Growth, physiological, and biochemical responses of thyme (Thymus vulgaris L.) to the application of arbuscular mycorrhizal fungi under cadmium stress conditions
Keywords:antioxidant activity, bio-fertilizers, heavy metal toxicity, number of leaves, proline content
Thyme (Thymus vulgaris L.) is one of the most important medicinal plants used in various pharmaceutical, osmotic, health, and food industries. Arbuscular mycorrhizal fungi (AMF) symbiosis is viewed as one of the several methods to improve growth under heavy metals stress. To investigate the effects of cadmium (Cd) and AMF bio-fertilizers on the growth and morpho-physiological characteristics of thyme, a greenhouse experiment was performed in three replications. Experimental treatments included Cd at three levels 0, 75, and 150 mg/kg of soil and AMF at three levels without inoculation, inoculation with Funneliformis etunicatum, and Funneliformis mosseae. Cadmium stressed plant showed reduced plant height, number of leaves, stem fresh and dry weight, and root fresh and dry weight while AMF inoculation enhanced the increased means of these traits considerably. Inoculation with F. mosseae also ameliorated the Cd stress (150 mg/kg) induced reduction in plant height, number of leaves, and stem and root dry weight by 13.41%, 8.42%, 30.3%, and 22.2%, respectively. Cadmium stress reduced membrane stability index while AMF inoculation enhanced membrane stability index considerably. An increase in soluble carbohydrate and proline content was observed due to Cd stress and AMF inoculation caused a further increase in these two metabolite contents ensuring better growth under Cd stressed conditions. Results indicated that F. mosseae had a higher efficiency in increasing morphological traits and improving physiological characteristics than F. etunicatum. Overall, AMF inoculation, especially F. mosseae significant ameliorative potential for Cd toxicity in thyme plants.
Abd_Allah EF, Hashem A, Alqarawi AA, Alwathnani HA (2015). Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pakistan Journal of Botany 47(2):785-795.
Abdelhameed RE, Metwally RA (2019). Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. International Journal of Phytoremediation 21:663-671. https://doi.org/10.1080/15226514.2018.1556584
Aghighi Shahverdi M, Omidi H, Tabatabaei SJ (2017). Effect of nutri-priming on germination indices and physiological characteristics of stevia seedling under salinity stress. Journal of Seed Science 39(4):353-362. https://doi.org/10.1590/2317-1545v39n4172539
Aghighi Shahverdi M, Omidi H, Tabatabaei SJ (2018). Morpho-physiological response of stevia (Stevia rebaudiana Bertoni) to salinity under hydroponic culture condition (a case study in Iran). Applied Ecology and Environmental Research 16(1):17-28. https://doi.org/10.15666/aeer/1601_017028
Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2018). Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163-174. https://doi.org/10.1007/s00709-017-1140-x
Ali A, Deng X, Hu X, Gill RA, Ali S, Wang S, Zhou W (2015). Deteriorative effects of cadmium stress on antioxidant system and cellular structure in germinating seeds of Brassica napus L. Journal of Agricultural Science and Technology 17:63-74.
Ali S, Farooq MA, Hussain S, Yasmeen T, Abbasi GH, Zhang G (2013). Alleviation
of chromium toxicity by hydrogen sulfide in barley. Environmental Toxicology Chemistry 10:2234-2239. https://doi.org/10.1002/etc.2309
Alqarawi AA, Abd-Allah EF, Abeer H (2014). Alleviation of salt-induced adverse impact via mycorrhizal fungi in Ephedra aphylla Forssk. Journal of Plant Interactions 9(1):802-810. https://doi.org/10.1080/17429145.2014.949886
Bates LS, Waldern RP, Teave ID (1973). Rapid determination of free proline for water stress studies. Plant and Soil 39:205-107. https://doi.org/10.1007/BF00018060
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, … Zhang L (2019). Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science 10:1068. https://doi.org/10.3389/fpls.2019.01068
Belimov AA, Dodd IC, Safronova VI, Malkov NV, Davies WJ, Tikhonovich IA (2015). The cadmium-tolerant pea (Pisum sativum L.) mutant SGECdt is more sensitive to mercury: assessing plant water relations. Journal of Experimental Botany 66(8):2359-2369. https://doi.org/10.1093/jxb/eru536
