AMF modulated rhizospheric microbial enzyme activities and their impact on sulphur assimilation along with thiol metabolism in pigeonpea under Cd stress

Aalipour, 2021, Physiological response of Arizona cypress to Cd-contaminated soil inoculated with arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria, Rhizosphere, 18, 100354, 10.1016/j.rhisph.2021.100354 Adhikari, 2018, Sulfate improves cadmium tolerance by limiting cadmium accumulation, modulation of sulfur metabolism and antioxidant defense system in maize, Environ. Exp. Bot., 153, 143, 10.1016/j.envexpbot.2018.05.008 Aebi, 1984, Catalase in vitro, 121, 10.1016/S0076-6879(84)05016-3 2019 Akinyemi, 2017, Effect of cadmium stress on non-enzymatic antioxidant and nitric oxide levels in two varieties of maize (Zea mays), Bull. Environ. Contam. Toxicol., 98, 845, 10.1007/s00128-017-2069-7 Alaraidh, 2018, Alteration of antioxidant gene expression in response to heavy metal stress in Trigonella foenum-graecum L, South Afr. J. Bot., 115, 90, 10.1016/j.sajb.2018.01.012 Axelrod, 1981, [53] Lipoxygenase from soybeans: EC 1.13. 11.12 Linoleate: oxygen oxidoreductase, Methods Enzymol., 71, 441, 10.1016/0076-6879(81)71055-3 Bari, 2019, Cadmium tolerance is associated with the root-driven coordination of cadmium sequestration, iron regulation, and ROS scavenging in rice, Plant Physiol Biochem, 136, 22, 10.1016/j.plaphy.2019.01.007 Bhargava, 2005, Phytochelatin plays a role in UV-B tolerance in N2-fixing cyanobacterium Anabaena doliolum, J. Plant Physiol., 162, 1220, 10.1016/j.jplph.2004.12.006 Bisht, 2021, Gene expression analysis for selection and validation of suitable housekeeping gene (s) in cadmium exposed pigeonpea plants inoculated with arbuscular mycorrhizae, Plant Physiol Biochem, 162, 592, 10.1016/j.plaphy.2021.03.024 Bisht, 2022, AMF species improve yielding potential of Cd stressed pigeonpea plants by modulating sucrose-starch metabolism, nutrients acquisition and soil microbial enzymatic activities, Plant Growth Regul., 3, 1 Bradford, 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, 10.1016/0003-2697(76)90527-3 Casarrubia, 2020, Modulation of plant and fungal gene expression upon Cd exposure and symbiosis in ericoid mycorrhizal Vaccinium myrtillus, Front. Microbiol., 11, 341, 10.3389/fmicb.2020.00341 Casida, 1964, Soil dehydrogenase activity, Soil Sci., 98, 371, 10.1097/00010694-196412000-00004 Castillo, 1988, Extracellular ascorbic acid and enzyme activities related to ascorbic acid metabolism in Sedum album L. leaves after ozone exposure, Environ. Exp. Bot., 28, 231, 10.1016/0098-8472(88)90033-0 Castillo, 1984, Peroxidase release induced by ozone in Sedum album leaves: involvement of Ca2+, Plant Physiol, 74, 846, 10.1104/pp.74.4.846 Çatav, 2020, Cadmium toxicity in wheat: impacts on element contents, antioxidant enzyme activities, oxidative stress, and genotoxicity, Bull. Environ. Contam. Toxicol., 104, 71, 10.1007/s00128-019-02745-4 Chang, 2018, Effects of arbuscular mycorrhizal symbiosis on growth, nutrient and metal uptake by maize seedlings (Zea mays L.) grown in soils spiked with Lanthanum and Cadmium, Environ. Pollut., 241, 607, 10.1016/j.envpol.2018.06.003 Cui, 2020, Transcriptome analysis reveals insight into molecular hydrogen-induced cadmium tolerance in alfalfa: the prominent role of sulfur and (homo) glutathione metabolism, BMC Plant Biol., 20, 1, 10.1186/s12870-020-2272-2 Curaqueo, 2014, Inoculation with arbuscular mycorrhizal fungi and addition of composted olive-mill waste enhance plant establishment and soil properties in the regeneration of a heavy metal-polluted environment, Environ. Sci. Pollut. Res., 21, 7403, 10.1007/s11356-014-2696-z Dhalaria, 2020, Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants, Agronomy, 10, 815, 