Korean Journal of Agricultural Science (농업과학연구)

Institute of Agricultural Science, CNU (충남대학교 농업과학연구소)
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Practical significance of plant growth-promoting rhizobacteria in sustainable agriculture: a review

  • Subhashini Wijeysingha (Department of Soil Science, Faculty of Agriculture, University of Ruhuna) ;
  • Buddhi C. Walpola (Department of Soil Science, Faculty of Agriculture, University of Ruhuna) ;
  • Yun-Gu Kang (Department of Bio-Environmental Chemistry, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Min-Ho Yoon (Department of Bio-Environmental Chemistry, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Taek-Keun Oh (Department of Bio-Environmental Chemistry, College of Agriculture and Life Sciences, Chungnam National University)
  • Received : 2023.07.27
  • Accepted : 2023.11.02
  • Published : 2023.12.01
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Abstract

Plant growth-promoting rhizobacteria (PGPR) are naturally occurring bacteria that intensively colonize plant roots and are crucial in promoting the crop growth. These beneficial microorganisms have garnered considerable attention as potential bio-inoculants for sustainable agriculture. PGPR directly interacts with plants by providing essential nutrients through nitrogen fixation and phosphate solubilization and accelerating the accessibility of other trace elements such as Cu, Zn, and Fe. Additionally, they produce plant growth-promoting phytohormones, such as indole acetic acids (IAA), indole butyric acids (IBA), gibberellins, and cytokinins.PGPR interacts with plants indirectly by protecting them from diseases and infections by producing antibiotics, siderophores, hydrogen cyanide, and fungal cell wall-degrading enzymes such as glucanases, chitinases, and proteases. Furthermore, PGPR protects plants against abiotic stresses such as drought and salinity by producing 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase and modulating plant stress markers. Bacteria belonging to genera such as Bacillus, Pseudomonas, Burkholderia, Pantoa, and Enterobacter exhibit multiple plant growth-promoting traits, that can enhance plant growth directly, indirectly, or through synergetic effects. This comprehensive review emphasizes how PGPR influences plant growth promotion and presents promising prospects for its application in sustainable agriculture.

Keywords

Acknowledgement

We are sincerely thankful to our advisor for their invaluable guidance throughout this research. We also extend my gratitude to the reviewers and editors in Korean Journal of Agricultural Science for their insightful feedback and valuable contributions. Their support and input have been instrumental in shaping and improving this work.

References

  1. Abbaszadeh-Dahaji P, Masalehi F, Akhgar A. 2020. Improved growth and nutrition of sorghum (Sorghum bicolor) plants in a low-fertility calcareous soil treated with plant growth-promoting rhizobacteria and Fe-EDTA. Journal of Soil Science and Plant Nutrition 20:31-42. 
  2. Abd El‑Mageed TA, Abd El‑Mageed SA, El‑Saadony MT, Abdelaziz S, Abdou NM. 2022. Plant growth‑promoting rhizobacteria improve growth, morph‑physiological responses, water productivity, and yield of rice plants under full and deficit drip irrigation. Rice 15:16. 
  3. Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University-Science 26:1-20. 
  4. Al-Wasify RS, Aboelwafa AM. 2009. Biodegradation of crude oil using local isolates. Australian Journal of Basic and Applied Sciences 3:4742-4751 
  5. Alori ET, Glick BR, Babalola OO. 2017. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Frontiers in Microbiology 8:971. 
  6. Amna, Xia Y, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, Tabassum T, Rehman SU, Munis MFH, et al. 2020. Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiology and Biochemistry 151:640-649. 
  7. Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL. 2018. Plant growth-promoting rhizobacteria: Context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers in Plant Science 9:1473. 
  8. Bahadou SA, Ouijja A, Karfach A, Tahiri A, Lahlali R. 2018. New potential bacterial antagonists for the biocontrol of fire blight disease (Erwinia amylovora) in Morocco. Microbial Pathogenesis 117:7-15. 
  9. Bennis M, Perez-Tapia V, Alami S, Bouhnik O, Lamin H, Abdelmoumen H, Bedmar EJ, El Idrissi MM. 2022. Characterization of plant growth-promoting bacteria isolated from the rhizosphere of Robinia pseudoacacia growing in metal-contaminated mine tailings in Eastern Morocco. Journal of Environmental Management 304:114321. 