Ben-Dor E, Banin A (1989). Determination of organic matter content in arid‐zone soils using a simple “loss‐on‐ignition” method. Communications in Soil Science and Plant Analysis 20(16):1675-1695. https://doi.org/10.1080/00103628909368175
Chance B, Maehly AC (1995). Assay of catalase and peroxidase. New York, NY: Academic Press, pp 764-775. https://doi.org/10.1016/S0076-6879(55)02300-8
Chanclud E, Moral JB (2016). Plant hormones: A fungal point of view. Molecular Plant Pathology 17(8):1289-1297. https://doi.org/10.1111/mpp.12393
Chaturvedi R, Favas PJC, Pratas J, Varun M, Paul MS (2018). Effect of Glomus mossae on accumulation efficiency, hazard index and antioxidant defense mechanisms in tomato under metal (loid) stress. International Journal of Phytoremediation 20(9):885-894. https://doi.org/10.1080/ 15226514.2018.1438360
Chmielowska-Bak J, Izbianska K, Ekner-Grzyb A, Bayar M, Deckert J (2018). Cadmium stress leads to rapid increase in RNA oxidative modifications in soybean seedlings. Front. Plant Science 8:2219. https://doi.org/10.3389/fpls.2017.02219
Cordero B, Lodeiro P, Herrero R, Esteban Sastre de Vicente M (2004). Biosorption of cadmium by Fucus spiralis. Environmental Chemistry 1:180-187. https://doi.org/10.1071/EN04039
Dehghani AS, Kazemeini A, Zarei M, Alinia M (2017). Effects of salt stress and mycorrhiza fungi on morpho-physiological characteristics of sweet corn (Zea mays var. saccharata). Journal of Crop Production and Processing 7(1):101-112. https://doi.org/10.18869/acadpub.jcpp.7.1.101
Dinakar N, Nagajyothi PC, Suresh S, Udaykiran Y, Damodharam T (2008). Phytotoxicity of cadmium on protein, proline and antioxidant enzyme activities in growing Arachis hypogaea L. seedlings. Environmental Science 20:199-206. https://doi.org/10.1016/S1001-0742(08)60032-7
Gee GW, Bauder JW (1986). Particle-size analysis. In: Page AL (Ed). Methods of Soil Analysis. Part 1. Physical and Mineralogical Methods. Second Edition, Agronomy Monograph 9, American Society of Agronomy, Madison, WI, pp 383-411.
Gerdeman JW, Nicolson TH (1963). Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society 46:235-244. https://doi.org/10.1016/S0007-1536(63)80079-0
Giovannetti M, Mosse B (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84:489-500.
Gupta AP, Dhar JK, Sharma G, Ram G, Bedi YS (2010). Volatile (As and Hg) and non-volatile (Pb and Cd) toxic heavy metals analysis in rhizome of Zingiber officinale collected from different locations of North Western Himalayas by atomic absorption spectroscopy. Food Chemical Toxicology Journal 8(10):2966-2971. https://doi.org/10.1016/j.fct.2010.07.034
Hashem A, Abd-Allah EF, Alqarawi AA, Egamberdieva D (2016). Bioremediation of adverse impact of cadmium toxicity on Cassia italica Mill by arbuscular mycorrhizal fungi. Saudi Journal of Biological Sciences 23:39-47. http://dx.doi.org/10.1016/j.sjbs.2015.11.007
Hashem A, Abd_Allah EF, Alqarawi AA, El-Didamony G, Alwhibi Mona S, Egamberdieva D, Ahmad P (2014). Alleviation of adverse impact of salinity on faba bean (Vicia faba L.) by arbuscular mycorrhizal fungi. Pakistan Journal Botany 46(6):2003-2013.
Hu J, Wang H, Wu F, Wu S, Cao Z, Lin X, Wong MH (2014). Arbuscular mycorrhizal fungi influence the accumulation and partitioning of Cd and P in bashful grass (Mimosa pudica L.) grown on a moderately Cd-contaminated soil. Applied Soil Ecology 73:51-57. https://doi.org/10.1016/j.apsoil.2013.08.010
Irfan M, Ahmad A, Hayat S (2014). Effect of cadmium on the growth and antioxidant enzymes in two varieties of Brassica juncea L. Saudi Journal of Biological Sciences 21:125-131. https://doi.org/10.1016/j.sjbs.2013.08.001
Kabir M, Iqbal MZ, Shafiq M, Farroqi ZR (2018). The effects of lead and cadmium individually and in combinations on germination and seedling growth of Leucaena leucocephala (Lam). American Scientific Research Journal for Engineering, Technology, and Sciences 43:33-43.
Kalvandi R, Mirza M, Atri M, Hesamzadeh Hejazi M, Jamzad Z, Safikhan K (2014). Introduction of seven new chemotypes of Thymus eriocalyx (Ronniger) Jalas in Iran based upon the variation of essential oil composition in different populations. Iranian Journal Medicinal and Aromatic Plants 30:101-22.
