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Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future

  • Abhinav Aeron
  • Ekta Khare
  • Chaitanya Kumar Jha
  • Vijay Singh MeenaEmail author
  • Shadia Mohammed Abdel Aziz
  • Mohammed Tofazzal Islam
  • Kangmin Kim
  • Sunita Kumari Meena
  • Arunava Pattanayak
  • Hosahatti Rajashekara
  • Ramesh Chandra Dubey
  • Bihari Ram Maurya
  • Dinesh Kumar Maheshwari
  • Meenu Saraf
  • Mahipal Choudhary
  • Rajhans Verma
  • H. N. Meena
  • A. R. N. S. Subbanna
  • Manoj Parihar
  • Shruti Shukla
  • Govarthanan Muthusamy
  • Ram Swaroop Bana
  • Vivek K. BajpaiEmail author
  • Young-Kyu HanEmail author
  • Mahfuzur Rahman
  • Dileep Kumar
  • Norang Pal Singh
  • Rajesh Kumar Meena
Mini-Review
  • 90 Downloads

Abstract

Plant beneficial rhizobacteria (PBR) is a group of naturally occurring rhizospheric microbes that enhance nutrient availability and induce biotic and abiotic stress tolerance through a wide array of mechanisms to enhance agricultural sustainability. Application of PBR has the potential to reduce worldwide requirement of agricultural chemicals and improve agro-ecological sustainability. The PBR exert their beneficial effects in three major ways; (1) fix atmospheric nitrogen and synthesize specific compounds to promote plant growth, (2) solubilize essential mineral nutrients in soils for plant uptake, and (3) produce antimicrobial substances and induce systemic resistance in host plants to protect them from biotic and abiotic stresses. Application of PBR as suitable inoculants appears to be a viable alternative technology to synthetic fertilizers and pesticides. Furthermore, PBR enhance nutrient and water use efficiency, influence dynamics of mineral recycling, and tolerance of plants to other environmental stresses by improving health of soils. This report provides comprehensive reviews and discusses beneficial effects of PBR on plant and soil health. Considering their multitude of functions to improve plant and soil health, we propose to call the plant growth-promoting bacteria (PGPR) as PBR.

Keywords

Plant-beneficial rhizobacteria (PBR) Agro-ecosystems Mineral solubilization Soil–plant–microbes interaction Microbial diversity 

Notes

Acknowledgements

AA and EK are thankful to National Research Foundation (NRF) of Korea. VSM, AP, HR, MC are thankful to Indian Council of Agricultural Research (ICAR), New Delhi India. DKM wishes to acknowledge UGC, UCOST and CSIR. MTI is thankful to the World Bank for funding this work through a Higher Education Quality Enhancement. DKM and AA conceived, outlined and wrote a part of the article. AA and SKM wrote the first draft of the manuscript and VSM designed figures, tabulation and finalizing the manuscript. All authors contributed equally to the work

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahkami AH, White RA III, Handakumbura PP, Jansson C (2017) Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3(2017):233–243CrossRefGoogle Scholar
  2. Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPRI. Mol Plant Microbe Interact 20:759–768PubMedCrossRefGoogle Scholar
  3. Alavi P, Starcher M, Zachow C, Müller H, Berg G (2013) Root-microbe systems: the effect and mode of interaction of Stress Protecting Agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front Plant Sci 4:141PubMedPubMedCentralCrossRefGoogle Scholar
  4. Anuradha N, Satyavathi CT, Bharadwaj C, Nepolean T, Sankar SM, Singh SP, Meena MC, Singhal T, Srivastava RK (2017) Deciphering genomic regions for high grain iron and zinc content using association mapping in pearl millet. Front Plant Sci 8:412PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aras S, Arıkan S, Ipek M, Esitken A, Pırlak L, Dönmez MF, Metin T (2018) Plant growth promoting rhizobacteria enhanced leaf organic acids, FCR activity and Fe nutrition of apple under lime soil conditions. Acta Physiol Plant 40:120.  https://doi.org/10.1007/s11738-018-2693-9 CrossRefGoogle Scholar
