Cited by 95Plant-Microbe Interactions and ImmunityPlant Stress Responses and TolerancePlant Growth Enhancement Techniques

Rhizospheric Bacillus spp. Rescues Plant Growth Under Salinity Stress via Regulating Gene Expression, Endogenous Hormones, and Antioxidant System of Oryza sativa L

Open access
Khan, Muhammad Aaqil, Hamayun, Muhammad, Asaf, Sajjad, Khan, Murtaza, Yun, Byung-Wook, Kang, Sang-Mo, Lee, In-Jung·2021·Frontiers in Plant Science

Abstract

Salinity has drastically reduced crop yields and harmed the global agricultural industry. We isolated 55 bacterial strains from plants inhabiting the coastal sand dunes of Pohang, Korea. A screening bioassay showed that 14 of the bacterial isolates secreted indole-3-acetic acid (IAA), 12 isolates were capable of exopolysaccharide (EPS) production and phosphate solubilization, and 10 isolates secreted siderophores. Based on our preliminary screening, 11 bacterial isolates were tested for salinity tolerance on Luria–Bertani (LB) media supplemented with 0, 50, 100, and 150 mM of NaCl. Three bacterial isolates, ALT11, ALT12, and ALT30, had the best tolerance against elevated NaCl levels and were selected for further study. Inoculation of the selected bacterial isolates significantly enhanced rice growth attributes, viz., shoot length (22.8–42.2%), root length (28.18–59%), fresh biomass (44.7–66.41%), dry biomass (85–90%), chlorophyll content (18.30–36.15%), Chl a (29.02–60.87%), Chl b (30.86–64.51%), and carotenoid content (26.86–70%), under elevated salt stress of 70 and 140 mM. Furthermore, a decrease in the endogenous abscisic acid (ABA) content (27.9–23%) and endogenous salicylic acid (SA) levels (11.70–69.19%) was observed in inoculated plants. Antioxidant analysis revealed an increase in total protein (TP) levels (42.57–68.26%), whereas it revealed a decrease in polyphenol peroxidase (PPO) (24.63–34.57%), glutathione (GSH) (25.53–24.91%), SOA (13.88–18.67%), and LPO levels (15.96–26.06%) of bacterial-inoculated plants. Moreover, an increase in catalase (CAT) (26–33.04%), peroxidase (POD) (59.55–78%), superoxide dismutase (SOD) (13.58–27.77%), and ascorbic peroxidase (APX) (5.76–22.74%) activity was observed. Additionally, inductively coupled plasma mass spectrometry (ICP-MS) analysis showed a decline in Na+content (24.11 and 30.60%) and an increase in K+(23.14 and 15.45%) and Mg+(2.82 and 18.74%) under elevated salt stress.OsNHX1 gene expression was downregulated (0.3 and 4.1-folds), whereas the gene expression of OsPIN1A, OsCATA, and OsAPX1 was upregulated by a 7–17-fold in bacterial-inoculated rice plants. It was concluded that the selected bacterial isolates, ALT11, ALT12, and ALT30, mitigated the adverse effects of salt stress on rice growth and can be used as climate smart agricultural tools in ecofriendly agricultural practices.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fpls.2021.665590

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 117 · Cited by 95

Research works printed but not linked: 110

  1. Adhikari A. Lee K.-E. Khan M. A. Kang S.-M. Adhikari B. Imran M.. (2020). Effect of silicate and phosphate solubilizing rhizobacterium enterobacter ludwigii GAK2 on Oryza sativa L. under cadmium stress. J. Microbiol. Biotechnol. 30, 118– 126. 10.4014/jmb.1906.06010 31650772 PMC9728408 · DOI
  2. Ahanger M. A. Aziz U. Alsahli A. A. Alyemeni M. N. Ahmad P. (2020). influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed vigna angularis. Biomolecules 10: 42. 10.3390/biom10010042 31888108 PMC7022326 · DOI
  3. Almeida D. M. Gregorio G. B. Oliveira M. M. Saibo N. J. M. (2017). Five novel transcription factors as potential regulators of OsNHX1 gene expression in a salt tolerant rice genotype. Plant Mol. Biol. 93, 61– 77. 10.1007/s11103-016-0547-7 27766460 · DOI
