Abstract
Environmental stress affects food productivity by producing reactive oxygen species (ROS) that damage cell organelles and biomolecules, leading to apoptosis. Plants have developed a variety of defense responses over time to counteract the detrimental effects of biotic and abiotic stresses. However, in order to combat climate change and the deterioration of ecosystems, it will be necessary to promote the use of beneficial bacteria including plant growth-promoting bacteria (PGPR) in agricultural ecosystems. PGPR potentially improves nutrient absorption, modulates hormone levels, and/or improves tolerance to abiotic stress factors and plant pathogens. PGPR offers a sustainable replacement for conventional agrochemicals and traditional farming practices by improving plant growth and stress tolerance. In this context, studying the fundamental evolutionary and ecological relationships among plants and their microbiomes is necessary to build vital approaches to strengthen traditional agricultural techniques. Stress-tolerant PGPR can release bioactive substances such as gibberellins and indole acetic acid which participate in mitigating stresses. PGPR could minimize the adverse effect of salinity, drought, heavy metals, floods, and other stresses on plants by inducing antioxidant enzymes, like catalase, peroxidase, and superoxide dismutase. This review summarizes the current developments in the PGPR-based strategy for tackling biotic and abiotic stresses.
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References
Abbaszadeh-Dahaji P, Atajan FA, Omidvari M, Tahan V, Kariman K (2021) Mitigation of copper stress in maize (Zea mays) and Sunflower (Helianthus annuus) plants by copper-resistant Pseudomonas strains. Curr Microbiol 78(4):1335–1343. https://doi.org/10.1007/s00284-021-02408-w
Abdelkrim S, Jebara SH, Saadani O, Chiboub M, Abid G, Jebara M (2018) 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
Abdelkrim S, Jebara SH, Saadani O, Abid G, Taamalli W, Zemni H et al (2020) In situ effects of Lathyrus sativus- PGPR to remediate and restore quality and fertility of Pb and Cd polluted soils. Ecotoxicol Environ Saf 192:110260. https://doi.org/10.1016/j.ecoenv.2020.110260
Abulfaraj AA, Jalal RS (2021) Use of plant growth-promoting bacteria to enhance salinity stress in soybean (Glycine max L.) plants. Saudi J Biol Sci 28(7):3823–3834. https://doi.org/10.1016/j.sjbs.2021.03.053
Agake SI, do Plucani Amaral F, Yamada T, Sekimoto H, Stacey G, Yokoyama T, Ohkama-Ohtsu N (2022) Plant growth-promoting effects of viable and dead spores of Bacillus pumilus TUAT1 on Setaria viridis. Microbes Environ. https://doi.org/10.1264/jsme2.ME21060
Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29(1):29–34
Ahmad HM, Fiaz S, Hafeez S, Zahra S, Shah AN, Gul B, et al, (2022a) Plant growth-promoting rhizobacteria eliminate the effect of drought stress in plants: a review. Front Plant Sci 13:875774. https://doi.org/10.3389/fpls.2022.875774
Ahmad M, Imtiaz M, Shoib Nawaz M, Mubeen F, Imran A (2022b) What Did we learn from current progress in heat stress tolerance in plants? Can microbes be a solution? Front Plant Sci 13:794782. https://doi.org/10.3389/fpls.2022.794782
Albdaiwi RN, Khyami-Horani H, Ayad JY, Alananbeh KM, Al-Sayaydeh R (2019) Isolation and characterization of halotolerant plant growth promoting rhizobacteria from durum wheat (Triticum turgidum subsp. durum) cultivated in saline areas of the dead sea region. Front Microbiol 10:1639. https://doi.org/10.3389/fmicb.2019.01639
Alexander A, Singh VK, Mishra A (2020) Halotolerant PGPR Stenotrophomonas maltophilia BJ01 induces salt tolerance by modulating physiology and biochemical activities of Arachis hypogaea. Front Microbiol 11:568289. https://doi.org/10.3389/fmicb.2020.568289
Ali SZ, Sandhya V, Grover M, Linga VR, Bandi V (2011) Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J Plant Interact 6(4):239–246
Ali SZ, Sandhya V, Venkateswar Rao L (2014) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Annals Microbiol 64(2):493–502. https://doi.org/10.1007/s13213-013-0680-3
