Abstract
Wheat is the second important cereal crop worldwide due to nutritional composition and role in meeting daily energy needs. Salinity is an abiotic stress factor that restricts crop productivity through influencing plant growth and development in arid and semi-arid regions. Nanomaterials and plant growth promoting bacteria (PGPBs) can be used in many different areas of agriculture for different purposes. In this study, changes in cytosine methylation and DNA damage levels in wheat (Triticum aestivum L.) exposed to salt stress (250 mM NaCl) were determined and possible preventive effects of copper (II) oxide nanoparticles (0, 50 and 100 mg/L; CuO-Nps > 100 nm) and plant growth promoting bacteria (no bacteria, Bacillus subtilis, Lactobacillus casei, Bacillus pumilis; PGPBs) treatments were investigated. Changes in cytosine methylation were analyzed by Coupled Restriction Enzyme Digestion-iPBS (CRED-iPBS) and genotoxic influences and genomic stability was analyzed with the aid of inter-primer binding site (iPBS) primers. Application of 250 mM NaCl remarkably increased polymorphism rate of iPBS profile. Besides, relieve effect of PGPBs with CuO-NPs was observed against adverse effect of 250 mM NaCl stress. The genomic template stability values clearly increased with PGPBs with CuO-NPs treatments, particularly Lactobacillus casei with 100 mg/L of CuO-Nps. In addition, DNA hypo-methylation was observed in all treatments. As a conclusion, PGPBs with CuO-NPs treatments showed a strong anti-genotoxic effect against NaCl stress and they could be used as an alternative molecule to alleviate genetic impairment in wheat under NaCl stress.
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Abbreviations
- PGPBs:
-
Plant growth-promoting bacteria
- PCR:
-
Polymerase chain reaction
- CuO:
-
Copper (II) oxide
- NP:
-
Nanoparticle
- CRED:
-
Coupled Restriction Enzyme Digestion
- iPBS:
-
Inter-primer binding site
- GTS:
-
Genomic template stability
References
Abbas G, Chen Y, Khan F, Feng Y, Palta J, Siddique K (2018) Salinity and low phosphorus differentially affect shoot and root traits in two wheat cultivars with contrasting tolerance to salt. Agronomy 8(8):155
Aly AA (2012) Application of DNA (RAPD) and ultrastructure to detect the effect of cadmium stress in Egyptian clover and Sudan grass plantlets. J Stress Physiol Biochem 8(1):241–257
Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, Dizdaroglu M, Xing B, Nelson BC (2012) Copper oxide nanoparticle mediated dna damage in terrestrial plant models. Environ Sci Technol 46(3):1819–1827. https://doi.org/10.1021/es202660k
Brinate SVB, Martins LD, Pereira Rosa GNG, Cunha VV, de Jesus Sotero A, do Amaral JFT, Tomaz MA, de Jesus WC (2015) Copper can influences growth, disease control and production in arabica coffee trees. Aust J Crop Sci 9(7):678
Citterio S, Aina R, Labra M, Ghiani A, Fumagalli P, Sgorbati S, Santagostino A (2002) Soil genotoxicity assessment: a new strategy based on biomolecular tools and plant bioindicators. Environ Sci Technol 36(12):2748–2753. https://doi.org/10.1021/es0157550
Cornelis G, Hund-Rinke K, Kuhlbusch T, Van den Brink N, Nickel C (2014) Fate and bioavailability of engineered nanoparticles in soils: a review. Crit Rev Environ Sci Technol 44(24):2720–2764
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21(1):1–18
Davenport SB, Gallego SM, Benavides MP, Tomaro ML (2003) Behaviour of antioxidant defense system in the adaptive response to salt stress in Helianthus annuus L. cells. Plant Growth Regul 40(1):81–88
Demirkiran A, Marakli S, Temel A, Gozukirmizi N (2013) Genetic and epigenetic effects of salinity on in vitro growth of barley. Genet Mol Biol 36(4):566–570. https://doi.org/10.1590/s1415-47572013000400016
Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694
Dimkpa CO, McLean JE, Latta DE, Manangón E, Britt DW, Johnson WP, Boyanov MI, Anderson AJ (2012) CuO and ZnO nanoparticles: phytotoxicity metal speciation and induction of oxidative stress in sand-grown wheat. J Nanopart Res. https://doi.org/10.1007/s11051-012-1125-9
Dimkpa CO, Bindraban PS, Fugice J, Agyin-Birikorang S, Singh U, Hellums D (2017) Composite micronutrient nanoparticles and salts decrease drought stress in soybean. Agron Sust Dev 37(1):5
Doğan İ, Kekeç G, Özyiğit İİ, Sakçalı MS (2012) Salinity induced changes in cotton (Gossypium hirsutum L.). Pak J Bot 44:21–25
Elmer WH, White JC (2016) The use of metallic oxide nanoparticles to enhance growth of tomatoes and eggplants in disease infested soil or soilless medium. Environ Sci Nano 3(5):1072–1079
