Mineral nutrition of crop plants is one of the major challenges faced by modern agriculture, particularly in arid and semi-arid regions. In alkaline calcareous soils, the availability of phosphorus and zinc is critically less due to their fixation and precipitation as complexes. Farmers use fertilizers to fulfill crop requirements, but their efficacy is less, which increases production costs. Plant growth-promoting rhizobacteria (PGPR) can improve the availability of crop nutrients through solubilizing the insoluble compounds of phosphorus and zinc in soil. In the present study, a total of 40 rhizobacterial isolates were isolated from cotton rhizosphere and screened for improving cotton growth through the solubilization of phosphorus and zinc. Out of these 40 isolates, seven isolates (IA2, IA3, IA6, IA7, IA8, IA13, and IA14) efficiently solubilized insoluble rock phosphate while seven isolates (IA10, IA16, IA20, IA23, IA24, IA28, and IA30) were more efficient in solubilizing insoluble zinc oxide. In liquid media, strain IA7 (2.75 μg/mL) solubilized the highest amount of phosphate while the highest concentration of soluble zinc was observed in the broth inoculated with strain IA20 (3.94 μg/mL). Seven phosphate-solubilizing and seven zinc-solubilizing strains were evaluated using jar trial to improve the growth of cotton seedlings, and the results were quite promising. All the inoculated treatments showed improvement in growth parameters in comparison with control. Best results were shown by the combined application of IA6 and IA16, followed by the combination of strains IA7 and IA20. Based on the jar trial, the selected isolates were further characterized by plant growth-promoting characters such as siderophores production, HCN production, ammonia production, and exopolysaccharides production. These strains were identified through 16S rRNA sequencing as Bacillus subtilis IA6 (accession # MN005922), Paenibacillus polymyxa IA7 (accession # MN005923), Bacillus sp. IA16 (accession # MN005924), and Bacillus aryabhattai IA20 (accession # MN005925). It is hence concluded that the integrated use of phosphate-solubilizing and zinc-solubilizing strains as potential inoculants can be a promising approach for improving cotton growth under semi-arid conditions.

Department of Soil Science University College of Agriculture and Environmental Sciences Islamia University of Bahawalpur Bahawalpur Pakistan

Zobrazit více v PubMed

Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001 DOI

Ahmad M, Ahmad I, Hilger TH, Nadeem SM, Akhtar MF, Jamil M, Hussain A, Zahir ZA (2018) Preliminary study on phosphate solubilizing Bacillus subtilis strain Q3 and Paenibacillus sp. strain Q6 for improving cotton growth under alkaline conditions. Peer J:2–22. https://doi.org/10.7717/peerj.5122

Ansari FA, Ahmad I (2019) Fluorescent pseudomonas-FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci Rep 9:1–12. https://doi.org/10.1038/s41598-019-40864-4 DOI

Atlas RM (1946) Handbook of microbiological media, 4th edn. CRC Press Taylor and Francis Group, Boca Raton

Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051. https://doi.org/10.1590/s1415-47572012000600020 PubMed DOI PMC

Bunt JS, Rovira AD (1955) Microbiological studies of some subantartic soils. J Soil Sci 6:119–128. https://doi.org/10.1111/j.1365-2389.1955.tb00836.x DOI

Cappuccino JC, Sherman N (1992) Negative staining. In: Cappuccino JC, Sherman N (eds) Microbiology: a laboratory manual. Benjamin/Cummings, Redwood City, pp 125–179

Chauhan AK, Maheshwari DK, Kim K, Bajpai VK (2016) Termitarium-inhabiting Bacillus endophyticus TSH42 and Bacillus cereus TSH77 colonizing Curcuma longa L.: isolation, characterization, and evaluation of their biocontrol and plant-growth-promoting activities. Can J Microbiol 62:880–892. https://doi.org/10.1139/cjm-2016-0249 PubMed DOI

Chernin LS, Winson MK, Thompson JM, Haran S, Bycroft BW, Chet I, Williams P, Stewart GSAB (1998) Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J Bacteriol 180:4435–4441. https://doi.org/10.1128/jb.180.17.4435-4441.1998 PubMed DOI PMC

