Assessment of heavy metal stress in the adaptation strategies of Tulipa luanica growing on serpentine soil through some biomarkers in comparison to Tulipa kosovarica

References

• Osmani, M.; Tuna, M.; Elezaj, I. Characterization of Nuclear DNA Content and Chromosome Numbers of Tulipa luanica Millaku, T. kosovarica Kit Tan, Shuka & Krasniqi and T. albanica Kit Tan & Shuka. AAS 2023, 119, 1–8. DOI: 10.14720/aas.2023.119.2.13280.
   Google Scholar
• Osmani, M.; Tuna, M.; Elezaj, I. R. Concentration of Some Metals in Soil and Plant Organs and Their Biochemical Profiles in Tulipa luanica, T. kosovarica and T. albanica Native Plant Species. Physiol. Mol. Biol. Plants 2018, 24, 1117–1126. DOI: 10.1007/s12298-018-0539-yMU.
   PubMed Web of Science ®Google Scholar
• Gashi, B.; Osmani, M.; Aliu, S. Breaking Seed Dormancy of Tulipa scardica Bornm. and Tulipa kosovarica Kit Tan, Shuka & Krasniqi by Pre-Chilling, Plant Growth Regulators and Some Chemical Treatments. AAS 2019, 113, 203–210. DOI: 10.14720/aas.2019.113.2.1.
   Google Scholar
• Millaku, F.; Elezaj, I. Tulipa luanica (Liliaceae), a New Species from Southern Kosovo. Ann. Bot. Fenn. 2015, 52, 315–320. DOI: 10.5735/085.052.0506.
   Web of Science ®Google Scholar
• Shuka, L.; Tan, K.; Krasniqi, E. Tulipa kosovarica (Liliaceae), A New Species of Tulip from Kosovo. Phytotaxa 2012, 62, 1–9. DOI: 10.11646/phytotaxa.62.1.1.
   Web of Science ®Google Scholar
• Jakovljević, K.; Lakušić, D.; Vukojičić, S.; Tomović, G.; Šinžar-Sekulić, J.; Stevanović, V. Richness and Diversity of Pontic Flora on Serpentine of Serbia. Cent. Eur. J. Biol. 2011, 6, 260–274. DOI: 10.2478/s11535-010-0110-5.
   Web of Science ®Google Scholar
• Millaku, F.; Elezaj, I.; Berisha, N. Sympatric Area and Ecology of Some Tulipa Species in the West Balkan Peninsula. Thaiszia J. Bot. 2018, 28, 35–47.
   Google Scholar
• Berisha, N.; Millaku, F.; Gashi, B.; Krasniqi, E.; Novak, J. Initial Determination of DNA Polymorphism of Some Primula veris L. populations from Kosovo and Austria. Physiol. Mol. Biol. Plants 2015, 21, 117–122. DOI: 10.1007/s12298-014-0275-x.
   PubMed Web of Science ®Google Scholar
• Harrison, S.; Rajakaruna, N. Serpentine: The Evolution and Ecology of a Model System. University of California Press, Berkeley, California, USA. 2011.
   Google Scholar
• Anacker, B. L. The Nature of Serpentine Endemism. Am. J. Bot. 2014, 101, 219–224. DOI: 10.3732/ajb.1300349.
   PubMed Web of Science ®Google Scholar
• Herath, I.; Kumarathilaka, P.; Navaratne, A.; Rajakaruna, N.; Vithanage, M. Immobilization and Phytotoxicity Reduction of Heavy Metals in Serpentine Soil Using Biochar. J. Soils Sediments 2015, 15, 126–138. DOI: 10.1007/s11368-014-0967-4.
   Web of Science ®Google Scholar
• Brady, K. U.; Kruckeberg, A. R.; Bradshaw, J. H. D. Evolutionary Ecology of Plant Adaptation to Serpentine. Annu. Rev. Ecol. Evol. Syst. 2005, 36, 243–266. DOI: 10.1146/annurev.ecolsys.35.021103.105730.
