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Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Ameliorative effect of Halopteris filicina extracts on growth parameters and genomic DNA template stability of tomato (Solanum lycopersicum) under lead chloride stress

Dilek Unal https://orcid.org/0000-0002-6915-9699 A * , Gulcin Sevim B , Gokay Varis A , Inci Tuney-Kizilkaya C , Bengu Turkyilmaz Unal https://orcid.org/0000-0003-4003-5200 D and Munir Ozturk C
+ Author Affiliations
- Author Affiliations

A Department of Molecular Biology and Genetics, Bilecik Seyh Edebali University, Bilecik 11230, Turkey.

B Biotechnology Application and Research Center, Department of Biotechnology, Institute of Undergraduate, Bilecik Seyh Edebali University, Bilecik 11230, Turkey.

C Department of Biology, Faculty of Science, Ege University, Izmir 35040, Turkey.

D Biotechnology Department, Arts and Sciences Faculty, Niğde Ömer Halisdemir University, Niğde 51240, Turkey.

* Correspondence to: dilek.unal@bilecik.edu.tr

Handling Editor: Shahid Hussain

Crop & Pasture Science - https://doi.org/10.1071/CP21455
Submitted: 28 June 2021  Accepted: 13 October 2021   Published online: 11 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Lead is a toxic element that accumulates in agricultural soils through various anthropogenic sources. It inhibits the growth and development of plants and causes mutations in DNA. Macroalgae such as Halopteris filicina contain multifunctional components that may improve plant tolerance to lead stress. In this study, seeds of tomato (Solanum lycopersicum) were subjected to six treatments comprising two levels of lead exposure (60 or 120 μM PbCl2) with or without H. filicina extract (0.5% in distilled water), a distilled water control, and a positive control (H. filicina extract) for 7 days. Physiological responses were investigated. Seedlings that had been treated with 60 and 120 μM PbCl2 without H. filicina extract showed root growth reduction of 55% and 68.6%, respectively, relative to the control, whereas for 60 and 120 μM PbCl2-treated seedlings with H. filicina extract applied, the reductions in root growth were lower, at 27.44% and 50.51%. The seedling viability index was decreased by 68.14% at 120 μM PbCl2 application without H. filicina extract, whereas a 42.48% reduction was recorded for 120 μM PbCl2-treated seedlings with H. filicina extract applied. Moreover, PbCl2 accumulation resulted in a decrease in leaf pigment content. Leaf pigment content was high in plants receiving the H. filicina extract. The rate of lipid peroxidation caused by PbCl2 was reduced with application of H. filicina extract. Genomic template stability was determined by using the inter simple sequence repeat-PCR technique, which revealed a decrease in DNA stabilisation with an increase in lead accumulation. However, this was alleviated by application of H. filicina extract. Our findings indicate that H. filicina extract both stimulates plant growth and protects from toxic effects by reducing accumulation of metals in the cell.

Keywords: chlorophyll content, DNA stability, ISSR-PCR, lead, macroalgae, metal tolerance, plant growth, tomato.


References

Abd-Elhady ESE (2015) Evaluation of algae dry biomass as a biochemical soil remediation for polluted soil. International Journal of Environment 4, 309–314.

Alamri SA, Siddiqui MH, Al-Khaishany MYY, et al. (2018) Ascorbic acid improves the tolerance of wheat plants to lead toxicity. Journal of Plant Interactions 13, 409–419.
Ascorbic acid improves the tolerance of wheat plants to lead toxicity.Crossref | GoogleScholarGoogle Scholar |

Akinci IE, Akinci S, Yilmaz K (2010) Response of tomato (Solanum lycopersicum L.) to lead toxicity: growth, element uptake, chlorophyll and water content. African Journal of Agriculture Research 5, 416–423.

Arias JA, Peralta-Videa JR, Ellzey JT, et al. (2010) Effects of Glomus deserticola inoculation on Prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques. Environmental and Experimental Botany 68, 139–148.
Effects of Glomus deserticola inoculation on Prosopis: enhancing chromium and lead uptake and translocation as confirmed by X-ray mapping, ICP-OES and TEM techniques.Crossref | GoogleScholarGoogle Scholar |

Bădescu IS, Bulgariu D, Bulgariu L (2017) Alternative utilization of algal biomass (Ulva sp.) loaded with Zn(II) ions for improving of soil quality. Journal of Applied Phycology 29, 1069–1079.
Alternative utilization of algal biomass (Ulva sp.) loaded with Zn(II) ions for improving of soil quality.Crossref | GoogleScholarGoogle Scholar |

Bali S, Jamwal VL, Kohli SK, et al. (2019) Jasmonic acid application triggers detoxification of lead (Pb) toxicity in tomato through the modifications of secondary metabolites and gene expression. Chemosphere 235, 734–748.
Jasmonic acid application triggers detoxification of lead (Pb) toxicity in tomato through the modifications of secondary metabolites and gene expression.Crossref | GoogleScholarGoogle Scholar | 31280042PubMed |

