DOI QR코드

DOI QR Code

Bacterial Exopolysaccharides: Insight into Their Role in Plant Abiotic Stress Tolerance

  • Bhagat, Neeta (Amity Institute of Biotechnology, Amity University Uttar Pradesh) ;
  • Raghav, Meenu (Amity Institute of Biotechnology, Amity University Uttar Pradesh) ;
  • Dubey, Sonali (Amity Institute of Biotechnology, Amity University Uttar Pradesh) ;
  • Bedi, Namita (Amity Institute of Biotechnology, Amity University Uttar Pradesh)
  • Received : 2021.05.10
  • Accepted : 2021.06.17
  • Published : 2021.08.28

Abstract

Various abiotic stressors like drought, salinity, temperature, and heavy metals are major environmental stresses that affect agricultural productivity and crop yields all over the world. Continuous changes in climatic conditions put selective pressure on the microbial ecosystem to produce exopolysaccharides. Apart from soil aggregation, exopolysaccharide (EPS) production also helps in increasing water permeability, nutrient uptake by roots, soil stability, soil fertility, plant biomass, chlorophyll content, root and shoot length, and surface area of leaves while also helping maintain metabolic and physiological activities during drought stress. EPS-producing microbes can impart salt tolerance to plants by binding to sodium ions in the soil and preventing these ions from reaching the stem, thereby decreasing sodium absorption from the soil and increasing nutrient uptake by the roots. Biofilm formation in high-salinity soils increases cell viability, enhances soil fertility, and promotes plant growth and development. The third environmental stressor is presence of heavy metals in the soil due to improper industrial waste disposal practices that are toxic for plants. EPS production by soil bacteria can result in the biomineralization of metal ions, thereby imparting metal stress tolerance to plants. Finally, high temperatures can also affect agricultural productivity by decreasing plant metabolism, seedling growth, and seed germination. The present review discusses the role of exopolysaccharide-producing plant growth-promoting bacteria in modulating plant growth and development in plants and alleviating extreme abiotic stress condition. The review suggests exploring the potential of EPS-producing bacteria for multiple abiotic stress management strategies.

Keywords

Acknowledgement

The authors thank the authorities of Amity University Uttar Pradesh for providing the opportunity to prepare this review article.