  6. Arif MS, Muhammad RIAZ, Shahzad SM, Yasmeen T, Shafaqat ALI, Akhtar MJ (2017) Phosphorus-mobilizing rhizobacterial strain Bacillus cereus GS6 improves symbiotic efficiency of soybean on an Aridisol amended with phosphorus-enriched compost. Pedosphere 27(6):1049–1061CrossRefGoogle Scholar
  7. Arıkan S, Esitken A, Ipek M, Aras S, Sahin M, Pırlak L, Dönmez MF, Metin T (2018) Effect of plant growth promoting rhizobacteria on Fe acquisition in peach (Prunus persica L.) under calcareous soil conditions. J Plant Nutr 41:2141–2150CrossRefGoogle Scholar
  8. Arnou DI (1953) Soil and fertilizer phosphorus in crop nutrition (IV). In: Pierre WH, Noramn AG (eds) Academic Press, New YorkGoogle Scholar
  9. Arora NK, Khare E, Oh JH, Kang SC, Maheshwari DK (2008) Diverse mechanisms adopted by fluorescent Pseudomonas PGC2 during the inhibition of Rhizoctonia solani and Phytophthora capsici. World J Microbiol Biotechnol 24(4):581–585CrossRefGoogle Scholar
  10. Asari S, Tarkowská D, Rolcík J, Novák O, Velázquez-Palmero D, Bejai S, Meijer J (2017) Analysis of plant growth-promoting properties of Bacillus amyloliquefaciens UCMB5113 using Arabidopsis thaliana as host plant. Planta 245:15–30PubMedCrossRefGoogle Scholar
  11. Badar R, Nisa Z, Ibrahim S (2015) Supplementation of P with rhizobial inoculants to improve growth of Peanut plants. Int J Appl Res 1:19–23Google Scholar
  12. Baltruschat H, Fodor J, Harrach BD, Niemczyk E, Barna B, Gullner G et al (2008) Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in anti-oxidants. New Phytol 180:501–510PubMedCrossRefGoogle Scholar
  13. Bhat MA (2019) Plant growth promoting rhizobacteria (PGPR) for sustainable and eco-friendly agriculture. Acta Sci Agric 3:23–25CrossRefGoogle Scholar
  14. Bhattacharyya P, Jha D (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350PubMedCrossRefGoogle Scholar
  15. Braud A, Jezequel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr-, Hg- and Pb-contaminated soil by bioaugmentation with siderophore producing bacteria. Chemosphere 74:280–286PubMedCrossRefGoogle Scholar
  16. Braun V, Hantke K (2013) The tricky ways bacteria cope with iron limitation. In: Chakraborty R (eds) Iron uptake in bacteria with emphasis on E. coli and Pseudomonas. Springer briefs in biometals. Springer, Berlin. https://doi.org/10.1007/978-94-007-6088-2_2 CrossRefGoogle Scholar
  17. Chang WT, Chen CS, Wang SL (2003) An antifungal chitinase produced by Bacillus cereus with shrimp and crab shell powder as carbon source. Curr Microbiol 47:102–108PubMedCrossRefGoogle Scholar
  18. Chen Y, Wang J, Yang N, Wen Z, Sun X, Chai Y, Ma Z (2018) Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation. Nat Commun 9:3429PubMedPubMedCentralCrossRefGoogle Scholar
  19. Disi JO, Mohammad HK, Lawrence K, Kloepper J, Fadamiro HA (2019) Soil bacterium can shape belowground interactions between maize, herbivores and entomopathogenic nematodes. Plant Soil 437:83–92CrossRefGoogle Scholar
  20. Doran J, Parkin T (1996) Defining and assessing soil quality. In: Doran JW, Coleman DC, Bezdicek DF, Stewart BA (eds) Defining soil quality for a sustainable environment. Soil Science Society of America, Madison, pp 3–21Google Scholar
  21. Egamberdieva, Dilfuza, Jaime A, Teixeira da Silva (2015) Medicinal plants and PGPR: a new frontier for phytochemicals. Plant-growth-promoting rhizobacteria (PGPR) and medicinal plants. Springer, Berlin, pp 287–303Google Scholar
