Skip to main content

Advertisement

SpringerLink
Log in

PGPR: the treasure of multifarious beneficial microorganisms for nutrient mobilization, pest biocontrol and plant growth promotion in field crops

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Plant growth-promoting rhizobacteria (PGPR) have multifarious beneficial activities for plant growth promotion; act as source of metabolites, enzymes, nutrient mobilization, biological control of pests, induction of disease resistance vis-a-vis bioremediation potentials by phytoextraction and detoxification of heavy metals, pollutants and pesticides. Agrochemicals and synthetic pesticides are currently being utilized widely in all major field crops, thereby adversely affecting human and animal health, and posing serious threats to the environments. Beneficial microorganisms like PGPR could potentially substitute and supplement the toxic chemicals and pesticides with promising application in organic farming leading to sustainable agriculture practices and bioremediation of heavy metal contaminated sites. Among field crops limited bio-formulations have been prepared till now by utilization of PGPR strains having plant growth promotion, metabolites, enzymes, nutrient mobilization and biocontrol activities. The present review contributes comprehensive description of PGPR applications in field crops including commercial, oilseeds, leguminous and cereal crops to further extend the utilization of these potent groups of beneficial microorganisms so that even higher level of crop productivity and quality produce of field crops could be achieved. PGPR and bacteria based commercialized bio-formulations available worldwide for its application in the field crops have been compiled in this review which can be a substitute for the harmful synthetic chemicals. The current knowledge gap and potential target areas for future research have also been projected.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

ACC:

1-Aminocyclopropane-1-carboxylate

PGP:

Plant growth promotion

EPS:

Exopolysaccharides

ISR:

Induced systemic resistance

SAR:

Systemic acquired resistance

VOCs:

Volatile organic compounds

PGPR:

Plant growth promoting rhizobacteria

HCN:

Hydrogen cyanide

IAA:

Indole-3-acetic acid

SA:

Salicylic acid

MAMPs:

Microbe associated molecular pattern

QS:

Quoram sensing

SynComs:

Synthetic microbial communities

References

  • Aasfar A, Bargaz A, Yaakoubi K, Hilali A, Bennis I, Zeroual Y, Meftah Kadmiri I (2021) Nitrogen fixing azotobacter species as potential soil biological enhancers for crop nutrition and yield stability. Front Microbiol 12:628379. https://doi.org/10.3389/fmicb.2021.628379

    Article  PubMed  PubMed Central  Google Scholar 

  • Abbaszadeh-Dahaji P, Masalehi F, Akhgar A (2019) Improved growth and nutrition of sorghum (Sorghum bicolor) plants in a low-fertility calcareous soil treated with plant growth-promoting rhizobacteria and Fe-EDTA. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-019-00098-9

    Article  Google Scholar 

  • Abdelkrim S, Jebara SH, Saadani O, Chiboub M, Abid G, Jebara M (2018a) Effect of Pb-resistant plant growth-promoting rhizobacteria inoculation on growth and lead uptake by Lathyrus sativus. J Basic Microbiol 58(7):579–589. https://doi.org/10.1002/jobm.201700626

    Article  CAS  PubMed  Google Scholar 

  • Abdelkrim S, Jebara SH, Saadani O, Jebara M (2018b) Potential of efficient and resistant plant growth-promoting rhizobacteria in lead uptake and plant defence stimulation in Lathyrus sativus under lead stress. Plant Biol (stuttg) 20(5):857–869. https://doi.org/10.1111/plb.12863

    Article  CAS  PubMed  Google Scholar 

  • Abdelkrim S, Jebara SH, Saadani O, Abida G, Taamallic W, Zemnid H, Mannaia K, Louatia F, Jebara M (2020) In situ effects of Lathyrus sativus- PGPR to remediate and restore quality and fertility of Pb and Cd polluted soils. Ecotoxicol Environ Safety 192:110260. https://doi.org/10.1016/j.ecoenv.2020.110260

    Article  CAS  PubMed  Google Scholar 

  • Abirami S, Nagarajan D, Rodrigo BCP (2018) Enhancement of black gram (Phaseolus mungo L.) growth by dual inoculation with Pseudomonas fluorescens and Rhizobium leguminosarum. J Pharmacognosy Phytochem SP5:01–07

    Google Scholar 

  • Abou-El-Hassan S, Elbatran HS (2020) Production of pea without chemical fertilizers via integrating biofertilizers with vermiwash. Plant Arch 20(2):4319–4325

    Google Scholar 

  • Ahmed N, Ahsen S, Ali MA, Hussain MB, Hussain SB, Rasheed MK, Butt B, Irshad I, Danish S (2020) Rhizobacteria and silicon synergy modulates the growth, nutrition and yield of mungbean under saline soil. Pak J Bot 52:9–15

    Article  CAS  Google Scholar 

  • Alberton D, Valdameri G, Moure VR, Monteiro RA, Pedrosa FO, Müller-Santos M, de Souza EM (2020) What did we learn from plant growth-promoting rhizobacteria (PGPR)-grass associations studies through proteomic and metabolomic approaches? Front Sustain Food Syst 4:607343. https://doi.org/10.3389/fsufs.2020.607343

    Article  Google Scholar 

  • Ali S, Khan MA, Kim WC (2018) Pseudomonas veronii KJ mitigates flood stress-associated damage in Sesamum indicum L. Appl Biol Chem 61:575–585. https://doi.org/10.1007/s13765-018-0392-2

    Article  CAS  Google Scholar 

  • Amna YX, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, Tabassum T, Rehman S, Munis MFH, Sultan T, Chaudhary HJ (2020) Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol Biochem 151:640–649

    Article  CAS  PubMed  Google Scholar 

  • Aquino JPA, Junior FBM, Antunes JEL, Figueiredo MVB, Neto FA, Araujo ASF (2019) Plant growth-promoting endophytic bacteria on maize and sorghum1. Pesqui Agropecu Trop 49(3):e56241. https://doi.org/10.1590/1983-40632019v4956241

    Article  Google Scholar 

  • Atchyuth V, Chaurasia AK, Reddy JK (2021) Impact of organic and inorganic seed priming methods on growth and yield attributes in lentil (Lens culinaris L.). Pharma Innov J 10(4):1063–1065

    CAS  Google Scholar 

  • Azadikhah M, Jamali F, Nooryazdan HR, Bayat F (2019) Growth promotion and yield enhancement of barley cultivars using ACC deaminase producing Pseudomonas fluorescens strains under salt stress. Spanish J Agric Res 17:e0801. https://doi.org/10.5424/sjar/2019171-13828

    Article  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant gowth promoting rhizobacteria: context, mechanisms of action and roadmap to commercialization of biostimulants for sutainable agriculture. Front Plant Sci 9:1473. https://doi.org/10.3389/fpls.2018.01473

    Article  PubMed  PubMed Central  Google Scholar 

  • Bahadori A, GHarineh MH, Bakhshandeh A, Enayatizamir N, Shafeinia A (2021) The effect of plant growth promoting rhizobacteria in reducing nitrogen and phosphorus fertilizers application in sugarcane. Plant Arch 21(1):1130–1137. https://doi.org/10.51470/PLANTARCHIVES.2021.v21.no1.149

    Article  Google Scholar 

  • Bala S, Devi R, Khanna V (2021) Exploration of rhizobacteria as bioagents against phytophthora blight and yield attributes of pigeonpea (Cajanus cajan L.): in vitro and in vivo Study. Int J Plant Soil Sci. https://doi.org/10.9734/ijpss/2021/v33i1830572

    Article  Google Scholar 

  • Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, El Enshasy H (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13:1140. https://doi.org/10.3390/su13031140