References

  1. Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, et al. 2019. Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants (Basel) 30: 8: 34.
  2. Lesk C, Rowhani P, Ramankutty N. 2016. Influence of extreme weather disasters on global crop production. Nature 529: 84-87 https://doi.org/10.1038/nature16467
  3. Etesami H, Beattie GA. 2017. Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. pp. 163-200. In: Probiotics and Plant Health. Springer, Singapore.
  4. Fita A, Rodriguez-Burruezo A, Boscaiu M, Prohens J, Vicente O. 2015. Breeding and domesticating crops adapted to drought and salinity: a new paradigm for increasing food production. Front. Plant Sci. 6: 978.
  5. Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, et al. 2021. Plant Growth Promoting Rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13: 1140. https://doi.org/10.3390/su13031140
  6. Bashan Y, de-Bashan LE, Prabhu SR. Hernandez J-P. 2014. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant Soil 378: 1-33. https://doi.org/10.1007/s11104-013-1956-x
  7. Vejan P, Abdullah R, Khadiran T, Ismail S. 2016. Role of plant growth promoting rhizobacteria in agricultural sustainability-A review. Molecules 21: 573. https://doi.org/10.3390/molecules21050573
  8. Paulin MM, Novinscak A, Lanteigne C, Gadkar VJ, Filion M.2017. Interaction between 2,4-diacetylphloroglucinol- and hydrogen cyanide-producing Pseudomonas brassicacearum LBUM300 and Clavibacter michiganensis subsp. michiganensis in the tomato rhizosphere. Appl. Environ. Microbiol. 83: e00073-17.
  9. Prabhukarthikeyan SR, Keerthana U, Raguchander T. 2018. Antibiotic-producing Pseudomonas fluorescens mediates rhizome rot disease resistance and promotes plant growth in turmeric plants. Microbiol. Res. 210: 65-73. https://doi.org/10.1016/j.micres.2018.03.009
  10. Liu XM, Zhang H. 2015. The effects of bacterial volatile emissions on plant abiotic stress tolerance. Front. Plant Sci. 6: 774. https://doi.org/10.3389/fpls.2015.00774
  11. Khan N, Bano A, Rahman MA, Guo J. 2019. 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. https://doi.org/10.1038/s41598-019-38702-8
  12. Upadhyay SK, Singh J S, Saxena A K, Singh D P. 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol. 14: 605-611. https://doi.org/10.1111/j.1438-8677.2011.00533.x
  13. Yadav VK, Raghav M, Sharma SK and Bhagat N. 2020. Rhizobacteriome: promising candidate for conferring drought tolerance in crops, J. Pure Appl. Microbiol. 14: 73-92. https://doi.org/10.22207/JPAM.14.1.10
  14. Boonchai R, Kaewsuk J, Seo G. 2014. Effect of nutrient starvation on nutrient uptake and extracellular polymeric substance for microalgae cultivation and separation. Desalin. Water Treat. 55: 360-367. https://doi.org/10.1080/19443994.2014.939501
  15. Ilyas N, Mumtaz K, Akhtar N, Yasmin H, Sayyed RZ, Khan W, et al. 2020. Exopolysaccharides producing bacteria for the amelioration of drought stress in wheat. Sustainability 12: 8876. https://doi.org/10.3390/su12218876
  16. Sayyed RZ, Patel PR, Shaikh SS. 2015. Plant growth promotion and root colonization by EPS producing Enterobacter sp. RZS5 under heavy metal contaminated soil. Indian J. Exp. Biol. 53: 116-123.
  17. Shultana R, Tan Kee Zuan A, Yusop MR, Mohd Saud H, Ayanda AF. 2020. Effect of Salt-tolerant bacterial inoculations on rice seedlings differing in salt-tolerance under saline soil conditions. Agronomy 10: 1030. https://doi.org/10.3390/agronomy10071030
  18. Shaik. Zulfikar Ali, Vardharajula Sandhya, Minakshi Grover, Venkateswar Rao Linga, Venkateswarlu Bandi. 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. 4: 239-246.
  19. Vardharajula S, Ali S Z. 2015. The production of exopolysaccharide by Pseudomonas putida GAP-P45 under various abiotic stress conditions and its role in soil aggregation. Microbiology 84: 512-519. https://doi.org/10.1134/S0026261715040153
  20. Saha I, Datta S, Biswas D. 2020. Exploring the role of bacterial extracellular polymeric substances for sustainable development in agriculture. Curr. Microbiol. 77: 3224-3239. https://doi.org/10.1007/s00284-020-02169-y
  21. Mathur P, Roy S. 2021. Insights into the plant responses to drought and decoding the potential of root associated microbiome for inducing drought tolerance. Physiol. Plant. 172: 1016-1029. https://doi.org/10.1111/ppl.13338
  22. Roca C, Alves V D, Freitas F, Reis MA. 2015. Exopolysaccharides enriched in rare sugars: bacterial sources, production, and applications. Front. Microbiol. 6: 288. https://doi.org/10.3389/fmicb.2015.00288
  23. Mishra A, Jha B. 2013. Microbial exopolysaccharides. In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds.), The Prokaryotes. Springer, Berlin, Heidelberg.