  4. Ansari M. Shekari F. Mohammadi M. H. Juhos K. Végvári G. Biró B. (2019). Salt-tolerant plant growth-promoting bacteria enhanced salinity tolerance of salt-tolerant alfalfa (Medicago sativa L.) cultivars at high salinity. Acta Physiol. Plantarum 41: 195. 10.1007/s11738-019-2988-5 · DOI · Paper page
  5. Arora M. Kaushik A. Rani N. Kaushik C. P. (2010). Effect of cyanobacterial exopolysaccharides on salt stress alleviation and seed germination. J. Environ. Biol. 31, 701– 704. 21387925
  6. Asaf S. Khan A. L. Khan M. A. Imran Q. M. Yun B.-W. Lee I.-J. (2017a). Osmoprotective functions conferred to soybean plants via inoculation with Sphingomonas sp. LK11 and exogenous trehalose. Microbiol. Res. 205, 135– 145. 10.1016/j.micres.2017.08.009 28942839 · DOI
  7. Asaf S. Khan M. A. Khan A. L. Waqas M. Shahzad R. Kim A.-Y.. (2017b). Bacterial endophytes from arid land plants regulate endogenous hormone content and promote growth in crop plants: an example of Sphingomonas sp. and Serratia marcescens. J. Plant Interact. 12, 31– 38. 10.1080/17429145.2016.1274060 · DOI
  8. Babu M. Singh D. Gothandam K. M. (2011). Effect of salt stress on expression of carotenoid pathway genes in tomato. J. Stress Physiol. Biochem. 7, 87– 94. Available online at: https://www.academia.edu/5771661/Effect_of_salt_stress_on_expression_of_carotenoid_pathway_genes_in_tomato
  9. Bal H. B. Nayak L. Das S. Adhya T. K. (2013). Isolation of ACC deaminase producing PGPR from rice rhizosphere and evaluating their plant growth promoting activity under salt stress. Plant Soil 366, 93– 105. 10.1007/s11104-012-1402-5 · DOI
  10. Bashan Y. Bustillos J. Leyva L. Hernandez J.-P. Bacilio M. (2006). Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biol. Fertil. Soils 42, 279– 285. 10.1007/s00374-005-0025-x · DOI
  11. Belimov A. A. Dodd I. C. Safronova V. I. Dumova V. A. Shaposhnikov A. I. Ladatko A. G.. (2014). Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol. Biochem. 74, 84– 91. 10.1016/j.plaphy.2013.10.032 24270514 · DOI
  12. Bhattacharyya C. Bakshi U. Mallick I. Mukherji S. Bera B. Ghosh A. (2017). Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile bacillus aryabhattai strain AB211. Front. Microbiol. 8: 411. 10.3389/fmicb.2017.00411 28377746 PMC5359284 · DOI
  13. Chen M. Chen Q. Niu X. Zhang R. Lin H. Xu C.. (2007). Expression of OsNHX1 gene in maize confers salt tolerance and promotes plant growth in the field. Plant Soil Environ. 53, 490– 498. 10.17221/2302-PSE · DOI
  14. Conklin P. L. Barth C. (2004). Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ. 27, 959– 970. 10.1111/j.1365-3040.2004.01203.x · DOI
  15. De Vleesschauwer D. Gheysen G. Höfte M. (2013). Hormone defense networking in rice: tales from a different world. Trends Plant Sci. 18, 555– 565. 10.1016/j.tplants.2013.07.002 23910453 · DOI
  16. Desale P. Patel B. Singh S. Malhotra A. Nawani N. (2014). Plant growth promoting properties of Halobacillus sp. and Halomonas sp. in presence of salinity and heavy metals. J. Basic Microbiol. 54, 781– 791. 10.1002/jobm.201200778 23775888 · DOI
  17. Dodd I. C. Theobald J. C. Richer S. K. Davies W. J. (2009). Partial phenotypic reversion of ABA-deficient flacca tomato (Solanum lycopersicum) scions by a wild-type rootstock: normalizing shoot ethylene relations promotes leaf area but does not diminish whole plant transpiration rate. J. Exp. Bot. 60, 4029– 4039. 10.1093/jxb/erp236 19648172 PMC2755025 · DOI
  18. Egamberdieva D. Berg G. Lindström K. Räsänen L. A. (2013). Alleviation of salt stress of symbiotic Galega officinalis L.(goat's rue) by co-inoculation of Rhizobium with root-colonizing Pseudomonas. Plant Soil 369, 453– 465. 10.1007/s11104-013-1586-3 · DOI