    Article  CAS  Google Scholar 

  • Bechtaoui N, El Alaoui A, Raklami A, Benidire L, Tahiri AI, Oufdou K (2019) Impact of intercropping and co-inoculation with strains of plant growth-promoting rhizobacteria on phosphorus and nitrogen concentrations and yield of durum wheat (Triticum durum) and faba bean (Vicia faba). Crop Pasture Sci 70(8):649–658. https://doi.org/10.1071/CP19067

    Article  CAS  Google Scholar 

  • Berg G, Köberl M, Rybakova D, Müller H, Grosch R, Smalla K (2017) Plant microbial diversity is suggested as the key to future biocontrol and health trends. Fems Microbiol Ecol 93:50

    Article  Google Scholar 

  • Bhardwaj G, Shah R, Joshi B, Patel P (2017) Klebsiella pneumoniae VRE36 as a PGPR isolated from Saccharum officinarum cultivar Co99004. J App Biol Biotech 5(01):047–052. https://doi.org/10.7324/JABB.2017.50108

    Article  CAS  Google Scholar 

  • Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65(5):497–503

    Article  CAS  PubMed  Google Scholar 

  • Bouras FZ, Ghanem M, Benine ML, Labdi M, Reguig M, Benali M, Abbouni B (2018) Isolation, screening, characterization of PGPR of lentils Lens culinaris. Pharm Lett 10(1):91–104

    CAS  Google Scholar 

  • Cao YY, Ni HT, Li T, Lay K, Liu DS, He XY, Ou KM, Tang XY, Wang XB, Qiu LJ (2020) Pseudomonas sp. TK35-L enhances tobacco root development and growth by inducing HRGPnt3 expression in plant lateral root formation. J Integ Agric 19(10):2549–2560. https://doi.org/10.1016/S2095-3119(20)63266-X

    Article  CAS  Google Scholar 

  • Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Labuschagne N (2019) Differential metabolic reprogramming in Paenibacillus alvei-primed Sorghum bicolor seedlings in response to Fusarium pseudograminearum infection. Metabolites 9:150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-Moretti FR, Gentzel IN, Mackey D, Alonso AP (2020) Metabolomics as an emerging tool for the study of plant-pathogen interactions. Metabolites 10:52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandran H, Meena M, Swapnil P (2021) Plant growth-promoting rhizobacteria as a green alternativefor sustainable agriculture. Sustainability 13:10986. https://doi.org/10.3390/su131910986

    Article  CAS  Google Scholar 

  • Chaurasia A, Meena BR, Tripathi AN et al (2018) Actinomycetes: an unexplored microorganisms for plant growth promotion and biocontrol in vegetable crops. World J Microbiol Biotechnol 34:132. https://doi.org/10.1007/s11274-018-2517-5

    Article  CAS  PubMed  Google Scholar 

  • Chaurasia A, Hawksworth DL, de Miranda MP (2020) GMOs: implications for biodiversity conservation and ecological processes. Springer, Cham. https://doi.org/10.1007/978-3-030-53183-6

    Book  Google Scholar 

  • Chen L, Hao Z, Li K, Sha Y, Wang E, Sui X, Mi G, Tian C, Chen W (2020) Effects of growth-promoting rhizobacteria on maize growth and rhizosphere microbial community under conservation tillage in Northeast China. Microbial Biotechnol 14(2):535–550. https://doi.org/10.1111/1751-7915.13693

    Article  CAS  Google Scholar 

  • Chowdhury FT, Zaman NR, Islam MR, Khan H (2020) Anti-fungal secondary metabolites and hydrolytic enzymes from rhizospheric bacteria in crop protection: a review. J Bangladesh Acad Sci 44(2):69–84

    Article  CAS  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. App Env Microbiol 71:4951–4959

    Article  CAS  Google Scholar 

  • Dangi S, Tirado-Corbalá R, Gerik J, Hanson B (2017) Effect of long-term continuous fumigation on soil microbial communities. Agronomy 7:37

    Article  Google Scholar 

  • de Souza RSC, Armanhi JSL, Arruda P (2020) From microbiome to traits: designing synthetic microbial communities for improved crop resiliency. Front Plant Sci 11:1–7

    Article  Google Scholar 

  • Dhawi F (2020) Plant growth promoting rhizobacteria (PGPR) regulated phyto and microbial beneficial protein interactions. Open Life Sci 15:68–78

    Article  CAS  Google Scholar 

  • Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiol 3(3):413–434. https://doi.org/10.3934/microbiol.2017.3.413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (2002) Identification of quorum-quenching N-acyl 6 homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • dos Santos RM, Diaz PAE, Lobo LLB, Rigobelo EC (2020) Use of plant growth-promoting rhizobacteria in maize and sugarcane: characteristics and applications. Front Sustain Food Syst 4:136. https://doi.org/10.3389/fsufs.2020.00136

    Article  Google Scholar 

  • Egamberdieva D, Wirth S, Jabborova D, Räsänen L, Liao H (2017) Coordination between Bradyrhizobium and Pseudomonas alleviates salt stress in soybean through altering root system architecture. J Plant Interac 12:100–107. https://doi.org/10.1080/17429145.2017.1294212

    Article  CAS  Google Scholar 

  • El-Nahrawy S, Yassin M (2020) Response of different cultivars of wheat plants (Triticum aestivum L.) to inoculation by Azotobacter sp. under salinity stress conditions. J Adv Microbiol 20(1):59–79. https://doi.org/10.9734/jamb/2020/v20i130209

    Article  CAS  Google Scholar 

  • Etesami H, Srivastava AK (2022) Bacterial induced alleviation of cadmium and arsenic toxicity stress in plants: mechanisms and future prospects. In: Dubey RC, Kumar P (eds) Rhizosphere engineering. Academic Press, Cambridge, pp 445–469. https://doi.org/10.1016/B978-0-323-89973-4.00013-2

    Chapter  Google Scholar 

  • Fathalla A, Abd El-Mageed A (2020) Salt tolerance enhancement of wheat (Triticum asativium L.) genotypes by selected plant growth promoting bacteria. AIMS Microbiol 6(3):250–271. https://doi.org/10.3934/microbiol.2020016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira CMH, Vilas-Boas Â, Sousa CA, Soares HMVM, Soares EV (2019) Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Expr 9:78. https://doi.org/10.1186/s13568-019-0796-3

    Article  CAS  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15. https://doi.org/10.6064/2012/963401

    Article  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase producing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140

    Article  PubMed  Google Scholar 

  • Guo D, Yuan C, Yunyan L, Chen Y, Lu M, Chen G, Ren G, Cui C, Zhang J, An D (2019) Biocontrol of PGPR strain Bacillus amyloliquefaciens Ba168 against Phytophthora nicotianae on tobacco. bioRxiv. https://doi.org/10.1101/700757

    Article  Google Scholar 

  • Gupta S, Seth R, Sharma A (2016) Plant growth-promoting rhizobacteria play a role as phytostimulators for sustainable agriculture. In: Choudhary DK, Varma A, Tuteja N (eds) Plant-microbe interaction: an approach to sustainable agriculture. Springer, Singapore, pp 475–493

    Chapter  Google Scholar 

  • Gupta S, Schillaci M, Roessner U (2022) Metabolomics as an emerging tool to study plant-microbe interactions. Emerg Top Life Sci 6(2):175–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haidar B, Ferdous M, Fatema B, Ferdous AS, Islam MR, Khan H (2018) Population diversity of bacterial endophytes from jute (Corchorus olitorius) and evaluation of their potential role as bioinoculants. Microbiol Res 208:43–53. https://doi.org/10.1016/j.micres.2018.01.008