Ali B, Wang X, Saleem MH, Sumaira H et al (2022) PGPR-mediated salt tolerance in maize by modulating plant physiology, antioxidant defense compatible solutes accumulation and bio-surfactant producing genes. Plants (basel). https://doi.org/10.3390/plants11030345
Alves ARA, Yin Q, Oliveira RS, Silva EF, Novo LAB (2022) Plant growth-promoting bacteria in phytoremediation of metal-polluted soils: current knowledge and future directions. Sci Total Environ 838(4):156435. https://doi.org/10.1016/j.scitotenv.2022.156435
Amna, Xia Y, Farooq MA, Javed MT, Kamran MA, Mukhtar T et al (2020) Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol Biochem 151:640–649. https://doi.org/10.1016/j.plaphy.2020.04.016
Anarakdim K, Gutierrez G, Cambiella A, Senhadji-Kebiche O, Matos M (2020) The effect of emulsifiers on the emulsion stability and extraction efficiency of Cr(VI) Using emulsion liquid membranes (ELMs) formulated with a green solvent. Membranes (basel). https://doi.org/10.3390/membranes10040076
Ashraf A, Bano A, Ali SA (2019) Characterisation of plant growth-promoting rhizobacteria from rhizosphere soil of heat-stressed and unstressed wheat and their use as bio-inoculant. Plant Biol (stuttg) 21(4):762–769. https://doi.org/10.1111/plb.12972
Bano QUDSIA, Ilyas N, Bano A, Zafar NADIA, Akram ABIDA, Hassan F (2013) Effect of Azospirillum inoculation on maize (Zea mays L.) under drought stress. Pak J Bot 45(S1):13–20
Barazani OZ, Friedman J (1999) Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J Chem Ecol 25(10):2397–2406
Bziuk N, Maccario L, Straube B, Wehner G, Sorensen SJ, Schikora A, Smalla K (2021) The treasure inside barley seeds: microbial diversity and plant beneficial bacteria. Environ Microbiome 16(1):20. https://doi.org/10.1186/s40793-021-00389-8
Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45(1):28–35
Checcucci A, Azzarello E, Bazzicalupo M, De Carlo A, Emiliani G, Mancuso S et al (2017a) Role and regulation of ACC deaminase gene in Sinorhizobium meliloti: is It a symbiotic, rhizospheric or endophytic gene? Front Genet 8:6. https://doi.org/10.3389/fgene.2017.00006
Checcucci A, Bazzicalupo M, Mengoni A (2017b) Exploiting nitrogen-fixing rhizobial symbionts genetic resources for improving phytoremediation of contaminated soils. In: Anjum NA, Gill SS, Tuteja N (eds) Enhancing cleanup of environmental pollutants. Springer, Cham, pp 275–288
Chen H, Ji C, Hu H, Hu S, Yue S, Zhao M (2022) Bacterial community response to chronic heavy metal contamination in marine sediments of the East China Sea. Environ Pollut 307:119280. https://doi.org/10.1016/j.envpol.2022.119280
Cheng X, Yang B, Zheng J, Wei H, Feng X, Yin Y (2021) Cadmium stress triggers significant metabolic reprogramming in Enterococcus faecium CX 2–6. Comput Struct Biotechnol J 19:5678–5687. https://doi.org/10.1016/j.csbj.2021.10.021
Chennappa G, Adkar-Purushothama CR, Naik MK, Suraj U, Sreenivasa MY (2014) Impact of pesticides on PGPR activity of Azotobacter sp. isolated from pesticide flooded paddy soils. Greener J Agric Sci 4(4):117–129
Cura JA, Franz DR, Filosofia JE, Balestrasse KB, Burgueno LE (2017) Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms. https://doi.org/10.3390/microorganisms5030041
Das A, Osborne JW (2018) Monitoring the stress resistance of Pennisetum purpureum in Pb (II) contaminated soil bioaugmented with Enterobacter cloacae as defence strategy. Chemosphere 210:495–502. https://doi.org/10.1016/j.chemosphere.2018.07.050
Deng D, Sun S, Wu W, Duan C, Wang Z, Zhang S, Zhu Z (2022) Identification of causal agent inciting powdery mildew on common bean and screening of resistance cultivars. Plants (basel). https://doi.org/10.3390/plants11070874
Dias MP, Bastos MS, Xavier VB, Cassel E, Astarita LV, Santarem ER (2017) Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiol Biochem 118:479–493. https://doi.org/10.1016/j.plaphy.2017.07.017
Ding LN, Liu R, Li T, Li M, Liu XY, Wang WJ et al (2022) Physiological and comparative transcriptome analyses reveal the mechanisms underlying waterlogging tolerance in a rapeseed anthocyanin-more mutant. Biotechnol Biofuels Bioprod 15(1):55. https://doi.org/10.1186/s13068-022-02155-5