  19. El-Esawi M. A. Alaraidh I. A. Alsahli A. A. Alamri S. A. Ali H. M. Alayafi A. A. (2018). Bacillus firmus (SW5) augments salt tolerance in soybean (Glycine max L.) by modulating root system architecture, antioxidant defense systems and stress-responsive genes expression. Plant Physiol. Biochem. 132, 375– 384. 10.1016/j.plaphy.2018.09.026 30268029 · DOI
  20. El-Tarabily K. A. Youssef T. (2010). Enhancement of morphological, anatomical and physiological characteristics of seedlings of the mangrove Avicennia marina inoculated with a native phosphate-solubilizing isolate of Oceanobacillus picturae under greenhouse conditions. Plant Soil 332, 147– 162. 10.1007/s11104-010-0280-y · DOI
  21. Etesami H. (2018). Can interaction between silicon and plant growth promoting rhizobacteria benefit in alleviating abiotic and biotic stresses in crop plants? Agric. Ecosyst. Environ. 253, 98– 112. 10.1016/j.agee.2017.11.007 · DOI
  22. Etesami H. Beattie G. (2018). Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 9: 148. 10.3389/fmicb.2018.00148 29472908 PMC5809494 · DOI
  23. Farhat N. Elkhouni A. Zorrig W. Smaoui A. Abdelly C. Rabhi M. (2016). Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiol. Plantarum 38: 145. 10.1007/s11738-016-2165-z · DOI
  24. Ferreira M. J. Silva H. Cunha A. (2019). Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: a review. Pedosphere 29, 409– 420. 10.1016/S1002-0160(19)60810-6 · DOI
  25. Filgueiras C. C. Martins A. D. Pereira R. V. Willett D. S. (2019). The ecology of salicylic acid signaling: primary, secondary and tertiary effects with applications in agriculture. Int. J. Mol. Sci. 20: 5851. 10.3390/ijms20235851 31766518 PMC6928651 · DOI
  26. Fu Y. Yang Y. Chen S. Ning N. Hu H. (2019). Arabidopsis IAR4 Modulates primary root growth under salt stress through ROS-mediated modulation of auxin distribution. Front. Plant Sci. 10: 522. 10.3389/fpls.2019.00522 31105724 PMC6494962 · DOI
  27. Fukuda A. Nakamura A. Hara N. Toki S. Tanaka Y. (2011). Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233, 175– 188. 10.1007/s00425-010-1289-4 20963607 · DOI
  28. Fukuda A. Nakamura A. Tagiri A. Tanaka H. Miyao A. Hirochika H.. (2004). Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol. 45, 146– 159. 10.1093/pcp/pch014 14988485 · DOI
  29. Giri B. Kapoor R. Agarwal L. Mukerji K. (2004). Preinoculation with arbuscular mycorrhizae helps Acacia auriculiformis grow in degraded Indian wasteland soil. Commun. Soil Sci. Plant Anal. 35, 193– 204. 10.1081/CSS-120027643 · DOI
  30. Gomes M. A. D. C. Suzuki M. S. Cunha M. D. Tullii C.F. (2011). Effect of salt stress on nutrient concentration, photosynthetic pigments, proline and foliar morphology of Salvinia auriculata Aubl. Acta Limnol. Brasiliensia 23, 164– 176. 10.1590/S2179-975X2011000200007 · DOI
  31. Grobelak A. Hiller J. (2017). Bacterial siderophores promote plant growth: screening of catechol and hydroxamate siderophores. Int. J. Phytoremed. 19, 825– 833. 10.1080/15226514.2017.1290581 28699782 · DOI
  32. Habib S. H. Kausar H. Saud H. M. (2016). Plant growth-promoting rhizobacteria enhance salinity stress tolerance in okra through ROS-scavenging enzymes. Biomed. Res. Int. 2016: 6284547. 10.1155/2016/6284547 26951880 PMC4756578 · DOI
  33. Hamayun M. Hussain A. Khan S. A. Kim H.-Y. Khan A. L. Waqas M.. (2017). Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt affected soybean. Front. Microbiol. 8: 686. 10.3389/fmicb.2017.00686 28473818 PMC5397423 · DOI
  34. Hauser F. Horie T. (2010). A conserved primary salt tolerance mechanism mediated by HKT transporters: a mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant Cell Environ. 33, 552– 565. 10.1111/j.1365-3040.2009.02056.x 19895406 · DOI