Erturk FA, Agar G, Arslan E, Nardemir G, Aydin M, Taspinar MS (2014a) Effects of lead sulfate on genetic and epigenetic changes, and endogenous hormone levels in corn (Zea mays L.). Pol J Environ Stud 23:1925–1932
Erturk FA, Agar G, Arslan E, Nardemir G, Sahin Z (2014b) Determination of genomic instability and DNA methylation effects of Cr on maize (Zea mays L.) using RAPD and CRED-RA analysis. Acta Physiol Plant 36(6):1529–1537. https://doi.org/10.1007/s11738-014-1529-5
Erturk FA, Agar G, Arslan E, Nardemir G (2015a) Analysis of genetic and epigenetic effects of maize seeds in response to heavy metal (Zn) stress. Environ Sci Pollut Res 22(13):10291–10297. https://doi.org/10.1007/s11356-014-3886-4
Erturk FA, Aydin M, Sigmaz B, Taspinar MS, Arslan E, Agar G, Yagci S (2015b) Effects of As2O3 on DNA methylation, genomic instability, and LTR retrotransposon polymorphism in Zea mays. Environ Sci Pollut Res 22(23):18601–18606
Fathi A, Zahedi M, Torabian S, Khoshgoftar A (2017) Response of wheat genotypes to foliar spray of ZnO and Fe2O3 nanoparticles under salt stress. J Plant Nutr 40(10):1376–1385. https://doi.org/10.1080/01904167.2016.1262418
Fu Q, Liu C, Ding N, Lin Y, Guo B (2010) Ameliorative effects of inoculation with the plant growth-promoting rhizobacterium Pseudomonas sp. DW1 on growth of eggplant (Solanum melongena L.) seedlings under salt stress. Agric Water Manag 97(12):1994–2000. https://doi.org/10.1016/j.agwat.2010.02.003
Graham P, Vance C (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65(2–3):93–106
Gupta M, Sarin NB (2009) Heavy metal induced DNA changes in aquatic macrophytes: Random amplified polymorphic DNA analysis and identification of sequence characterized amplified region marker. J Environ Sci 21(5):686–690. https://doi.org/10.1016/s1001-0742(08)62324-4
Hosseinpour A, Özkan G, Nalci Ö, Haliloğlu K (2019) Estimation of genomic instability and DNA methylation due to aluminum (Al) stress in wheat (Triticum aestivum L.) using iPBS and CRED-iPBS analyses. Turk J Bot 43(1):27–37
Hosseinpour A, Haliloglu K, Cinisli KT, Ozkan G, Ozturk HI, Pour-Aboughadareh A, Poczai P (2020) Application of zinc oxide nanoparticles and plant growth promoting bacteria reduces genetic impairment under salt stress in tomato (Solanum lycopersicum L‘Linda’). Agriculture 10(11):521
Hossein-Pour A, Ozkan G, Nalci OB, Haliloglu K (2018) Estimation of genomic instability and DNA methylation due to aluminum (Al) stress in wheat (Triticum aestivum L.) using iPBS and CRED-iPBS analyses Turkish Journal of Botany
Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57(1):395–418
Kalendar R, Antonius K, Smykal P, Schulman AH (2010) iPBS: a universal method for DNA fingerprinting and retrotransposon isolation. Theor Appl Genet 121(8):1419–1430. https://doi.org/10.1007/s00122-010-1398-2
Katsuhara M, Kawasaki T (1996) Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol 37(2):169–173
Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15(6):1692
Kim J-M, Sasaki T, Ueda M, Sako K, Seki M (2015) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114
Kumar S, Beena AS, Awana M, Singh A (2017) Salt-induced tissue-specific cytosine methylation downregulates expression of HKT genes in contrasting Wheat (Triticum aestivum L.) genotypes. DNA Cell Biol 36(4):283–294. https://doi.org/10.1089/dna.2016.3505
Maksymiec W (1998) Effect of copper on cellular processes in higher plants. Photosynthetica 34(3):321–342
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, Cambridge
McManus P, Hortin J, Anderson AJ, Jacobson AR, Britt DW, Stewart J, McLean JE (2018) Rhizosphere interactions between copper oxide nanoparticles and wheat root exudates in a sand matrix: Influences on copper bioavailability and uptake. Environ Toxicol Chem 37(10):2619–2632
McManus P (2016) Rhizosphere interactions between copper oxide nanoparticles and wheat root exudate in a sand matrix; Influences on bioavailability and uptake
Miao L, Wang C, Hou J, Wang P, Ao Y, Li Y, Lv B, Yang Y, You G, Xu Y (2016) Effect of alginate on the aggregation kinetics of copper oxide nanoparticles (CuO NPs): bridging interaction and hetero-aggregation induced by Ca 2+. Environ Sci Pollut Res 23(12):11611–11619
Michaud AM, Chappellaz C, Hinsinger P (2008) Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.). Plant Soil 310(1–2):151–165
Monreal C, DeRosa M, Mallubhotla S, Bindraban P, Dimkpa C (2016) Nanotechnologies for increasing the crop use efficiency of fertilizer-micronutrients. Biol Fertil Soils 52(3):423–437
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Murali Achary VM, Panda BB (2009) Aluminium-induced DNA damage and adaptive response to genotoxic stress in plant cells are mediated through reactive oxygen intermediates. Mutagenesis 25(2):201–209