    Article  PubMed  Google Scholar 

  • Hassan MK, McInroy JA, Jones J, Shantharaj D, Liles MR, Kloepper JW (2019) Pectin-rich amendment enhances soybean growth promotion and nodulation mediated by Bacillus Velezensis strains. Plants (basel) 8(5):120. https://doi.org/10.3390/plants8050120

    Article  CAS  PubMed  Google Scholar 

  • Hassan MK, Lawrence KS, Sikora EJ, Liles MR, Kloepper JW (2021) Enhanced biological control of root-knot nematode, Meloidogyne incognita, by combined inoculation of cotton or soybean seeds with a plant growth-promoting rhizobacterium and pectin-rich orange peel. J Nematol 53:e2021–e2058. https://doi.org/10.21307/jofnem-2021-058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, Liu Z, Li S, XuB GY, Yang Y, Sun H (2016) Isolation and engineering of plant growth promoting rhizobacteria Pseudomonas aeruginosa for enhanced cadmium bioremediation. J Gen Appl Microbiol 62:258–265. https://doi.org/10.2323/jgam.2016.04.007

    Article  CAS  PubMed  Google Scholar 

  • Ikram R, Ali B (2018) Co-inoculation of auxin producing PGPR and rhizobia enhanced growth of Vigna mungo (L.) under cadmium stress. Asian J Agri Biol 6(1):46–54

    Google Scholar 

  • Iqbal HI, Zahir ZA, Rehman O, Khalid R, Waheed A, Raza RA, Saleem S, Rashid M, Alvi ST, Munir A (2021) Improving the growth and yield of maize through multi-strain inoculation (PGPR) under saline conditions. Pakistan J Agri Res 34(2):400–406

    Google Scholar 

  • Javoreková S, Artimová R, Maková J, Hricáková N (2020) Isolation and identification of rhizobacteria from maize (Zea mays L.) in luvisols and documentation their plant growth promoting traits. J Microbiol Biotechnol Food Sci 10(3):505–510. https://doi.org/10.15414/jmbfs2020.10.3.505-510

    Article  Google Scholar 

  • Jeon JS, Rybka D, Carreno-Quintero N, De Vos R, Raaijmakers JM, Etalo DW (2022) Metabolic signatures of rhizobacteria-induced plant growth promotion. Plant Cell Environ 45(10):3086–3099

    Article  CAS  PubMed  Google Scholar 

  • Jha Y, Sablok G, Subbarao N, Sudhakar R, Fazil MH, Subramanian RB, Squartini A, Kumar S (2014) Bacterial-induced expression of RAB18 protein in Orzya sativa salinity stress and insights into molecular interaction with GTP ligand. J Mol Recognit 27(9):521–527. https://doi.org/10.1002/jmr.2371

    Article  CAS  PubMed  Google Scholar 

  • Jha Y, Dehury B, Kumar SPJ et al (2022) Delineation of molecular interactions of plant growth promoting bacteria induced β-1,3-glucanases and guanosine triphosphate ligand for antifungal response in rice: a molecular dynamics approach. Mol Biol Rep 49:2579–2589. https://doi.org/10.1007/s11033-021-07059-5

    Article  CAS  PubMed  Google Scholar 

  • Kalam S, Basu A, Podile AR (2020) Functional and molecular characterization of plant growth promoting Bacillus isolates from tomato rhizosphere. Heliyon 6:e04734

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaminsky LM, Trexler RV, Malik RJ, Hockett KL, Bell TH (2019) The inherent conflicts in developing soil microbial inoculants. Trends Biotechnol 37:140–151

    Article  CAS  PubMed  Google Scholar 

  • Kamkar B (2016) Sustainable development principles for agricultural activities. Adv Plant Agric Res 3(5):1–2

    Google Scholar 

  • Kanjanasopa D, Aiedhet W, Thitithanakul S, Paungfoo-Lonhienne C (2021) Plant growth promoting rhizobacteria as biological control agent in rice. Agri Sci 12(1):1–8. https://doi.org/10.4236/as.2021.121001

    Article  CAS  Google Scholar 

  • Kaur G, Khanna V (2017) Evaluation of thermotolerant rhizobacteria for multiple plant growth promoting traits from pigeonpea rhizosphere. J Appl Nat Sci 9:920–923. https://doi.org/10.31018/jans.v9i2.1298

    Article  CAS  Google Scholar 

  • Kaur M, Kalia S, Mathur A (2021) Growth promotion activities of plant growth promoting rhizobacteria (PGPRs) isolated from Vidarbha region, Maharashtra, India: Study on Cotton Crop. Annals of RSCB 25(6):4193–4208

    Google Scholar 

  • Kaur S, Egidi E, Qiu Z, Macdonald CA, Verma JP, Trivedi P, Wang J, Liu H, Singh BK (2022) Synthetic community improves crop performance and alters rhizosphere microbial communities. J Sustain Agric Environ 1:118–131

    Article  Google Scholar 

  • Ke J, Wang B, Yoshikuni Y (2021) Microbiome engineering: synthetic biology of plant-associated microbiomes in sustainable agriculture. Trends Biotechnol 39:244–261

    Article  CAS  PubMed  Google Scholar 

  • Kenneth OC, Nwadibe EC, Kalu AU, Unah UV (2019) Plant growth promoting rhizobacteria (PGPR): a novel agent for sustainable food production. Am J Agric Biol Sci 14(35):54

    Google Scholar 

  • Khalil Manal SM, Abdel-Rahem Hassan MH, Fayz Mahmoud A, Mohamed Morsy KM (2022) Involvement of secondary metabolites and extracellular lytic enzymes produced by plant growth promoting rhizobacteria in inhibiting the soil borne pathogens in faba bean plants. J Mycol Mycological Sci 5(1):000161

    Google Scholar 

  • Khamseh SR, Saeedi K, Ghobadinia M, Shahrak ARD (2019) Changes in agro-morphological traits of flax (Linum usitatissimum L.) under plant growth promoting bacteria effect and drought stress. Environ Stress Crop Sci 12(3):793–804. https://doi.org/10.22077/ESCS.2019.1567.1353

    Article  Google Scholar 

  • Khan N, Bano A (2019) Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 14(9):e0222302. https://doi.org/10.1371/journal.pone.0222302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MR, Mohidin FA, Khan U, Ahamad F (2016) Native Pseudomonas spp. suppressed the root-knot nematode in in vitro and in vivo and promoted the nodulation and grain yield in the field grown mungbean. Biol Control 101:159–168. https://doi.org/10.1016/j.biocontrol.2016.06.012

    Article  Google Scholar 

  • Khan AI, Bhandari RR, Pokhrel A, Yadav RN (2018a) A study on root exudation pattern and effect of plant growth promoting fungi during biotic and abiotic stress in Pigeonpea. World J Agric Res 6(4):122–131. https://doi.org/10.12691/wjar-6-4-2

  • Khan N, Martínez-Hidalgo P, Ice TA, Maymon M, Humm EA, Nejat N, Sanders ER, Kaplan D, Hirsch AM (2018b) Antifungal activity of Bacillus species against Fusarium and analysis of the potential mechanisms used in biocontrol. Front Microbiol 9:2363. https://doi.org/10.3389/fmicb.2018.02363

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan N, Zandi P, Ali S, Mehmood A, Shahid M (2018c) 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan MA, Asaf S, Khan A, Adhikari A, Jan R, Ali S, Imran M, Kim K, Lee I (2019a) Halotolerant rhizobacterial strains mitigate the adverse effects of NaCl stress in soybean seedlings. BioMed Res Int. https://doi.org/10.1155/2019/9530963