  10. Bhatt MK, Labanya R, Joshi HC. 2019. Influence of long-term chemical fertilizers and organic manures on soil fertility-A review. Universal Journal of Agricultural Research 7:177-188. 
  11. Bhattacharyya PN, Jha DK. 2012. Plant growth-promoting rhizobacteria (PGPR): Emergence in agriculture. World Journal of Microbiology and Biotechnology 28:1327-1350. 
  12. Boukerma L, Benchabane M, Charif A, Khelifi L. 2017. Activity of plant growth promoting rhizobacteria (PGPRs) in the biocontrol of tomato Fusarium wilt. Plant Protection Science 53:78-84. 
  13. Breedt G, Labuschagne N, Coutinho TA. 2017. Seed treatment with selected plant growth-promoting rhizobacteria increases maize yield in the field. Annals of Applied Biology 171:229-236. 
  14. Chen J, Zhao G, Wei Y, Dong Y, Hou L, Jiao R. 2021. Isolation and screening of multifunctional phosphate solubilizing bacteria and its growth-promoting effect on Chinese fir seedlings. Scientific Reports 11:9081. 
  15. Chu TN, Tran BTH, Van Bui L, Hoang MTT. 2019. Plant growth-promoting rhizobacterium Pseudomonas PS01 induces salt tolerance in Arabidopsis thaliana. BMC Research Notes 12:11. 
  16. Cohen AC, Travaglia CN, Bottini R, Piccoli PN. 2009. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize.Botany 87:455-462. 
  17. Costa-Gutierrez SB, Lami MJ, Santo MCCD, Zenoff AM, Vincent PA, Molina-Henares MA, Espinosa-Urgel M, de Cristobal RE. 2020. Plant growth promotion by Pseudomonas putida KT2440 under saline stress: Role of eptA. Applied Microbiology and Biotechnology 104:4577-4592. 
  18. Di Salvo LP, Cellucci GC, Carlino ME, de Salamone IEG. 2018. Plant growth-promoting rhizobacteria inoculation and nitrogen fertilization increase maize (Zea mays L.) grain yield and modified rhizosphere microbial communities. Applied Soil Ecology 126:113-120. 
  19. dos Santos RM, Diaz PAE, Lobo LLB, Rigobelo EC. 2020. Use of plant growth-promoting rhizobacteria in maize and sugarcane: Characteristics and applications. Frontiers in Sustainable Food Systems 4:136. 
  20. Duca D, Lorv J, Patten CL, Rose D, Glick BR. 2014. Indole-3-acetic acid in plant-microbe interactions. Antonie Van Leeuwenhoek 106:85-125. 
  21. Ejaz M, Zhao B, Wang X, Bashir S, Haider FU, Aslam Z, Khan MI, Shabaan M, Naveed M, Mustafa A. 2021. Isolation and characterization of oil-degrading Enterobacter sp. from naturally hydrocarbon-contaminated soils and their potential use against the bioremediation of crude oil. Applied Sciences 11:3504. 
  22. FAO (Food and Agricultural Organization of the United Nations). 2023. Sustainable agricultural practices. Accessed in https://www.fao.org/agriculture/crops/thematic-sitemap/theme/spi/soil-biodiversity/agriculture-and-soil-biodiversity/sustainable-agricultural-practices/en/ on 30 October 2023. 
  23. Fernandez-San Millan A, Larraya L, Farran I, Ancin M, Veramendi J. 2021. Successful biocontrol of major postharvest and soil-borne plant pathogenic fungi by antagonistic yeasts. Biological Control 160:104683. 
  24. Figueiredo MDVB, Seldin L, Araujo FFD, Mariano RDLR. 2010. Plant growth promoting rhizobacteria: Fundamentals and applications. Plant Growth and Health Promoting Bacteria. pp. 21-43. Springer, Berlin, Heidelberg, Germany. 
  25. Gatiboni L, Brunetto G, Pavinato PS, George TS. 2020. Editorial: Legacy phosphorus in agriculture: Role of past management and perspectives for the future. Frontiers in Earth Science 8:619935. 
  26. Ghani MU, Asghar HN, Niaz A, Zahir ZA, Nawaz MF, Haggblom MM. 2022. Efficacy of rhizobacteria for degradation of profenofos and improvement in tomato growth. International Journal of Phytoremediation 24:463-473. 
