Zinc solubilizing Bacillus strains that modulate growth, yield and zinc biofortification of soybean and wheat

Aghili, 2014, Green manure addition to soil increases grain zinc concentration in bread wheat, PLoS One, 9, e101487, 10.1371/journal.pone.0101487 Aslim, 2002, Determination of some properties of Bacillus isolated from soils, Turk J. Biol., 26, 41 Baruah, 1999 Bashan, 2013, Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure, Biol. Fertil. Soils, 49, 465, 10.1007/s00374-012-0737-7 Bavykin, 2004, Use of 16S rRNA, 23S rRNA, and gyrB gene sequence analysis to determine phylogenetic relationships of Bacillus cereus group microorganisms, J. Clin. Microbiol., 42, 3711, 10.1128/JCM.42.8.3711-3730.2004 Bazzicalupo, 1994, The use of RAPD for generating specific DNA probes for microorganisms, 50, 155 Beckett, 1989, The use of extractants in studies on trace metals in soils, sewage sludges and sludge treated soils, Adv. Soil Sci., 9, 144 Behera, 2011, Distribution variability of total and extractable zinc in cultivated acid soils of India and their relationship with some selected soil properties, Geoderma, 162, 242, 10.1016/j.geoderma.2011.01.016 Bhandari, 2013, Molecular signatures for Bacillus species: demarcation of the Bacillus cereus clades in molecular terms and proposal to limit the placement of new species in to the genus Bacillus, Int. J. Syst. Evol. Microbiol., 63, 2712, 10.1099/ijs.0.048488-0 Cakmak, 2008, Enrichment of cereal grains with zinc: agronomic or genetic biofortification?, Plant Soil, 302, 1, 10.1007/s11104-007-9466-3 Chowdhury, 2015, Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42- a review, Front. Microbiol., 6, 780, 10.3389/fmicb.2015.00780 ChunJuan, 2015, Enhancement of tomato (Lycopersicon esculentum) tolerance to drought stress by plant-growth-promoting rhizobacterium (PGPR) Bacillus cereus AR156, J. Agr. Biotechnol., 20, 1097 Di Simine, 1998, Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from forest soil, Biol. Fertil. Soils, 28, 87, 10.1007/s003740050467 Dimkpa, 2016, Fortification of micronutrients for efficient agronomic production: a review, Agron. Sustain. Dev., 36, 1, 10.1007/s13593-015-0346-6 Dimkpa, 2017, Composite micronutrient nanoparticles and salts decrease drought stress in soybean, Agron. Sustain. Dev., 37, 5, 10.1007/s13593-016-0412-8 Fasim, 2002, Solubilization of zinc salts by bacterium isolated by the air environment of tannery, FEMS Microbiol. Lett., 213, 1, 10.1111/j.1574-6968.2002.tb11277.x Felsenstein, 1985, Confidence limits on phylogenies: an approach using the bootstrap, Evolution, 39, 783, 10.1111/j.1558-5646.1985.tb00420.x Franz, 1991, Leaching with Penicillium simplicimum: Influence on metals and buffers on proton extrusion and citric acid production, Appl. Environ. Microbiol., 57, 769, 10.1128/AEM.57.3.769-774.1991 Gandhi, 2016, Assessment of zinc solubilizing potentiality of Acinetobacter sp. isolated from rice rhizosphere, Eur. J. Soil Biol., 76, 1, 10.1016/j.ejsobi.2016.06.006 Garcia, 2007 Gontia-Mishra, 2017, Zinc solubilizing bacteria from rhizosphere of rice as prospective modulator of zinc biofortification in rice, Rhizosphere, 3, 185, 10.1016/j.rhisph.2017.04.013 Goteti, 2013, Prospective zinc solubilizing bacteria for enhanced nutrient uptake and growth promotion in maize (Zea mays L.) rhizosphere, Int. J. Microbiol., 10.1155/2013/869697 Hafeez, 2013, Role of zinc in plant nutrition- a review, Am. J. Exp. Agric., 3, 374 Han, 2011, Zinc fractions and availability to soybeans in representative soils of Northeast China, J. Soils Sediments, 11, 596, 10.1007/s11368-011-0336-5 He, 2010, Effect of Zn-tolerant bacterial strains on growth and Zn accumulation in Orychophragmus violaceus, Appl. Soil Ecol., 44, 1, 10.1016/j.apsoil.2009.07.003 Helfenstein, 2016, Organic wheat farming improves grain zinc concentration, PLoS One, 11, 1, 10.1371/journal.pone.0160729 Jorquera, 2008, Isolation of culturable phosphobacteria with both phytate-mineralization and phosphate-solubilization activity from the rhizosphere of plants grown in a volcanic soil, Biol. Fertil. Soils, 44, 1025, 10.1007/s00374-008-0288-0 Joy, 2015, Zinc-enriched fertilizers as a potential public health intervention in Africa, Plant