    Article  PubMed  PubMed Central  Google Scholar 

  • Khan N, Bano A, Rahman MA, Guo J, Kang Z, Babar MA (2019b) Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci Rep 9:2097

    Article  PubMed  PubMed Central  Google Scholar 

  • Khani AG, Enayatizamir N, Norouzi Masir M (2019) Impact of plant growth promoting rhizobacteria on different forms of soil potassium under wheat cultivation. Lett Appl Microbiol 68(6):514–521. https://doi.org/10.1111/lam.13132

    Article  CAS  Google Scholar 

  • Khatabi B, Gharechahi J, Ghaffari MR, Liu D, Haynes PA, Mckay MJ, Mirzaei M, Salekdeh GH (2019) Plant–microbe symbiosis: what has proteomics taught us? Proteomics 19(16):1800105

    Article  Google Scholar 

  • Khiyami MA, Omar MR, Abd-Elsalam KA, Aly AA (2014) Bacillus-based biological control of cotton seedling disease complex. J Plant Protec Res 54:340–348

    Article  Google Scholar 

  • Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes, In: Proceedings of the IVth International Conference on Plant Pathogenic Bacteria Vol. 2. Station de Pathologie Vegetale et Phyto-Bacteriologie. INRA, Angers, France, pp. 879–882

  • Kumar GP, Desai S, Moerschbacher BM, Gueddari NE (2019) Seed treatment with chitosan synergizes plant growth promoting ability of Pseudomonas aeruginosa-P17 in sorghum (Sorhum bicolor L.). bioRxiv 8:968

    Google Scholar 

  • Kumari ER, Vijaya Gopal MA, Lakshmipathy R (2018) Effect of stress tolerant plant growth promoting rhizobacteria on growth of blackgram under stress condition. Int J Curr Microbiol App Sci 7(01):1479–1487. https://doi.org/10.20546/ijcmas.2018.701.180

    Article  CAS  Google Scholar 

  • Kumari S, Bharat NK, Thakur AK (2022) Role of Plant Growth-Promoting Rhizobacteria (PGPR) and Bio-Control Agents (BCAs) in crop production. Int J Economic Plants 7(3):144–150

    Article  Google Scholar 

  • Kuramae EE, Derksen S, Schlemper TR, Dimitrov MR, Costa OYA, Silveira APDD (2020) Sorghum growth promotion by Paraburkholderia tropica and Herbaspirillum frisingense: putative mechanisms revealed by genomics and metagenomics. Microorganisms 8(5):725. https://doi.org/10.3390/microorganisms8050725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lade SB, Román C, del Cueto-Ginzo AI, Serrano L, Sin E, Achón MA, Medina V (2019) Differential proteomics analysis reveals that Azospirillium brasilense (Sp7) promotes virus tolerance in maize and tomato seedlings. Eur J Plant Pathol 155:1241–1263

    Article  CAS  Google Scholar 

  • Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, El Hamss H, Belabess Z, Barka EA (2022) Biological control of plant pathogens: a global perspective. Microorganisms 10:596. https://doi.org/10.3390/microorganisms10030596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemboub C, Chekireb D (2018) Rock phosphate solubilization and heavy metals resistance of rhizbacteria isolated from nodules of Lathyrus ochrus. J Pure Appl Microbiol 12(2):473–482

    Article  CAS  Google Scholar 

  • Liu H, Wang J, Sun H, Han X, Peng Y, Liu J, Liu K, Ding Y, Wang C, Du B (2020) Transcriptome profiles reveal the growth-promoting mechanisms of Paenibacillus polymyxa YC0136 on tobacco (Nicotiana tabacum L.). Front Microbiol 11:584174. https://doi.org/10.3389/fmicb.2020.584174

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Baena FJ, Monreal JA, Pérez-Montaño F, Guasch-Vidal B, Bellogín RA, Vinardell JM, Ollero FJ (2009) The absence of nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams Soybean. MPMI 22(11):1445–1454. https://doi.org/10.1094/MPMI-22-11-1445

    Article  CAS  PubMed  Google Scholar 

  • Lyu D, Backer R, Subramanian S, Smith DL (2020) Phytomicrobiome coordination signals hold potential for climate change-resilient agriculture. Front Plant Sci 11:634. https://doi.org/10.3389/fpls.2020.00634

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahmoud OMB, Hidri R, Talbi-Zribi O, Taamalli W, Abdelly C, Djébali N, Djébali N (2020) Auxin and proline producing rhizobacteria mitigate salt-induced growth inhibition of barley plants by enhancing water and nutrient status. South African J Bot 128:209–217. https://doi.org/10.1016/j.sajb.2019.10.023

    Article  CAS  Google Scholar 

  • Majid M, Ali M, Shahzad K, Ahmad F, Ikram RM, Ishtiaq M, Alaraidh IA, Al-hashimi A, Ali HM, Zarei T, Datta R, Fahad S, Sabagh AE, Hussain GS, Salem MZM, Habib-ur-Rahman M, Danish S (2020) Mitigation of osmotic stress in cotton for the improvement in growth and yield through inoculation of rhizobacteria and phosphate solubilizing bacteria coated diammonium phosphate. Sustainability 12(24):1–14. https://doi.org/10.3390/su122410456

    Article  CAS  Google Scholar 

  • Malviya MK, Li C-N, Solanki MK, Singh RK, Htun R, Singh P, Verma KK, Yang LT, Li YR (2020) Comparative analysis of sugarcane root transcriptome in response to the plant growth-promoting Burkholderia anthina MYSP113. PLoS ONE 15(4):e0231206. https://doi.org/10.1371/journal.pone.0231206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mashabela MD, Piater LA, Dubery IA, Tugizimana F, Mhlongo MI (2022) Rhizosphere tripartite interactions and PGPR-mediated metabolic reprogramming towards ISR and plant priming: a metabolomics review. Biology 11:346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meena M, Swapnil P, Divyanshu K, Kumar S, Tripathi YN, Zehra A, Marwal A, Upadhyay RS (2020) PGPR-mediated induction of systemic resistance and physiochemical alterations in plants against the pathogens: current perspectives. J Basic Microbiol 60:828–861

    CAS  PubMed  Google Scholar 

  • Mohanty S, Swain CK (2018) Role of microbes in climate smart agriculture. In: Panpatte D, Jhala Y, Shelat H, Vyas R (eds) Microorganisms for green revolution. Microorganisms for sustainability 7. Springer, Singapore. https://doi.org/10.3389/fsufs.2021.667150

    Chapter  Google Scholar 

  • Mohanty P, Singh PK, Chakraborty D, Mishra S, Pattnaik R (2021) Insight into the role of PGPR in sustainable agriculture and environment. Front Sustain Food Syst 5:667150. https://doi.org/10.3389/fsufs.2021.667150

    Article  Google Scholar 

  • Molina-Romero D, Juárez-Sánchez S, Venegas B, Ortíz-González CS, Baez A, Morales-García YE, Muñoz-Rojas J (2021) A bacterial consortium interacts with different varieties of maize, promotes the plant growth, and reduces the application of chemical fertilizer under field conditions. Front Sustain Food Syst 4:616757. https://doi.org/10.3389/fsufs.2020.616757

    Article  Google Scholar 

  • Mondani F, Khani K, Honarmand SJ, Saeidi M (2019) Evaluating effects of plant growth-promoting rhizobacteria on the radiation use efficiency and yield of soybean (Glycine max) under water deficit stress condition. Agric Water Management 213:707–713. https://doi.org/10.1016/j.agwat.2018.11.004