  27. Glick BR. 2012. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica 2012:963401. 
  28. Gonzalez D, Blanco C, Probanza A, Jimenez PA, Robas M. 2021. Evaluation of the PGPR capacity of four bacterial strains and their mixtures, tested on Lupinus albus var. Dorado seedlings, for the bioremediation of mercury-polluted soils. Processes 9:1293. 
  29. Gopalakrishnan S, Srinivas V, Samineni S. 2017. Nitrogen fixation, plant growth and yield enhancements by diazotrophic growth-promoting bacteria in two cultivars of chickpea (Cicer arietinum L.). Biocatalysis and Agricultural Biotechnology 11:116-123. 
  30. Goswami D, Thakker JN, Dhandhukia PC. 2016. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food and Agriculture 2:1127500. 
  31. Guo Y, Ren C, Yi J, Doughty R, Zhao F. 2020. Contrasting responses of rhizosphere bacteria, fungi and arbuscular mycorrhizal fungi along an elevational gradient in a temperate montane forest of China. Frontiers in Microbiology 11:2042. 
  32. Gupta A, Bano A, Rai S, Kumar M, Ali J, Sharma S, Pathak N. 2021. ACC deaminase producing plant growth promoting rhizobacteria enhance salinity stress tolerance in Pisum sativum. 3 Biotech 11:514. 
  33. Hayat R, Ahmed I, Sheirdil RA. 2012. An overview of plant growth promoting rhizobacteria (PGPR) for sustainable agriculture. Crop Production for Agricultural Improvement. pp. 557-579. Springer, Dordrecht, Netherlands. 
  34. Hosseini A, Hosseini M, Schausberger P. 2021. Plant growth promoting rhizobacteria enhance defense of strawberry plants against spider mites. Frontiers in Plant Science 12:783578. 
  35. Islam S, Akanda AM, Prova A, Islam MT, Hossain MM. 2016. Isolation and identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Frontiers in Microbiology 6:1360. 
  36. Jha CK, Saraf M. 2015. Plant growth promoting rhizobacteria (PGPR): A review. E3 Journal of Agricultural Research and Development 5:108-119. 
  37. Kang SM, Khan AL, Waqas M, Asaf S, Lee KE, Park YG, Kim AY, Khan MA, You YH, Lee IJ. 2019. Integrated phytohormone production by the plant growth-promoting rhizobacterium Bacillus tequilensis SSB07 induced thermotolerance in soybean. Journal of Plant Interactions 14:416-423. 
  38. Khalid A, Arshad M, Zahir ZA. 2004. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. Journal of Applied Microbiology 96:473-480. 
  39. Khan A, Singh P, Srivastava A. 2018. Synthesis, nature and utility of universal iron chelator-Siderophore: A review. Microbiological Research 212-213:103-111. 
  40. Kramer J, Ozkaya O, Kummerli R. 2020. Bacterial siderophores in community and host interactions. Nature Reviews Microbiology 18:152-163. 
  41. Lahlali R, Mchachti O, Radouane N, Ezrari S, Belabess Z, Khayi S, Mentag R, Tahiri A, Barka EA. 2020. The potential of novel bacterial isolates from natural soil for the control of brown rot disease (Monilinia fructigena) on apple fruits. Agronomy 10:1814. 
  42. Lin S, Litaker RW, Sunda WG. 2016. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. Journal of Phycology 52:10-36. 
  43. Liu J, Zhang J, Zhu M, Wan H, Chen Z, Yang N, Duan J, Wei Z, Hu T, Liu F. 2022. Effects of plant growth promoting rhizobacteria (PGPR) strain Bacillus licheniformis with biochar amendment on potato growth and water use efficiency under reduced irrigation regime. Agronomy 12:1031. 
  44. Lobo LLB, dos Santos RM, Rigobelo EC. 2019. Promotion of maize growth using endophytic bacteria under greenhouse and field conditions. Australian Journal of Crop Science 13:2067-2074. 
  45. Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63:541-556. 
  46. Lyu D, Backer R, Smith DL. 2022. Three plant growth-promoting rhizobacteria alter morphological development, physiology, and flower yield of Cannabis sativa L. Industrial Crops and Products 178:114583. 
