The Photochemical and Antioxidant Defence Strategies of Two Maize Genotypes Exposed to Zinc Toxicity at the Seedling Stage

Year 2024, Volume: 30 Issue: 3, 488 - 500, 23.07.2024

Yasemin Ekmekci , Sekure Culha Erdal , Şeniz Ünalan Okar Nuran Çiçek , Deniz Tanyolaç

https://doi.org/10.15832/ankutbd.1333983

Abstract

The main objective of the current study was to elucidate photochemical and antioxidant strategies in two maize genotypes, namely DK626 and 3223 at the early seedling stage under zinc (Zn2+) toxicity. The seedlings were grown in a controlled growth room at a temperature regime of 25±1 °C, with 40±5 % humidity, 16 h photoperiod and at 300 μmol m–2 s–1 light intensity for 8 days. Then, the seedlings were exposed to toxic zinc concentrations (2, 5 and 8 mM ZnSO4.7H2O) for 12 days. Both genotypes accumulated approximately the same amounts of Zn in leaves; however, the shoot and root lengths, and biomass decreased further in DK626 compared to 3223. The malondialdehyde content in the leaves increased gradually depending on the Zn concentrations, and the deterioration of the membrane structure was greater in DK626 compared to 3223 at highly toxic Zn levels. A reduction in photochemical activity was accompanied by non-photochemical quenching and excess energy was removed from the reaction centers by fluorescence and non-radiative inactivation in genotypes under Zn toxicity. The chlorophyll and carotenoid contents were significantly decreased, and the anthocyanin accumulation was increased with increasing Zn levels, especially in DK626. In addition, the activities of antioxidant enzymes and isoenzymes were induced at different levels in genotypes depending on the Zn toxicity level. The seedlings exposed to toxic Zn concentrations had achieved to sustain their growth by regulating their photosynthetic efficiency and their antioxidant defence system. Consequently, these genotypes could potentially be successfully used for the phytoremediation of Zn-contaminated areas. However, further studies are required to screen all growth stages for Zn tolerance capacity before making a more informed decision regarding the phytoremediation potentials of these two genotypes.

Keywords

Antioxidant defense system, Chlorophyll a fluorescence induction, Growth characteristics, Maize (Zea mays L.), Photochemical activity, Zinc toxicity