    Article  Google Scholar 

  • Mufti R, Bano A (2019) PGPR-induced defense responses in the soybean plant against charcoal rot disease. Eur J Plant Pathol 155:983–1000. https://doi.org/10.1007/s10658-019-01828-6

    Article  CAS  Google Scholar 

  • Muscolo A, Panuccio M, Zahir Z, Mahmood S, Nadeem S (2019) Use of plant growth-promoting rhizobacteria to ameliorate the performance of lentil under salinity. J Appl Bot Food Qual. https://doi.org/10.5073/JABFQ.2019.092.024

    Article  Google Scholar 

  • Mussa A, Million T, Assefa F (2018) Rhizospheric bacterial isolates of grass pea (Lathyrus sativus L.) endowed with multiple plant growth promoting traits. J Appl Microbiol 125:1786–1801. https://doi.org/10.1111/jam.13942

    Article  CAS  Google Scholar 

  • Mutumba F, Zagal E, Gerding M, Castillo D, Paulino L, Schoebitz M (2018) Plant growth promoting rhizobacteria for improved water stress tolerance in wheat genotypes. J Soil Sci Plant Nutri 18(4):1080–1096. https://doi.org/10.4067/S0718-95162018005003003

    Article  CAS  Google Scholar 

  • Naeem M, Aslam Z, Khaliq A, Ahmed JN, Nawaz A, Hussain M (2018) Plant growth promoting rhizobacteria reduce aphid population and enhance the productivity of bread wheat. Braz J Microbiol 49(Suppl 1):9–14. https://doi.org/10.1016/j.bjm.2017.10.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagrale D, Gawande S, Shah V, Verma P, Hiremani N, Prabhulinga T, Gokte-Narkhedkar N, Waghmare V (2022) Biocontrol potential of volatile organic compounds (VOCs) produced by cotton endophytic rhizobacteria against Macrophomina phaseolina. Eur J Plant Pathol 163(2):467–482. https://doi.org/10.1007/s10658-022-02503-z

    Article  CAS  Google Scholar 

  • Nakade D (2020) Biodiversity and plant growth promoting potential of bacteria from soybean rhizosphere of saline soil. Am J Agric for 8:77. https://doi.org/10.11648/j.ajaf.20200803.14

    Article  Google Scholar 

  • 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(12):1009–1022. https://doi.org/10.1002/jobm.201800309

    Article  CAS  PubMed  Google Scholar 

  • Nawaz A, Shahbaz M, Asadullah IA, Marghoob MU, Imtiaz M, Mubeen F (2020) Potential of salt tolerant PGPR in growth and yield augmentation of wheat (Triticum aestivum L.) under saline conditions. Front Microbiol 11:2019. https://doi.org/10.3389/fmicb.2020.02019

    Article  PubMed  PubMed Central  Google Scholar 

  • Nazir U, Zargar MY, Baba ZA, Mir SA, Mohiddin FA, Bhat NA (2020) Isolation and characterization of plant growth promoting rhizobacteria associated with pea rhizosphere in North Himalayan region. Int J Chem Stud 8(1):1131–1135

    Article  CAS  Google Scholar 

  • Nihayati E, Roviq M, Lintang CW (2019) Improvement of mungbean (Vigna radiata L.) yield through supplementing the plant growth-promoting rhizobacter (PGPR) and mycorriza. Eurasia J Biosci 13:2065–2070

    CAS  Google Scholar 

  • Nosheen A, Bano A, Naz R, Yasmin H, Hussain I, Ullah F, Keyani R, Hassan MN, Tahir AT (2019) Nutritional value of Sesamum indicum L. was improved by Azospirillum and Azotobacter under low input of NP fertilizers. BMC Plant Biol 19(1):466. https://doi.org/10.1186/s12870-019-2077-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omara AED, El-Din M, Hauka F, Hafez A, El-Nahrawy S, Ghazi A, Elsakhawy T, Fusco V (2018) Suppression of Rhizoctonia solani damping-off in soybean (Glycine max L.) by plant growth promoting rhizobacteria strains. Environ Biodiver Soil Secu 2:210–220. https://doi.org/10.21608/jenvbs.2018.3231.1024

    Article  Google Scholar 

  • Osman N, Yin SX (2018) Isolation and characterization of pea plant (Pisum sativum L.) growth-promoting rhizobacteria. African J Microbiol Res 12:820–828. https://doi.org/10.5897/AJMR2018.8859

    Article  CAS  Google Scholar 

  • Pal AK, Mandal S, Sengupta C (2019) Exploitation of IAA producing PGPR on mustard (Brassica nigra L.) seedling growth under cadmium stress condition in comparison with exogenous IAA application. Plant Sci Today 6(1):22–30. https://doi.org/10.14719/pst.2019.6.1.440

    Article  CAS  Google Scholar 

  • Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop Improvement by exploiting physio-morphological traits. Front Plant Sci 8:537

    Article  PubMed  PubMed Central  Google Scholar 

  • Park S, Kim AL, Hong YK, Shin JH, Joo SH (2021) A highly efficient auxin-producing bacterial strain and its effect on plant growth. J Genet Eng Biotechnol 19(1):179. https://doi.org/10.1186/s43141-021-00252-w

    Article  PubMed  PubMed Central  Google Scholar 

  • Patel TM, Minocheherhomji FP (2019) Multitrait PGPRs as potential inoculants for cotton plant. Int J Adv Res 7(8):694–701. https://doi.org/10.21474/IJAR01/9550

    Article  CAS  Google Scholar 

  • Patel P, Shah R, Modi K (2017) Isolation and characterization of plant growth promoting potential of Acinetobacter sp. RSC7 isolated from Saccharum officinarum cultivar Co 671. J Exp Bio Agric Sci 5:483–491. https://doi.org/10.18006/2017.5(4).483.491

    Article  CAS  Google Scholar 

  • Paungfoo-Lonhienne C, Watanarojanaporn N, Jaemsaeng R (2020) Plant growth promoting rhizobacteria enhance the efficiency of the combination of organic and chemical fertilisers in sugarcane. OJE 10:440–444

    Article  Google Scholar 

  • Pena RT, Blasco L, Ambroa A, González-Pedrajo B, Fernández-García L, López M, Bleriot I, Bou G, García-Contreras R, Wood TK, Tomás M (2019) Relationship between quorum sensing and secretion systems. Front Microbiol 10:1100. https://doi.org/10.3389/fmicb.2019.01100

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira SIA, Abreu D, Moreira H, Vega A, Castro PML (2020) Plant growth-promoting rhizobacteria (PGPR) improve the growth and nutrient use efficiency in maize (Zea mays L.) under water deficit conditions. Heliyon 6(10):e05106. https://doi.org/10.1016/j.heliyon.2020.e05106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez YM, Charest C, Dalpe Y, Seguin S, Wang X, Khanizadeh S (2016) Effect of inoculation with arbuscular mycorrhizal fungi on selected spring wheat lines. Sustain Agric Res 5(4):24–29

    Google Scholar 

  • Pérez-Montaño F, Jiménez-Guerrero I, Contreras Sánchez-Matamoros R, López-Baena FJ, Ollero FJ, Rodríguez-Carvajal MA, Bellogín RA, Espuny MR (2013) Rice and bean AHL-mimic quorum-sensing signals specifically interfere with the capacity to form biofilms by plant-associated bacteria. Res Microbiol 164(7):749–760. https://doi.org/10.1016/j.resmic.2013.04.001

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LCA (1998) Novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Ton J, Van Pelt JA, Van Loon LC (2002) Signalling in rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biol 4:535–544

    Article  CAS  Google Scholar 

  • Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Ann Rev Phytopathol 52:347–375. https://doi.org/10.1146/annurev-phyto-082712-102340