Duan J, Müller KM, Charles TC, Vesely S, Glick BR (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from southern Saskatchewan. Microb Ecol 57(3):423–436
El-Esawi MA, Alaraidh IA, Alsahli AA, Alzahrani SM, Ali HM, Alayafi AA, Ahmad M (2018) Serratia liquefaciens KM4 improves salt stress tolerance in maize by regulating redox potential, ion homeostasis, leaf gas exchange and stress-related gene expression. Int J Mol Sci. https://doi.org/10.3390/ijms19113310
El-Shamy MA, Alshaal T, Mohamed HH, Rady AMS, Hafez EM, Alsohim AS, Abd El-Moneim D (2022) Quinoa response to application of Phosphogypsum and plant growth-promoting rhizobacteria under water stress associated with salt-affected soil. Plants (basel). https://doi.org/10.3390/plants11070872
Etesami H, Mirseyed Hosseini H, Alikhani HA (2014) Bacterial biosynthesis of 1-aminocyclopropane-1-caboxylate (ACC) deaminase, a useful trait to elongation and endophytic colonization of the roots of rice under constant flooded conditions. Physiol Mol Biol Plants 20(4):425–434
Ferreira CM, Vilas-Boas Â, Sousa CA, Soares HM, Soares EV (2019) Comparison of five bacterial strains producing siderophores with ability to chelate iron under alkaline conditions. AMB Express 9(1):1–12
Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant Soil 410(1):335–356
Gao Y, Han Y, Li X, Li M, Wang C, Li Z et al (2022) A salt-tolerant Streptomyces paradoxus D2–8 from rhizosphere soil of Phragmites communis Augments Soybean Tolerance to Soda Saline-Alkali Stress. Pol J Microbiol 71(1):43–53. https://doi.org/10.33073/pjm-2022-006
Ghosh PG, Sawant NA, Patil SN, Aglave BA (2010) Microbial biodegradation of organophosphate pesticides. Int J Biotechnol Biochem 6(6):871–877
Ghosh D, Gupta A, Mohapatra S (2019) Dynamics of endogenous hormone regulation in plants by phytohormone secreting rhizobacteria under water-stress. Symbiosis 77(3):265–278. https://doi.org/10.1007/s13199-018-00589-w
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39
Grosskinsky DK, Tafner R, Moreno MV, Stenglein SA, Garcia de Salamone IE, Nelson LM et al (2016) Cytokinin production by Pseudomonas fluorescens G20–18 determines biocontrol activity against Pseudomonas syringae in Arabidopsis. Sci Rep. https://doi.org/10.1038/srep23310
Gupta A, Bano A, Rai S, Kumar M, Ali J, Sharma S, Pathak N (2021a) ACC deaminase producing plant growth promoting rhizobacteria enhance salinity stress tolerance in Pisum sativum. 3 Biotech 11(12):514. https://doi.org/10.1007/s13205-021-03047-5
Gupta S, Kaushal R, Sood G, Bhardwaj S, Chauhan A (2021b) Indigenous plant growth promoting rhizobacteria and chemical fertilizers: impact on soil health and productivity of Capsicum (Capsicum annuum L.) in North Western Himalayan region. Commun Soil Sci Plant Anal 52(9):948–963
Hamid B, Zaman M, Farooq S, Fatima S, Sayyed RZ, Baba ZA, Sheikh TA, Reddy MS, El Enshasy H, Gafur A, Suriani NL (2021) Bacterial plant biostimulants: a sustainable way towards improving growth, productivity, and health of crops. Sustainability 13:2856. https://doi.org/10.3390/su13052856
Horstmann JL, Dias MP, Ortolan F, Medina-Silva R, Astarita LV, Santarem ER (2020) Streptomyces sp. CLV45 from Fabaceae rhizosphere benefits growth of soybean plants. Braz J Microbiol 51(4):1861–1871. https://doi.org/10.1007/s42770-020-00301-5
Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 40(12):1019–1025
Jangra M, Devi S, Satpal Kumar N, Goyal V, Mehrotra S (2022) Amelioration effect of salicylic acid under salt stress in Sorghum bicolor L. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-022-03853-4
Jasrotia S, Salgotra RK, Sharma M (2021) Efficacy of bioinoculants to control of bacterial and fungal diseases of rice (Oryza sativa L.) in northwestern Himalaya. Braz J Microbiol 52(2):687–704. https://doi.org/10.1007/s42770-021-00442-1