  22. Esitken A, Pirlak L, Turan M, Sahin F (2006) Effects of floral and foliar application of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrition of sweet cherry. Sci Hortic 110:324–327CrossRefGoogle Scholar
  23. Fan X, Zhang S, Xiaodan MO, Yuncong LI, Yuqing FU, Zhiguang LIU (2017) Effects of plant growth-promoting rhizobacteria and N source on plant growth and N and P uptake by tomato grown on calcareous soils. Pedosphere 27(6):1027–1036CrossRefGoogle Scholar
  24. Ghazijahani N, Hadavi E, Jeong BR (2014) Foliar sprays of citric acid and salicylic acid alter the pattern of root acquisition of some minerals in sweet basil (Ocimum basilicum L.). Front Plant Sci 5:573PubMedPubMedCentralCrossRefGoogle Scholar
  25. Grady EN, MacDonald J, Liu L, Richman A, Yuan ZC (2016) Current knowledge and perspectives of Paenibacillus: a review. Microb Cell Fact 15:203.  https://doi.org/10.1186/s12934-016-0603-7 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Grover M, Nain L, Singh SB, Saxena AK (2010) Molecular and biochemical approaches for characterization of antifungal trait of a potent biocontrol agent Bacillus subtilis RP24. Curr Microbiol 60(2):99–106PubMedCrossRefGoogle Scholar
  27. Guo Q, Li Y, Lou Y, Shi M, Jiang Y, Zhou J, Sun Y, Xue Q, Lai H (2019) Bacillus amyloliquefaciens Ba13 induces plant systemic resistance and improves rhizosphere micro ecology against tomato yellow leaf curl virus disease. Appl Soil Ecol 137:154–166CrossRefGoogle Scholar
  28. Gupta V, Rovira A, Roger D (2011) Principles and management of soil biological factors for sustainable rainfed farming systems. In: Tow P, Cooper I, Partridge I, Birch C (eds) Rainfed farming systems. Springer, Dordrecht, pp 149–184CrossRefGoogle Scholar
  29. Habib SH, Kausar H, Saud H (2016) Plant growth promoting rhizobacteria enhance salinity stress tolerance in Okra through ROS-Scavenging enzymes. Biol Med Res Int 2016:1–10Google Scholar
  30. Haney CH, Wiesmann CL, Shapiro LR, Melnyk RA, O’Sullivan LR, Khorasani S, Xiao L, Han J, Bush J, Carrillo J (2018) Rhizosphere-associated Pseudomonas induce systemic resistance to herbivores at the cost of susceptibility to bacterial pathogens. Mol Ecol 27:1833–1847PubMedCrossRefGoogle Scholar
  31. Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 209:1–25CrossRefGoogle Scholar
  32. Hassan MK, McInroy JA, Jones J, Shantharaj D, Liles MR, Kloepper JW (2019a) Pectin-rich amendment enhances soybean growth promotion and nodulation mediated by Bacillus velezensis strains. Plants 8:120PubMedCentralCrossRefGoogle Scholar
  33. Hassan MK, McInroy JA, Kloepper JW (2019b) The interactions of rhizodeposits with plant growth-promoting rhizobacteria in the rhizosphere: a review. Agriculture 9(7):142.  https://doi.org/10.3390/agriculture9070142 CrossRefGoogle Scholar
  34. Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6(1):58PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598CrossRefGoogle Scholar
  36. Hossain MT, Khan A, Harun-Or-Rashid M, Chung YR (2019) A volatile producing endophytic Bacillus siamensis YC7012 promotes root development independent on auxin or ethylene/jasmonic acid pathway. Plant Soil 439:309–324CrossRefGoogle Scholar
  37. Islam F, Yasmeen T, Ali S, Ali B, Farooq MA, Gill RA (2015) Priming-induced antioxidative responses in two wheat cultivars under saline stress. Acta Physiol Plant 37(8):1–12CrossRefGoogle Scholar
  38. Islam MT (2008) Disruption of ultra-structure and cytoskeleton network is involved with biocontrol of damping-off pathogen Aphanomyces cochlioides by Lysobacter sp. SB-K88. Biol Control 46:312–321CrossRefGoogle Scholar