  35. Heidari M. Golpayegani A. (2012). Effects of water stress and inoculation with plant growth promoting rhizobacteria (PGPR) on antioxidant status and photosynthetic pigments in basil (Ocimum basilicum L.). J. Saudi Soc. Agric. Sci. 11, 57– 61. 10.1016/j.jssas.2011.09.001 · DOI
  36. Hermans C. Bourgis F. Faucher M. Strasser R. J. Delrot S. Verbruggen N. (2005). Magnesium deficiency in sugar beets alters sugar partitioning and phloem loading in young mature leaves. Planta 220, 541– 549. 10.1007/s00425-004-1376-5 15580527 · DOI
  37. Hoang T. M. L. Tran T. N. Nguyen T. K. T. Williams B. Wurm P. Bellairs S.. (2016). Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6: 54. 10.3390/agronomy6040054 · DOI
  38. Hu Y. Schmidhalter U. (2005). Drought and salinity: a comparison of their effects on mineral nutrition of plants. J. Plant Nutr. Soil Sci. 168, 541– 549. 10.1002/jpln.200420516 · DOI
  39. Jaleel C. A. Riadh K. Gopi R. Manivannan P. Inès J. Al-Juburi H. J.. (2009). Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plantarum 31, 427– 436. 10.1007/s11738-009-0275-6 · DOI
  40. Jamil A. Riaz S. Ashraf M. Foolad M. R. (2011). Gene expression profiling of plants under salt stress. CRC. Crit. Rev. Plant Sci. 30, 435– 458. 10.1080/07352689.2011.605739 · DOI
  41. Jampeetong A. Brix H. (2009). Effects of NaCl salinity on growth, morphology, photosynthesis and proline accumulation of Salvinia natans. Aquat. Bot. 91, 181– 186. 10.1016/j.aquabot.2009.05.003 · DOI
  42. Jan R. Khan M. A. Asaf S. Lubna Lee I.-J. Kim K. M. (2019). Metal resistant endophytic bacteria reduces cadmium, nickel toxicity, and enhances expression of metal stress related genes with improved growth of oryza sativa, via regulating its antioxidant machinery and endogenous hormones. Plants 8: 363. 10.3390/plants8100363 31547575 PMC6844085 · DOI
  43. Jha Y. Subramanian R. (2013). Paddy plants inoculated with PGPR show better growth physiology and nutrient content under saline condition. Chilean J. Agric. Res. 73, 213– 219. 10.4067/S0718-58392013000300002 · DOI
  44. Jiang F. Chen L. Belimov A. A. Shaposhnikov A. I. Gong F. Meng X.. (2012). Multiple impacts of the plant growth-promoting rhizobacterium Variovorax paradoxus 5C-2 on nutrient and ABA relations of Pisum sativum. J. Exp. Bot. 63, 6421– 6430. 10.1093/jxb/ers301 23136167 PMC3504497 · DOI
  45. Kang S.-M. Khan A. L. Waqas M. You Y.-H. Kim J.-H. Kim J.-G.. (2014). Plant growth-promoting rhizobacteria reduce adverse effects of salinity and osmotic stress by regulating phytohormones and antioxidants in Cucumis sativus. J. Plant Interact. 9, 673– 682. 10.1080/17429145.2014.894587 · DOI
  46. Kang S.-M. Shahzad R. Bilal S. Khan A. L. Park Y.-G. Lee K.-E.. (2019). Indole-3-acetic-acid and ACC deaminase producing Leclercia adecarboxylata MO1 improves Solanum lycopersicum L. growth and salinity stress tolerance by endogenous secondary metabolites regulation. BMC Microbiol. 19: 80. 10.1186/s12866-019-1450-6 31023221 PMC6485084 · DOI
  47. Kang S. M. Adhikari A. Lee K. E. Khan M. A. Khan A. L. Shahzad R.. (2020). Inoculation with Indole-3-Acetic acid-producing rhizospheric Rhodobacter sphaeroides KE149 Augments growth of adzuki bean plants under water stress. J. Microbiol. Biotechnol. 30, 717– 725. 10.4014/jmb.1911.11063 32482937 PMC9728276 · DOI
  48. Karlidag H. Esitken A. Yildirim E. Donmez M. F. Turan M. (2010). Effects of plant growth promoting bacteria on yield, growth, leaf water content, membrane permeability, and ionic composition of strawberry under saline conditions. J. Plant Nutr. 34, 34– 45. 10.1080/01904167.2011.531357 · DOI