   Web of Science ®Google Scholar
• Vicic, D. D.; Stoiljković, M. M.; Bojat, N. Č.; Sabovljević, M. S.; Stevanović, B. M. Physiological Tolerance Mechanisms of Serpentine Tolerant Plants from Serbia. Rev. Ecol. 2014, 69, 185–195. DOI: 10.3406/revec.2014.1744.
   Google Scholar
• Singh, S.; Parihar, P.; Singh, R.; Singh, V. P.; Prasad, S. M. Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics. Front Plant. Sci. 2015, 6, 1143. DOI: 10.3389/fpls.2015.01143.
   PubMed Web of Science ®Google Scholar
• Bertrand, M.; Poirier, I. Photosynthetic Organisms and Excess of Metals. Photosynthetica 2005, 43, 345–353. DOI: 10.1007/s11099-005-0058-2.
   Web of Science ®Google Scholar
• Jaffe, E. K. The Porphobilinogen Synthase Family of Metalloenzymes. Acta Crystallogr. D Biol. Crystallogr. 2000, 56, 115–128. DOI: 10.1107/S0907444999014894.
   PubMedGoogle Scholar
• Gupta, P.; Jain, M.; Sarangthem, J.; Gadre, R. Inhibition of 5-Aminolevulinic Acid Dehydratase by Mercury in Excised Greening Maize Leaf Segments. Plant Physiol. Biochem. 2013, 62, 63–69. DOI: 10.1016/j.plaphy.2012.10.008.
   PubMed Web of Science ®Google Scholar
• Noriega, G. O.; Balestrasse, K. B.; Batlle, A.; Tomaro, M. A. Cadmium Induced Oxidative Stress in Soybean Plants Also by the Accumulation of δ-Aminolevulinic Acid. Biometals 2007, 20, 841–851. DOI: 10.1007/s10534-006-9077-0.
   PubMed Web of Science ®Google Scholar
• Solymosi, K.; Lenti, K.; Myśliwa-Kurdziel, B.; Fidy, J.; Strzałka, K.; Böddi, B. Depending on Concentration, Hg2+ Reacts with Different Components of the NADPH: Protochlorophyllide Oxidoreductase Macrodomains. Plant Biol. (Stuttg) 2004, 6, 358–368. DOI: 10.1055/s-2004-817893.
   PubMed Web of Science ®Google Scholar
• Mittler, R.; Vanderauwera, S.; Gollery, M.; Van Breusegem, F. Reactive Oxygen Gene Network of Plants. Trends Plant Sci. 2004, 9, 490–498. DOI: 10.1016/j.tplants.2004.08.009.
   PubMed Web of Science ®Google Scholar
• Auer, T.; Khoschsorurn, G. A.; Rabl, H.; Iberer, F.; Petutschnigg, B.; Wasler, A.; Tscheliessnigg, K. H. Detection of Lipid Peroxidation Products by Malondialdehyde (MDA-TBA Reaction) in Organ Transplantation. Transplant. Proc. 1995, 27, 2749–2751.
   PubMed Web of Science ®Google Scholar
• Hasanuzzaman, M.; Nahar, K.; Anee, T. I.; Fujita, M. Glutathione in Plants: Biosynthesis and Physiological Role in Environmental Stress Tolerance. Physiol. Mol. Biol. Plants 2017, 23, 249–268. DOI: 10.1007/s12298-017-0422-2.
   PubMed Web of Science ®Google Scholar
• Ahmeti, I. Diversity of Vaskular Flora in Serpentines of the Malësia e Gjakovës (Section Qafë e Morinës-Qafë e Prushit). PhD Thesis, University of Prishtina, Prishtinë, Kosovë, 2023.