    Article  CAS  Google Scholar 

  • Pirttilä AM, Mohammad Parast Tabas H, Baruah N, Koskimäki JJ (2021) Biofertilizers and biocontrol agents for agriculture: how to identify and develop new potent microbial strains and traits. Microorganisms 9:817. https://doi.org/10.3390/microorganisms9040817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qureshi MA, Ali MA, Mujeeb F, Ahmad MJ, Rashid S, Ullah S, Anjum MA (2017) Yield and quality response of cotton to a consortium of PGPR at graded fertilizer levels. Int J Biosci 10(3):46–53. https://doi.org/10.12692/ijb/10.3.46-53

    Article  Google Scholar 

  • Raffa CM, Chiampo F (2021) Bioremediation of agricultural soils polluted with pesticides: a review. Bioengineering 8:92. https://doi.org/10.3390/bioengineering8070092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajendran SK, Sundaram L (2020) Degradation of heavy metal contaminated soil using plant growth promoting rhizobacteria (PGPR): assess their remediation potential and growth influence of Vigna radiate L. Int J Agric Technol 16(2):365–376

    CAS  Google Scholar 

  • Rajesh K, Tamilselvan N, Sasikala E (2019) Effect of indole acetic acid (IAA) produced Rhizobium species on groundnut and black gram seed germination. Int Res J Pharmaceu Biosci 5(2):1–9

    Google Scholar 

  • Rasheed MT, Naseer A, Hassan HF, Hayat R, Jilani G, Vaseer SG, Ali MB (2020) Isolation of nodule associated bacteria for promotion of lentil growth. Pakistan J Agric Res 33(1):170–179

    Google Scholar 

  • Razak MH, Brahim Z, Saud HM (2019) Effcets of inoculation of plant growth promoting rhizobacteria to minimize panicle grain shattering habit for increased yield of rice (Oryza sativa L.). African J Microbiol Res 13(13):256–263

    Article  CAS  Google Scholar 

  • Rocha I, Ma Y, Souza-Alonso P, Vosátka M, Freitas H, Oliveira RS (2019) Seed coating: a tool for delivering beneficial microbes to agricultural crops. Front Plant Sci 10:1357

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodrigues AA, Araújo MVF, Soares RS, Oliveira BFR, Ribeiro IDA, Sibov ST, Vieira JDG (2018) Isolation and prospection of diazotrophic rhizobacteria associated with sugarcane under organic management. An Acad Bras Cienc 90(4):3813–3829. https://doi.org/10.1590/0001-3765201820180319

    Article  CAS  PubMed  Google Scholar 

  • Romera FJ, García MJ, Lucena C, Martínez-Medina A, Aparicio MA, Ramos J, Alcántara E, Angulo M, Pérez-Vicente R (2019) Induced Systemic Resistance (ISR) and Fe deficiency responses in dicot plants. Front Plant Sci 10:287. https://doi.org/10.3389/fpls.2019.00287

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosier A, Medeiros FHV, Bais HP (2018) Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil 428:35–55. https://doi.org/10.1007/s11104-018-3679-5

    Article  CAS  Google Scholar 

  • Saberi Riseh R, Skorik YA, Thakur VK, Moradi PM, Tamanadar E, Noghabi SS (2021) Encapsulation of plant biocontrol bacteria with alginate as a main polymer material. Int J Mol Sci 22(20):11165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeed Q, Xiukang W, Haider FU, Kučerik J, Mumtaz MZ, Holatko J, Naseem M, Kintl A, Ejaz M, Naveed M, Brtnicky M, Mustafa A (2021) Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int J Mol Sci 22(19):10529. https://doi.org/10.3390/ijms221910529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Safni I, Antastia W (2020) In vitro antagonism of five rhizobacterial species against Athelia rolfsii collar rot disease in soybean. Open Agric 3(1):264–272

    Article  Google Scholar 

  • Samaras A, Nikolaidis M, Antequera-Gómez ML, Cámara-Almirón J, Romero D, Moschakis T, Amoutzias GD, Karaoglanidis GS (2021) Whole genome sequencing and root colonization studies reveal novel insights in the biocontrol potential and growth promotion by Bacillus subtilis MBI 600 on cucumber. Front Microbiol 11:600393. https://doi.org/10.3389/fmicb.2020.600393

    Article  PubMed  PubMed Central  Google Scholar 

  • Santos RM, Kandasamy S, Rigobelo EC (2018) Sugarcane growth and nutrition levels are differentially affected by the application of PGPR and cane waste. Microbiol Open 7(6):e00617. https://doi.org/10.1002/mbo3.617

    Article  CAS  Google Scholar 

  • Sarkar J, Chakraborty B, Chakraborty U (2018) Plant growth promoting rhizobacteria protect wheat plants against temperature stress through antioxidant signalling and reducing chloroplast and membrane injury. J Plant Growth Regul 37:1396–1412. https://doi.org/10.1007/s00344-018-9789-8

    Article  CAS  Google Scholar 

  • Sayyed RZ, Seifi S, Patel PR, Shaikh SS, Jadhav HP, El Enshasy H (2019) Siderophore production in groundnut rhizosphere isolate, Achromobacter sp. RZS2 influenced by physicochemical factors and metal ions. Environ Sustain 2:117–124

    Article  CAS  Google Scholar 

  • Sebihi FZ, Saoudi M, Derouiche F, Bendjemana K, Benguedouar A, Benhizia Y, Sanchez J (2020) Effect of PGPR inoculation on durum wheat growth varieties. Asian J Microbiol Biotech Env Sci 22(4):676–684

    Google Scholar 

  • Senghor LA, Ortega-Beltran A, Atehnkeng J, Callicott K, Cotty P, Bandyopadhyay R (2020) The atoxigenic biocontrol product Aflasafe SN01 is a valuable tool to mitigate aflatoxin contamination of both maize and groundnut cultivated in Senegal. Plant Dis 104:510–520

    Article  CAS  PubMed  Google Scholar 

  • Sepúlveda-Caamaño M, Gerding M, Vargas M, Moya-Elizondo E, Oyarzúa P, Campos J (2018) Lentil (Lens culinaris L.) growth promoting rhizobacteria and their effect on nodulation in coinoculation with rhizobia. Archi Agro Soil Sci 64(2):244–256. https://doi.org/10.1080/03650340.2017.1342034

    Article  CAS  Google Scholar 

  • Shafique M, Elahi NN, Rashid M, Farooq A, Shah KH (2019) Application of PGPR enhances development and nodulation of Vigna radiata L. grown under salt stress. Sarhad J Agric 35(3):763–769

    Google Scholar 

  • Shah A, Nazari M, Antar M, Msimbira LA, Naamala J, Lyu D, Rabileh M, Zajonc J, Smith DL (2021) PGPR in agriculture: a sustainable approach to increasing climate change resilience. Front Sustain Food Syst 5:667546. https://doi.org/10.3389/fsufs.2021.667546

    Article  Google Scholar 

  • Sharma IP, Chandra S, Kumar N, Chandra D (2017) PGPR: Heart of soil and their role in soil fertility. Agic Important Microbes Sustain Agric. https://doi.org/10.1007/978-981-10-5589-8_3

    Article  Google Scholar 

  • Shayanthan A, Ordoñez PAC, Oresnik IJ (2022) The Role of Synthetic Microbial Communities (SynCom) in sustainable agriculture. Front Agron 4:896307

    Article  Google Scholar 

  • Shultana R, Zuan ATK, Yusop MR, Saud HM, Fatai A (2020) Effect of salt-tolerant bacterial inoculations on rice seedlings differing in salt-tolerance under saline soil conditions. Agronomy 10(7):1030. https://doi.org/10.3390/agronomy10071030