10.3390/agronomy10060815 Dhindsa, 1981, Leaf senescence, correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase, J. Exp. Bot., 32, 93, 10.1093/jxb/32.1.93 Doke, 1983, Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components, Physiol. Plant Pathol., 23, 345, 10.1016/0048-4059(83)90019-X Faostat Garg, 2021, Relative roles of Arbuscular Mycorrhizae in establishing a correlation between soil properties, carbohydrate utilization and yield in Cicer arietinum L. under as stress, Ecotoxicol. Environ. Saf., 207, 111196, 10.1016/j.ecoenv.2020.111196 Gigolashvili, 2014, Transporters in plant sulfur metabolism, Front. Plant Sci., 5, 442, 10.3389/fpls.2014.00442 Gill, 2012, Cadmium at high dose perturbs growth, photosynthesis and nitrogen metabolism while at low dose it up regulates sulfur assimilation and antioxidant machinery in garden cress (Lepidium sativum L.), Plant Sci., 182, 112, 10.1016/j.plantsci.2011.04.018 Giovannetti, 1980, An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots, New Phytol., 84, 489, 10.1111/j.1469-8137.1980.tb04556.x Głowacka, 2019, The effect of cadmium on the activity of stress-related enzymes and the ultrastructure of pea roots, Plants, 8, 413, 10.3390/plants8100413 Hasanuzzaman, 2017, Exogenous silicon attenuates cadmium-induced oxidative stress in Brassica napus L. by modulating AsA-GSH pathway and glyoxalase system, Front. Plant Sci., 8, 1061, 10.3389/fpls.2017.01061 Heath, 1968, Photoperoxidation in isolated chloroplast I, kinetics and stoichiometry of fatty acid peroxidation, Arch. Biochem. Biophys., 125, 189, 10.1016/0003-9861(68)90654-1 Hetrick, 1992, Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors, Can. J. Bot., 70, 2032, 10.1139/b92-253 Hristozkova, 2017, Symbiotic association between golden berry (Physalis peruviana) and arbuscular mycorrhizal fungi in heavy metal-contaminated soil, J. Plant Protect. Res., 57, 173, 10.1515/jppr-2017-0024 Huang, 2017, Adaptive response of arbuscular mycorrhizal symbiosis to accumulation of elements and translocation in Phragmites australis affected by cadmium stress, J. Environ. Manag., 197, 448, 10.1016/j.jenvman.2017.04.014 Khaliq, 2019, Uptake, translocation, and accumulation of Cd and its interaction with mineral nutrients (Fe, Zn, Ni, Ca, Mg) in upland rice, Chemosphere, 215, 916, 10.1016/j.chemosphere.2018.10.077 Khan, 2016, Modulation and significance of nitrogen and sulfur metabolism in cadmium challenged plants, Plant Growth Regul., 78, 1, 10.1007/s10725-015-0071-9 Kiers, 2011, Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis, Science, 333, 880, 10.1126/science.1208473 Lappartient, 1996, Demand-driven control of root ATP sulfurylase activity and SO42-uptake in intact canola (the role of phloem-translocated glutathione), Plant Physiol, 111, 147, 10.1104/pp.111.1.147 Li, 2016, Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice?, Sci. Total Environ., 571, 1183, 10.1016/j.scitotenv.2016.07.124 Liang, 2016, Sulfur decreases cadmium translocation and enhances cadmium tolerance by promoting sulfur assimilation and glutathione metabolism in Brassica chinensis L, Ecotoxicol. Environ. Saf., 124, 129, 10.1016/j.ecoenv.2015.10.011 Liu, 2018, Identification and functional characterization of a maize phosphate transporter induced by mycorrhiza formation, Plant Cell Physiol., 59, 1683, 10.1093/pcp/pcy094 Lou, 2017, Sulfur protects pakchoi (Brassica chinensis L.) seedlings against cadmium stress by regulating ascorbate-glutathione metabolism, Int. J. Mol. Sci., 18, 1628, 10.3390/ijms18081628 Lu, 2019, Effects of exogenous sulfur on alleviating cadmium stress in tartary buckwheat, Sci. Rep., 9, 1 Manquián-Cerda, 2016, Effect of cadmium on phenolic compounds, antioxidant enzyme activity and oxidative stress in blueberry (Vaccinium corymbosum L.) plantlets grown in vitro, Ecotoxicol. Environ. Saf., 133, 316, 10.1016/j.ecoenv.2016.07.029 Marguí, 2007, XRF spectrometry for trace element analysis of vegetation samples, Spectrosc. Eur., 19, 13 May, 1976, Assay for soil urease activity, Plant Soil, 45, 301, 10.1007/BF00011156 Nagalakshmi, 2001, Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus, Plant Sci., 160, 291, 10.1016/S0168-9452(00)00392-7 Njaci, 2021, Comparative analysis delineates the transcriptional resistance mechanisms for pod borer resistance in the pigeonpea wild relative Cajanus scarabaeoides (L.) Thouars, Int. J. Mol. Sci., 22, 309, 10.3390/ijms22010309 Pellegrino, 2014, Enhancing ecosystem services in sustainable agriculture: biofertilization and biofortification of chickpea (Cicer arietinum L.) by arbuscular mycorrhizal fungi, Soil Biol. Biochem., 68, 429, 10.1016/j.soilbio.2013.09.030 Pérez-Tienda, 2011, GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices, Fungal Genet. Biol., 48, 1044, 10.1016/j.fgb.2011.08.003 Qin, 2020, Effect of arbuscular mycorrhizal fungi on soil enzyme activity is coupled with increased plant biomass, Eur. J. Soil Sci., 71, 84, 10.1111/ejss.12815 Qin, 2018, Influence of selenium on root morphology and photosynthetic characteristics of winter wheat under cadmium stress, Environ. Exp. Bot., 150, 232, 10.1016/j.envexpbot.2018.03.024 Qiu, 2021, Strigolactone GR24 improves cadmium tolerance by regulating cadmium uptake, nitric oxide signaling and antioxidant metabolism in barley (Hordeum vulgare L.), Environ. Pollut., 273, 116486, 10.1016/j.envpol.2021.116486 Riaz, 2021, Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review, J. Hazard Mater., 14, 123919, 10.1016/j.jhazmat.2020.123919 Rohani, 2019, Growth and some physiological characteristics of Pistacia vera L. cv Ahmad Aghaei in response to cadmium stress and Glomus mosseae symbiosis, South Afr. J. Bot., 124, 499, 10.1016/j.sajb.2019.06.001 Ruíz-Torres, 2017, Arsenic-induced stress activates sulfur metabolism in different organs of garlic (Allium sativum L.) plants accompanied by a general decline of the NADPH-generating systems in roots, J. Plant Physiol., 211, 27, 10.1016/j.jplph.2016.12.010 Sairam, 1997, Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat, J. Agron. Crop Sci., 178, 171, 10.1111/j.1439-037X.1997.tb00486.x Sarker, 2018, Drought stress effects on growth, ROS markers, compatible solutes, phenolics, flavonoids, and antioxidant activity in Amaranthus tricolor, Appl. Biochem. Biotechnol., 186, 999, 10.1007/s12010-018-2784-5 Sarker, 2018, Response of nutrients, minerals, antioxidant leaf pigments, vitamins, polyphenol, flavonoid and antioxidant activity in selected vegetable amaranth under four soil water content, Food Chem., 252, 72, 10.1016/j.foodchem.2018.01.097 Sarker, 2020, Nutritional and bioactive constituents and scavenging capacity of radicals in Amaranthus hypochondriacus, Sci. Rep., 10, 19962, 10.1038/s41598-020-71714-3 Sarker, 2020, The response of salinity stress-induced A. tricolor to growth, anatomy, physiology, non-enzymatic and enzymatic antioxidants, Front. Plant Sci., 11, 559876, 10.3389/fpls.2020.559876 Sarker, 2021, Color attributes, betacyanin, and carotenoid profiles, bioactive components, and radical quenching capacity in selected Amaranthus gangeticus leafy vegetables, Sci. Rep., 11, 11559, 10.1038/s41598-021-91157-8 Smith, 1988, Assay of glutathione reductase in crude tissue homogenates using 5,5-dithiobis (2-nitrobenzoic acid), Anal. Biochem., 175, 408, 10.1016/0003-2697(88)90564-7 Tabatabai, 1969, Use of p-nitrophenyl phosphate for assay of soil phosphatase activity, Soil Biol. Biochem., 1, 301, 10.1016/0038-0717(69)90012-1 Varshney, 2010, Pigeonpea genomics initiative (PGI): an international