   Google Scholar
• Jain, M.; Gadre, R. P. Inhibition of 5-Aminolevulinic Acid Dehydratase Activity by Arsenic in Excised Etiolated Maize Leaf Segments during Greening. J. Plant Physiol. 2004, 161, 251–255. DOI: 10.1078/0176-1617-00879.
   PubMed Web of Science ®Google Scholar
• Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein Measurement with the Folin Phenol Reagent. J. Biol. Chem. 1951, 193, 265–275.
   PubMed Web of Science ®Google Scholar
• Tewari, A. K.; Tripathy, S. Temperature-Stress-Induced Impairment of Chlorophyll Biosynthetic Reactions in Cucumber and Wheat. Plant Physiol. 1998, 117, 851–858. DOI: 10.1104/pp.117.3.851.
   PubMed Web of Science ®Google Scholar
• Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Determination of Accurate Extinction Coefficients and Simultaneous Equations for Assaying Chlorophylls a and b Extracted with Four Different Solvents: Verification of the Concentration of Chlorophyll Standards by Atomic Absorption Spectrometry. Biochim. Biophys. Acta 1989, 975, 384–394. DOI: 10.1016/S0005-2728(89)80347-0.
   Web of Science ®Google Scholar
• Primiano, T.; Novak, R. F. Enhanced Expression, Purification, and Characterisation of a Novel Class a Glutathione-s-Transferase Isozyme Appearing in Rabbit Hepatic Cytosol Following Treatment with 4-Picoline. Toxicol. Appl. Pharmacol. 1992, 112, 291–299. DOI: 10.1016/0041-008X(92)90199-3.
   PubMed Web of Science ®Google Scholar
• Hodges, D. M.; Delong, J. M.; Forney, C. F.; Prange, R. K. Improving the Thiobarbituric Acidreactive-Substances Assay for Estimating Lipid Peroxidation in Plant Tissue Containing Anthocyanin and Other Interfering Compounds. Planta 1999, 207, 604–611. DOI: 10.1007/s004250050524.
   Web of Science ®Google Scholar
• Shallari, S.; Schwartz, C.; Hasko, A.; Morel, J. L. Heavy Metals in Soils and Plants of Serpentine and Industrial Sites of Albania. Sci. Total Environ. 1998, 209, 133–142. DOI: 10.1016/S0048-9697(98)80104-6.
   PubMed Web of Science ®Google Scholar
• Bani, A.; Imeri, A.; Echevarria, G.; Pavlova, D.; Reeves, R. D.; Morel, J. L.; Sulçe, S. Nickel Hyperaccumulation in the Serpentine Flora of Albania. Fresenius Environ. Bull. 2013, 22, 1792–1801.
   Web of Science ®Google Scholar
• Burzynski, M. The Uptake and Transpiration of Water and the Accumulation of Lead by Plants Growing on Lead Chloride Solutions. Acta Soc. Bot. Pol. 1987, 56, 271–280.
   Web of Science ®Google Scholar
• Yusuf, M.; Fariduddin, Q.; Hayat, S.; Ahmad, A. Nickel: An Overview of Uptake, Essentiality and Toxicity in Plants. Bull. Environ. Contam. Toxicol. 2011, 86, 1–17. DOI: 10.1007/s00128-010-0171-1.
   PubMed Web of Science ®Google Scholar
• Meindl, G. A.; Bain, D. J.; Ashman, T.-L. Nickel Accumulation in Leaves, Floral Organs and Rewards Varies by Serpentine Soil Affinity. AoB Plants 2014, 6, plu036. DOI: 10.1093/aobpla/plu036.
   PubMed Web of Science ®Google Scholar
• Altinozlu, H.; Karagoz, A.; Polat, T.; Unver, I. Nickel Hyperaccumulation by Natural Plants in Turkish Serpentine Soils. Turk. J. Bot. 2012, 36, 269–280. DOI: 10.3906/bot-1101-10.
