Mechanism of the synergistic impact of Piriformospora indica and Azotobacter chroococcum on Zn and Fe biofortification

Abadi, 2021, Alleviation of zinc deficiency in wheat inoculated with root endophytic fungus Piriformospora indica and rhizobacterium Pseudomonas putida, Rhizosphere, 17, 100311, 10.1016/j.rhisph.2021.100311 Achatz, 2010, Piriformospora indica mycorrhization increases grain yield by accelerating early development of barley plants, Plant Signal. Behav., 5, 1685, 10.4161/psb.5.12.14112 Baghaie, 2020, Iron enriched green manure can increase wheat Fe concentration in Pb-polluted soil in the presence of Piriformospora indica (P. indica), Soil Sediment Contam., 29, 721, 10.1080/15320383.2020.1771274 Bajaj, 2014, Co-cultivation of Curcuma longa with Piriformospora indica enhances the yield and active ingredients, Am. J. Curr. Microbiol., 2, 6 Bandyopadhyay, 2022, Piriformospora indica and Azotobacter chroococcum consortium facilitates higher acquisition of N, P with improved carbon allocation and enhanced plant growth in Oryza sativa, J. Fungi., 8, 453, 10.3390/jof8050453 Bhuyan, 2015, Interaction of Piriformospora indica with Azotobacter chroococcum, Sci. Rep., 5, 1 Chhabra, 2017, Endophyte-promoted nutrient acquisition: phosphorus and iron, 21 Clemens, 2002, A long way ahead: understanding and engineering plant metal accumulation, Trends Plant Sci., 7, 309, 10.1016/S1360-1385(02)02295-1 Daneshkhah, 2013, Piriformospora indica antagonizes cyst nematode infection and development in Arabidopsis roots, J. Exp. Bot., 64, 3763, 10.1093/jxb/ert213 Durmaz, 2011, Expression and cellular localization of ZIP1 transporter under zinc deficiency in wild emmer wheat, Plant Mol. Biol. Rep., 29, 582, 10.1007/s11105-010-0264-3 Elzemrany, H.M., Faiyad, R., 2021. Maximizing use efficiency of mineral fertilizers using K fulvate and Azotobacter chroococcum DSM 2286 and their effect on wheat production and nutrients uptake. Egypt. J. Soil Sci. 61, 13–25. Evens, 2017, The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum), Plant J., 92, 291, 10.1111/tpj.13655 Ferrol, 2016, The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications, J. Exp. Bot., 67, 6253, 10.1093/jxb/erw403 Ghorbani, 2021, Piriformospora indica augments arsenic tolerance in rice (Oryza sativa) by immobilizing arsenic in roots and improving iron translocation to shoots, Ecotoxicol. Environ. Saf., 209, 10.1016/j.ecoenv.2020.111793 Grotz, 1998, Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency, Proc. Natl. Acad. Sci., 95, 7220, 10.1073/pnas.95.12.7220 Hoberg, 2005, Organic acid exudation and pH changes by Gordonia sp. and Pseudomonas fluorescens grown with P adsorbed to goethite, Microbiol. Res., 160, 177, 10.1016/j.micres.2005.01.003 Hughes, 2008, Mycorrhizal respiration: implications for global scaling relationships, Trends Plant Sci., 13, 583, 10.1016/j.tplants.2008.08.010 Karthikeyan, 2011, Efficacy of Azotobacter chroococcum in rooting and growth of Eucalyptus camaldulensis stem cuttings, Res. J. Microbiol., 6, 618, 10.3923/jm.2011.618.624 Khosravi, 2009, Inoculation of ‘Golden Delicious’ apple trees on M9 rootstock with Azotobacter improves nutrient uptake and growth indices, J. Plant Nutr., 32, 946, 10.1080/01904160902870713 Kuang, 2003, Root exudates and their roles in phytoremediation, Chin. J. Plant Ecol., 27, 709, 10.17521/cjpe.2003.0103 Li, 2013, Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize, BMC Plant Biol., 13, 1, 10.1186/1471-2229-13-114 Li, X., Li, Y., Lj–Wang, L.L., 2021. Effect of endophyte inoculation on the accumulation of mineral elements and organic acids in rice (Oryza sativa L.) under osmotic stress. Appl. Ecol. Environ. Res. 19, 763–775. Ludwig, 2019, Genetic biofortification to enrich rice and wheat grain iron: from genes to product, Front. Plant Sci., 10, 833, 10.3389/fpls.2019.00833 Michal Johnson, 2011, Protocols for Arabidopsis thaliana and Piriformospora indica co-cultivation–A model system to study plant beneficial traits, Endocytobiosis Cell Res., 21, 101 Nguyen, 2019, The effects of soil phosphorus and zinc availability