Soil, 389, 1, 10.1007/s11104-015-2430-8 Krithika, 2016, Expression of zinc transporter genes in rice as influenced by zinc solubilizing Enterobacter cloacae strain ZSB14, Front. Plant Sci., 7, 446, 10.3389/fpls.2016.00446 Kimura, 1980, A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences, J. Mol. Evol., 16, 111, 10.1007/BF01731581 Lindsay, 1978, Development of a DTPA soil test for zinc, iron, manganese and copper, Soil Sci. Soc. Am. J., 42, 421, 10.2136/sssaj1978.03615995004200030009x Logan, 2009, Bacillus, 21 Mäder, 2007, Wheat quality in organic and conventional farming: results of a 21 year field experiment, J. Sci. Food Agric., 87, 1826, 10.1002/jsfa.2866 Mäder, 2010, Inoculation of root microorganisms for sustainable wheat-rice and wheat-blackgram rotations in India, Soil Biol. Biochem., 43, 609, 10.1016/j.soilbio.2010.11.031 Mumtaz, 2017, Zinc solubilizing Bacillus spp potential candidates for biofortification of maize, Microbiol. Res., 202, 51, 10.1016/j.micres.2017.06.001 Nguyen, 1992, Genetic variability of phosphate solubilization activity by monocaryotic and diacaryotic mycelia of the ectomycorrhizal fungus Laccaria bicolor (Marie) PD Orton, Plant Soil, 143, 193, 10.1007/BF00007873 Oburger, 2009, Interactive effects of organic acids in the rhizosphere, Soil Biol. Biochem., 41, 449, 10.1016/j.soilbio.2008.10.034 Pérez-García, 2011, Plant protection and growth stimulation by microorganisms: biotechnological applications of bacilli in agriculture, Curr. Opin. Biotechnol., 22, 187, 10.1016/j.copbio.2010.12.003 Poblaciones, 2016, Soil and foliar zinc biofortification in field pea (Pisum sativum L.): Grain accumulation and bioavailability in raw and cooked grains, Food Chem., 212, 427, 10.1016/j.foodchem.2016.05.189 Prasad, 2010, Zinc biofortification of food grains in relation to food security and alleviation of zinc malnutrition, Curr. Sci., 98, 1300 Prasad, 2013, Zinc fertilization of cereals for increased production and alleviation of zinc malnutrition in India, Agric. Res., 2, 111, 10.1007/s40003-013-0064-8 Raliya, 2016, Enhancing the mobilization of native phosphorus in the mung bean rhizosphere using ZnO nanoparticles synthesized by soil fungi, J. Agric. Food Chem., 64, 3111, 10.1021/acs.jafc.5b05224 Ramesh, 2011, Phytase activity and P-nutrition of soybean as influenced by inoculation of Bacillus, Indian J. Microbiol., 51, 94, 10.1007/s12088-011-0104-7 Ramesh, 2014, Plant growth-promoting traits in Enterobacter cloacae subsp. dissolvens MDSR9 isolated from soybean rhizosphere and its impact on growth and nutrition of soybean and wheat upon inoculation, Agric. Res., 3, 53, 10.1007/s40003-014-0100-3 Ramesh, 2014, Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization, and biofortification of zinc in soybean and wheat cultivated in vertisols of Central India, Appl. Soil Ecol., 73, 87, 10.1016/j.apsoil.2013.08.009 Ramirez, 2010, Plant growth promotion by Bacillus amyloliquefaciens FZB45 depends on inoculums rate and P-related soil properties, Biol. Fertil. Soils, 46, 835, 10.1007/s00374-010-0488-2 Rana, 2012, Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria, Eur. J. Soil Biol., 50, 118, 10.1016/j.ejsobi.2012.01.005 Reddy, 2008, Bacillus cecembensis sp. nov., isolated from the Pindari glacier of the Indian Himalayas, Int. J. Syst. Evol. Microbiol., 58, 2330, 10.1099/ijs.0.65515-0 Rengel, 1996, Uptake of zinc from chelate buffered nutrient solution by wheat genotypes differing in Zn efficiency, J. Exp. Bot., 47, 217, 10.1093/jxb/47.2.217 Roesti, 2006, Plant growth stage, fertilizer management and bioinoculant of arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria affect the rhizobacterial community structure in rain-fed wheat fields, Soil Biol. Biochem., 38, 1111, 10.1016/j.soilbio.2005.09.010 Saitou, 1987, The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 4, 406 Saravanan, 2003, Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates, Brazil J. Microbiol., 34, 121 Saravanan, 2007, Solubilization of zinc compounds by the diaztrophic, plant growth-promoting bacterium Gluconacetobacter diazotrophicus, Chemosphere, 66, 1794, 10.1016/j.chemosphere.2006.07.067 Saravanan, 2007, Solubilization of insoluble zinc compounds