Clescerie LS, Greenberg AE, Eaton AD (1998) Standard methods for examination of water and wastewater. 20th edn. APHA-AWWA-WEF, Washington, D.C., p 1325

Daniels C, Michan C, Ramos JL (2009) New molecular tools for enhancing methane production, explaining thermodynamically limited lifestyles and other important biotechnological issues. Microb Biotechnol 2:533–536. https://doi.org/10.1111/j.1751-7915.2009.00134.x PubMed DOI PMC

Dinesh R, Srinivasan V, Hamza S, Sarathambal C, Gowda SJA, Ganeshamurthy AN, Gupta SB, Nair VA, Subila KP, Lijina A, Divya VC (2018) Isolation and characterization of potential Zn solubilizing bacteria from soil and its effects on soil Zn release rates, soil available Zn and plant Zn content. Geoderma 321:173–186. https://doi.org/10.1016/j.geoderma.2018.02.013 DOI

Dworkin M, Foster J (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603. https://doi.org/10.1128/jb.75.5.592-603.1958 PubMed DOI PMC

Gopalakrishnan S, Humayun PBK, Kiran IGK, Kannan MS, Vidya K, Deepthi RO (2011) Evaluation of bacteria isolated from rice rhizosphere for biological control of charcoal rot of sorghum caused by Macrophomina phaseolina (Tassi) Goid. World J Microbiol Biotechnol 27:1313–1321. https://doi.org/10.1007/s11274-010-0579-0 PubMed DOI

Gouda S, Kerry RG, Das G, Paramithiotis S, Shin SH, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140. https://doi.org/10.1016/j.micres.2017.08.016 PubMed DOI

Habib SH, Kausar H, Saud HM, Ismail MR, Othman R (2016) Molecular characterization of stress tolerant plant growth promoting rhizobacteria (PGPR) for growth enhancement of rice. Int J Agric Biol 18:1560–8530. https://doi.org/10.17957/IJAB/15.0094 DOI

Hafeez B, Khanif YM, Saleem M (2013) Role of zinc in plant nutrition-a review. Am J Exp Agric 3:374–391. https://doi.org/10.9734/AJEA/2013/2746 DOI

Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Circ Calif Agric Exp Station 347:32

Holt JC, Krieg NR, Sneath PHA, Stanley JY, Williams ST (1994) Subgroup 2: Family vibrionaceae. Bergey’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, Baltimore, pp 190–274

Hussain S, Devers-Lamrani M, El-Azhari N, Martin-Laurent F (2011) Isolation and characterization of an isoproturon mineralizing Sphingomonas sp. strain SH from a French agricultural soil. Biodegradation 22:637–650. https://doi.org/10.1007/s10532-010-9437-x PubMed DOI

Hussain A, Arshad M, Zahir ZA, Asghar M (2015) Prospects of zinc solubilizing bacteria for enhancing growth of maize. Pak J Agric Sci 52:915–922 http://www.pakjas.com.pk/

Iqbal S, Khan MY, Asghar HN, Akhtar MJ (2016) Combined use of phosphate solubilizing bacteria and poultry manure to enhance the growth and yield of mung bean in calcareous soil. Soil Environ 35:146–154 http://www.sss-pakistan.or

Islam M, Sultana T, Joe MM, Yim W, Cho JC, Sa T (2013) Nitrogen-fixing bacteria with multiple plant growth promoting activities enhances growth of tomato and red pepper. J Basic Microbiol 53:1004–1015. https://doi.org/10.1002/jobm.201200141 PubMed DOI

Kafle A, Cope KR, Raths R, Yakha JK, Subramanian S, Bücking H, Garcia K (2019) Harnessing soil microbes to improve plant phosphate efficiency in cropping systems. Review. Agronomy 9:2–15. https://doi.org/10.3390/agronomy9030127 DOI

Kloepper JW, Okon Y (1994) Plant growth-promoting rhizobacteria (other systems). In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, pp 111–118

Korir H, Mungai NW, Thuita M, Hamba Y, Masso C (2017) Co inoculation effect of rhizobia and plant growth promoting rhizobacteria on common bean growth in a low phosphorus soil. Front. Plant Sci 141:1–10. https://doi.org/10.3389/fpls.2017.00141 DOI

Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054 DOI

Li Y, Liu X, Hao T, Chen S (2017) Colonization and maize growth promotion induced by phosphate solubilizing bacterial isolates. Int J Mol Sci 18:1253. https://doi.org/10.3390/ijms18071253 PubMed DOI PMC

MacFaddin JF (1980) Biochemical tests for identification of medical bacteria, 2nd edn. Williams and Wilkins, Baltimore, pp 51–54

Maheshwari DK, Dheeman S, Agarwal M (2015) Phytohormone-producing PGPR for sustainable agriculture. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer, Cham, pp 159–182 DOI

Mendez J (2014) Characterization of phosphate-solubilizing bacteria isolated from the arid soils of a semi-desert region of north-east Mexico. Biol Agric Hortic 30:211–217. https://doi.org/10.1080/01448765.2014.909742 DOI

Miller SH, Browne P, Prigent-Cambaret C, Combes-Meynet E, Morrissey JP, Gara OF (2010) Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ Microbiol Rep 2:403–411. https://doi.org/10.1111/j.1758-2229.2009.00105.x PubMed DOI

Mumtaz MZ, Ahmad M, Jamila M, Hussain T (2017) Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiol Res 202:51–60. https://doi.org/10.1016/j.micres.2017.06.001 PubMed DOI

Mumtaz MZ, Barry KM, Baker AL, Nichols DS, Ahmad M, Zahir ZA, Britz ML (2019) Production of lactic and acetic acids by Bacillus sp. ZM20 and Bacillus cereus following exposure to zinc oxide: a possible mechanism for Zn solubilization. Rhizosphere 12:00170. https://doi.org/10.1016/j.rhisph.2019.100170 DOI

Nadeem S, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448. https://doi.org/10.1016/j.biotechadv.2013.12.005 PubMed DOI

Naseem H, Ahsan M, Shahid MA, Khan N (2018) Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J Basic Microbiol 58:1009–1022. https://doi.org/10.1002/jobm.201800309 PubMed DOI

Nehra V, Choudhary M (2015) A review on plant growth promoting rhizobacteria acting as bioinoculants and their biological approach towards the production of sustainable agriculture. JANS 7:540–556. https://doi.org/10.31018/jans.v7i1.642 DOI

Noulas C, Tziouvalekas M, Karyotis T (2018) Zinc in soils, water and food crops. J Trace Elem Med Biol 49:252–260. https://doi.org/10.1016/j.jtemb.2018.02.009 PubMed DOI

Pikovskaya RI (1948) Mobilization of phosphorous in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370

Prasad AA, Babu S (2017) Compatibility of Azospirillum brasilense and Pseudomonas fluorescens in growth promotion of groundnut (Arachis hypogea L.). An Acad Bras Cienc 89:1027–1040. https://doi.org/10.1590/0001-3765201720160617 PubMed DOI

Radhakrishnan R, Hashem A, Abd-Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667. https://doi.org/10.3389/fphys.2017.00667 PubMed DOI PMC

Rafique M, Sultan T, Ortas I, Chaudhary HJ (2017) Enhancement of maize plant growth with inoculation of phosphate-solubilizing bacteria and biochar amendment in soil. J Soil Sci Plant Nutr 63:460–469. https://doi.org/10.1080/00380768.2017.1373599 DOI

Ramadan EM, Abdel-Hafez AA, Hassan EA, Saber FM (2016) Plant growth promoting rhizobacteria and their potential for biocontrol of phytopathogens. Afr J Microbiol Res 10:486–504. https://doi.org/10.5897/AJMR2015.7714 DOI

Rasul M, Yasmin S, Suleman S, Zaheer A, Reitz T, Tarkka MT, Islam E, Mirza MS (2019) Glucose dehydrogenase gene containing phosphobacteria for biofortification of phosphorus with growth promotion of rice. Microbiol Res 223–225:1–12. https://doi.org/10.1016/j.micres.2019.03.004 PubMed DOI

Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 1:1–30 https://astonjournals.com/lsmr

Saitou N, Nei M (1987) The neighbor-joining method: a new method for recon- structing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454 PubMed DOI PMC