Nair R, Varghese SH, Nair BG, Maekawa T, Yoshida Y, Kumar DS (2010) Nanoparticulate material delivery to plants. Plant Sci 179(3):154–163
Nemli S, Kianoosh T, Tanyolac MB (2015) Genetic diversity and population structure of common bean (Phaseolus vulgaris L.) accessions through retrotransposon-based interprimer binding sites (iPBSs) markers. Turk J Agric Forest 39(6):940–948
Peng H, Zhang J (2009) Plant genomic DNA methylation in response to stresses: potential applications and challenges in plant breeding. Prog Nat Sci 19(9):1037–1045
Printz B, Lutts S, Hausman J-F, Sergeants K (2016) Copper trafficking in plants and its implication on cell wall dynamics. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00601
Rinaldi M, Garofalo P, Rubino P, Steduto P (2011) Processing tomatoes under different irrigation regimes in Southern Italy: agronomic and economic assessments in a simulation case study. J Agrometeorol 3(3):39–56
Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287(1–2):15–21
Saleh B (2016) DNA changes in cotton (Gossypium hirsutum L.) under salt stress as revealed by RAPD marker. Adv Horticult Sci 30(1):13–21
Shams M, Yildirim E, Agar G, Ercisli S, Ekinci M, Dursun A, Kul R (2018) Nitric oxide alleviates copper toxicity in germinating seed and seedling growth of Lactuca sativa L. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 46(1):167–172. https://doi.org/10.15835/nbha46110912
Shilev S, Sancho ED, Benlloch-González M (2012) Rhizospheric bacteria alleviate salt-produced stress in sunflower. J Environ Manag 95:S37–S41
Sigmaz B, Agar G, Arslan E, Aydin M, Taspinar MS (2015) The role of putrescine against the long terminal repeat (LTR) retrotransposon polymorphisms induced by salinity stress in Triticum aestivum. Acta Physiol Plant 37(11):251
Singh A, Singh N, Hussain I, Singh H, Yadav V (2017) Synthesis and characterization of copper oxide nanoparticles and its impact on germination of Vigna radiata (L.) R. Wilczek. Trop Plant Biol 4(2):246–253
Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J Biol Chem 277(40):37741–37746
Tanee T, Chadmuk P, Sudmoon R, Chaveerach A, Noikotr K (2012) Genetic analysis for identification, genomic template stability in hybrids and barcodes of the Vanda species (Orchidaceae) of Thailand. Afr J Biotech 11(55):11772–11781
Taspinar MS, Aydin M, Arslan E, Sigmaz B, Agar G (2017) Salinity and putrescine effects on DNA methylation changes in Triticum aestivum. J Biotechnol 256:S101
Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255(2):571–586
Wang Y, Wisniewski M, Meilan R, Uratsu SL, Cui M, Dandekar A, Fuchigami L (2007) Ectopic expression of Mn-SOD in Lycopersicon esculentum leads to enhanced tolerance to salt and oxidative stress. J Appl Hortic 9:3–8
Yang X, Zhang W, Zhao Z, Li N, Mou Z, Sun D, Cai Y, Wang W, Lin Y (2017) Quercetin loading CdSe/ZnS nanoparticles as efficient antibacterial and anticancer materials. J Inorg Biochem 16736–16748. https://doi.org/10.1016/j.jinorgbio.2016.11.023
Yao L, Wu Z, Zheng Y, Kaleem I, Li C (2010) Growth promotion and protection against salt stress by Pseudomonas putida Rs-198 on cotton. Eur J Soil Biol 46(1):49–54. https://doi.org/10.1016/j.ejsobi.2009.11.002
Yruela I (2005) Copper in plants. Braz J Plant Physiol 17(1):145–156
Zeinalzadehtabrizi H, Hosseinpour A, Aydin M, Haliloglu K (2015) A modified genomic DNA extraction method from leaves of sunflower for PCR based analyzes. J Biodivers Environ Sci 7(6):222–225
Zhang Q, Liu H, Hu H, Li S, Ying Y, Wu J (2014) Analysis of the DNA methylation on Camptotheca acuminata decne plants growing in vitro in response to sodium chloride stress. Propag Ornam Plants 14(2):76–83
Zhong L, Wang J-B (2007) The role of DNA hypermethylation in salt resistence of Triticum aestivum L. J Wuhan Bot Res 1:019
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AH conceived and designed the experiments and worked for writing and editing of the English of this paper. TC, EI, GO, HIO and KH performed the experiments, collected and analyzed the data. EI went through literature and helped in drafting the manuscript.
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Hosseinpour, A., Ilhan, E., Özkan, G. et al. Plant growth-promoting bacteria (PGPBs) and copper (II) oxide (CuO) nanoparticle ameliorates DNA damage and DNA Methylation in wheat (Triticum aestivum L.) exposed to NaCl stress. J. Plant Biochem. Biotechnol. 31, 751–764 (2022). https://doi.org/10.1007/s13562-021-00713-w
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DOI: https://doi.org/10.1007/s13562-021-00713-w