  24. Alami Y, Achouak W, Marol C, Heulin T. 2000. Rhizosphere soil aggregation and plant growth promotion of sunflowers by exopolysaccharide producing Rhizobium sp. strain isolated from sunflower roots. Appl. Environ. Microbiol. 66: 33933398.108.
  25. Schmid J, Sieber V, Rehm B. 2015. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front. Microbiol. 6: 496. https://doi.org/10.3389/fmicb.2015.00496
  26. Flemming HC, Wingender J. 2001. Relevance of microbial extracellular polymeric substances (EPSs)-parts I: structural and ecological aspects. Water Sci. Technol. 43: 1-8. https://doi.org/10.2166/wst.2001.0326
  27. Czaczyk K, Myszka K. 2007. Biosynthesis of extracellular polymeric substances (EPS) and its role in microbial biofilm formation. Polish J. Environ. Stud. 16: 799-806.
  28. Donot F, Fontana A, Baccou JC, Schorr-Galindo S. 2012. Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction. Carbohydr. Polym. 87: 951-962. https://doi.org/10.1016/j.carbpol.2011.08.083
  29. Sutherland IW. 2001. Microbial polysaccharides from Gram-negative bacteria. Int. Dairy J. 11: 663-674. https://doi.org/10.1016/S0958-6946(01)00112-1
  30. Velmourougane K, Prasanna R, Saxena AK 2017. Agriculturally important microbial biofilms: present status and prospects. J. Basic Microbiol. 57: 548-573. https://doi.org/10.1002/jobm.201700046
  31. More T T, Yadav J S S, Yan S, Tyagi R D, Surampalli R Y. 2014. Extracellular polymeric substances of bacteria and their potential environmental applications. J. Environ. Manage. 144: 1-25. https://doi.org/10.1016/j.jenvman.2014.05.010
  32. Laspidou CS, Rittmann BE. 2002. A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass. Water Res. 36: 2711-20. https://doi.org/10.1016/S0043-1354(01)00413-4
  33. Drogue B, Combes-Meynet E, Moenne-Loccoz Y, Wisniewski-Dye F, Prigent-Combaret C. 2013. "Control of the cooperation between plant growth-promoting rhizobacteria and crops by rhizosphere signals," in Vol. 1 and 2, pp. 281-294. Mol. Microb. Ecol. Rhizosphere, ed. F. J. de Bruijn (NJ, USA: John Wiley & Sons, Inc.).
  34. Prigent-Combaret C. 2013. "Control of the cooperation between plant growth-promoting rhizobacteria and crops by rhizosphere signals," in Vol. 1 and 2, pp. 281-294. Molecular Microbial Ecology of the Rhizosphere, ed. F. J. de Bruijn (NJ, USA: John Wiley & Sons, Inc.).
  35. Smith DL, Gravel V, Yergeau E. 2017. Editorial: signaling in the phytomicrobiome. Front. Plant Sci. 8: 611. https://doi.org/10.3389/fpls.2017.00611
  36. Miller MB, Bassler BL. 2001.Quorum sensing in bacteria. Annu. Rev. Microbiol. 55: 165-199. https://doi.org/10.1146/annurev.micro.55.1.165
  37. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
  38. Von Bodman SB, Majerczak DR, Coplin DL. 1998. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA 95: 7687-7692. https://doi.org/10.1073/pnas.95.13.7687
  39. Kalia VC, Gong C, Patel SKS, Lee JK. 2021. Regulation of plant mineral nutrition by signal molecules. Microorganisms 9: 774. https://doi.org/10.3390/microorganisms9040774
  40. 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
  41. Costa OYA, Raaijmakers JM, Kuramae EE. 2018. Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front. Microbiol. 23: 1636.
  42. Martin JP. 1971 Decomposition and binding action of polysaccharides in soil. Soil Biol. Biochem. 3: 33-41. https://doi.org/10.1016/0038-0717(71)90029-0
  43. Hillel D. 1982. Introduction to soil Physics. Academic Press Limited, 24-28 Oval Road, London.
  44. Sengupta S, Dey S. 2019. Microbial exo-polysaccharides (EPS): role in agriculture and environment. Agric. Food 1: 4-8M.
  45. Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, et al. 2021. Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 10: 259. https://doi.org/10.3390/plants10020259
  46. FAO. 2020. World Food and Agriculture - Statistical Yearbook 2020. Rome.
  47. Bouskill, NJ, Wood TE, Baran R, Ye Z, Bowen B P, Lim H, et al. 2016b. Below ground response to drought in a tropical forest soil. I. Changes in microbial functional potential and metabolism. Front. Microbiol. 7: 525. https://doi.org/10.3389/fmicb.2016.00525
  48. Kaci Y, Heyraud A, Barakat M and Heulin T. 2005. Isolation and identification of an EPS-producing Rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res. Microbiol. 156: 522-531. https://doi.org/10.1016/j.resmic.2005.01.012
  49. Konnova Svetlana, Brykova O, Sachkova O. Egorenkova I. Ignatov V. 2001. Protective role of the polysaccharide-containing capsular components of Azospirillum brasilense. Microbiology 70: 436-440. https://doi.org/10.1023/A:1010434227671
  50. Kohler J. Fuensanta C. Roldan, A. 2009. Effect of drought on the stability of Rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl. Soil Ecol. 42: 160-165. https://doi.org/10.1016/j.apsoil.2009.03.007
