Abstract
Sustainable agricultural practices based on the development of native arbuscular mycorrhizal fungi (AMF) can improve crop growth and stress tolerance in acidic soils with manganese toxicity. The beneficial effects are stronger when crops are colonized early in development by an intact extraradical mycelium (ERM), but are dependent on AMF assemblage. In wheat colonized by AMF associated to Lolium rigidum L. (LOL) or Ornithopus compressus (ORN), growth and stress tolerance are differently influenced. In the present study, this functional diversity was studied by evaluating the activity of ascorbate peroxidase (APX), catalase (CAT), glutathione reductase (GR), guaiacol peroxidase (GPX), superoxide dismutase (SOD) and Mn-SOD. ORN treatment promoted higher wheat shoot and root dry weights, a higher root protein content, decreased root APX, GR and SOD activities but a higher proportion of MnSOD activity. ORN associated microbiota differently manage antioxidant enzyme activity of succeeding wheat to improve growth.
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References
Aebi H (1984) Oxygen radicals in biological systems. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Alho L, Carvalho M, Brito I, Goss MJ (2015) The effect of arbuscular mycorrhiza fungal propagules on the growth of subterranean clover (Trifolium subterraneum L.) under Mn toxicity in ex situ experiments. Soil Use Manag 31:337–344. https://doi.org/10.1111/sum.12183
Aravind P, Prasad MNV (2003) Zinc alleviates cadmium-induced oxidative stress in Ceratophyllum demersum L.: a free floating freshwater macrophyte. Plant Physiol Biochem 41:391–397. https://doi.org/10.1016/S0981-9428(03)00035-4
Baek K-H, Skinner DZ (2006) Differential expression of manganese superoxide dismutase sequence variants in near isogenic lines of wheat during cold acclimation. Plant Cell Rep 25:223–230. https://doi.org/10.1007/s00299-005-0073-6
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brígido C, van Tuinen D, Brito I et al (2017) Management of the biological diversity of AM fungi by combination of host plant succession and integrity of extraradical mycelium. Soil Biol Biochem 112:237–247. https://doi.org/10.1016/j.soilbio.2017.05.018
Brito I, Carvalho M, Alho L, Goss MJ (2014) Managing arbuscular mycorrhizal fungi for bioprotection: Mn toxicity. Soil Biol Biochem 68:78–84. https://doi.org/10.1016/j.soilbio.2013.09.018
Campos C, Carvalho M, Brígido C et al (2018) Symbiosis specificity of the preceding host plant can dominate but not obliterate the association between wheat and its arbuscular mycorrhizal fungal partners. Front Microbiol. https://doi.org/10.3389/fmicb.2018.02920
Campos C, Nobre T, Goss MJ et al (2019) Transcriptome analysis of wheat roots reveals a differential regulation of stress responses related to arbuscular mycorrhizal fungi and soil disturbance. Biology (Basel) 8:93. https://doi.org/10.3390/biology8040093
Carvalho M, Goss MJ, Teixeira D (2015) Manganese toxicity in Portuguese Cambisols derived from granitic rocks: causes, limitations of soil analyses and possible solutions. Rev Ciências Agrárias 38:518–527. https://doi.org/10.19084/RCA15137
Chang W, Sui X, Fan XX et al (2018) Arbuscular mycorrhizal symbiosis modulates antioxidant response and ion distribution in salt-stressed Elaeagnus angustifolia seedlings. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00652
Faria JMS, Teixeira DM, Pinto AP et al (2020) Toxic levels of manganese in an acidic Cambisol alters antioxidant enzymes activity, element uptake and subcellular distribution in Triticum aestivum. Ecotoxicol Environ Saf 193:110355. https://doi.org/10.1016/j.ecoenv.2020.110355
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25. https://doi.org/10.1007/BF00386001
Garg N, Kaur H (2013) Impact of cadmium-zinc interactions on metal uptake, translocation and yield in pigeonpea genotypes colonized by arbuscular mycorrhizal fungi. J Plant Nutr 36:67–90. https://doi.org/10.1080/01904167.2012.733051
Goss MJ, Carvalho MJGPR, Cosimini V, Fearnhead ML (1992) An approach to the identification of potentially toxic concentrations of manganese in soils. Soil Use Manag 8:40–43. https://doi.org/10.1111/j.1475-2743.1992.tb00891.x