Kamran MA, Eqani S, Bibi S, Xu RK et al (2016) Bioaccumulation of nickel by E. sativa and role of plant growth promoting rhizobacteria (PGPRs) under nickel stress. Ecotoxicol Environ Saf 126:256–263. https://doi.org/10.1016/j.ecoenv.2016.01.002
Kang JP, Huo Y, Yang DU, Yang DC (2021) Influence of the plant growth promoting Rhizobium panacihumi on aluminum resistance in Panax ginseng. J Ginseng Res 45(3):442–449. https://doi.org/10.1016/j.jgr.2020.01.001
Kantharaj V, Ramasamy NK, Yoon YE, Cheong MS, Kim YN, Lee KA et al (2021) Auxin-glucose conjugation protects the rice (Oryza sativa L.) seedlings against hydroxyurea-induced phytotoxicity by activating UDP-glucosyltransferase enzyme. Front Plant Sci 12:767044. https://doi.org/10.3389/fpls.2021.767044
Kapadia C, Patel N, Rana A, Vaidya H, Alfarraj S, Ansari MJ et al (2022) Evaluation of plant growth-promoting and salinity ameliorating potential of halophilic bacteria isolated from saline soil. Front Plant Sci 13:946217. https://doi.org/10.3389/fpls.2022.946217
Karadeniz A, Topcuoğlu ŞF, İnan S (2006) Auxin, gibberellin, cytokinin and abscisic acid production in some bacteria. World J Microbiol Biotechnol 22(10):1061–1064. https://doi.org/10.1007/s11274-005-4561-1
Karnwal A (2020) Effect of halotolerant plant growth-promoting rhizobacteria from Bougainvillea glabra on wheat and maize seedlings under NaCl stress. Biotechnologia 101(4):349–359. https://doi.org/10.5114/bta.2020.100426
Karnwal A, Dohroo A (2018) Effect of maize root exudates on indole-3-acetic acid production by rice endophytic bacteria under influence of L-tryptophan. F1000Res 7:112. https://doi.org/10.12688/f1000research.13644.1
Kaur J, Sharma J (2021) Orchid root associated bacteria: linchpins or accessories? Front Plant Sci 12:661966. https://doi.org/10.3389/fpls.2021.661966
Khalifa T, Elbagory M, Omara AE (2021) Salt stress amelioration in maize plants through phosphogypsum application and bacterial inoculation. Plants (basel). https://doi.org/10.3390/plants10102024
Khan A, Singh AV (2021) Multifarious effect of ACC deaminase and EPS producing Pseudomonas sp. and Serratia marcescens to augment drought stress tolerance and nutrient status of wheat. World J Microbiol Biotechnol 37(12):198. https://doi.org/10.1007/s11274-021-03166-4
Khumairah FH, Setiawati MR, Fitriatin BN, Simarmata T, Alfaraj S, Ansari et al (2022) Halotolerant plant growth-promoting rhizobacteria isolated from saline soil improve nitrogen fixation and alleviate salt stress in rice plants. Front Microbiol 13:905210. https://doi.org/10.3389/fmicb.2022.905210
Kuan KB, Othman R, Abdul Rahim K, Shamsuddin ZH (2016) Plant growth-promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilisation of maize under greenhouse conditions. PLoS ONE 11(3):e0152478. https://doi.org/10.1371/journal.pone.0152478
Kumar A, Verma JP (2018) Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52
Kumar P, Thakur S, Dhingra GK, Singh A, Pal MK, Harshvardhan K et al (2018) Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatal Agric Biotechnol 15:264–269
Kumar A, Devi S, Agrawal H, Singh S, Singh J (2020) Rhizoremediation: a unique plant microbiome association of biodegradation. In: Varma A, Tripathi S, Prasad R (eds) Plant microbe symbiosis. Springer, Cham, pp 203–220
Lade SB, Roman C, Cueto-Ginzo AI, Serrano L, Sin E, Achon MA, Medina V (2018) Host-specific proteomic and growth analysis of maize and tomato seedlings inoculated with Azospirillum brasilense Sp7. Plant Physiol Biochem 129:381–393. https://doi.org/10.1016/j.plaphy.2018.06.024
Lalay G, Ullah S, Ahmed I (2022) Physiological and biochemical responses of Brassica napus L. to drought-induced stress by the application of biochar and plant growth promoting rhizobacteria. Microsc Res Tech 85(4):1267–1281. https://doi.org/10.1002/jemt.23993
Li X, Li D, Yan Z, Ao Y (2018) Biosorption and bioaccumulation characteristics of cadmium by plant growth-promoting rhizobacteria. RSC Adv 8(54):30902–30911. https://doi.org/10.1039/c8ra06270f
Li W, Lee SY, Cho YJ, Ghim SY, Jung HY (2020a) Mediation of induced systemic resistance by the plant growth-promoting rhizobacteria Bacillus pumilus S2–3-2. Mol Biol Rep 47(11):8429–8438. https://doi.org/10.1007/s11033-020-05883-9