  39. Islam MT, Fukushi Y (2010) Growth inhibition and excessive branching in Aphanomyces cochlioides induced by 2,4-diacetylphloroglucinol is linked to disruption of filamentous actin cytoskeleton in the hyphae. World J Microbiol Biotechnol 26:1163–1170PubMedCrossRefPubMedCentralGoogle Scholar
  40. Islam MT, Hossain MM (2013) Biological control of peronosporomycete phytopathogen by bacterial antagonist. In: Maheshwari DK (ed) Bacteria in agrobiology: disease management. Springer, Heidelberg, pp 167–218CrossRefGoogle Scholar
  41. Jaiswal AK, Elad Y, Graber ER, Frenkel O (2014) Rhizoctonia solani suppression and plant growth promotion in cucumber as affected by biochar pyrolysis temperature, feedstock and concentration. Soil Biol Biochem 69:110–118CrossRefGoogle Scholar
  42. Jiang CH, Xie YS, Zhu K, Wang N, Li ZJ, Yu GJ, Guo JH (2019) Volatile organic compounds emitted by Bacillus sp. JC03 promote plant growth through the action of auxin and strigolactone. Plant Growth Regul 87:317–328CrossRefGoogle Scholar
  43. Jimtha CJ, Jishma P, Sreelekha S, Chithra S, Radhakrishnan EK (2017) Antifungal properties of prodigiosin producing rhizospheric Serratia sp. Rhizosphere 3:105–108CrossRefGoogle Scholar
  44. Johansen JE, Binnerup SJ (2002) Contribution of Cytophaga-like bacteria to the potential of turnover of carbon, nitrogen, and phosphorus by bacteria in the rhizosphere of barley (Hordeum vulgare L.). Microb Ecol 43:298–306PubMedCrossRefGoogle Scholar
  45. Kamensky M, Ovadis M, Chet I, Chernin L (2003) Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol Biochem 35(2):323–331CrossRefGoogle Scholar
  46. Khan AL, Halo BA, Elyassi A, Ali S, Al-Hosni K, Hussain J, Al-Harrasi A, Lee IJ (2016) Indole acetic acid and ACC deaminase from endophytic bacteria improves the growth of Solanum lycopersicum. Elec J Biotechnol 21:58–64CrossRefGoogle Scholar
  47. Khan N, Zandi P, Ali S, Mehmood A, Shahid MA (2018) Impact of salicylic acid and PGPR on the drought tolerance and phytoremediation potential of helianthus annus. Front Microbiol 9:2507.  https://doi.org/10.3389/fmicb.2018.02507 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Khilyas IV, Shirshikova TV, Matrosova LE, Sorokina AV, Sharipova MR, Bogomolnaya LM (2016) Production of siderophores by Serratia marcescens and the role of MacAB efflux pump in siderophore secretion. Bio Nano Sci.  https://doi.org/10.1007/s12668-016-0264-3 CrossRefGoogle Scholar
  49. Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885–886CrossRefGoogle Scholar
  50. Kudoyarova GR, Vysotskaya LB, Arkhipova TN, Kuzmina LY, Galimsyanova NF, Gabbasova SLV, Ilusa M, Melentiev AI, Veselov YuS (2017) Effect of auxin producing and phosphate solubilizing bacteria on mobility of soil phosphorus, growth rate, and P acquisition by wheat plants. Acta Physiol lant. 39:253CrossRefGoogle Scholar
  51. Kumar A, Maurya BR, Raghuwanshi R (2015) Characterization of bacterial strains and their impact on plant growth promotion and yield of wheat and microbial populations of soil. Afr J Agric Res 10(12):1367–1375CrossRefGoogle Scholar
  52. Kumar A, Singh VK, Tripathi V, Singh PP, Singh AK (2018) Plant growth-promoting rhizobacteria (PGPR): perspective in agriculture under biotic and abiotic stress. In: Crop improvement through microbial biotechnology. Elsevier, Oxford, pp 333–342CrossRefGoogle Scholar
  53. Kumar A, Verma JP (2017) Does plant–microbe interaction confer stress tolerance in plants?: a review. Microbiol Res 207:41–52PubMedCrossRefGoogle Scholar
  54. Kumawat K, Sharma P, Sirari A, Singh I, Gill B, Singh U, Saharan K (2019) Synergism of Pseudomonas aeruginosa (LSE-2) nodule endophyte with Bradyrhizobium sp. (LSBR-3) for improving plant growth, nutrientt acquisition and soil health in soybean. World J Microbiol Biotechnol 35:47PubMedCrossRefGoogle Scholar