by Gluconacetobacter diazotrophicus and the detrimental action of zinc ion (Zn+2) and zinc chelates on root knot nematode Meloidogyne incognita, Lett. Appl. Microbiol., 44, 235, 10.1111/j.1472-765X.2006.02079.x Sasser, M., 1990. Tracking a strain using the microbial identification system. Technical Note 102, MIS, Newark, DE. Sasser, 1991, Identification of microorganisms through use of gas chromatography and high-performance liquid chromatography, 111 Schmidt, 2011, Whole-genome phylogenies of the family Bacillaceae and expansion of the sigma factor gene family in the Bacillus cereus species-group, BMC Genomics, 12, 430, 10.1186/1471-2164-12-430 Senthil Kumar, 2004, Effect of Zn-enriched manure and zinc solubilizer application on yield, curcumin content and nutrient status of soil under turmeric cultivation, J. Appl. Hort., 6, 82 Shaikh, 2016, Biofortification of Triticum aestivum through the inoculation of zinc solubilizing plant growth promoting rhizobacteria in field experiment, Biocatal. Agric. Biotechnol., 9, 120, 10.1016/j.bcab.2016.12.008 Shakeel, 2015, Root associated Bacillus sp. improves growth, yield and zinc translocation for basmati rice (Oryza sativa) varieties, Front. Microbiol., 6, 1286, 10.3389/fmicb.2015.01286 Sharma, 2011, Microbial community structure and diversity as indicators for evaluating soil quality, 317 Sharma, 2012, Characterization of zinc-solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds, J. Microbiol. Biotechnol., 22, 352, 10.4014/jmb.1106.05063 Shivaji, 2009, Janibacter hoylei sp.nov., Bacillus isronensis sp.nov., and Bacillus aryabhattai sp. nov., isolated from cryotubes used for collecting air from the upper atmosphere, Int. J. Syst. Evol. Microbiol., 59, 2977, 10.1099/ijs.0.002527-0 Singh, 2005, Improving zinc efficiency of cereals under deficiency, Curr. Sci., 88, 36 Singh, 2017, Beneficial role of endophytes in biofortification of Zn in wheat genotypes varying in nutrient use efficiency grown in soils sufficient and deficient in Zn, Plant Soil, 416, 107, 10.1007/s11104-017-3189-x Singh, 2017, Deciphering the mechanisms of endophytic-mediated biofortification of Fe and Zn in wheat, J. Plant Growth Regul. Subramanian, 2013, Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival, Immunity, 39, 697, 10.1016/j.immuni.2013.09.006 Sunithakumari, 2016, Zinc solubilizing bacterial isolates from the agricultural field of Coimbatore, Tamil Nadu, India, Curr. Sci., 110, 196, 10.18520/cs/v110/i2/196-205 Suresh, 2011, Characterization and phylogenetic diversity of carboxymethylcellulase producing Bacillus species from a landfill ecosystem, Int. J. Microbiol., 51, 531 Tamura, 2011, MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods, Mol. Biol. Evol., 28, 2731, 10.1093/molbev/msr121 Ullah, 2015, Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review, Environ. Exp. Bot., 117, 28, 10.1016/j.envexpbot.2015.05.001 Wang, 2015, Effects of increasing rates of zinc fertilization on phytic acid and phytic acid/zinc molar ratio in zinc bio-fortified wheat, Field Crops Res., 184, 58, 10.1016/j.fcr.2015.09.007 Wani, 2007, Chromium reduction, plant growth-promoting potentials and metal solubilization by Bacillus sp. isolated from alluvial soil, Curr. Microbiol., 54, 237, 10.1007/s00284-006-0451-5 White, 2009, Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine, New Phytol., 182, 49, 10.1111/j.1469-8137.2008.02738.x White, 2011, Physiological limits to zinc biofortification of edible crops, Front. Plant Sci., 80, 1 Yu, 2011, Isolation and characterization of phosphate-solubilizing bacteria from walnut and their effect on growth and phosphorus mobilization, Biol. Fertil. Soils, 47, 437, 10.1007/s00374-011-0548-2 Zhang, 2012, Zinc biofortification of wheat through fertilizer applications in different locations of China, Field Crops Res., 125, 1, 10.1016/j.fcr.2011.08.003 Zhou, 2008, The occurrence of Bacillus cereus, B. thuringiensis and B. mycoides in Chinese pasteurized full fat milk, Int. J. Food Microbiol., 121, 195, 10.1016/j.ijfoodmicro.2007.11.028 Zwick, 2012, Genomic characterization of the Bacillus cereus sensu lato species: Backdrop to the evolution of Bacillus anthracis, Genome Res., 22, 1512, 10.1101/gr.134437.111