  49. Kartik V. P. Jinal H. N. Amaresan N. (2020). Inoculation of cucumber (Cucumis sativus L.) seedlings with salt-tolerant plant growth promoting bacteria improves nutrient uptake, plant attributes and physiological profiles. J. Plant Growth Regul. 1– 13. 10.1007/s00344-020-10226-w · DOI
  50. Khan M. A. Asaf S. Khan A. L. Adhikari A. Jan R. Ali S.. (2019a). Halotolerant rhizobacterial strains mitigate the adverse effects of NaCl stress in soybean seedlings. BioMed. Res. Int. 2019: 9530963. 10.1155/2019/9530963 31886270 PMC6925695 · DOI
  51. Khan M. A. Asaf S. Khan A. L. Adhikari A. Jan R. Ali S.. (2020a). Plant growth-promoting endophytic bacteria augment growth and salinity tolerance in rice plants. Plant Biol. 22, 850– 862. 10.1111/plb.13124 32329163 · DOI
  52. Khan M. A. Asaf S. Khan A. L. Jan R. Kang S.-M. Kim K.-M.. (2019b). Rhizobacteria AK1 remediates the toxic effects of salinity stress via regulation of endogenous phytohormones and gene expression in soybean. Biochem. J. 476, 2393– 2409. 10.1042/BCJ20190435 31375565 · DOI
  53. Khan M. A. Asaf S. Khan A. L. Jan R. Kang S.-M. Kim K.-M.. (2020c). Thermotolerance effect of plant growth-promoting Bacillus cereus SA1 on soybean during heat stress. BMC Microbiol. 20: 175. 10.1186/s12866-020-01822-7 32571217 PMC7310250 · DOI
  54. Khan M. A. Asaf S. Khan A. L. Jan R. Kang S. M. Kim K. M.. (2020b). Extending thermotolerance to tomato seedlings by inoculation with SA1 isolate of Bacillus cereus and comparison with exogenous humic acid application. PLoS ONE 15: e0232228. 10.1371/journal.pone.0232228 32353077 PMC7192560 · DOI
  55. Khan M. A. Asaf S. Khan A. L. Ullah I. Ali S. Kang S.-M.. (2019c). Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1. Ann. Microbiol. 69, 797– 808. 10.1007/s13213-019-01470-x · DOI
  56. Khan M. A. Hamayun M. Iqbal A. Khan S. A. Hussain A. Asaf S.. (2018). Gibberellin application ameliorates the adverse impact of short-term flooding onGlycine max L. Biochem. J. 475, 2893– 2905. 10.1042/BCJ20180534 30127090 · DOI
  57. Khan M. A. Khan A. L. Imran Q. M. Asaf S. Lee S.-U. Yun B.-W.. (2019d). Exogenous application of nitric oxide donors regulates short-term flooding stress in soybean. PeerJ 7: e7741. 10.7717/peerj.7741 31608169 PMC6788439 · DOI
  58. Khan M. A. Sahile A. A. Jan R. Asaf S. Hamayun M. Imran M.. (2021). Halotolerant bacteria mitigate the effects of salinity stress on soybean growth by regulating secondary metabolites and molecular responses. BMC Plant Biol. 21: 176. 10.1186/s12870-021-02937-3 33845762 PMC8040224 · DOI
  59. Khan M. A. Ullah I. Waqas M. Hamayun M. Khan A. L. Asaf S.. (2019e). Halo-tolerant rhizospheric Arthrobacter woluwensis AK1 mitigates salt stress and induces physio-hormonal changes and expression of GmST1 and GmLAX3 in soybean. Symbiosis 77, 9– 21. 10.1007/s13199-018-0562-3 · DOI
  60. Khan M. S. Zaidi A. Wani P. A. (2007). Role of phosphate-solubilizing microorganisms in sustainable agriculture — a review. Agron. Sustain. Dev. 27, 29– 43. 10.1051/agro:2006011 · DOI
  61. Kim D. W. Shibato J. Agrawal G. K. Fujihara S. Iwahashi H. Kim Du H.. (2007). Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol Cells 24, 45– 59. 17846498
  62. Kim T.-H. Böhmer M. Hu H. Nishimura N. Schroeder J. I. (2010). Guard Cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61, 561– 591. 10.1146/annurev-arplant-042809-112226 20192751 PMC3056615 · DOI
  63. Kim Y.-N. Khan M. A. Kang S.-M. Hamayun M. Lee I.-J. (2020). Enhancement of drought-stress tolerance of Brassica oleracea var. italica L. by newly isolated Variovorax sp. YNA59. J. Microbiol. Biotechnol. 30, 1500– 1509. 10.4014/jmb.2006.06010 32807757 PMC9728237 · DOI