on plant responses to mycorrhizal fungi: a physiological and molecular assessment, Sci. Rep., 9, 1, 10.1038/s41598-019-51369-5 Oelmüller, R., Shrivastava, N., Pohani, M., Upadhyaya, K.C., Sherameti, I., Murugan, P., Singh, S., Varma, A., 2011. In: Witzany, G (Ed.), Microbe–microbe, microbe–plant biocommunication. Biocommunication in soil microorganisms. Springer, Berlin, Heidelberg, pp. 439–464. Padash, 2016, A practicable method for zinc enrichment in lettuce leaves by the endophyte fungus Piriformospora indica under increasing zinc supply, Sci. Hortic., 213, 367, 10.1016/j.scienta.2016.10.040 Pedas, 2009, Identification and characterization of zinc-starvation-induced ZIP transporters from barley roots, Plant Physiol. Biochem., 47, 377, 10.1016/j.plaphy.2009.01.006 Shi, 2020, Success to iron biofortification of wheat grain by combining both plant and microbial genetics, Rhizosphere, 15, 10.1016/j.rhisph.2020.100218 Shrivastava, 2018, Proteomic approach to understand the molecular physiology of symbiotic interaction between Piriformospora indica and Brassica napus, Sci. Rep., 8, 1, 10.1038/s41598-018-23994-z Shrivastava, 2019, Mutualistic interaction of Piriformospora indica (Serendipita indica) with Aloe vera, the wonder plant for modern living, Am. J. Plant Sci., 10, 2002, 10.4236/ajps.2019.1011140 Singh, 2005, Improving zinc efficiency of cereals under zinc deficiency, Curr. Sci., 88, 36 Singh, 2018, Deciphering the mechanisms of endophyte-mediated biofortification of Fe and Zn in wheat, J. Plant Growth Regul., 37, 174, 10.1007/s00344-017-9716-4 Singh, S., Sakshi, Annapurna, K., Shrivastava, N., Varma, A., 2022. Symbiotic interplay of Piriformospora indica and Azotobacter chroococcum augments crop productivity and biofortification of zinc and iron. Microbiol. Res. 127075. Sirrenberg, 2007, Piriformospora indica affects plant growth by auxin production, Physiol. Plant., 131, 581, 10.1111/j.1399-3054.2007.00983.x Stephens, 2011, Characterization of zinc transport by divalent metal transporters of the ZIP family from the model legume Medicago truncatula, Biometals, 24, 51, 10.1007/s10534-010-9373-6 Su, 2017, Piriformospora indica promotes growth, seed yield and quality of Brassica napus L, Microbiol. Res., 199, 9, 10.1016/j.micres.2017.02.006 Sultana, 2016, Successful colonization of roots and plant growth promotion of sorghum (Sorghum bicolor L.) by seed treatment with Pseudomonas putida and Azotobacter chroococcum, World J. Microbiol., 3, 043 Van Hees, 2005, Organic acid concentrations in soil solution: effects of young coniferous trees and ectomycorrhizal fungi, Soil Biol. Biochem., 37, 771, 10.1016/j.soilbio.2004.10.009 Van Schöll, 2006, Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to nutrient deficiencies, New Phytol., 170, 153, 10.1111/j.1469-8137.2006.01649.x Verbon, 2016, Beneficial microbes affect endogenous mechanisms controlling root development, Trends Plant Sci., 21, 218, 10.1016/j.tplants.2016.01.013 Verma, 2021, Functional characterization of a high-affinity iron transporter (PiFTR) from the endophytic fungus Piriformospora indica and its role in plant growth and development, Environ. Microbiol., 24, 689, 10.1111/1462-2920.15659 Watts-Williams, 2017, The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression, Plant Soil, 420, 375, 10.1007/s11104-017-3409-4 Watts-Williams, 2018, Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar, Plant Sci., 274, 163, 10.1016/j.plantsci.2018.05.015 Wang, 2019, Effect of arbuscular mycorrhizal fungi on rhizosphere organic acid content and microbial activity of trifoliate orange under different low P conditions, Arch. Agron. Soil Sci., 65, 2029, 10.1080/03650340.2019.1590555 Xu, 2018, Role of phytohormones in Piriformospora indica-induced growth promotion and stress tolerance in plants: more questions than answers, Front. Microbiol., 9, 1646, 10.3389/fmicb.2018.01646 Yao, 2009, Effect of arbuscular mycorrhizal fungal inoculation on root system architecture of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings, Sci. Hortic., 121, 458, 10.1016/j.scienta.2009.03.013