  47. Mansour E, Mahgoub HAM, Mahgoub SA, El-Sobky ESEA, Abdul-Hamid MI, Kamara MM, AbuQamar SF, El-Tarabily KA, Desoky ESM. 2021. Enhancement of drought tolerance in diverse Vicia faba cultivars by inoculation with plant growth-promoting rhizobacteria under newly reclaimed soil conditions. Scientific Reports 11:24142. 
  48. Martinez C, Espinosa-Ruiz A, Prat S. 2018. Gibberellins and plant vegetative growth. Annual Plant Reviews, Volume 49. In The gibberellins edited by Hedden P, Thomas SG. pp. 285-322. John Wiley & Sons Ltd., New Jersey, USA. 
  49. Miransari M. 2014. Plant growth promoting rhizobacteria. Journal of Plant Nutrition 37:2227-2235. 
  50. Nandini B, Puttaswamy H, Saini RK, Prakash HS, Geetha N. 2021. Trichovariability in rhizosphere soil samples and their biocontrol potential against downy mildew pathogen in pearl millet. Scientific Reports 11:9517. 
  51. Nosheen A, Bano A. 2014. Potential of plant growth promoting rhizobacteria and chemical fertilizers on soil enzymes and plant growth. Pakistan Journal of Botany 46:1521-1530. 
  52. Numan M, Bashir S, Khan Y, Mumtaz R, Shinwari ZK, Khan AL, Khan A, Al-Harrasi A. 2018. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: A review. Microbiological Research 209:21-32. 
  53. O'Brien JA, Benkova E. 2013. Cytokinin cross-talking during biotic and abiotic stress responses. Frontiers in Plant Science 4:451. 
  54. Omara A, Hauka F, Afify A, Nour El-Din M, Kassem M. 2017. The role of some PGPR strains to biocontrol Rhizoctonia solani in soybean and enhancement the growth dynamics and seed yield. Environment. Biodiversity and Soil Security 1:47-59. 
  55. Pappas ML, Samaras K, Koufakis I, Broufas GD. 2021. Beneficial soil microbes negatively affect spider mites and aphids in pepper. Agronomy 11:1831. 
  56. Patel PR, Shaikh SS, Sayyed RZ. 2016. Dynamism of PGPR in bioremediation and plant growth promotion in heavy metal contaminated soil. Indian Journal of Experimental Biology 54:286-290. 
  57. Patel T, Saraf M. 2017. Biosynthesis of phytohormones from novel rhizobacterial isolates and their in vitro plant growth-promoting efficacy. Journal of Plant Interactions 12:480-487. 
  58. Perez-Montano F, Alias-Villegas C, Bellogin RA, del Cerro P, Espuny MR, Jimenez-Guerrero I, Lopez-Baena FJ, Ollero FJ, Cubo T. 2014. Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production. Microbiological Research 169:325-336. 
  59. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P. 2011. Vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. The Plant Cell 23:550-566. 
  60. Pinter IF, Salomon MV, Berli F, Bottini R, Piccoli P. 2017. Characterization of the As (III) tolerance conferred by plant growth promoting rhizobacteria to in vitro-grown grapevine. Applied Soil Ecology 109:60-68. 
  61. Poupin MJ, Greve M, Carmona V, Pinedo I. 2016. A complex molecular interplay of auxin and ethylene signaling pathways is involved in Arabidopsis growth promotion by Burkholderia phytofirmans PsJN. Frontiers in Plant Science 7:492. 
  62. Qiao J, Yu X, Liang X, Liu Y, Borriss R, Liu Y. 2017. Addition of plant-growth-promoting Bacillus subtilis PTS-394 on tomato rhizosphere has no durable impact on composition of root microbiome. BMC Microbiology 17:131. 
  63. Radhakrishnan R, Hashem A, Abd_Allah EF. 2017. Bacillus: A biological tool for crop improvement through biomolecular changes in adverse environments. Frontiers in Physiology 8:667. 
  64. Rani R, Kumar V, Gupta P, Chandra A. 2021. Potential use of Solanum lycopersicum and plant growth promoting rhizobacterial (PGPR) strains for the phytoremediation of endosulfan stressed soil. Chemosphere 279:130589. 