  64. Kubi H. A. A. Khan M. A. Adhikari A. Imran M. Kang S.-M. Hamayun M.. (2021). Silicon and plant growth-promoting Rhizobacteria pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture 11: 272. 10.3390/agriculture11030272 · DOI
  65. Kumar A. Singh S. Gaurav A. K. Srivastava S. Verma J. P. (2020). Plant growth-promoting bacteria: biological tools for the mitigation of salinity stress in plants. Front. Microbiol. 11: 1216. 10.3389/fmicb.2020.01216 32733391 PMC7358356 · DOI
  66. Li X.-J. Yang M.-F. Chen H. Qu L.-Q. Chen F. Shen S.-H. (2010). Abscisic acid pretreatment enhances salt tolerance of rice seedlings: proteomic evidence. Biochim. Biophys. Acta 1804, 929– 940. 10.1016/j.bbapap.2010.01.004 20079886 · DOI
  67. Liu J. Tang L. Gao H. Zhang M. Guo C. (2019). Enhancement of alfalfa yield and quality by plant growth-promoting rhizobacteria under saline-alkali conditions. J. Sci. Food Agric. 99, 281– 289. 10.1002/jsfa.9185 29855046 · DOI
  68. Marklund S. Marklund G. (1974). Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem., 47, 469– 474. 10.1111/j.1432-1033.1974.tb03714.x 4215654 · DOI
  69. Masalha J. Kosegarten H. Elmaci Ö. Mengel K. (2000). The central role of microbial activity for iron acquisition in maize and sunflower. Biol. Fertil. Soils 30, 433– 439. 10.1007/s003740050021 · DOI
  70. Mukherjee P. Mitra A. Roy M. (2019). Halomonas rhizobacteria of Avicennia marina of Indian sundarbans promote rice growth under saline and heavy metal stresses through exopolysaccharide production. Front. Microbiol. 10: 1207. 10.3389/fmicb.2019.01207 31191507 PMC6549542 · DOI
  71. Munns R. (2005). Genes and salt tolerance: bringing them together. New phytol. 167, 645– 663. 10.1111/j.1469-8137.2005.01487.x 16101905 · DOI
  72. Nautiyal C. S. Srivastava S. Chauhan P. S. Seem K. Mishra A. Sopory S. K. (2013). Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol. Biochem. 66, 1– 9. 10.1016/j.plaphy.2013.01.020 23454292 · DOI
  73. Pandey S. Fartyal D. Agarwal A. Shukla T. James D. Kaul T.. (2017). Abiotic stress tolerance in plants: myriad roles of ascorbate peroxidase. Front. Plant Sci. 8: 581. 10.3389/fpls.2017.00581 28473838 PMC5397514 · DOI
  74. Panhwar Q. Othman R. A. Rahman Z. Meon S. Razi I. Naher U. (2011). Contribution of phosphate-solubilizing bacteria in phosphorus bioavailability and growth enhancement of aerobic rice. Spanish J. Agric. Res. 9, 810– 820. 10.5424/sjar/20110903-330-10 · DOI
  75. Paulucci N. S. Gallarato L. A. Reguera Y. B. Vicario J. C. Cesari A. B. García De Lema M. B.. (2015). Arachis hypogaea PGPR isolated from Argentine soil modifies its lipids components in response to temperature and salinity. Microbiol. Res. 173, 1– 9. 10.1016/j.micres.2014.12.012 25801965 · DOI
  76. Peng Y. Hou F. Bai Q. Xu P. Liao Y. Zhang H.. (2018). Rice calcineurin B-Like protein-interacting protein kinase 31 (OsCIPK31) is involved in the development of panicle apical spikelets. Front. Plant Sci. 9: 1661. 10.3389/fpls.2018.01661 30524455 PMC6262370 · DOI
  77. Radhakrishnan R. Lee I. J. (2013). Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiol. Plant. 35, 263– 269. 10.1007/s11738-012-1072-1 · DOI
  78. Rafiq K. Akram M. S. Shahid M. Qaisar U. Rashid N. (2020). Enhancement of salt tolerance in maize (Zea mays L.) using locally isolated Bacillus sp. SR-2-1/1. Biologia 75, 1425– 1436. 10.2478/s11756-020-00435-9 · DOI
  79. Rodrigues A. C. Bonifacio A. Antunes J. E. L. Da Silveira J. A. G. Figueiredo M. D. V. B. (2013). Minimization of oxidative stress in cowpea nodules by the interrelationship between Bradyrhizobium sp. and plant growth-promoting bacteria. Appl. Soil Ecol. 64, 245– 251. 10.1016/j.apsoil.2012.12.018 · DOI