  55. Lal R (2013) Soils and ecosystem services. In: Lal R, Lorenz K, Hüttl RF, Schneider BU, Braun JV (eds) Ecosystem services and carbon sequestration in the biosphere. Springer, Dordrecht, pp 11–38CrossRefGoogle Scholar
  56. Liu H, He Y, Jiang H, Peng H, Huang X, Zhang X, Thomashow LS, Xu Y (2007) Characterization of a phenazine-producing strain Pseudomonas chlororaphis GP72 with broad-spectrum antifungal activity from green pepper rhizosphere. Curr Microbiol 54(4):302–306PubMedCrossRefGoogle Scholar
  57. Loper JE, Gross H (2007) Genomic analysis of antifungal metabolite production by Pseudomonas fluorescens Pf-5. Eur J Plant Pathol 119(3):265–278CrossRefGoogle Scholar
  58. Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258PubMedCrossRefGoogle Scholar
  59. Maheshwari DK, Dubey RC, Agarwal M, Dheeman S, Aeron A, Bajpai VK (2015) Carrier based formulations of biocoenotic consortia of disease suppressive Pseudomonas aeruginosa KRP1 and Bacillus licheniformis KRB1. Ecol Eng 81:272–277CrossRefGoogle Scholar
  60. Majeed A, Muhammad Z, Ahmad H (2018) Plant growth promoting bacteria: role in soil improvement, abiotic and biotic stress management of crops. Plant Cell Rep 37(12):1599–1609PubMedCrossRefGoogle Scholar
  61. Malviya J, Singh K (2012) Characterization of novel plant growth promoting and biocontrol strains of fluorescent Pseudomonads for crop. J Int Med Res 1:235–244Google Scholar
  62. Maurya BR, Meena VS, Meena OP (2014) Influence of inceptisol and alfisol’s potassium solubilizing bacteria (KSB) isolates on release of K from waste mica. Vegetos 27(1):181–187Google Scholar
  63. Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017a) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172.  https://doi.org/10.3389/fpls.2017.00172 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Meena OP, Maurya BR, Meena VS (2013) Influence of K-solubilizing bacteria on release of potassium from waste mica. Agric Sustain Dev 1(1):53–56Google Scholar
  65. Meena VS, Maurya BR, Bahadur I (2014a) Potassium solubilization by bacterial strain in waste mica. Bangl J Bot 43(2):235–237CrossRefGoogle Scholar
  66. Meena VS, Maurya BR, Verma JP (2014b) Does a rhizospheric microorganism enhance K+ availability in agricultural soils? Microbiol Res 169:337–347PubMedCrossRefGoogle Scholar
  67. Meena VS, Meena SK, Verma JP, Kumar A, Aeron A, Mishra PK, Bisht JK, Pattanayaka A, Naveed M, Dotaniya ML (2017b) Plant beneficial rhizospheric microorganism (PBRM) strategies to improve nutrients use efficiency: a review. Ecol Eng 107:8–32CrossRefGoogle Scholar
  68. Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389PubMedCrossRefGoogle Scholar
  69. Mohanram S, Kumar P (2019) Rhizosphere microbiome: revisiting the synergy of plant–microbe interactions. Ann Microbiol 69:307–320CrossRefGoogle Scholar
  70. Munees A (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. Biotechnology 5:111–121Google Scholar
  71. Mwajita M, Murage H, Tani A, Kahangi E (2013) Evaluation of rhizosphere, rhizoplane and phyllosphere bacteria and fungi isolated from rice in Kenya for plant growth promoters. Sprigerplus 2:606CrossRefGoogle Scholar
  72. Nadeem SM, 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 32:429–448PubMedPubMedCentralCrossRefGoogle Scholar
  73. Nawaz HH, Rajaofera MN, He Q, Anam U, Lin C, Miao W (2018) Evaluation of antifungal metabolites activity from Bacillus licheniformis OE-04 against Colletotrichum gossypii. Pest Biochem Physiol.  https://doi.org/10.1016/j.pestbp.2018.02.007 CrossRefGoogle Scholar