Supporting Institution

Hacettepe University, Scientific Research Unit

Project Number

02 02 602 013

References

• Abedi T, Gavanji S & Mojiri A (2022). Lead and zinc uptake and toxicity in maize and their management. Plants 11: 1922. https://doi.org/10.3390/plants11151922
• Alonso-Blázquez N, García-Gómez C & Fernández MD (2015). Influence of Zn-contaminated soils in the antioxidative defence system of wheat (Triticum aestivum) and maize (Zea mays) at different exposure times: potential use as biomarkers. Ecotoxicology 24: 279-291. https://doi.org/10.1007/s10646-014-1376-6
• Alsafran M, Saleem MH, Al Jabri H, Rizwan M & Usman K (2023). Principles and applicability of integrated remediation strategies for heavy metal removal/recovery from contaminated environments. Journal of Plant Growth Regulation 42: 3419-3440. https://doi.org/10.1007/s00344-022-10803-1
• Andrejić G, Gajić G, Prica M, Dželetović Ž & Rakić T. (2018). Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus×giganteus plants. Photosynthetica 56(4): 1249-1258. https://doi.org/10.1007/s11099-018-0827-3
• Antoniadis V, Shaheen S M, Tsadilas C D, Selim M H & Rinklebe J (2018). Zinc sorption by different soils as affected by selective removal of carbonates and hydrous oxides. Applied Geochemistry 88: 49-58. https://doi.org/10.1016/j.apgeochem.2017.04.007
• Anwaar S A, Ali S, Ali S, Ishaque W, Farid M, Farooq M A, Najeeb U, Abbas F & Sharif M (2015). Silicon (Si) alleviates cotton (Gossypium hirsutum L.) from zinc (Zn) toxicity stress by limiting Zn uptake and oxidative damage. Environmental Science and Pollution Research 22(5): 3441-3450. https://doi.org/10.1007/s11356-014-3938-9
• Ayyar S & Appavoo S (2017). Effect of graded levels of Zn in combination with or without microbial inoculation on Zn transformation in soil, yield and nutrient uptake by maize for black soil. Environment & Ecology 35(1): 172-176
• Balafrej H, Bogusz D, Triqui Z-E A, Guedira A, Bendaou N, Smouni A & Fahr M (2020). Zinc hyperaccumulation in plants: A review. Plants 9(562): 2-22. https://doi.org/10.3390/plants9050562
• Baran U & Ekmekçi Y (2022). Physiological, photochemical, and antioxidant responses of wild and cultivated Carthamus species exposed to nickel toxicity and evaluation of their usage potential in phytoremediation. Environmental Science and Pollution Research 29: 4446-4460. https://doi.org/10.1007/s11356-021-15493-y
• Beauchamp C & Fridovich I (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44: 276-287. https://doi.org/10.1016/0003-2697(71)90370-8
• Beyer W F & Fridovich I (1987). Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Analytical Biochemistry 161(2): 559-566. https://doi.org/10.1016/0003-2697(87)90489-1
• Bradford M M (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1-2): 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
• Calvo B O, Parapugna T L & Lagorio M G (2017). Variability in chlorophyll fluorescence spectra of eggplant fruit grown under different light environments: A case study. Photochemical & Photobiological Sciences16: 711-720. https://doi.org/10.1039/c6pp00475j
• Chaney R L (1993). Zinc Phytotoxicity. In: Robson A D (ed) Zinc in Soils and Plants. Developments in Plant and Soil Sciences, 55. Springer, Dordrecht, pp 135-150. https://doi.org/10.1007/978-94-011-0878-2-10
• Chen Q, Zhang X, Liu Y, Wei J, Shen W, Shen Z & Cui J (2017). Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regulation 81: 253-264. https://doi.org/10.1007/s10725-016-0202-y
• Çiçek N & Çakirlar H (2008). Effects of salt stress on some physiological and photosynthetic parameters at three different temperatures in six soya bean (Glycine max L. Merr.) cultivars. Journal of Agronomy & Crop Science 194: 34-46. https://doi.org/10.1111/j.1439-037X.2007.00288.x
• Cordon G, Iriel A, Cirelli A F & Lagorio M G (2018). Arsenic effects on some photophysical parameters of Cichorium intybus under different radiation and water irrigation regimes. Chemosphere 204: 398-404. https://doi.org/10.1016/j.chemosphere.2018.04.048
• DalCorso G, Manara A, Piasentin S & Furini A (2014). Nutrient metal elements in plants. Metallomics 6: 1770-1788. https://doi.org/10.1039/c4mt00173g