Li Z, Song C, Yi Y, Kuipers OP (2020b) Characterization of plant growth-promoting rhizobacteria from perennial ryegrass and genome mining of novel antimicrobial gene clusters. BMC Genomics 21(1):157. https://doi.org/10.1186/s12864-020-6563-7
Liu J, Kharat M, Tan Y, Zhou H, Muriel Mundo JL, McClements DJ (2020) Impact of fat crystallization on the resistance of W/O/W emulsions to osmotic stress: potential for temperature-triggered release. Food Res Int 134:109273. https://doi.org/10.1016/j.foodres.2020.109273
Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Van Leeuwenhoek 83(3):285–291
Mahmood S, Daur I, Yasir M, Waqas M, Hirt H (2022) Synergistic practicing of rhizobacteria and silicon improve salt tolerance: implications from boosted oxidative metabolism, nutrient uptake growth and grain yield in mung bean. Plants (basel). https://doi.org/10.3390/plants11151980
Manjunatha N, Li H, Sivasithamparam K, Jones MGK, Edwards I et al (2022) Fungal endophytes from salt-adapted plants confer salt tolerance and promote growth in wheat (Triticum aestivum L.) at early seedling stage. Microbiology (reading). https://doi.org/10.1099/mic.0.001225
Mariotti L, Scartazza A, Curadi M, Picciarelli P, Toffanin A (2021) Azospirillum baldaniorum Sp245 induces physiological responses to alleviate the adverse effects of drought stress in purple basil. Plants (basel). https://doi.org/10.3390/plants10061141
Meesungnoen O, Chantiratikul P, Thumanu K, Nuengchamnong N, Hokura A, Nakbanpote W (2021) Elucidation of crude siderophore extracts from supernatants of Pseudomonas sp ZnCd2003 cultivated in nutrient broth supplemented with Zn, Cd, and Zn plus Cd. Arch Microbiol 203(6):2863–2874. https://doi.org/10.1007/s00203-021-02274-x
Mekureyaw MF, Pandey C, Hennessy RC, Nicolaisen MH, Liu F, Nybroe O, Roitsch T (2022) The cytokinin-producing plant beneficial bacterium Pseudomonas fluorescens G20–18 primes tomato (Solanum lycopersicum) for enhanced drought stress responses. J Plant Physiol 270:153629. https://doi.org/10.1016/j.jplph.2022.153629
Mellidou I, Karamanoli K (2022) Unlocking PGPR-mediated abiotic stress tolerance what lies beneath. Front Sustain Food Syst 6:832896. https://doi.org/10.3389/fsufs.2022.832896
Miga P, Bélanger RR, Paulitz TC, Benhamou N (1997) Increased resistance to Fusarium oxysporumf. sp.radicis-lycopersiciin tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain. Physiol Mol Plant Pathol 50(5):301–320. https://doi.org/10.1006/pmpp.1997.0088
Mishra SK, Khan MH, Misra S, Dixit VK, Khare P, Srivastava S, Chauhan PS (2017) Characterisation of Pseudomonas spp. and Ochrobactrum sp. isolated from volcanic soil. Antonie Van Leeuwenhoek 110(2):253–270. https://doi.org/10.1007/s10482-016-0796-0
Moon YS, Ali S (2022) Isolation and identification of multi-trait plant growth-promoting rhizobacteria from coastal sand dune plant species of Pohang beach. Folia Microbiol (praha) 67(3):523–533. https://doi.org/10.1007/s12223-022-00959-4
Muthusamy M, Kim JY, Yoon EK, Kim JA, Lee SI (2020) BrEXLB1, a Brassica rapa expansin-like B1 gene is associated with root development, drought stress response, and seed germination. Genes (basel). https://doi.org/10.3390/genes11040404
Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53(10):1141–1149. https://doi.org/10.1139/w07-081
Nadeem SM, Ahmad M, Tufail MA, Asghar HN, Nazli F, Zahir ZA (2021) Appraising the potential of EPS-producing rhizobacteria with ACC-deaminase activity to improve growth and physiology of maize under drought stress. Physiol Plant 172(2):463–476. https://doi.org/10.1111/ppl.13212
Naeem K, Filippi R, Periche-Tomas E, Papageorgiou A, Bright P (2018) The importance of socioeconomic status as a modulator of the bilingual advantage in cognitive ability. Front Psychol 9:1818
Najafi Vafa Z, Sohrabi Y, Mirzaghaderi G, Heidari G (2022) Soil microorganisms and seaweed application with supplementary irrigation improved physiological traits and yield of two dryland wheat cultivars. Front Plant Sci 13:855090. https://doi.org/10.3389/fpls.2022.855090