  80. Rodriguez H. Gonzalez T. Goire I. Bashan Y. (2004). Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91, 552– 555. 10.1007/s00114-004-0566-0 15502903 · DOI
  81. Rojas-Tapias D. Moreno-Galván A. Pardo-Díaz S. Obando M. Rivera D. Bonilla R. (2012). Effect of inoculation with plant growth-promoting bacteria (PGPB) on amelioration of saline stress in maize (Zea mays). Applied Soil Ecol. 61, 264– 272. 10.1016/j.apsoil.2012.01.006 · DOI
  82. Rossatto T. Do Amaral M. N. Benitez L. C. Vighi I. L. Braga E. J. B. De Magalhães Júnior A. M.. (2017). Gene expression and activity of antioxidant enzymes in rice plants, cv. BRS AG, under saline stress. Physiol. Mol. Biol. Plants 23, 865– 875. 10.1007/s12298-017-0467-2 29158635 PMC5671449 · DOI
  83. Sah S. K. Reddy K. R. Li J. (2016). Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7: 571. 10.3389/fpls.2016.00571 27200044 PMC4855980 · DOI
  84. Sahile A. A. Khan M. A. Hamayun M. Imran M. Kang S.-M. Lee I.-J. (2021). Novel Bacillus cereus strain, ALT1, enhance growth and strengthens the antioxidant system of soybean under cadmium stress. Agronomy 11: 404. 10.3390/agronomy11020404 · DOI
  85. Salomon M. V. Bottini R. De Souza Filho G. A. Cohen A. C. Moreno D. Gil M.. (2014). Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine. Physiol. Plant. 151, 359– 374. 10.1111/ppl.12117 24118032 · DOI
  86. Santos A. D. A. Silveira J. A. G. D. Bonifacio A. Rodrigues A. C. Figueiredo M. D. V. B. (2018). Antioxidant response of cowpea co-inoculated with plant growth-promoting bacteria under salt stress. Braz. J. Microbiol. 49, 513– 521. 10.1016/j.bjm.2017.12.003 29482998 PMC6066742 · DOI
  87. Santos R. Hérouart D. Puppo A. Touati D. (2000). Critical protective role of bacterial superoxide dismutase in rhizobium-legume symbiosis. Mol. Microbiol. 38, 750– 759. 10.1046/j.1365-2958.2000.02178.x 11115110 · DOI
  88. Shahid M. Imran Q. M. Hussain A. Khan M. Lee S. U. Mun B. G.. (2019). Comprehensive analyses of nitric oxide-induced plant stem cell-related genes in Arabidopsis thaliana. Genes. 10: 190. 10.3390/genes10030190 30813477 PMC6471024 · DOI
  89. Shameer S. Prasad T. N. V. K. V. (2018). Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul. 84, 603– 615. 10.1007/s10725-017-0365-1 · DOI
  90. Sharma P. Jha A. B. Dubey R. S. Pessarakli M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Botany 2012: 217037. 10.1155/2012/217037 · DOI
  91. Sharma S. B. Sayyed R. Z. Trivedi M. H. Gobi T. A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2: 587. 10.1186/2193-1801-2-587 25674415 PMC4320215 · DOI
  92. Shin W. Siddikee A. Joe M. M. Benson A. Kim K. Selvakumar G.. (2016). Halotolerant plant growth promoting bacteria mediated salinity stress amelioration in plants. Korean J. Soil Sci. Fertil. 49, 355– 367. 10.7745/KJSSF.2016.49.4.355 · DOI
  93. Shrivastava P. Kumar R. (2015). Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22, 123– 131. 10.1016/j.sjbs.2014.12.001 25737642 PMC4336437 · DOI
  94. Shukla P. S. Agarwal P. K. Jha B. (2012). Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul. 31, 195– 206. 10.1007/s00344-011-9231-y · DOI
  95. Shultana R. Kee Zuan A. T. Yusop M. R. Saud H. M. (2020a). Characterization of salt-tolerant plant growth-promoting rhizobacteria and the effect on growth and yield of saline-affected rice. PLoS ONE 15: e0238537. 10.1371/journal.pone.0238537 32886707 PMC7473536 · DOI
  96. Shultana R. Tan Kee Zuan A. Yusop M. R. Mohd Saud H. Ayanda A. F. (2020b). Effect of salt-tolerant bacterial inoculations on rice seedlings differing in salt-tolerance under saline soil conditions. Agronomy 10: 1030. 10.3390/agronomy10071030 · DOI
  97. Sytar O. Kumar A. Latowski D. Kuczynska P. Strzałka K. Prasad M. N. V. (2013). Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol. Plant. 35, 985– 999. 10.1007/s11738-012-1169-624984833 · DOI