   Web of Science ®Google Scholar
• Leon, V.; Rabier, J.; Notonier, R.; Barthelemy, R.; Moreau, X.; Bouraïma-Madjèbi, S.; Viano, J.; Pineau, R. Effects of Three Nickel Salts on Germinating Seeds of Grevillea Exul var. Rubiginosa, an Endemic Serpentine Proteaceae. Ann. Bot. 2005, 95, 609–618. DOI: 10.1093/aob/mci066.
   PubMed Web of Science ®Google Scholar
• Bani, A.; Echevarria, G.; Sulçe, S.; Morel, J. L.; Mullai, A. In-Situ Phytoextraction of Nickel by Native Population of A. murale on Ultramafic Site in Albania. Plant Soil 2007, 293, 79–89. DOI: 10.1007/s11104-007-9245-1.
   Web of Science ®Google Scholar
• Wislocka, M.; Krawczyk, J.; Klink, A.; Morrison, L. Bioaccumulation of Heavy Metals by Selected Plant Species from Uranium Mining Dumps in the Sudety Mts., Poland. Pol. J. Environ. Stud. 2006, 15, 811–818.
   Web of Science ®Google Scholar
• Gashi, B.; Osmani, M.; Aliu, S.; Zogaj, M.; Kastrati, F. Risk Assessment of Heavy Metal Toxicity by Sensitive Biomarker δ-Aminolevulinic Acid Dehydratase (ALA-D) for Onion Plants Cultivated in Polluted Areas in Kosovo. J. Environ. Sci. Health B 2020, 55, 462–469. DOI: 10.1080/03601234.2020.1721229.
   PubMed Web of Science ®Google Scholar
• Buqaj, L.; Gashi, B.; Zogaj, M.; Vataj, R.; Sota, V.; Tuna, M. Stress Induced by Soil Contamination with Heavy Metals and Their Effects on Some Biomarkers and DNA Damage in Maize Plants at the Vicinity of Ferronikel Smelter in Drenas, Kosovo. J. Environ. Sci. Health B 2023, 58, 617–627. DOI: 10.1080/03601234.2023.2253114.
   PubMed Web of Science ®Google Scholar
• Tian, L.; Zheng, G.; Sommar, J. N.; Liang, Y.; Lundh, T.; Broberg, K.; Lei, L.; Guo, W.; Li, Y.; Tan, M.; et al. Lead Concentration in Plasma as a Biomarker of Exposure and Risk, and Modification of Toxicity by δ-Aminolevulinic Acid Dehydratase Gene Polymorphism. Toxicol. Lett. 2013, 221, 102–109. DOI: 10.1016/j.toxlet.2013.06.214.
   PubMed Web of Science ®Google Scholar
• La-Llave-León, O.; Méndez-Hernández, E.; Castellanos-Juárez, F.; Esquivel-Rodríguez, E.; Vázquez-Alaniz, F.; Sandoval-Carrillo, A.; García-Vargas, G.; Duarte-Sustaita, J.; Candelas-Rangel, J.; Salas-Pacheco, J. Association between Blood Lead Levels and Delta-Aminolevulinic Acid Dehydratase in Pregnant Women. IJERPH 2017, 14, 432. DOI: 10.3390/ijerph14040432.
   Web of Science ®Google Scholar
• Bollinger, L.; Bartel, A.; Weber, C.; Gehlen, H. Pre-Ride Biomarkers and Endurance Horse Welfare: Analyzing the Impact of the Elimination of Superoxide Dismutase, δ-Aminolevulinic-Dehydratase, Thiobarbituric Acid Reactive Substances, Iron, and Serum Amyloid a Levels in Elite 160 km Endurance Rides. Animals (Basel) 2023, 13, 1670. DOI: 10.3390/ani13101670.