Najafi Zilaie M, Mosleh Arani A, Etesami H, Dinarvand M (2022) Improved salinity and dust stress tolerance in the desert halophyte Haloxylon aphyllum by halotolerant plant growth-promoting rhizobacteria. Front Plant Sci 13:948260. https://doi.org/10.3389/fpls.2022.948260
Nakbanpote W, Panitlurtumpai N, Sangdee A, Sakulpone N, Sirisom P, Pimthong A (2014) Salt-tolerant and plant growth-promoting bacteria isolated from Zn/Cd contaminated soil: identification and effect on rice under saline conditions. Journal of Plant Interactions 9(1):379–387. https://doi.org/10.1080/17429145.2013.842000
Nascimento FX, Brígido C, Glick BR, Oliveira S (2012) ACC deaminase genes are conserved among Mesorhizobium species able to nodulate the same host plant. FEMS Microbiol Lett 336(1):26–37. https://doi.org/10.1111/j.1574-6968.2012.02648.x
Nautiyal KM, Ribeiro AC, Pfaff DW, Silver R (2008) Brain mast cells link the immune system to anxiety-like behavior. Proc Natl Acad Sci 105(46):18053–18057
Neshat M, Abbasi A, Hosseinzadeh A, Sarikhani MR, Dadashi Chavan D, Rasoulnia A (2022) Plant growth promoting bacteria (PGPR) induce antioxidant tolerance against salinity stress through biochemical and physiological mechanisms. Physiol Mol Biol Plants 28(2):347–361. https://doi.org/10.1007/s12298-022-01128-0
Niu X, Song L, Xiao Y, Ge W (2017) Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semi-arid agroecosystem and their potential in alleviating drought stress. Front Microbiol 8:2580. https://doi.org/10.3389/fmicb.2017.02580
Orozco-Mosqueda MDC, Fadiji AE, Babalola OO, Glick BR, Santoyo G (2022) Rhizobiome engineering: unveiling complex rhizosphere interactions to enhance plant growth and health. Microbiol Res 263:127137. https://doi.org/10.1016/j.micres.2022.127137
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
Pishchik VN, Chernyaeva II, Kozhemaykov AP, Vorobyov NI, Lazarev AM, Kozlov LP (1998) Effect of inoculation with nitrogen-fixing Klebsiella on potato yield. In: KA Malik, MS Mirza, JK Ladha (Eds.), Nitrogen Fixation with Non-Legumes: Proceedings of the 7th International Symposium on Nitrogen Fixation with Non-Legumes, held 16–21 October 1996 in Faisalabad, Pakistan (pp. 223–235). Dordrecht, Springer
Rajput L, Imran A, Mubeen F, Hafeez FY (2013) Salt-tolerant pgpr strain Planococcus rifietoensis promotes the growth and yield of wheat (Triticum aestivum L.) cultivated in saline soil. Pak J Bot 45(6):1955–1962
Rashid U, Yasmin H, Hassan MN, Naz R, Nosheen A, Sajjad M et al (2022) Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Rep 41(3):549–569. https://doi.org/10.1007/s00299-020-02640-x
Renoud S, Abrouk D, Prigent-Combaret C, Wisniewski-Dye F, Legendre L, Moenne-Loccoz Y, Muller D (2022) Effect of inoculation level on the impact of the PGPR Azospirillum lipoferum CRT1 on selected microbial functional groups in the rhizosphere of field maize. Microorganisms. https://doi.org/10.3390/microorganisms10020325
Rodriguez MV, Tano J, Ansaldi N, Carrau A, Srebot MS, Ferreira V et al (2019) Anatomical and biochemical changes induced by Gluconacetobacter diazotrophicus stand up for Arabidopsis thaliana seedlings from Ralstonia solanacearum Infection. Front Plant Sci 10:1618. https://doi.org/10.3389/fpls.2019.01618
Saeed Q, Xiukang W, Haider FU, Kucerik J, Mumtaz MZ, Holatko J et al (2021) Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int J Mol Sci. https://doi.org/10.3390/ijms221910529
Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34(10):635–648
Saleem S, Iqbal A, Ahmed F, Ahmad M (2021) Phytobeneficial and salt stress mitigating efficacy of IAA producing salt tolerant strains in Gossypium hirsutum. Saudi J Biol Sci 28(9):5317–5324. https://doi.org/10.1016/j.sjbs.2021.05.056
Santoyo G, Urtis-Flores CA, Loeza-Lara PD, Orozco-Mosqueda MDC, Glick BR (2021) Rhizosphere colonization determinants by plant growth-promoting rhizobacteria (PGPR). Biology (basel). https://doi.org/10.3390/biology10060475