  74. Noumavo P, Agbodjato N, Gachomo E, Salami H, Farid B, Adjanohoun A, Kotchoni S, Lamine B (2015) Metabolic and biofungicidal properties of maize rhizobacteria for growth promotion and plant disease resistance. Afr J Biotechnol 14:811–819CrossRefGoogle Scholar
  75. Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, Ahmed AH (2018a) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32PubMedCrossRefGoogle Scholar
  76. Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, Khan A, Al-Harrasi A (2018b) Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review. Microbiol Res 209:21–32PubMedCrossRefGoogle Scholar
  77. Pandey A, Yarzábal LA (2019) Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl Microbiol Biotechnol 103:643PubMedCrossRefGoogle Scholar
  78. Potarzycki J, Grzebisz W (2009) Effect of zinc foliar application on grain yield of maize and its yielding components. Plant Soil Environ 55:519–527CrossRefGoogle Scholar
  79. Rakshit A, Kumari S, Pal S, Singh A, Singh HB (2015) Bio-priming mediated nutriant use efficiency of crop species. Nutr Use Efficiency Basics Adv 2015:181–191CrossRefGoogle Scholar
  80. Reichling J (2018) Plant–microbe interactions and secondary metabolites with antibacterial, antifungal and antiviral properties. Annu Plant Rev 324:214–347CrossRefGoogle Scholar
  81. Rishad KS, Rebello S, Shabanamol PS, Jisha MS (2016) Biocontrol potential of Halotolerant bacterial chitinase from high yielding novel Bacillus Pumilus MCB-7 autochthonous to mangrove ecosystem. Pest Biochem Physiol 137:36–41CrossRefGoogle Scholar
  82. Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932PubMedCrossRefGoogle Scholar
  83. Saleem M, Law AD, Sahib MR, Pervaiz ZH, Zhang Q (2018) Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6:47–51CrossRefGoogle Scholar
  84. Sarkar A, Saha M, Meena VS (2017) Plant beneficial rhizospheric microbes (PBRMs): prospects for increasing productivity and sustaining the resilience of soil fertility. In: Meena V, Mishra P, Bisht J, Pattanayak A (eds) Agriculturally important microbes for sustainable agriculture. Springer, Singapore, pp 3–29CrossRefGoogle Scholar
  85. Scagliola M, Pii Y, Mimmo T, Cesco S, Ricciuti P, Crecchio C (2016) Characterization of plant growth promoting traits of bacterial isolates from the rhizosphere of barley (Hordeum vulgare L.) and tomato (Solanum lycopersicon L.) grown under Fe sufficiency and deficiency. Plant Physiol Biochem 107:187–196PubMedCrossRefGoogle Scholar
  86. Schloter M, Nannipieri P, Sorensen SJ, van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10CrossRefGoogle Scholar
  87. Schmid M, Hartmann A (2013) The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol Plant Microbe Interact 26:937–945PubMedCrossRefGoogle Scholar
  88. Selvakumar G, Bindu GH, Bhatt RM, Upreti KK, Paul AM, Asha A, Shweta K, Sharma M (2018) Osmotolerant cytokinin producing microbes enhance tomato growth in deficit irrigation conditions. Proc Natl Acad Sci India Sect B Biol Sci 88(2):459–465CrossRefGoogle Scholar
  89. Sen S, Chandrasekhar CN (2014) Effect of PGPR on growth promotion of rice (Oryza sativa L.) under salt stress. Asian J Plant Sci Res 4:62–67Google Scholar
  90. Shaikh S, Wani S, Sayyed R (2018) Impact of interactions between rhizosphere and rhizobacteria: a review. J Bacteriol Mycol 5:1058Google Scholar
  91. Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84:603–615CrossRefGoogle Scholar
  92. Singh D, Geat N, Rajawat MVS, Mahajan MM, Prasanna R, Singh S, Kaushik R, Singh RN, Kumar K, Saxena AK (2017a) Deciphering the mechanisms of endophyte-mediated biofortification of Fe and Zn in wheat. J Plant Growth Regul 37(1):174–182CrossRefGoogle Scholar
  93. Singh D, Rajawat MVS, Kaushik R, Prasanna R, Saxena AK (2017b) 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(1–2):107–116CrossRefGoogle Scholar