  65. Rawat P, Das S, Shankhdhar D, Shankhdhar SC. 2021. Phosphate solubilizing microorganisms: Mechanism and their role in phosphate solubilization and uptake. Journal of Soil Science and Plant Nutrition 21:49-68. 
  66. Sagbara G, Zabbey N, Sam K, Nwipie GN. 2020. Heavy metal concentration in soil and maize (Zea mays L.) in partially reclaimed refuse dumpsite 'borrow-pit' in Port Harcourt, Nigeria. Environmental Technology & Innovation 18:100745. 
  67. Saharan BS, Nehra V. 2011. Plant growth promoting rhizobacteria: A critical review. Life Sciences and Medicine Research 21:1-30. 
  68. Saleem M, Asghar HN, Khan MY, Zahir ZA. 2015. Gibberellic acid in combination with pressmud enhances the growth of sunflower and stabilizes chromium (VI)-contaminated soil. Environmental Science and Pollution Research 22:10610-10617. 
  69. Schaller GE, Bishopp A, Kieber JJ. 2015. The yin-yang of hormones: cytokinin and auxin interactions in plant development. The Plant Cell 27:44-63. 
  70. Sekar S, Kandavel D. 2010. Interaction of plant growth promoting rhizobacteria (PGPR) and endophytes with medicinal plants-New avenues for phytochemicals. Journal of Phytology 2:91-100. 
  71. Singh JS. 2013. Plant growth promoting rhizobacteria. Resonance 18:275-281. 
  72. Song C, Wang W, Gan Y, Wang L, Chang X, Wang Y, Yang W. 2021. Growth promotion ability of phosphate-solubilizing bacteria from the soybean rhizosphere under maize-soybean intercropping systems. Journal of the Science of Food and Agriculture 102:1430-1442. 
  73. Sun G, Yao T, Feng C, Chen L, Li J, Wang L. 2017. Identification and biocontrol potential of antagonistic bacteria strains against Sclerotinia sclerotiorum and their growth-promoting effects on Brassica napus. Biological Control 104:35-43. 
  74. Tabassum B, Khan A, Tariq M, Ramzan M, Khan MSI, Shahid N, Aaliya K. 2017. Bottlenecks in commercialisation and future prospects of PGPR. Applied Soil Ecology 121:102-117. 
  75. Umer M, Mubeen M, Iftikhar Y, Shad MA, Usman HM, Sohail MA, Atiq MN, Abbas A, Ateeq M. 2021. Role of rhizobacteria on plants growth and biological control of plant diseases: A review. Plant Protection 5:59-73. 
  76. UN (United Nations). 2019. World population prospects 2019. Highlights. ST/ESA/SER.A/423. Accessed in https://www.un.org/en/desa on 17 August 2022. 
  77. Verma JP, Yadav J, Tiwari KN, Lavakush, Singh V. 2010. Impact of plant growth promoting rhizobacteria on crop production. International Journal of Agricultural Research 5:954-983. 
  78. Walpola BC, Arunakumara KKIU. 2015. Assessment of phosphate solubilization and indole acetic acid production in plant growth promoting bacteria isolated from green house soils of Gonju-Gun, South Korea. Tropical Agricultural Research and Extension 18:31-39. 
  79. Walpola BC, Yoon MH. 2012. Prospectus of phosphate solubilizing microorganisms and phosphorus availability in agricultural soils: A review. African Journal of Microbiology Research 6:6600-6605. 
  80. Wang Y, Zhang G, Huang Y, Guo M, Song J, Zhang T, Long Y, Wang B, Liu H. 2022. A potential biofertilizer-Siderophilic bacteria isolated from the rhizosphere ofParis polyphylla var.yunnanensis. Frontiers in Microbiology 13:870413. 
  81. Xu C, Lin P, Sun L, Chen H, Xing W, Kamalanathan M. 2020. Micolecular nature of marine particulate organic iron-carrying moieties revealed by electrospray ionization fourier transform ion cyclotron resonance mass spectrometry (ESI-FTICRMS). Frontiers in Earth Science 8:266. 
  82. Yu H, Wu X, Zhang G, Zhou F, Harvey PR, Wang L, Fan S, Xie X, Li F, Zhou H, Zhao X. 2022. Identification of the phosphorus solubilizing bacteria strain JP233 and its effects on soil phosphorus leaching loss and crop growth. Frontiers in Microbiology 13:892533-892533.