• Díaz-Pontones D M, Corona-Carrillo J I, Herrera-Miranda C & González S (2021). Excess zinc alters cell wall class III peroxidase activity and flavonoid content in the maize scutellum. Plants 10: 197. https://doi.org/10.3390/plants10020197
• Dobrikova A, Apostolova E, Adamakis I S & Han A (2022). Combined impact of excess zinc and cadmium on elemental uptake, leaf anatomy and pigments, antioxidant capacity, and function of photosynthetic apparatus in clary sage (Salvia sclarea L.). Plants 11: 2407. https://doi.org/10.3390/plants11182407
• Dobrikova A, Apostolova E, Hanć A, Yotsova E, Borisova P, Sperdouli I, Adamakis I-D S & Moustakas M (2021). Tolerance mechanisms of the aromatic and medicinal plant Salvia sclarea L. to excess zinc. Plants 10: 194. https://doi.org/10.3390/plants10020194
• Ekmekçi Y, Tanyolaç D & Ayhan B (2008). Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. Journal of Plant Physiology 165: 600-611.
• Fatemi H, Zaghdoud C, Nortes P A, Carvajal M & Martínez-Ballesta M C (2020). Differential aquaporin response to distinct effects of two Zn concentrations after foliar application in pak choi (Brassica rapa L.) plants. Agronomy 10: 450. https://doi.org/10.3390/agronomy10030450
• Genty B, Briantais J M & Baker N R (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) - General Subjects 990(1): 87-92. https://doi.org/10.1016/S0304-4165(89)80016-9
• Glińska S, Gapińska M, Michlewska S, Skiba E & Kubicki J (2016). Analysis of Triticum aestivum seedling response to the excess of zinc. Protoplasma 253: 367-377.https://doi.org/10.1007/s00709-015-0816-3
• Guadagno C R, Virzo De Santo A & D’Ambrosio N (2010). A revised energy partitioning approach to assess the yields of non-photochemical quenching components. Biochimica et Biophysica Acta 1797: 525-530. https://doi.org/10.1016/j.bbabio.2010.01.016
• Iriel A, Cordon G, Fernández Cirelli A & Lagorio M G (2019). Non-destructive methodologies applied to track the occurrence of natural micropollutants in watering: Glycine max as a biomonitor. Ecotoxicology and Environmental Safety 182: 109368. https://doi.org/10.1016/j.ecoenv.2019.109368
• Janeeshma E, Kalaji H M & Puthur J T (2021). Differential responses in the photosynthetic efficiency of Oryza sativa and Zea mays on exposure to Cd and Zn toxicity. Acta Physiologiae Plantarum 43: 12. https://doi.org/10.1007/s11738-020-03178-x
• Jayasri M A & Suthindhiran K (2017). Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna minor: its potential role in phytoremediation. Applied Water Science 7: 1247-1253. https://doi.org/10.1007/s13201-015-0376-x
• Karahan F, Ozyigit I I, Saracoglu I A, Yalcin I E, Ozyigit A H & Ilcim A (2020). Heavy metal levels and mineral nutrient status in different parts of various medicinal plants collected from eastern mediterranean region of Turkey. Biological Trace Element Research 197: 316-329. https://doi.org/10.1007/s12011-019-01974-2
• Kaur H & Garg N (2021). Zinc toxicity in plants: a review. Planta 253: 129.https://doi.org/10.1007/s00425-021-03642-z
• Küpper H & Andresen E (2016). Mechanisms of metal toxicity in plants. Metallomics 8: 269-285. https://doi.org/10.1039/c5mt00244c
• Laemmli U K (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685. https://doi.org/10.1038/227680a0
• Lichtenthaler H K, Buschmann C & Knapp M (2005). How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 43(3): 379-393. https://doi.org/10.1007/s11099-005-0062-6
• Lichtenthaler H K (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology 148: 350-382. https://doi.org/10.1016/0076-6879(87)48036-1
• M’Rah S, Marichali A, M’Rabet Y, Chatti S, Saber C, Casabianca H & Hosni K (2023). Morphology, physiology, and biochemistry of zinc-stressed caraway plants. Protoplasma 260: 853-868. https://doi.org/10.1007/s00709-022-01818-2
• Mancinelli A L, Yang C P H, Lindquist P, Anderson O R & Rabino I (1975). Photocontrol of anthocyanin synthesis: III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiology 55(2): 251-257. https://doi.org/10.1104/pp.55.2.251