Saravanan SV, Sudalayandy RS, Savariappan (2003) Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates. Braz J Microbiol 34:121–125. https://doi.org/10.1590/S1517-83822004000100020 DOI

Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2:587. https://doi.org/10.1186/2193-1801-2-587 PubMed DOI PMC

Sheirdil RA, Hayat R, Zhang X-X, Abbasi NA, Ali S, Ahmed M, Khattak JZK, Ahmad S (2019) Exploring potential soil bacteria for sustainable wheat (Triticum aestivum L.) production. Sustainability 11:3361. https://doi.org/10.3390/su11123361 DOI

Shen X, Hu H, Peng H, Wang W, Zhang X (2013) Comparative genomic analysis of four representative plant growth-promoting rhizobacteria in Pseudomonas. BMC Genomics 14:271. https://doi.org/10.1186/1471-2164-14-271 PubMed DOI PMC

Shruti K, Arun K, Yuvneet R (2013) Potential plant growth-promoting activity of rhizobacteria Pseudomonas sp. in Oryza sativa. J Nat Prod Plant Resour 3:38–50 https://www.scholarsresearchlibrary.com/

Steel RGD, Torrie JH, Dicky DA (1997) Principles and procedures of statistics a biometrical approach, 3rd edn. McGraw Hill Book International Co, Singapore, pp 204–227

Suman B, Gopal AV, Reddy RS, Triveni S (2018) Cultural and morphological characterization of native Pseudomonas fluorescens isolates from Telangana. Int J Pure App Biosci 6:592–597. https://doi.org/10.18782/2320-7051.6910 DOI

Tallgren AH, Airaksinen U, Von Weissenberg R, Ojamo H, Kuusisto J, Leisola M (1999) Exopolysaccharide producing bacteria from sugar beets. Appl Environ Microbiol 65:862–864. https://doi.org/10.1128/aem.65.2.862-864.1999 PubMed DOI PMC

Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035. https://doi.org/10.1073/pnas.0404206101 PubMed DOI PMC

Tsegaye Z, Assefa F, Tefera G, Alemu T, Gizaw B (2018) Characterization and identification of Tef (Eragrostis tef) seed endophytic bacterial species and evaluate their effect on plant growth promotion. J Plant Pathol Microbiol 9:438–446. https://doi.org/10.4172/2157-7471.1000438 DOI

Tsegaye Z, Gizaw B, Tefera G, Feleke A, Chaniyalew S, Alemu T, Assefa F (2019) Isolation and biochemical characterization of plant growth promoting (PGP) bacteria colonizing the rhizosphere of Tef crop during the seedling stage. Biomed J Sci Tech Res 14:10586–10596. https://doi.org/10.26717/BJSTR.2019.14.002534 DOI

Vazquez P, Holguin G, Puente ME, Lopez-Cortes A, Bashan Y (2000) Phosphate solubilizing microorganisms associated with the rhizosphere of mangroves growing in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468. https://doi.org/10.1007/s003740050024 DOI

Vincent JM (1970) A manual for the practical study of root-nodule bacteria. Blackwell Scientific, Oxford

Xi-wen Y, Xiao-hong T, Xin-chun L, William G, Yu-xian C (2013) Foliar zinc fertilization improves the zinc nutritional value of wheat (Triticumaestivum L.) grain. Afr J Biotechnol 10:14778–14785. https://doi.org/10.5897/AJB11.780 DOI

Zaheer A, Malik A, Sher A, Qaisrani MM, Mehmood A, Khan SU, Ashraf M, Mirza Z, Karim S, Rasool M (2019) Isolation, characterization, and effect of phosphate-zinc-solubilizing bacterial strains on chickpea (Cicer arietinum L.) growth. Saudi J Biol Sci 26:1061–1067. https://doi.org/10.1016/j.sjbs.2019.04.004 PubMed DOI PMC

Stimulation of Arabidopsis thaliana Seed Germination at Suboptimal Temperatures through Biopriming with Biofilm-Forming PGPR Pseudomonas putida KT2440

Insights Into Manganese Solubilizing Bacillus spp. for Improving Plant Growth and Manganese Uptake in Maize