Saradadevi GP, Das D, Mangrauthia SK, Mohapatra S, Chikkaputtaiah C, Roorkiwal M et al (2021) Genetic, epigenetic genomic and microbial approaches to enhance salt tolerance of plants: a comprehensive review. Biology (basel). https://doi.org/10.3390/biology10121255
Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102(5):1283–1292. https://doi.org/10.1111/j.1365-2672.2006.03179.x
Shahid M, Shah AA, Basit F, Noman M, Zubair M, Ahmed T et al (2020) Achromobacter sp. FB-14 harboring ACC deaminase activity augmented rice growth by upregulating the expression of stress-responsive CIPK genes under salinity stress. Braz J Microbiol 51(2):719–728. https://doi.org/10.1007/s42770-019-00199-8
Sharma A, Dev K, Sourirajan A, Choudhary M (2021) Isolation and characterization of salt-tolerant bacteria with plant growth-promoting activities from saline agricultural fields of Haryana. India J Genet Eng Biotechnol 19(1):99. https://doi.org/10.1186/s43141-021-00186-3
Sharma R, Gal L, Garmyn D, Bru D, Sharma S, Piveteau P (2022) Plant growth promoting bacterial consortium induces shifts in indigenous soil bacterial communities and controls Listeria monocytogenes in rhizospheres of Cajanus cajan and Festuca arundinacea. Microb Ecol 84(1):106–121. https://doi.org/10.1007/s00248-021-01837-1
Shi-Ying Z, Cong F, Yong-xia W, Yun-sheng X, Wei X, Xiao-Long C (2018) Salt-tolerant and plant growth-promoting bacteria isolated from high-yield paddy. Can. J Microbiol 64:968–978. https://doi.org/10.1139/cjm-2017-0571
Siddiqui ZA, Futai K (2009) Biocontrol of Meloidogyne incognita on tomato using antagonistic fungi, plant-growth-promoting rhizobacteria and cattle manure. Pest Manag Sci 65(9):943–948. https://doi.org/10.1002/ps.1777
Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 Augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945. https://doi.org/10.3389/fmicb.2017.01945
Singh R, Soni SK, Patel RP, Kalra A (2013) Technology for improving essential oil yield of Ocimum basilicum L. (sweet basil) by application of bioinoculant colonized seeds under organic field conditions. Ind Crops Prod 45:335–342. https://doi.org/10.1016/j.indcrop.2013.01.003
Singh RP, Pandey DM, Jha PN, Ma Y (2022) ACC deaminase producing rhizobacterium Enterobacter cloacae ZNP-4 enhance abiotic stress tolerance in wheat plant. PLoS ONE 17(5):e0267127. https://doi.org/10.1371/journal.pone.0267127
Somal MK, Karnwal A (2022) Effect of stress tolerance endophytic bacteria on the growth of Rheum emodi under abiotic stress. Plant Biol (stuttg). https://doi.org/10.1111/plb.13463
Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201(3):850–861
Sumbul A, Ansari RA, Rizvi R, Mahmood I (2020) Azotobacter: a potential bio-fertilizer for soil and plant health management. Saudi J Biol Sci 27(12):3634–3640
Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53(11):1195–1202. https://doi.org/10.1139/W07-082
Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49(2):195–204. https://doi.org/10.1002/jobm.200800090
Thakur R, Sharma KC, Gulati A, Sud RK, Gulati A (2017) Stress-tolerant Viridibacillus arenosi strain IHB B 7171 from tea rhizosphere as a potential broad-spectrum microbial inoculant. Indian J Microbiol 57(2):195–200
Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson AC (2017) Perspectives and challenges of microbial application for crop improvement. Front Plant Sci 8:49
Wang R, Wang M, Chen K, Wang S, Mur LAJ, Guo S (2018) Exploring the roles of aquaporins in plant(-)microbe interactions. Cells. https://doi.org/10.3390/cells7120267
Wang DC, Jiang CH, Zhang LN, Chen L, Zhang XY, Guo JH (2019) Biofilms positively contribute to Bacillus amyloliquefaciens 54-induced drought tolerance in tomato plants. Int J Mol Sci. https://doi.org/10.3390/ijms20246271
Wang X, Liu H, Zhang D, Zou D, Wang J, Zheng H, Jia Y, Qu Z, Sun B, Zhao H, (2022) Photosynthetic carbon fixation and sucrose metabolism supplemented by weighted gene Co-expression network analysis in response to water stress in rice with overlapping growth stages. Front Plant Sci. https://doi.org/10.3389/fpls.2022.864605
