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.
Similar content being viewed by others
References
Ahkami AH, White RA III, Handakumbura PP, Jansson C (2017) Rhizosphere engineering: enhancing sustainable plant ecosystem productivity. Rhizosphere 3(2017):233–243
Ahn IP, Lee SW, Suh SC (2007) Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPRI. Mol Plant Microbe Interact 20:759–768
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 4:141
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 8:412
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
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):1049–1061
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 41:2141–2150
Arnou DI (1953) Soil and fertilizer phosphorus in crop nutrition (IV). In: Pierre WH, Noramn AG (eds) Academic Press, New York
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):581–585
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 245:15–30
Badar R, Nisa Z, Ibrahim S (2015) Supplementation of P with rhizobial inoculants to improve growth of Peanut plants. Int J Appl Res 1:19–23
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 180:501–510
Bhat MA (2019) Plant growth promoting rhizobacteria (PGPR) for sustainable and eco-friendly agriculture. Acta Sci Agric 3:23–25
Bhattacharyya P, Jha D (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350
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 74:280–286
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
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 47:102–108
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 9:3429
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 437:83–92
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 3–21
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 287–303
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 110:324–327
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):1027–1036
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 5:573
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
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):99–106
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 137:154–166
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 149–184
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 2016:1–10
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 27:1833–1847
Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 209:1–25
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 8:120
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
Hassani MA, Durán P, Hacquard S (2018) Microbial interactions within the plant holobiont. Microbiome 6(1):58
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 60:579–598
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 439:309–324
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):1–12
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 46:312–321
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 26:1163–1170
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 167–218
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 69:110–118
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 87:317–328
Jimtha CJ, Jishma P, Sreelekha S, Chithra S, Radhakrishnan EK (2017) Antifungal properties of prodigiosin producing rhizospheric Serratia sp. Rhizosphere 3:105–108
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 43:298–306
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):323–331
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 21:58–64
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
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
Kloepper JW, Leong J, Teintze M, Schiroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885–886
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. 39:253
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):1367–1375
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 333–342
Kumar A, Verma JP (2017) Does plant–microbe interaction confer stress tolerance in plants?: a review. Microbiol Res 207:41–52
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 35:47
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 11–38
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):302–306
Loper JE, Gross H (2007) Genomic analysis of antifungal metabolite production by Pseudomonas fluorescens Pf-5. Eur J Plant Pathol 119(3):265–278
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
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 81:272–277
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):1599–1609
Malviya J, Singh K (2012) Characterization of novel plant growth promoting and biocontrol strains of fluorescent Pseudomonads for crop. J Int Med Res 1:235–244
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):181–187
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
Meena OP, Maurya BR, Meena VS (2013) Influence of K-solubilizing bacteria on release of potassium from waste mica. Agric Sustain Dev 1(1):53–56
Meena VS, Maurya BR, Bahadur I (2014a) Potassium solubilization by bacterial strain in waste mica. Bangl J Bot 43(2):235–237
Meena VS, Maurya BR, Verma JP (2014b) Does a rhizospheric microorganism enhance K+ availability in agricultural soils? Microbiol Res 169:337–347
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 107:8–32
Mercado-Blanco J, Bakker PAHM (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389
Mohanram S, Kumar P (2019) Rhizosphere microbiome: revisiting the synergy of plant–microbe interactions. Ann Microbiol 69:307–320
Munees A (2015) Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: a review. Biotechnology 5:111–121
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 2:606
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 32:429–448
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
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 14:811–819
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 209:21–32
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 209:21–32
Pandey A, Yarzábal LA (2019) Bioprospecting cold-adapted plant growth promoting microorganisms from mountain environments. Appl Microbiol Biotechnol 103:643
Potarzycki J, Grzebisz W (2009) Effect of zinc foliar application on grain yield of maize and its yielding components. Plant Soil Environ 55:519–527
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 2015:181–191
Reichling J (2018) Plant–microbe interactions and secondary metabolites with antibacterial, antifungal and antiviral properties. Annu Plant Rev 324:214–347
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 137:36–41
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 100:4927–4932
Saleem M, Law AD, Sahib MR, Pervaiz ZH, Zhang Q (2018) Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6:47–51
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 3–29
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 107:187–196
Schloter M, Nannipieri P, Sorensen SJ, van Elsas JD (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10
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 26:937–945
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):459–465
Sen S, Chandrasekhar CN (2014) Effect of PGPR on growth promotion of rice (Oryza sativa L.) under salt stress. Asian J Plant Sci Res 4:62–67
Shaikh S, Wani S, Sayyed R (2018) Impact of interactions between rhizosphere and rhizobacteria: a review. J Bacteriol Mycol 5:1058
Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84:603–615
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):174–182
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):107–116
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):3494–3506
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):4951–4959
Subbanna ARNS, Khan MS, Shivashankara H (2016) Characterization of antifungal Paenibacillus illinoisensis strain UKCH21 and its chitinolytic properties. Afr J Microbiol Res 10(34):1380–1387
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
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 167:1009–1017
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 63:5035–5043
Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signalling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588
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 91:728–734
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 70:33–37
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 51:282–286
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):45–51
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 352:45–53
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):697–704
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 60:81–87
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–e02118
Ye X, Junjiang S, Williams E (2015) Use of non-agrobacterium bacterial species for plant transformation. US Patent No. 20150040266, 5 Feb 2015
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 3:470
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 82:18–25
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
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Aeron, A., Khare, E., Jha, C.K. et al. Revisiting the plant growth-promoting rhizobacteria: lessons from the past and objectives for the future. Arch Microbiol 202, 665–676 (2020). https://doi.org/10.1007/s00203-019-01779-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-019-01779-w