Kanwal S, Bano A, Malik RN (2015). Effects of arbuscular mycorrhizal fungi on metals uptake, physiological and biochemical response of Medicago sativa L. with increasing Zn and Cd concentrations in soil. American Journal of Plant Sciences 6:2906-2923. https://doi.org/10.4236/ajps.2015.618287
Kapoor R, Giri B, Mukerji KG (2004). Improved growth and essential oil yield and quality in Foeniculum vulgare on mycorrhizal inoculation supplemented with P-fertilizer. Journal of Biological Resource Technology 93:307-311. https://doi.org/10.1016/j.biortech.2003.10.028
Kaya C, Akram NA, Surucu A, Ashraf M (2019). Alleviating effect of nitric oxide on oxidative stress and antioxidant defence system in pepper (Capsicum annuum L.) plants exposed to cadmium and lead toxicity applied separately or in combination. Scientia Horticulturae 255:52-60. https://doi.org/10.1016/j.scienta.2019.05.029
Kaya C, Ashraf M, Alymeni MN, Ahmad P (2020). The role of nitrate reductase in brassinosteroid-induced endogenous nitric oxide generation to improve cadmium stress tolerance of pepper plants by upregulating the ascorbate-glutathione cycle. Ecotoxicology and Environmental Safety 196:110483. https://doi.org/10.1016/j.ecoenv.2020.110483
Kucukaydin S, Tel-Cayan G, Duru ME, Kesdek M, Ozturk M (2020). Chemical composition and insecticidal activities of the essential oils and various extracts of two Thymus species: Thymus cariensis and Thymus cilicicus. Toxin Reviews. https://doi.org/10.1080/15569543.2020.1731552
Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY (2016). Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Science of the Total Environment 571:1183-1190. https;//doi.org/10.1016/j.scitotenv.2016.07.124
Luo Z, Wu C, Zhang C, Li H, Lipka U, Polle A (2014). The role of ectomycorrhizas in heavy metal stress tolerance of host plants. Environmental and Experimental Botany 108:47-62. https://doi.org/10.1016/j.envexpbot.2013.10.018
Miransari M (2017). Arbuscular mycorrhizal fungi and heavy metal tolerance in plants. In: Wu QS (Ed). Arbuscular Mycorrhizas and Stress Tolerance of Plants. Singapore: Springer Nature, pp 174-161. https://doi.org/10.1007/978-3-319-68867-1_4
Nareshkumar A, Nagamallaiah GV, Pandurangaiah M, Kiranmai K, Amaranathareddy V, Lokesh U, … Sudhakar C (2015). Pb-Stress induced oxidative stress caused alterations in antioxidant efficacy in two groundnut (Arachis hypogaea L.) cultivars. Agricultural Sciences 6:1283-1297. https://doi.org/10.4236/as.2015.610123
Nas FS, Ali M (2018). The effect of lead on plants in terms of growing and biochemical parameters: a review. MOJ Ecology & Environmental Sciences 3(4):265-268.
Neagoe A, Stancu P, Nicoara A, Onete M, Bodescu F, Gheorghe R, Iordache V (2014). Effects of arbuscular mycorrhizal fungi on Agrostis capillaris grown on amended mine tailing substrate at pot, lysimeter, and field plot scales. Environmental Science and Pollution Research 21:6859-6876. https://doi.org/10.1007/s11356-013-1908-2
Pirbalouti AG, Bistghani ZE, Malekpoor F (2015). An overview on genus Thymus. Journal of Herbal Drugs 6(2):93-100.
Polle A, Otter T, Seifert F (1994). Apoplastic peroxidase and lignification in needles of Norway Spruce Picea abies L. Plant Physiology 106:53-60. https://doi.org/10.1104/pp.106.1.53
Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Da P (2010). Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass Chrysopogon zizanioides L. Journal of Hazardous Materials 177:465-474. https://doi.org/10.1016/j. jhazmat.2009.12.056
Rahimzadeh MR, Rahimzadeh MR, Kazemi S, Moghadamnia AA (2017). Cadmium toxicity and treatment: An update. Caspian Journal Internal Medicine 8(3):135-145. https://doi.org/10.22088/cjim.8.3.135
Rasheed R, Ashraf MA, Kamran S, Iqbal M, Hussain I (2018). Menadione sodium bisulphite mediated growth, secondary metabolism, nutrient uptake and oxidative defense in okra (Abelmoschus esculentus Moench) under cadmium stress. Journal of Hazardous Materials 360:604-614. https://doi.org/10.1016/j.jhazmat.2018.08.043
Ruiz E, Alonso-Azcárate J, Rodríguez L (2011). Lum bricus terrestris L. activity increases the availability of metals and their accumulation in maize and barley. Environmental Pollution 159:722-728. https://doi.org/10.1016/j.envpol.2010.11.032
Sairam RK (1994). Effect of homobrassinolide application on metabolism and grain yield under irrigated and moisture stress conditions of two wheat varieties. Plant Growth Regulation 14:173-181. https://doi.org/10.1007/BF00025220
Shekoofeh E, Sepideh H, Roya R (2012). Role of mycorrhizal fungi and salicylic acid in salinity tolerance of Ocimum basilicum resistance to salinity. African Journal of Biotechnology 11(9):2223-2235. https://doi.org/10.5897/AJB11.1672
Siddhu G, Ali, MA (2012). Effect of cadmium on growth and metabolism of Phaseolus mungo. Journal of Environmental Biology 33(2):173-179.