effort to improve crop productivity of pigeonpea (Cajanus cajan L.), Mol. Breed., 26, 393, 10.1007/s11032-009-9327-2 Velikova, 2000, Oxidative stress and some antioxidative systems in acid rain treated bean plants, Plant Sci., 151, 59, 10.1016/S0168-9452(99)00197-1 Vijendra, 2016, Physiological and biochemical changes in moth bean (Vigna aconitifolia L.) under cadmium stress, J. Bot., Le, 10.1155/2016/6403938 Vilela, 2018, Symbiotic microorganisms enhance antioxidant defense in plants exposed to metal/metalloid-contaminated soils, 337 Walder, 2016, Regulation of plants' phosphate uptake in common mycorrhizal networks: role of intraradical fungal phosphate transporters, Plant Signal. Behav., 11, 10.1080/15592324.2015.1131372 Wan, 2019, Effect of selenium on the subcellular distribution of cadmium and oxidative stress induced by cadmium in rice (Oryza sativa L.), Environ. Sci. Pollut. Res., 26, 16220, 10.1007/s11356-019-04975-9 Wang, 2017, Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis, Mol. Plant, 10, 1147, 10.1016/j.molp.2017.07.012 Wright, 1998, A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi, Plant Soil, 198, 97, 10.1023/A:1004347701584 Wu, 2019, Silicon decreases cadmium concentrations by modulating root endodermal suberin development in wheat plants, J. Hazard Mater., 364, 581, 10.1016/j.jhazmat.2018.10.052 Wu, 2015, Antioxidant enzyme systems and the ascorbate–glutathione cycle as contributing factors to cadmium accumulation and tolerance in two oilseed rape cultivars (Brassica napus L.) under moderate cadmium stress, Chemosphere, 138, 526, 10.1016/j.chemosphere.2015.06.080 Xiao, 2019, Effects of re-vegetation type and arbuscular mycorrhizal fungal inoculation on soil enzyme activities and microbial biomass in coal mining subsidence areas of Northern China, Catena, 177, 202, 10.1016/j.catena.2019.02.019 Xu, 2019, Growth, accumulation, and antioxidative responses of two Salix genotypes exposed to cadmium and lead in hydroponic culture, Environ. Sci. Pollut. Res., 26, 19770, 10.1007/s11356-019-05331-7 Yang, 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, 10.1371/journal.pone.0145726 Yang, 2017, The effects of arbuscular mycorrhizal fungi on glomalin-related soil protein distribution, aggregate stability and their relationships with soil properties at different soil depths in lead-zinc contaminated area, PLoS One, 12 Zhan, 2018, Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize, Environ. Sci. Pollut. Res., 25, 24338, 10.1007/s11356-018-2487-z Zhang, 2019, Effects of arbuscular mycorrhizal fungi, biochar and cadmium on the yield and element uptake of Medicago sativa, Sci. Total Environ., 655, 1150, 10.1016/j.scitotenv.2018.11.317 Zhang, 2014, Effects of nitrogen on the activity of antioxidant enzymes and gene expression in leaves of Populus plants subjected to cadmium stress, J. Plant Interact., 9, 599, 10.1080/17429145.2013.879676 Zhang, 2020, Exogenous application of glycine betaine alleviates cadmium toxicity in super black waxy maize by improving photosynthesis, the antioxidant system and glutathione-ascorbic acid cycle metabolites, Cereal Res. Commun., 48, 449, 10.1007/s42976-020-00062-9 Zheng, 2019, The inhibitory effect of cadmium and/or mercury on soil enzyme activity, basal respiration, and microbial community structure in coal mine–affected agricultural soil, Ann. Microbiol., 69, 849, 10.1007/s13213-019-01478-3 Zou, 2012, Effects of cadmium stress on root tip cells and some physiological indexes in Allium cepa var, agrogarum L. Acta Biol Crac Ser Bot, 54 Zwiazek, 1990, Effects of preconditioning on electrolyte leakage and lipid composition in black spruce (Picea mariand) stressed with polyethylene glycol, Physiol. Plantarum, 79, 71, 10.1111/j.1399-3054.1990.tb05868.x