:16–22. https://doi.org/10.1016/j.vibspec.2018.01.003
Sethi P (2012) Biochemical composition of the marine brown algae Padina tetrastromatica Hauck. Int J Curr Pharm Res 4:117–118
Sivasankari S, Venkatesalu V, Anantharaj M, Chandrasekaran M (2006) Effect of seaweed extracts on the growth and biochemical constituents of Vigna sinensis. Bioresour Technol 97:1745–1751. https://doi.org/10.1016/j.biortech.2005.06.016
Soares C, Švarc-Gajić J, Oliva-Teles MT, Pinto E, Nastić N, Savić S, Almeida A, Delerue-Matos C (2020) Mineral composition of subcritical water extracts of Saccorhiza polyschides, a brown seaweed used as fertilizer in the North of Portugal. J Mar Sci Eng 8:1–11. https://doi.org/10.3390/jmse8040244
Sridhar S, Rengasamy R (2010) Effect of seaweed liquid fertilizer on the growth, biochemical constituents and yield of Tagetes erecta under field trials. J Phytol 2:61–68
Sunarpi H, Pebriani SA, Ambana Y, Putri FE, Nikmatullah A, Ghazali M, Kurnianingsih R, Prasedya ES (2019) Effect of inorganic fertilizer and brown alga solid extract on growth and yield of rice plants. AIP Conf Proc 2199:1–5. https://doi.org/10.1063/1.5141320
Teixeira da Silva JA, Dobránszki J, Ross S (2013) Phloroglucinol in plant tissue culture. In Vitro Cell Dev Biol Plant 49:1–16. https://doi.org/10.1007/s11627-013-9491-2
Thomas NV, Diyya ASM, Ghafour DD, Kim SK (2020) Marine algal Phlorotannins and their biological importance. Enc Mar Biotech 3:1535–1558. https://doi.org/10.1002/9781119143802.ch65
Uthirapandi V, Suriya S, Boomibalagan P, Eswaran S, Ramya SS, Vijayanand N, Kathiresan D (2018) Bio-fertilizer potential of seaweed liquid extracts of marine macroalgae on growth and biochemical parameters of Ocimum sanctum. J Pharmacogn Phytochem 7:3528–3532
Verlaque M, Ruitton S, Mineur F, Boudouresque CF (2007) CIESM Atlas of exotic macrophytes in the Mediterranean Sea. Rapport de la Commission de l'Exploration de la mer Méditerranée, Monaco. 38. available online at http://www.ciesm.org/atlas/appendix4.html#top. Accessed 12 Dec 2022
Vitamvas J, Viehmannova I, Cepkova PH, Mrhalova H, Eliasova K (2019) Assessment of somaclonal variation in indirect morphogenesis-derived plants of Arracacia xanthorrhiza. Pesqui Agropecu Bras 54:1–9. https://doi.org/10.1590/s1678-3921.pab2019.v54.00301
Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites methods in ecology. Blackwell Scientific Publications, Oxford
Yamagata K (2021) Prevention of cardiovascular disease through modulation of endothelial cell function by dietary seaweed intake. Phytomedic. Plus 1:100026. https://doi.org/10.1016/j.phyplu.2021.100026
Ye YS, Wu M, Jiang NN, Lao YZ, Fu WW, Liu X, Yang XW, Zhang J, Xu HX, Xu G (2020) Dearomatized isoprenylated acylphloroglucinol derivatives with potential antitumor activities from Hypericum henryi. Nat Prod Bioprospect 10:1–11. https://doi.org/10.1007/s13659-019-00229-w
Zeng X, Du Z, Sheng Z, Jiang W (2019a) Characterization of the interactions between banana condensed tannins and biologically important metal ions (Cu2+, Zn2+ and Fe2+). Food Res Int 123:518–528. https://doi.org/10.1016/j.foodres.2019.04.064
Zeng X, Du Z, Xu Y, Sheng Z, Jiang W (2019b) Characterization of the interactions between apple condensed tannins and biologically important metal ions [Fe2+ (3d6), Cu2+ (3d9) and Zn2+ (3d10)]. LWT 114:108384. https://doi.org/10.1016/j.lwt.2019.108384
Author information
Authors and Affiliations
Contributions
DU: Conceptualization, Methodology, Validation, Formal analysis, Investigation, Writing—Original Draft, Review & Editing, Visualization. RG: Investigation, Resources, Data Curation, Writing—Original Draft GS: Investigation, Methodology GS: Investigation, Methodology GV: Investigation, FOK: Investigation, Writing—Original Draft, Review & Editing, ITK: Methodology, Investigation, Writing—Original Draft, Review & Editing, Visualization
Corresponding author
Ethics declarations
Conflict of interest
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.
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
Unal, D., Gurbanov, R., Sevim, G. et al. Dose-dependent Plant-promoting Effect of Macroalgae Stypopodium schimperi Extracts in Solanum lycopersicum and Detection of Phloroglucinol Composition. J Soil Sci Plant Nutr 23, 2018–2029 (2023). https://doi.org/10.1007/s42729-023-01156-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-023-01156-z