  94. Slimene IB, Tabbene O, Gharbi D, Mnasri B, Schmitter JM, Urdaci MC, Limam F (2015) Isolation of a chitinolytic Bacillus licheniformis S213 strain exerting a biological control against phoma medicaginis infection. Biotechnol Appl Biochem 175(7):3494–3506CrossRefGoogle Scholar
  95. Stephane C, Brion D, Jerzy N, Christophe C, Essaid AB (2005) Use of plant growth bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl Environ Microbiol 71(9):4951–4959CrossRefGoogle Scholar
  96. Subbanna ARNS, Khan MS, Shivashankara H (2016) Characterization of antifungal Paenibacillus illinoisensis strain UKCH21 and its chitinolytic properties. Afr J Microbiol Res 10(34):1380–1387CrossRefGoogle Scholar
  97. Sulieman S, Chien V, Esfahani M, Yasuko W, Rie N, Chung T, Dong V, Tran L (2015) DT2008: a promising new genetic resource for improved drought tolerance in soybean when solely dependent on symbiotic N2 fixation. BioMed Res.  https://doi.org/10.1155/2015/687213 CrossRefGoogle Scholar
  98. Sun C, Johnson J, Cai D, Sherameti I, Oelmüeller R, Lou B (2010) Piriformospora indica confers drought tolerance in Chinese cabbage leaves by stimulating antioxidant enzymes, the expression of drought-related genes and the plastid-localized CAS protein. J Plant Physiol 167:1009–1017PubMedCrossRefGoogle Scholar
  99. Talbi C, Sánchez C, Hidalgo-Garcia A, González E, Arrese-Igorm C, Girard L, Bedmar E, Delgado MJ (2012) Enhanced expression of Rhizobiumetli cbb3 oxidase improves drought tolerance of common bean symbiotic nitrogen fixation. J Exp Bot 63:5035–5043PubMedCrossRefGoogle Scholar
  100. Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signalling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588PubMedCrossRefGoogle Scholar
  101. Van Peer R, Niemann GJ, Schippers B (1991) Induced resistance and phytoalexin accumulation in biological control of Fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathol 91:728–734CrossRefGoogle Scholar
  102. Verma JP, Yadav J, Tiwari KN, Jaiswal DK (2014) Evaluation of plant growth promoting activities of microbial strains and their effect on growth and yield of chickpea (Cicer arietinum L.) in India. Soil Biol Biochem 70:33–37CrossRefGoogle Scholar
  103. Verma JP, Yadav J, Tiwari KN, Kumar A (2013) Effect of indigenous Mesorhizobium spp. and plant growth promoting rhizobacteria on yields and nutrients uptake of chickpea (Cicer arietinum L.) under sustainable agriculture. Ecol Eng 51:282–286CrossRefGoogle Scholar
  104. Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y, Cui H (2013) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341(1):45–51PubMedCrossRefGoogle Scholar
  105. Weise T, Thürmer A, Brady S, Kai M, Daniel R, Gottschalk G, Piechulla B (2014) VOC emission of various Serratia species and isolates and genome analysis of Serratia plymuthica 4Rx13. FEMS Microbiol Lett 352:45–53PubMedCrossRefGoogle Scholar
  106. Wu L, Kobayashi Y, Wasaki J, Koyama H (2018) Organic acid excretion from roots: a plant mechanism for enhancing phosphorus acquisition, enhancing aluminiumaluminum tolerance, and recruiting beneficial rhizobacteria. Soil Sci Plant Nutr 64(6):697–704CrossRefGoogle Scholar
  107. Wu Z, Peng Y, Guo L, Li C (2014) Root colonization of encapsulated Klebsiella oxytoca Rs-5 on cotton plants and its promoting growth performance under salinity stress. Eur J Soil Biol 60:81–87CrossRefGoogle Scholar
  108. Xu Z, Zhang H, Sun X, Liu Y, Yan W, Xun W, Shen Q, Zhang R (2019) Bacillus velezensis wall teichoic acids are required for biofilm formation and root colonization. Appl Environ Microbiol 85:e02116–e02118PubMedPubMedCentralGoogle Scholar