    Article  CAS  Google Scholar 

  • Sibponkrung S (2018) Determinants derived from PGPR capable of increasing soybean and mung bean production via Bradyrhizobium inoculation. A thesis Submitted in partial fulfillment of the requirements for the Degree of Doctor of Philosophy in Biotechnology Suranaree University of Technology, Thailand

  • Singh I (2018) Plant Growth Promoting Rhizobacteria (PGPR) and their various mechanisms for plant growth enhancement in stressful conditions: a review. European J Biol Res 8(4):191–213

    CAS  Google Scholar 

  • Singh K, Rani A, Padder S, Gera R (2017) Plant growth promoting (PGP) attributes of stress tolerant rhizobial isolates from root nodules of pigeon pea [Cajanus cajan (L.) Millspaugh] growing in Haryana, India. Int J Curr Microbiol Appl Sci 6:461–473. https://doi.org/10.20546/ijcmas.2017.612.057

    Article  CAS  Google Scholar 

  • Singh N, Singh G, Aggarwal N, Khanna V (2018) Yield enhancement and phosphorus economy in lentil (Lens culinaris Medikus) with integrated use of phosphorus, Rhizobium and plant growth promoting rhizobacteria. J Plant Nutrition. https://doi.org/10.1080/01904167.2018.1425437

    Article  Google Scholar 

  • Singh BS, Gowtham HG, Murali M, Hariprasad P, Lakshmeesha TR, Narasimha Murthy K, Amrutesh KN, Niranjana SR (2019a) Plant growth promoting ability of ACC deaminase producing rhizobacteria native to Sunflower (Helianthus annuus L.). Biocatal Agric Biotechnol 18:101089. https://doi.org/10.1016/j.bcab.2019.101089

    Article  Google Scholar 

  • Singh S, Kumar V, Sidhu G, Datta S, Dhanjal DS, Koul B, Janeja HS, Singh J (2019b) Plant growth promoting rhizobacteria from heavy metal contaminated soil promote growth attributes of Pisum sativum L. Biocatal Agric Biotechnol 17:665–671. https://doi.org/10.1016/j.bcab.2019.01.035

    Article  Google Scholar 

  • Singh RK, Singh P, Li HB, Song QQ, Gup DJ, Solanki MK, Verma KK, Malviya MK, Song XP, Lakshmanan P, Yang LT, Li YR (2020a) Diversity of nitrogen-fixing rhizobacteria associated with sugarcane: a comprehensive study of plant-microbe interactions for growth enhancement in Saccharum spp. BMC Plant Biol 20:220. https://doi.org/10.1186/s12870-020-02400-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RK, Singh P, Li HB, Guo DJ, Song QQ, Yang LT, Malviya MK, Song XP, Li YR (2020b) Plant- PGPR interaction study of plant growth-promoting diazotrophs Kosakonia radicincitans BA1 and Stenotrophomonas maltophilia COA2 to enhance growth and stress-related gene expression in Saccharum spp. J Plant Interac 15(1):427–445. https://doi.org/10.1080/17429145.2020.1857857

    Article  CAS  Google Scholar 

  • Singh RK, Singh P, Li HB, Song QQ, Guo DJ, Solanki MK, Verma KK, Malviya MK, Song XP, Lakshmanan P, Yang LT, Li YR (2020c) Diversity of nitrogen-fixing rhizobacteria associated with sugarcane: a comprehensive study of plant-microbe interactions for growth enhancement in Saccharum spp. BMC Plant Biol 20:220. https://doi.org/10.1186/s12870-020-02400-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sood G, Kaushal R, Chauhan A, Gupta S (2018) Indigenous plant-growth-promoting rhizobacteria and chemical fertilisers: Impact on wheat (Triticum aestivum) productivity and soil properties in North Western Himalayan region. Crop Pasture Sci 69:460–468. https://doi.org/10.1071/CP18016

    Article  CAS  Google Scholar 

  • Sudana IM, Raka IGN, Pradnyawathi NLM (2020) Improvement of seed quality and stimulated the growth of brown rice with matriconditioning plus plant growth promoting rhizobacteria (PGPR) agents in Jatiluih Tourism. Int J Curr Microbiol App Sci 9(8):2788–2798. https://doi.org/10.20546/ijcmas.2020.908.314

    Article  CAS  Google Scholar 

  • Szopa D, Mielczarek M, Skrzypczak D, Izydorczyk G, Mikula K, Chojnacka K, Witek-Krowiak A (2022) Encapsulation efficiency and survival of plant growth-promoting microorganisms in an alginate-based matrix—a systematic review and protocol for a practical approach. Ind Crops Prod 181:114846

    Article  Google Scholar 

  • Trivedi P, Schenk PM, Wallenstein MD, Singh BK (2017) Tiny microbes, big yields: enhancing food crop production with biological solutions. Microb Biotechnol 10:999–1003

    Article  PubMed  PubMed Central  Google Scholar 

  • Ulfat N, Zargar MY, Baba ZA, Mir SA, Mohidin FA, Bhat NA (2020) Isolation and characterization of plant growth promoting rhizobacteria associated with pea rhizosphere in North Himalayan region. Int J Chem Stud 8(1):1131–1135. https://doi.org/10.22271/chemi.2020.v8.i1o.8401

    Article  CAS  Google Scholar 

  • Valette M, Rey M, Gerin F, Comte G, Wisniewski-Dyé F (2020) A common metabolomic signature is observed upon inoculation of rice roots with various rhizobacteria. J Integr Plant Biol 62:228–246

    Article  CAS  PubMed  Google Scholar 

  • Vorholt JA, Vogel C, Carlstrom CI, Muller DB (2017) Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22:142–155

    Article  CAS  PubMed  Google Scholar 

  • Wahid F, Fahad S, Danish S, Adnan M, Yue Z, Saud S, Siddiqui MH, Brtnicky M, Hammerschmiedt T, Datta R (2020) Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture 10:334

    Article  CAS  Google Scholar 

  • Wang K, Zhao Y, Wang X, Qu C, Miao J (2020) Complete genome sequence of Bacillus sp. N1–1, a kappa-selenocarrageenan degrading bacterium isolated from the cold seep in the South China Sea. Mar Genomics. https://doi.org/10.1016/j.margen.2020.100771

    Article  PubMed  Google Scholar 

  • Wang C, Li Y, Li M, Zhang K, Ma W, Zheng L, Xu H, Cui B, Liu R, Yang Y, Zhong Y, Liao H (2021) Functional assembly of root-associated microbial consortia improves nutrient efficiency and yield in soybean. J Integr Plant Biol 63(6):1021–1035

    Article  CAS  PubMed  Google Scholar 

  • Willsey T, Chatterton S, Cárcamo H (2017) Interactions of root-feeding insects with fungal and oomycete plant pathogens. Front Plant Sci 8:1764

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiang N, Lawrence KS, Kloepper JW, Donald PA, McInroy JA, Lawrence GW (2017a) Biological control of Meloidogyne incognita by spore-forming plant growth-promoting rhizobacteria on cotton. Plant Dis 101:774–784. https://doi.org/10.1094/PDIS-09-16-1369-RE

    Article  CAS  PubMed  Google Scholar 

  • Xiang N, Lawrence KS, Kloepper JW, Donald PA, McInroy JA (2017b) Biological control of Heterodera glycines by spore-forming plant growth-promoting rhizobacteria (PGPR) on soybean. PLoS ONE 12(7):e0181201. https://doi.org/10.1371/journal.pone.0181201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao AW, Li WC, Ye ZH (2020) The effect of plant growth-promoting rhizobacteria (PGPR) on arsenic accumulation and the growth of rice plants (Oryza sativa L.). Chemosphere 242:125136