Hashem A, Alqarawi AA, Radhakrishnan R et al (2018) Arbuscular mycorrhizal fungi regulate the oxidative system, hormones and ionic equilibrium to trigger salt stress tolerance in Cucumis sativus L. Saudi J Biol Sci 25:1102–1114. https://doi.org/10.1016/j.sjbs.2018.03.009
Hossain MA, Piyatida P, da Silva JAT, Fujita M (2012) Molecular mechanism of heavy metal toxicity and tolerance in plants: central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. J Bot 2012:1–37. https://doi.org/10.1155/2012/872875
Huang X, Zhu S, Ho S-H et al (2017) Arbuscular mycorrhizal fungus modulates the phytotoxicity of Cd via combined responses of enzymes, thiolic compounds, and essential elements in the roots of Phragmites australis. Chemosphere 187:221–229. https://doi.org/10.1016/j.chemosphere.2017.08.021
Islam F, Yasmeen T, Ali Q et al (2014) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293. https://doi.org/10.1016/j.ecoenv.2014.03.008
Kapoor D, Singh S, Kumar V et al (2019) Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene. https://doi.org/10.1016/j.plgene.2019.100182
Karimi J, Mohsenzadeh S (2017) Expression of some genes in response to cadmium stress in Triticum aestivum. Int Lett Nat Sci 63:10–17.
Khabaz-Saberi H, Rengel Z (2010) Aluminum, manganese, and iron tolerance improves performance of wheat genotypes in waterlogged acidic soils. J Plant Nutr Soil Sci 173:461–468. https://doi.org/10.1002/jpln.200900316
Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in arabidopsis: An eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650. https://doi.org/10.1104/pp.118.2.637
Li Y, Sun H, Li H et al (2013) Dynamic changes of rhizosphere properties and antioxidant enzyme responses of wheat plants (Triticum aestivum L.) grown in mercury-contaminated soils. Chemosphere 93:972–977. https://doi.org/10.1016/j.chemosphere.2013.05.063
Liu X, Feng Z, Zhao Z et al (2020) Acidic soil inhibits the functionality of arbuscular mycorrhizal fungi by reducing arbuscule formation in tomato roots. Soil Sci Plant Nutr 66:275–284. https://doi.org/10.1080/00380768.2020.1721320
Luo J, Li X, Jin Y et al (2020) Effects of arbuscular mycorrhizal fungi Glomus mosseae on the growth and medicinal components of Dysosma versipellis under copper stress. Bull Environ Contam Toxicol. https://doi.org/10.1007/s00128-019-02780-1
Malarz J, Wężowicz K, Rozpądek P et al (2014) Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere 112:217–224. https://doi.org/10.1016/j.chemosphere.2014.04.023
Millaleo R, Reyes- Diaz M, Ivanov A et al (2013) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:470–481. https://doi.org/10.4067/s0718-95162010000200008
Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136. https://doi.org/10.1104/pp.110.1.125
Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16. https://doi.org/10.1007/s10725-010-9526-1
Tounsi S, Feki K, Kamoun Y et al (2019) Highlight on the expression and the function of a novel MnSOD from diploid wheat (T. monococcum) in response to abiotic stress and heavy metal toxicity. Plant Physiol Biochem 142:384–394. https://doi.org/10.1016/j.plaphy.2019.08.001
Yadav SK (2010) Heavy metals toxicity in plants: An overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. South African J Bot 76:167–179. https://doi.org/10.1016/j.sajb.2009.10.007
Yang Y, Han X, Liang Y et al (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE 10:e0145726. https://doi.org/10.1371/journal.pone.0145726
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This study was partially funded by Fundo Europeu de Desenvolvimento Regional (FEDER), Programa Operacional Regional Alentejo 2020 under research contract ALT20-03-0145-FEDER-000039.
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Faria, J.M.S., Pinto, A.P., Teixeira, D. et al. Diversity of Native Arbuscular Mycorrhiza Extraradical Mycelium Influences Antioxidant Enzyme Activity in Wheat Grown Under Mn Toxicity. Bull Environ Contam Toxicol 108, 451–456 (2022). https://doi.org/10.1007/s00128-021-03240-5
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DOI: https://doi.org/10.1007/s00128-021-03240-5