  109. Ye X, Junjiang S, Williams E (2015) Use of non-agrobacterium bacterial species for plant transformation. US Patent No. 20150040266, 5 Feb 2015Google Scholar
  110. Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, Cho H, Karaoz U, Loqué D, Bowen BP (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470PubMedCrossRefGoogle Scholar
  111. Zhang C, Kong F (2014) Isolation and identification of potassium-solubilizing bacteria from tobacco rhizospheric soil and their effect on tobacco plants. Appl Soil Ecol 82:18–25CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Abhinav Aeron
    • 1
    • 9
  • Ekta Khare
    • 1
    • 2
  • Chaitanya Kumar Jha
    • 3
  • Vijay Singh Meena
    • 4
    Email author
  • Shadia Mohammed Abdel Aziz
    • 5
  • Mohammed Tofazzal Islam
    • 6
  • Kangmin Kim
    • 1
  • Sunita Kumari Meena
    • 7
    • 8
  • Arunava Pattanayak
    • 4
  • Hosahatti Rajashekara
    • 4
  • Ramesh Chandra Dubey
    • 9
  • Bihari Ram Maurya
    • 10
  • Dinesh Kumar Maheshwari
    • 9
  • Meenu Saraf
    • 13
  • Mahipal Choudhary
    • 4
  • Rajhans Verma
    • 11
  • H. N. Meena
    • 12
  • A. R. N. S. Subbanna
    • 4
  • Manoj Parihar
    • 4
  • Shruti Shukla
    • 20
  • Govarthanan Muthusamy
    • 21
  • Ram Swaroop Bana
    • 14
  • Vivek K. Bajpai
    • 15
    Email author
  • Young-Kyu Han
    • 15
    Email author
  • Mahfuzur Rahman
    • 16
  • Dileep Kumar
    • 17
  • Norang Pal Singh
    • 18
  • Rajesh Kumar Meena
    • 19
  1. 1.Division of Biotechnology, College of Environmental and Bioresource SciencesChonbuk National UniversityIksanRepublic of Korea
  2. 2.Department of Microbiology, Institute of Biosciences and BiotechnologyChhatrapati Shahu Ji Maharaj UniversityKanpurIndia
  3. 3.Department of MicrobiologyGovernment Science College, VankalSuratIndia
  4. 4.ICAR-Vivekananda Parvatiya Krishi Anusandhan Sansthan (VPKAS)AlmoraIndia
  5. 5.Microbial Chemistry DepartmentNational Research CenterDokki, GizaEgypt
  6. 6.Department of BiotechnologyBangabandhu Sheikh Mujibur Rahman Agricultural UniversityDhakaBangladesh
  7. 7.Division of Soil Science and Agricultural ChemistryICAR-Indian Agriculture Research Institute (IARI)New DelhiIndia
  8. 8.Sugarcane Research Institute, Dr. Rajendra Prasad Central Agriculture UniversitySamastipurIndia
  9. 9.Department of Botany and MicrobiologyGurukula Kangri UniversityHaridwarIndia
  10. 10.Department of Soil Science and Agricultural Chemistry, Institute of Agricultural SciencesBanaras Hindu University (BHU)VaranasiIndia
  11. 11.Department of Soil Science and Agricultural ChemistrySKN College of Agriculture, Jobner, SKN, Agriculture University, JobnerJaipurIndia
  12. 12.ICAR-Agricultural Technology Application Research Institute (ATARI)JodhpurIndia
  13. 13.University School of Sciences, Gujarat UniversityDepartment of Microbiology and BiotechnologyAhmedabadIndia
  14. 14.Division of AgronomyICAR-Indian Agricultural Research Institute (IARI)New DelhiIndia
  15. 15.Department of Energy and Materials EngineeringDongguk University-SeoulSeoulRepublic of Korea
  16. 16.Extension ServiceWest Virginia UniversityMorgantownUSA
  17. 17.Anand Agricultural University (AAU)AnandIndia
  18. 18.Microbial Genetics and PGPR Research Laboratory, Department of Genetics and Plant Breeding, Institute of Agriculture SciencesBanaras Hindu University (BHU)VaranasiIndia
  19. 19.Department of Plant Sciences, School of Life SciencesUniversity of HyderabadHyderabadIndia
  20. 20.Department of Food Science and TechnologyNational Institute of Food Technology Entrepreneurship and Management (NIFTEM)SonipatIndia
  21. 21.Department of Environmental EngineeringKyungpook National UniversityDaeguSouth Korea

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