  98. Tisarum R. Theerawitaya C. Samphumphuang T. Polispitak K. Thongpoem P. Singh H. P.. (2020). Alleviation of salt stress in upland rice (Oryza sativa L. ssp. indica cv. Leum Pua) using arbuscular mycorrhizal fungi inoculation. Front. Plant Sci. 11: 348. 10.3389/fpls.2020.00348 32273880 PMC7113393 · DOI
  99. Tränkner M. Tavakol E. Jákli B. (2018). Functioning of potassium and magnesium in photosynthesis, photosynthate translocation and photoprotection. Physiol. Plant. 163, 414– 431. 10.1111/ppl.12747 29667201 · DOI
  100. Vázquez P. Holguin G. Puente M. López-Cortés A. Bashan Y. (2000). Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol. Fertil. Soils 30, 460– 468. 10.1007/s003740050024 · DOI
  101. Vessey J. K. (2003). Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255, 571– 586. 10.1023/A:102603721689333914091 · DOI
  102. Volkov V. (2015). Salinity tolerance in plants. quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front. Plant Sci. 6: 873. 10.3389/fpls.2015.00873 26579140 PMC4621421 · DOI
  103. Wang W. Wu Z. He Y. Huang Y. Li X. Ye B.-C. (2018). Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. Ecotoxicol. Environ. Safety 164, 520– 529. 10.1016/j.ecoenv.2018.08.070 30149350 · DOI
  104. Waters B. M. (2011). Moving magnesium in plant cells. New Phytol. 190, 510– 513. 10.1111/j.1469-8137.2011.03724.x 21496026 · DOI
  105. Xiong L. Schumaker K. S. Zhu J.-K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell 14, S165– S183. 10.1105/tpc.000596 12045276 PMC151254 · DOI
  106. Yildirim E. Turan M. Ekinci M. Dursun A. Çakmakçi R. (2011). Plant growth promoting rhizobacteria ameliorate deleterious effect of salt stress on lettuce. Sci. Res. Essays 6, 4389– 4396. 10.5897/SRE11.219 · DOI
  107. Yu Z. Duan X. Luo L. Dai S. Ding Z. Xia G. (2020). How plant hormones mediate salt stress responses. Trends Plant Sci. 25, 1117– 1130. 10.1016/j.tplants.2020.06.008 32675014 · DOI
  108. Zhang H. Xie X. Kim M. S. Kornyeyev D. A. Holaday S. Paré P. W. (2008). Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J. 56, 264– 273. 10.1111/j.1365-313X.2008.03593.x 18573192 · DOI
  109. Zhang Y. Fang J. Wu X. Dong L. (2018). Na+/K+ balance and transport regulatory mechanisms in weedy and cultivated rice (Oryza sativa L.) under salt stress. BMC Plant Biol. 18: 375. 10.1186/s12870-018-1586-9 30594151 PMC6311050 · DOI
  110. Zhou W. Qin S. Lyu D. Zhang P. (2015). Soil sterilisation and plant growth-promoting rhizobacteria promote root respiration and growth of sweet cherry rootstocks. Arch. Agron. Soil Sci. 61, 361– 370. 10.1080/03650340.2014.935346 · DOI

Authors
Khan, M. A., Hamayun, M., Asaf, S., Khan, M., Yun, B.-W., Kang, S.-M., & Lee, I.-J.
Affiliations
  • Kyungpook National University (KR)
  • Abdul Wali Khan University Mardan (PK)
  • University of Nizwa (OM)
Corresponding author
Lee, In-Jung
Venue
Frontiers in Plant Science
Published
2021-06-11
Volume
12
Pages
665590-665590
ISSN
1664-462X (ISSN-L)
OpenAlex
W3169566112
Cited by
95
References
117
Citations by year
2026: 16 · 2025: 24 · 2024: 18 · 2023: 19 · 2022: 15 · 2021: 3
Type
book review
Language
en
Open access
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Research Foundation of Korea
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Growth Enhancement Techniques
Keywords
rhizosphere bacteria, Bacillus, salt stress, rice, plant growth promotion, indole-3-acetic acid, exopolysaccharide production, phosphate solubilization, siderophores, abscisic acid, salicylic acid, endogenous plant hormones, antioxidant enzymes, lipid peroxidation, glutathione, catalase

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review