Yildirim E, Turan M, Guvenc I (2008) Effect of foliar salicylic acid applications on growth, chlorophyll and mineral content of cucumber grown under salt stress. Biol Planta 31(3):593–612
Yin X, Gao Y, Song S, Hassani D, Lu J (2021) Identification, characterization and functional analysis of grape (Vitis vinifera L.) mitochondrial transcription termination factor (mTERF) genes in responding to biotic stress and exogenous phytohormone. BMC Genomics 22(1):136. https://doi.org/10.1186/s12864-021-07446-z
Zebelo S, Song Y, Kloepper JW, Fadamiro H (2016) Rhizobacteria activates (+)-delta-cadinene synthase genes and induces systemic resistance in cotton against beet armyworm (Spodoptera exigua). Plant Cell Environ 39(4):935–943. https://doi.org/10.1111/pce.12704
Zehra A, Raytekar NA, Meena M, Swapnil P (2021) Efficiency of microbial bio-agents as elicitors in plant defense mechanism under biotic stress: a review. Curr Res Microb Sci 2:100054. https://doi.org/10.1016/j.crmicr.2021.100054
Zhang LN, Wang DC, Hu Q, Dai XQ, Xie YS, Li Q et al (2019) Consortium of plant growth-promoting Rhizobacteria strains suppresses sweet pepper disease by altering the rhizosphere microbiota. Front Microbiol 10:1668. https://doi.org/10.3389/fmicb.2019.01668
Zhang M, Liu L, Chen C, Zhao Y, Pang C, Chen M (2022) Heterologous expression of a Fraxinus velutina SnRK2 gene in Arabidopsis increases salt tolerance by modifying root development and ion homeostasis. Plant Cell Rep 41(9):1895–1906. https://doi.org/10.1007/s00299-022-02899-2
Zhao B, Liu Q, Wang B, Yuan F (2021) Roles of phytohormones and their signaling pathways in leaf development and stress responses. J Agric Food Chem 69(12):3566–3584. https://doi.org/10.1021/acs.jafc.0c07908
Zhao M, Haxim Y, Liang Y, Qiao S, Gao B, Zhang D, Li X (2022) Genome-wide investigation of AP2/ERF gene family in the desert legume Eremosparton songoricum: identification, classification, evolution, and expression profiling under drought stress. Front Plant Sci 13:885694. https://doi.org/10.3389/fpls.2022.885694
Zhou Z, Zhu L, Dong Y, You L, Zheng S, Wang G, Xia X (2022) Identification of a novel chromate and selenite reductase FesR in Alishewanella sp. WH16–1. Front Microbiol 13:834293. https://doi.org/10.3389/fmicb.2022.834293
Zhu D, Ouyang L, Xu Z, Zhang L (2015) Rhizobacteria of Populus euphratica promoting plant growth against heavy metals. Int J Phytoremediation 17(10):973–980. https://doi.org/10.1080/15226514.2014.981242
Zhu N, Meng T, Li S, Yu C, Tang D, Wang Y et al (2022) Improved growth and metabolite accumulation in Codonopsis pilosula (Franch.) Nannf. by inoculation with the endophytic Geobacillu sp. RHBA19 and Pseudomonas fluorescens RHBA17. J Plant Physiol 274:153718. https://doi.org/10.1016/j.jplph.2022.153718
Zia R, Nawaz MS, Yousaf S, Amin I, Hakim S, Mirza MS, Imran A (2021) Seed inoculation of desert-plant growth-promoting rhizobacteria induce biochemical alterations and develop resistance against water stress in wheat. Physiol Plant 172(2):990–1006. https://doi.org/10.1111/ppl.13362
Zubair M, Hanif A, Farzand A, Sheikh TMM, Khan AR, Suleman M et al (2019) Genetic screening and expression analysis of psychrophilic Bacillus spp. reveal their potential to alleviate cold stress and modulate phytohormones in wheat. Microorganisms. https://doi.org/10.3390/microorganisms7090337
Zytynska SE, Eicher M, Rothballer M, Weisser WW (2020a) Microbial-mediated plant growth promotion and pest suppression varies under climate change. Front Plant Sci 11:573578. https://doi.org/10.3389/fpls.2020.573578
Zytynska SE, Eicher M, Rothballer M, Weisser WW (2020b) Microbial-mediated plant growth promotion and pest suppression varies under climate change. Front Plant Sci 11:573578
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Karnwal, A., Shrivastava, S., Al-Tawaha, A.R.M.S. et al. PGPR-Mediated Breakthroughs in Plant Stress Tolerance for Sustainable Farming. J Plant Growth Regul (2023). https://doi.org/10.1007/s00344-023-11013-z
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DOI: https://doi.org/10.1007/s00344-023-11013-z