Bornet B, Branchard M (2001) Nonanchored inter simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting. Plant Molecular Biology Reporter 19, 209–215.
Nonanchored inter simple sequence repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting.Crossref | GoogleScholarGoogle Scholar |

Castellanos-Barriga LG, Santacruz-Ruvalcaba F, Hernández-Carmona G, et al. (2017) Effect of seaweed liquid extracts from Ulva lactuca on seedling growth of mungbean (Vigna radiata). Journal of Applied Phycology 29, 2479–2488.
Effect of seaweed liquid extracts from Ulva lactuca on seedling growth of mungbean (Vigna radiata).Crossref | GoogleScholarGoogle Scholar |

Castro J, Vera J, González A, et al. (2012) Oligo-carrageenans stimulate growth by enhancing photosynthesis, basal metabolism, and cell cycle in tobacco plants (var. Burley). Journal of Plant Growth Regulation 31, 173–185.
Oligo-carrageenans stimulate growth by enhancing photosynthesis, basal metabolism, and cell cycle in tobacco plants (var. Burley).Crossref | GoogleScholarGoogle Scholar |

Çekiç FÖ, Ekinci S, Inal MS, et al. (2017) Silver nanoparticles induced genotoxicity and oxidative stress in tomato plants. Turkish Journal of Biology 41, 700–707.
Silver nanoparticles induced genotoxicity and oxidative stress in tomato plants.Crossref | GoogleScholarGoogle Scholar |

Cenkci S, Cigerci IH, Yildiz M (2010) Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L. Environmental and Experimental Botany 67, 467–473.
Lead contamination reduces chlorophyll biosynthesis and genomic template stability in Brassica rapa L.Crossref | GoogleScholarGoogle Scholar |

Correia S, Matos M, Ferreira V, et al. (2014) Molecular instability induced by aluminum stress in Plantago species. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 770, 105–111.
Molecular instability induced by aluminum stress in Plantago species.Crossref | GoogleScholarGoogle Scholar | 25344171PubMed |

Das C, Naseera K, Ram A (2017) Bioremediation of tannery waste water by a salt tolerant strain of Chlorella vulgaris. Journal of Applied Phycology 29, 235–243.
Bioremediation of tannery waste water by a salt tolerant strain of Chlorella vulgaris.Crossref | GoogleScholarGoogle Scholar |

Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13, 207–209.
Microprep protocol for extraction of DNA from tomato and other herbaceous plants.Crossref | GoogleScholarGoogle Scholar |

Goñi O, Quille P, O’Connell S (2018) Ascophyllum nodosum extract biostimulants and their role in enhancing tolerance to drought stress in tomato plants. Plant Physiology and Biochemistry 126, 63–73.
Ascophyllum nodosum extract biostimulants and their role in enhancing tolerance to drought stress in tomato plants.Crossref | GoogleScholarGoogle Scholar | 29501894PubMed |

Gottesfeld P, Were FH, Adogame L, et al. (2018) Soil contamination from lead battery manufacturing and recycling in seven African countries. Environmental Research 161, 609–614.
Soil contamination from lead battery manufacturing and recycling in seven African countries.Crossref | GoogleScholarGoogle Scholar | 29248873PubMed |

Hernández-Herrera RM, Santacruz-Ruvalcaba F, Ruiz-López MA, et al. (2014) Effect of liquid seaweed extracts on growth of tomato seedlings (Solanum lycopersicum L.). Journal of Applied Phycology 26, 619–628.
Effect of liquid seaweed extracts on growth of tomato seedlings (Solanum lycopersicum L.).Crossref | GoogleScholarGoogle Scholar |

Hu X, Jiang X, Hwang H, et al. (2004) Promotive effects of alginate-derived oligosaccharide on maize seed germination. Journal of Applied Phycology 16, 73–76.
Promotive effects of alginate-derived oligosaccharide on maize seed germination.Crossref | GoogleScholarGoogle Scholar |

Karabal E, Yücel M, Öktem HA (2003) Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Science 164, 925–933.
Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity.Crossref | GoogleScholarGoogle Scholar |

Kasim EA, Abd W, Saad-Allah KM, et al. (2016) Seed priming with extracts of two seaweeds alleviates the physiological and molecular impacts of salinity stress on radish (Raphanus sativus). International Journal of Agriculture and Biology 18, 653–660.
Seed priming with extracts of two seaweeds alleviates the physiological and molecular impacts of salinity stress on radish (Raphanus sativus).Crossref | GoogleScholarGoogle Scholar |

Kushwaha A, Hans N, Kumar S, et al. (2018) A critical review on speciation, mobilization and toxicity of lead in soil-microbe-plant system and bioremediation strategies. Ecotoxicology and Environmental Safety 147, 1035–1045.
A critical review on speciation, mobilization and toxicity of lead in soil-microbe-plant system and bioremediation strategies.Crossref | GoogleScholarGoogle Scholar | 29976006PubMed |