• Marschner H (1995). Mineral nutrition of higher plants. London: Academic Press. Maxwell K & Johnson G H (2000). Chlorophyll fluorescence-a practical guide. Journal of Experimental Botany 51(345): 659-668. https://doi.org/10.1093/jxb/51.345.659
• Miller G, Shulaev V & Mittler R (2008). Reactive oxygen signaling and abiotic stress. Physiologia Plantarum 133: 481-489. https://doi.org/10.1111/j.1399-3054.2008.01090.x
• Mittler R & Zilinskas B A (1993). Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Analitical Biochemistry 212: 540-546. https://doi.org/10.1006/abio.1993.1366
• Moustaka J, Panteris E, Adamakis I-D S, Tanou G, Giannakoula A, Eleftheriou E P & Moustakas M (2018). High anthocyanin accumulation in poinsettia leaves is accompanied by thylakoid membrane unstacking, acting as a photoprotective mechanism, to prevent ROS formation. Environmental and Experimental Botany 154: 44-55. https://doi.org/10.1016/j.envexpbot.2018.01.006
• Mukhopadhyay M, Das A, Subba P, Bantawa P, Sarkar B, Ghosh P & Mondal T D (2013). Structural, physiological, and biochemical profiling of tea plants under zinc stress. Biologia Plantarum 57(3): 474-480. https://doi.org/10.1007/s10535-012-0300-2
• Natasha N, Shahid M, Bibi I, Iqbal J, Khalid S, Murtaza B, Bakhat H F, Farooq A B U, Amjad M, Hammadd H M, Niazi N K & Arshad M, (2022). Zinc in soil-plant-human system: A data-analysis review. Science of the Total Environment 808: 152024. https://doi.org/10.1016/j.scitotenv.2021.152024
• Pan L, Li J, Yin H, Fan Z & Li X (2020). Integrated physiological and transcriptomic analyses reveal a regulatory network of anthocyanin metabolism contributing to the ornamental value in a novel hybrid cultivar of Camellia japonica. Plants 9: 1724. https://doi.org/10.3390/plants9121724
• Paunov M, Koleva L, Vassilev A, Vangronsveld J & Goltsev V (2018). Effects of different metals on photosynthesis: Cadmium and zinc affect chlorophyll fluorescence in durum wheat. International Journal of Molecular Science 19: 787. https://doi.org/10.3390/ijms19030787
• Petrovic D & Krivokapic S (2020). The effect of Cu, Zn, Cd, and Pb accumulation on biochemical parameters (proline, chlorophyll) in the water caltrop (Trapa natans L.), Lake Skadar, Montenegro. Plants 9: 1287. https://doi.org/10.3390/plants9101287
• Pütter J (1974). Peroxidases. In: Bergmeyer HU (ed) In Methods of Enzymatic Analysis, Academic P. Academic Press, NY, USA, pp. 685-690
• Rai P K, Lee S S, Zhang M, Tsang Y F & Kim K-H (2019). Heavy metals in food crops: Health risks, fate, mechanisms, and management. Environment International 125: 365-385. https://doi.org/10.1016/j.envint.2019.01.067
• Ramakrishna B & Rao S S R (2015). Foliar application of brassinosteroids alleviates adverse effects of zinc toxicity in radish (Raphanus sativus L.) plants. Protoplasma 252: 665-677. https://doi.org/10.1007/s00709-014-0714-0
• Rao M V, Hale B A & Ormrod D P (1995). Amelioration of ozone-induced oxidative damage in wheat plants grown under high carbon dioxide: Role of antioxidant enzymes. Plant Physiology 109(2): 421-432. https://doi.org/10.1104/pp.109.2.421
• Roccotiello E, Manfredi A, Drava G, Minganti V, Mariotti M G, Berta G & Cornara L (2010). Zinc tolerance and accumulation in the ferns Polypodium cambricum L. and Pteris vittata L. Ecotoxicology and Environmental Safety 73: 1264-1271. https://doi.org/10.1016/j.ecoenv.2010.07.019
• Saboor A, Ali M A, Hussain S, Enshasy H A E, Hussain S, Ahmed N, Gafur A, Sayyed R Z, Fahad S, Danish S & Datta R (2021). Zinc nutrition and arbuscular mycorrhizal symbiosis effects on maize (Zea mays L.) growth and productivity. Saudi Journal of Biological Sciences 28: 6339-6351. https://doi.org/10.1016/j.sjbs.2021.06.096
• Sapeta H, Yokono M, Takabayashi A, Ueno Y, Cordeiro A M, Hara T, Tanaka A, Akimoto S, Oliveira M. M. & Tanaka R (2023). Reversible down-regulation of photosystems I and II leads to fast photosynthesis recovery after long-term drought in Jatropha curcas. Journal of Experimental Botany 74(1): 336-351. https://doi.org/10.1093/jxb/erac423