Song L, Chen J, Islam E, Ying W, Wu J, Ye Z, … Liu D (2016). Cadmium-induced oxidative stress response of antioxidants and detection of intracellular cadmium in organs of moso bamboo (Phyllostachys pubescens) seedlings. Chemosphere 153:107-114. https://doi.org/10.1016/j.chemosphere.2016.02.062
Song X, Yue X, Chen W, Jiang H, Han Y, Li X (2019). Detection of cadmium risk to the photosynthetic performance of Hybrid pennisetum. Frontiers in Plant Science 10:798-806. https://doi.org/10.3389/fpls.2019.00798
Tan SY, Jiang Q, Zhuo F, Liu H, Wang YT, Li SS, … Jing YX (2015). Effect of inoculation with Glomus versiforme on cadmium accumulation, antioxidant activities and phytochelatins of Solanum photeinocarpum. PLoS One 10:1-16.
Usman K, Al-ghouti A, Abu-Dieyeh MH (2019). The assessment of cadmium, chromium, copper, and nickel tolerance and bioaccumulation by shrub plant Tetraena qataranse. Scientific Reports 9:5658. https://doi.org/10.1038/s41598-019-42029-9
Vasiljeva S, Smirnova G, Basova N, Babarykin D (2018). Cadmium-induced oxidative damage and protective action of fractioned red beet (Beta vulgaris) root juice in chickens. Agronomy Research 16:1517-1526. https://doi.org/10.15159/AR.18.117
Whitfield LAJ, Richards DL (2004). Rimmer. Relationships between soil heavy metal concentration and mycorrhizal colonization in Thymus polytrichus in northern England. Mycorrhiza Journal 14(1):55-62. https://doi.org/10.1007/s00572-003-0268-z
Wu QS, Xia RX (2006). Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. Journal of Plant Physiology 163:417-425. https://doi.org/10.1016/j.jplph.2005.04.024
Wuana RA, Okieimen FE (2011). Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. International Scholarly Research Notices https://doi.org/10.5402/2011/402647
Yang Y, Liang Y, Han X, Chiu TY, Ghosh A, Chen H, Tang M (2016). The roles of arbuscular mycorrhizal fungi (AMF) in phytoremediation and tree-herb interactions in Pb contaminated soil. Scientific Reports 6:20469. https://doi.org/10.1038/srep20469
Yao Q, Yang R, Long L, Zhu HH (2014). Phosphate application enhances the resistance of arbuscular mycorrhizae in clover plants to cadmium via polyphosphate accumulation in fungal hyphae. Environmental and Experimental Botany 108:63-70. https://doi.org/10.1016/j.envexpbot.2013.11.007
Yemm EW, Folkes BF (1953). The estimation of carbohydrates in plant extracts by anthrone. Biochemistry Journal 55:700-701.
Yooyongwech S, Phaukinsang N, Cha-um S, Supaibulwatana K (2013). Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regulation 69:285-293. https://doi.org/10.1007/s10725-012-9771-6
Zhang Y, Hu J, Bai J, Wang J, Yin R, Wang J, Lin X (2018). Arbuscular mycorrhizal fungi alleviate the heavy metal toxicity on sunflower (Helianthus annuus L.) plants cultivated on a heavily contaminated field soil at a WEEE-recycling site. Science of the Total Environment 629:282-290. https://doi.org/10.1016/j.scitotenv.2018.01.331
Zhao Y (2011). Cadmium accumulation and antioxidative defenses in leaves of Triticum aestivum L. and Zea mays L. African Journal of Biotechnology 10:2936-2943. https://doi.org/10.5897/AJB10.1230
Zou YN, Srivastava AK, Wu QS, Huang YM (2014). Increased tolerance of trifoliate orange (Poncirus trifoliata) seedlings to waterlogging after inoculation with arbuscular mycorrhizal fungi. Journal of Animal and Plant Sciences 24:1415-1420.
How to Cite
Copyright (c) 2021 Notulae Botanicae Horti Agrobotanici Cluj-Napoca
This work is licensed under a Creative Commons Attribution 4.0 International License.
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.