Lamhamdi M, Bakrim A, Aarab A, et al. (2011) Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth. Comptes Rendus Biologies 334, 118–126.
Lead phytotoxicity on wheat (Triticum aestivum L.) seed germination and seedlings growth.Crossref | GoogleScholarGoogle Scholar | 21333942PubMed |

Malar S, Manikandan R, Favas PJC, et al. (2014) Effect of lead on phytotoxicity, growth, biochemical alterations and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation. Ecotoxicology and Environmental Safety 108, 249–257.
Effect of lead on phytotoxicity, growth, biochemical alterations and its role on genomic template stability in Sesbania grandiflora: a potential plant for phytoremediation.Crossref | GoogleScholarGoogle Scholar | 25103568PubMed |

Mesmar MN, Jaber K (1991) The toxic effect of lead on seed germination, growth, chlorophyll and protein contents of wheat and lens. Acta Biologica Hungarica 42, 331–344.

Michalak I, Chojnacka K (2015) Algae as production systems of bioactive compounds. Engineering in Life Sciences 15, 160–176.
Algae as production systems of bioactive compounds.Crossref | GoogleScholarGoogle Scholar |

Mzibra A, Aasfar A, Benhima R, et al. (2021) Biostimulants derived from moroccan seaweeds: seed germination metabolomics and growth promotion of tomato plant. Journal of Plant Growth Regulation 40, 353–370.
Biostimulants derived from moroccan seaweeds: seed germination metabolomics and growth promotion of tomato plant.Crossref | GoogleScholarGoogle Scholar |

Nasab SMH, Naji A, Yousefzadi M (2017) Kinetic and equilibrium studies on biosorption of cadmium(II) from aqueous solution by Gracilaria corticata and agar extraction algal waste. Journal of Applied Phycology 29, 2107–2116.
Kinetic and equilibrium studies on biosorption of cadmium(II) from aqueous solution by Gracilaria corticata and agar extraction algal waste.Crossref | GoogleScholarGoogle Scholar |

Nazal K (2019) Marine algae bioadsorbents for adsorptive removal of heavy metals. In ‘Advanced sorption process applications’. (Ed. S Edebali) pp. 151–164. (IntechOpen: London, UK)

Pourrut B, Shahid M, Dumat C, et al. (2011) Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology 213, 113–136.
Lead uptake, toxicity, and detoxification in plants.Crossref | GoogleScholarGoogle Scholar | 21541849PubMed |

Rouphael Y, De Micco V, Arena C, et al. (2017) Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. Journal of Applied Phycology 29, 459–470.
Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions.Crossref | GoogleScholarGoogle Scholar |

Soares TFSN, dos Santos Dias DCF, Oliveira AMS, et al. (2020) Exogenous brassinosteroids increase lead stress tolerance in seed germination and seedling growth of Brassica juncea L. Ecotoxicology and Environmental Safety 193, 110296
Exogenous brassinosteroids increase lead stress tolerance in seed germination and seedling growth of Brassica juncea L.Crossref | GoogleScholarGoogle Scholar | 32092579PubMed |

Sukumaran S, Grant A (2013) Effects of genotoxicity and its consequences at the population level in sexual and asexual Artemia assessed by analysis of inter-simple sequence repeats (ISSR). Mutation Research 757, 8–14.
Effects of genotoxicity and its consequences at the population level in sexual and asexual Artemia assessed by analysis of inter-simple sequence repeats (ISSR).Crossref | GoogleScholarGoogle Scholar | 23872504PubMed |

Venkatachalam P, Jayalakshmi N, Geetha N, et al. (2017) Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress. Chemosphere 171, 544–553.
Accumulation efficiency, genotoxicity and antioxidant defense mechanisms in medicinal plant Acalypha indica L. under lead stress.Crossref | GoogleScholarGoogle Scholar | 28039833PubMed |

Vinoth S, Gurusaravanan P, Jayabalan N (2014) Optimization of somatic embryogenesis protocol in Lycopersicon esculentum L. using plant growth regulators and seaweed extracts. Journal of Applied Phycology 26, 1527–1537.
Optimization of somatic embryogenesis protocol in Lycopersicon esculentum L. using plant growth regulators and seaweed extracts.Crossref | GoogleScholarGoogle Scholar |

Wang C-R, Wang X-R, Tian Y, et al. (2008) Oxidative stress, defense response, and early biomarkers for lead-contaminated soil in Vicia faba seedlings. Environmental Toxicology Chemistry 27, 970–977.
Oxidative stress, defense response, and early biomarkers for lead-contaminated soil in Vicia faba seedlings.Crossref | GoogleScholarGoogle Scholar | 18333686PubMed |

Wang C-R, Tian Y, Wang X-R, et al. (2010) Hormesis effects and implicative application in assessment of lead-contaminated soils in roots of Vicia faba seedlings. Chemosphere 80, 965–971.
Hormesis effects and implicative application in assessment of lead-contaminated soils in roots of Vicia faba seedlings.Crossref | GoogleScholarGoogle Scholar | 20591469PubMed |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.Crossref | GoogleScholarGoogle Scholar |