    Article  CAS  Google Scholar 

  • Yasin NA, Khan WU, Ahmad SR, Ali A, Ahmad A, Akram W (2018) Imperative roles of halotolerant plant growth-promoting rhizobacteria and kinetin in improving salt tolerance and growth of black gram (Phaseolus mungo). Environ Sci Pollut Res Int 25(5):4491–4505. https://doi.org/10.1007/s11356-017-0761-0

    Article  CAS  PubMed  Google Scholar 

  • Yasmeen T, Ahmad A, Arif MS, Mubin M, Rehman K, Shahzad SM, Iqbal S, Rizwan M, Ali S, Alyemeni MN, Wijaya L (2020) Biofilm forming rhizobacteria enhance growth and salt tolerance in sunflower plants by stimulating antioxidant enzymes activity. Plant Physiol Biochem 156:242–256. https://doi.org/10.1016/j.plaphy.2020.09.016

    Article  CAS  PubMed  Google Scholar 

  • Yin C, Hagerty CH, Paulitz TC (2022) Synthetic microbial consortia derived from rhizosphere soil protect wheat against a soilborne fungal pathogen. Front Microbiol 13:908981

    Article  PubMed  PubMed Central  Google Scholar 

  • Yousaf S, Zohaib A, Anjum SA, Tabassum T, Abbas T, Irshad S, Javed U, Farooq N (2018) Effect of seed inoculation with plantgrowth promoting rhizobacteria on yield and quality of soybean. Pakistan J Agric Res 32(1):177–184

    Google Scholar 

  • Zafar-ul-Hye M, Danish S, Abbas M, Ahmad M, Munir TM (2019) ACC deaminase producing PGPR Bacillus amyloliquefaciens and Agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy 9:343

    Article  CAS  Google Scholar 

  • Zafar-ul-Hye M, Zahra MB, Danish S, Abbas M, Rehim A, Akbar MN, Iftikhar A, Gul M, Nazir I, Abid M, Tahzeeb-Ul-Hassan M, Murtaza M (2020) Multi-strain inoculation with pgpr producing acc deaminase is more effective than single-strain inoculation to improve wheat (Triticum aestivum) growth and yield. Phyton 89:405–413

    Article  Google Scholar 

  • Zain M, Yasmin S, Hafeez FY (2019) Isolation and characterization of plant growth promoting antagonistic bacteria from cotton and sugarcane plants for suppression of phytopathogenic Fusarium species. Iranian J Biotech 17(2):e1974. https://doi.org/10.21859/ijb.1974

    Article  Google Scholar 

  • Zainab N, Amna DBU, Javed MT, Afridi MS, Mukhtar T, Kamran MA, Ain QU, Khan AA, Ali J, Jatoi WN, Hussain Munis MF, Chaudhary HJ (2020) Deciphering metal toxicity responses of flax (Linum usitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils. Plant Physiol Biochem 152:90–99. https://doi.org/10.1016/j.plaphy.2020.04.039

    Article  CAS  PubMed  Google Scholar 

  • Zeffa DM, Fantin LH, Koltun A, de Oliveira ALM, Nunes MPBA, Canteri MG, Gonçalves LSA (2020) Effects of plant growth-promoting rhizobacteria on co-inoculation with Bradyrhizobium in soybean crop: a meta-analysis of studies from 1987 to 2018. PeerJ 8:e7905. https://doi.org/10.7717/peerj.7905

    Article  PubMed  PubMed Central  Google Scholar 

  • Zerrouk IZ, Rahmoune B, Khelifi L, Kherroubi M, Baluska F, Ludwig-Müller J (2019) Algerian Sahara PGPR confers maize root tolerance to salt and aluminum toxicity via ACC deaminase and IAA. Acta Physiol Plant 41:1–10. https://doi.org/10.1007/s11738-019-2881-2

    Article  CAS  Google Scholar 

  • Zhang Z, Yin L, Li X, Zhang C, Liu C, Wu Z (2018) The complete genome sequence of Bacillus halotolerans ZB201702 isolated from a drought- and salt-stressed rhizosphere soil. Microb Pathog 123:246–249. https://doi.org/10.1016/j.micpath.2018.07.019

    Article  CAS  PubMed  Google Scholar 

  • Zheng W, Zeng S, Bais H, LaManna J, Hussey D, Jacobson D, Jin Y (2018) Plant growth-promoting rhizobacteria (PGPR) reduce evaporation and increase soil water retention. Water Resour Res. https://doi.org/10.1029/2018WR022656

    Article  Google Scholar 

  • Zhou XG, Kumar KVK, Zhou LW, Reddy MS, Kloepper JW (2021) Combined use of PGPRs and reduced rates of azoxystrobin to improve management of sheath blight of rice. Plant Dis 105:1034–1041. https://doi.org/10.1094/PDIS-07-20-1596-RE

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Huang J, Lu X, Zhou C (2022) Development of plant systemic resistance by beneficial rhizobacteria: recognition, initiation, elicitation and regulation. Front Plant Sci 13:952397. https://doi.org/10.3389/fpls.2022.952397

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The Director, ICAR-CICR, Nagpur, Head, Division of Crop Protection, ICAR-CICR, Nagpur and Department of Biotechnology, Govt. of India for BIC project grant (BT/PR40161/BTIS/137/32/2021) are duly acknowledged.

Funding

Funding was provided under institute research project IXX12577 by ICAR-Central Institute for Cotton Research, Nagpur.

Author information

Authors and Affiliations

  1. ICAR-Central Institute for Cotton Research, Nagpur, Maharashtra, 440010, India

    D. T. Nagrale, S. P. Gawande, N. S. Hiremani, N. Gokte-Narkhedkar & Y. G. Prasad

  2. ICAR-Indian Institute of Vegetable Research, Varanasi, Uttar Pradesh, 221305, India

    A. Chaurasia

  3. Division of Agricultural Bioinformatics, ICAR-Indian Agricultural Statistics Research Institute, Library Avenue, Pusa, New Delhi, 110012, India

    S. Kumar

  4. ICAR-Indian Institute of Horticultural Research, Hessaraghatta Lake Post, Bengaluru, 560089, India

    Raja Shankar

  5. Indian Council of Agricultural Research, Krishi Bhawan, New Delhi, 110001, India

    Renu

Authors
  1. D. T. Nagrale
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Chaurasia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. P. Gawande
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. S. Hiremani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raja Shankar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. Gokte-Narkhedkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Renu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Y. G. Prasad
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DTN: Conceived the idea and wrote the manuscript. AC: Wrote biotechnology component, review and edited the manuscript. SK: Wrote bioinformatics component, review and edited the manuscript. SPG: Review and edited the manuscript. NSH: Review and edited the manuscript. RS: Review and edited the manuscript. NG-N: Review and edited manuscript. R: Wrote biotechnology component, review and edited the manuscript. YGP: Supervision in preparing the review article.

Corresponding authors

Correspondence to D. T. Nagrale or A. Chaurasia.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors declare that they have no conflict ofinterest.

Disclaimer

The mention of specific products, trade names, or manufacturersis intended only for accuracy, and should not be consideredas an endorsement, or otherwise, of that product.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nagrale, D.T., Chaurasia, A., Kumar, S. et al. PGPR: the treasure of multifarious beneficial microorganisms for nutrient mobilization, pest biocontrol and plant growth promotion in field crops. World J Microbiol Biotechnol 39, 100 (2023). https://doi.org/10.1007/s11274-023-03536-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-023-03536-0

Keywords

Search

Navigation