• Seregin I V, Ivanova T V, Voronkov A S, Kozhevnikova A D & Schat H (2023). Zinc- and nickel-induced changes in fatty acid profiles in the zinc hyperaccumulator Arabidopsis halleri and non-accumulator Arabidopsis lyrata. Plant Physiology and Biochemistry 197: 107640. https://doi.org/10.1016/j.plaphy.2023.107640
• Sgherri C L M, Loggini B, Puliga S & Navari-Izzo F (1994). Antioxidant system in Sporobolus stapfianus: Changes in response to desiccation and rehydration. Phytochemistry 35(3): 561-565. https://doi.org/10.1016/S0031-9422(00)90561-2
• Sharma J K, Kumar N, Singh N P& Santal A R (2023). Phytoremediation technologies and their mechanism for removal of heavy metal from contaminated soil: An approach for a sustainable environment. Frontier in Plant Science 14: 1076876. https://doi.org/10.3389/fpls.2023.1076876
• Sofo A, Moreira I, Gattullo C E, Martins L L & Mou M (2018). Antioxidant responses of edible and model plant species subjected to subtoxic zinc concentrations. Journal of Trace Elements in Medicine and Biology 49: 261-268. https://doi.org/10.1016/j.jtemb.2018.02.010
• Sofo A, Vitti A, Nuzzaci M, Tataranni G, Scopa A, Vangronsveld J, Remans T, Falasca G, Altamura M M, Degola F & di Toppi L S (2013). Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context. Physiologia Plantarum 149: 487-498. https://doi.org/10.1111/ppl.12050
• Sperdouli I, Adamakis I D S, Dobrikova A, Apostolova E, Hanć A & Moustakas M (2022). Excess zinc supply reduces cadmium uptake and mitigates cadmium toxicity effects on chloroplast structure, oxidative stress, and photosystem II photochemical efficiency in Salvia sclarea plants. Toxics 10: 36. https://doi.org/10.3390/toxics10010036
• Sperdouli I, Mellidou I & Moustakas M (2021). Harnessing chlorophyll fluorescence for phenotyping analysis of wild and cultivated tomato for high photochemical efficiency under water deficit for climate change resilience. Climate 9:154. https://doi.org/10.3390/cli9110154
• Stanton C, Sanders D, Krämer U & Podar D (2022). Zinc in plants: Integrating homeostasis and biofortification. Molecular Plant 15: 65-85. https://doi.org/10.1016/j.molp.2021.12.008
• Suganya A, Saravanan A & Manivannan N (2020). Role of zinc nutrition for increasing zinc availability, uptake, yield, and quality of maize (Zea Mays L.) grains: an overview. Communications in Soil Science and Plant Analysis 51(15): 2001-2021. https://doi.org/10.1080/00103624.2020.1820030
• Szopiński M, Sitko K, Gieroń Ż, Rusinowski S, Corso M, Hermans C, Verbruggen N & Małkowski E (2019). Toxic effects of Cd and Zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes. Frontier in Plant Science 10: 748. https://doi.org/10.3389/fpls.2019.00748
• Tiecher T L, Tiecher T, Ceretta C A, Ferreira P A A, Nicoloso F T, Soriani H H, De Conti L, Kulmann M S S, Schneider R O & Brunetto G (2017). Tolerance and translocation of heavy metals in young grapevine (Vitis vinifera) grown in sandy acidic soil with interaction of high doses of copper and zinc. Scientia Horticulturae 222: 203-212. https://doi.org/10.1016/j.scienta.2017.05.026
• Ünalan Ş (2006) Response of antioxidant enzyme defence system on the maize cultivars under the heavy metal stress and investigation of maize’s usability for removal of heavy metal. MSc thesis, Hacettepe University (in Turkish).
• Vaillant N, Monnet F, Hitmi A, Sallanon H & Coudret A (2005). Comparative study of responses in four Datura species to a zinc stress. Chemosphere 59: 1005-1013. https://doi.org/10.1016/j.chemosphere.2004.11.030
• Wang S Y, Jiao H J & Faust M (1991). Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron‐induced bud break of apple. Physiologia Plantarum 82(2): 231-236. https://doi.org/10.1111/j.1399-3054.1991.tb00086.x
• Wieczorek J, Baran A, Bubak A (2023). Mobility, bioaccumulation in plants, and risk assessment of metals in soils. Science of The Total Environment 882: 163574. https://doi.org/10.1016/j.scitotenv.2023.163574
• Yin J, Gentine P, Zhou S, Sullivan S C, Wang R, Zhang Y, & Guo S (2018). Large increase in global storm runoff extremes driven by climate and anthropogenic changes. Nature communications 9(1): 4389. https://doi.org/10.1038/s41467-018-06765-2