   PubMedGoogle Scholar
• Gonçalves, J. F.; Nicoloso, F. T.; Becker, A. G.; Pereira, L. B.; Tabaldi, L. A.; Cargnelutti, D.; de Pelegrin, C. M. G.; Dressler, V. L.; da Rocha, J. B.; Schetinger, M. R. C. Photosynthetic Pigments Content, δ-Aminolevulinic Acid Dehydratase and Acid Phosphatase Activities and Mineral Nutrients Concentration in Cadmium-Exposed Cucumis Sativus L. Biologia 2009, 64, 310–318. DOI: 10.2478/s11756-009-0034-6.
   Web of Science ®Google Scholar
• Sarangthem, J.; Jain, M.; Gadre, R. Inhibition of δ-Aminolevulinic Acid Dehydratase Activityby Cadmium in Excised Etiolated Maize Leaf Segmentsduring Greening. Plant Soil Environ. 2011, 57, 332–337. DOI: 10.17221/45/2011-PSE.
   Web of Science ®Google Scholar
• Morsch, V. M.; Schetinger, M. R. C.; Martins, A. F.; Rocha, J. B. T. Effects of Cadmium, Lead, Mercury and Zinc on on δ-Aminolevulinic Acid Dehydratase Activity from Radish Leaves. Biol. Plant 2002, 45, 85–89. DOI: 10.1023/A:1015196423320.
   Web of Science ®Google Scholar
• Manankina, E. E.; Mel’nikov, S. S.; Budakova, E. A.; Shalygo, N. V. Effect of Ni2+ on Early Stages of Chlorophyll Biosynthesis and Pheophytinization in Euglena gracilis. Russ. J. Plant. Physiol. 2003, 50, 390–394. DOI: 10.1023/A:1023834606806.
   Web of Science ®Google Scholar
• Delfani, M.; Firouzabadi, M. B.; Farrokhi, N.; Makarian, H. Some Physiological Responses of Black-Eyed Pea to Iron and Magnesium Nanofertilizers. Commun. Soil Sci. Plant Anal. 2014, 45, 530–540. DOI: 10.1080/00103624.2013.863911.
   Web of Science ®Google Scholar
• Stancheva, I.; Geneva, M.; Markovska, Y.; Tzvetkova, N.; Mitova, I.; Todorova, M.; Petrov, P. A Comparative Study on Plant Morphology, Gas Exchange Parameters, and Antioxidant Response of Ocimum basilicum L. and Origanum vulgare L. Grown on Industrially Polluted Soil. Turk. J. Biol. 2014, 38, 89–102. DOI: 10.3906/biy-1304-94.
   Web of Science ®Google Scholar
• Panda, S. K. Impact of Copper on Reactive Oxygen Species, Lipid Peroxidation and Antioxidants in Lemna Minor. Biol. Plant 2008, 52, 561–564. DOI: 10.1007/s10535-008-0111-7.
   Web of Science ®Google Scholar
• Stancheva, I.; Geneva, M.; Hristozkova, M.; Markovska, Y.; Salamon, I. Antioxidant Capacity of Sage Grown on Heavy Metal-Polluted Soil. Russ. J. Plant Physiol. 2010, 57, 799–805. DOI: 10.1134/S1021443710060087.
   Web of Science ®Google Scholar
• Aydogan, S.; Erdag, B.; Aktas, L. Y. Bioaccumulation and Oxidative Stress Impact of Pb, Ni, Cu, and Cr Heavy Metals in Two Bryophyte Species, Pleurochaete squarrosa and Timmiella barbuloides. Turk. J. Bot. 2017, 41, 464–475. DOI: 10.3906/bot-1608-33.
   Web of Science ®Google Scholar
• Kazakou, E.; Dimitrakopoulos, P. G.; Baker, A. J. M.; Reeves, R. D.; Troumbis, A. Y. Hypotheses, Mechanisms and Trade-Offs of Tolerance and Adaptation to Serpentine Soils: From Species to Ecosystem Level. Biol. Rev. Camb. Philos. Soc. 2008, 83, 495–508. DOI: 10.1111/j.1469-185X.2008.00051.x.
   PubMed Web of Science ®Google Scholar