  51. Kohler J, Caravaca F. Carrasco L. Roldan A. 2006. Contribution of Pseudomonas mendocina and Glomus intraradices to aggregate stabilization and promotion of biological fertility in rhizosphere soil of lettuce plants under field conditions. Soil Use Manage. 22: 298-304. https://doi.org/10.1111/j.1475-2743.2006.00041.x
  52. Sandhya V, Ali SK, Minakshi G, Reddy G. Venkateswarlu B. 2009. Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAPP45. Biol. Fertil. Soils 46 : 17-26. https://doi.org/10.1007/s00374-009-0401-z
  53. Vardharajula S, Sk Z A. 2014. Exopolysaccharide production by drought tolerant Bacillus spp. and effect on soil aggregation under drought stress. J. Microbiol. Biotechnol. Food Sci. 4: 51-57. https://doi.org/10.15414/jmbfs.2014.4.1.51-57
  54. Sayyed RZ, Jamadar D, Patel PR. 2011 Production of Exopolysaccharide by Rhizobium sp. Indian J. Microbiol. 51: 294-300. https://doi.org/10.1007/s12088-011-0115-4
  55. Aureen, LG, Saroj B. 2009. Sand aggregation by exopolysaccharide producing Microbacterium arborescens-AGSB. Curr. Microbiol. 58: 616-621. https://doi.org/10.1007/s00284-009-9400-4
  56. Naseem H, Bano A. 2014. Role of plant growth-promoting rhizobacteria and their exopolysaccharide in drought tolerance of maize. J. Plant Interact. 9: 689-701. https://doi.org/10.1080/17429145.2014.902125
  57. Batool T, Ali S, Seleiman MF, Naveed NH, Ali A, Ahmed K, et al. 2020. Plant growth promoting rhizobacteria alleviates drought stress in potato in response to suppressive oxidative stress and antioxidant enzymes activities. Sci. Rep. 10: 16975 https://doi.org/10.1038/s41598-020-73489-z
  58. Hussain M B, Zahir ZA, Asghar HN, Asghar M. 2014. Can catalase and exopolysaccharides producing rhizobia ameliorate drought stress in wheat? Int. J. Agric. Biol. 16: 3-13
  59. Zhang X, Yang Z, Li Z. Zhang F, Hao L. 2020. Effects of drought stress on physiology and antioxidative activity in two varieties of Cynanchum thesioides. Braz. J. Bot. 43: 1-10. https://doi.org/10.1007/s40415-019-00573-8
  60. 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: e0222302. https://doi.org/10.1371/journal.pone.0222302
  61. Yadav J, Verma JP, Tiwari K N. 2010. Effect of plant growth promoting Rhizobacteria on seed germination and plant growth Chickpea (Cicer arietinum L) under in vitro condition Biological Forum. Int. J. 2: 15-18.
  62. Ansari FA, Ahmad I. 2019. Fluorescent pseudomonas-FAP2 and Bacillus licheniformis interact positively in biofilm mode enhancing plant growth and photosynthetic attributes. Sci. Rep. 9: 4547. https://doi.org/10.1038/s41598-019-40864-4
  63. Ali SZ, Sandhya V, Venkateswar Rao L. 2014. Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann. Microbiol. 64: 493-502. https://doi.org/10.1007/s13213-013-0680-3
  64. Lim JH, Kim SD. 2013. Induction of drought stress resistance by multi-functional PGPR Bacilluslicheniformis K11 in pepper. Plant Pathol. J. 29: 201-208. https://doi.org/10.5423/PPJ.SI.02.2013.0021
  65. Khan N, Bano A, Cura JA. 2020. Role of beneficial microorganisms and salicylic acid in improving rainfed agriculture and future food safety. Microorganisms 8: 1018. https://doi.org/10.3390/microorganisms8071018
  66. Lu X, Liu SF, Yue L, Zhao X, Zhang Y-B, Xie Z-K, et al. 2018. Epsc involved in the encoding of exopolysaccharides produced by Bacillus amyloliquefaciens FZB42 act to boost the drought tolerance of Arabidopsis thaliana. Int. J. Mol. Sci. 19: 3795. https://doi.org/10.3390/ijms19123795
  67. 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. 20: 6271. https://doi.org/10.3390/ijms20246271
  68. Ghosh D, Gupta A, Mohapatra S. 2019. A comparative analysis of exopolysaccharide and phytohormone secretions by four drought-tolerant rhizobacterial strains and their impact on osmotic-stress mitigation in Arabidopsis thaliana. World J. Microbiol. Biotechnol. 35: 90. https://doi.org/10.1007/s11274-019-2659-0
  69. Igiehon NO, Babalola OO, Aremu BR. 2019. Genomic insights into plant growth promoting rhizobia capable of enhancing soybean germination under drought stress. BMC Microbiol. 19: 159. https://doi.org/10.1186/s12866-019-1536-1
  70. Susilowati A, Puspita AA, and Yunus, A. 2018. Drought resistant of bacteria producing exopolysaccharide and IAA in rhizosphere of soybean plant (Glycine max) in Wonogiri Regency Central Java Indonesia. IOP Conf. Series: Earth and Environmental Science 142 (2018) 012058.
  71. Niu X, Song L, Xiao Y, Ge W. 2018. Drought-tolerant plant growth-promoting rhizobacteria associated with foxtail millet in a semiarid agroecosystem and their potential in alleviating drought stress. Front. Microbiol. 8: 2580. https://doi.org/10.3389/fmicb.2017.02580
  72. Cho SM, Anderson AJ, Kim YC. 2018. Extracellular polymeric substances of Pseudomonaschlororaphis 06 induce systemic drought tolerance in plants. Res. Plant Dis. 24: 242-247.2018. https://doi.org/10.5423/RPD.2018.24.3.242
  73. Vardharajula S, Ali Sk Z. 2014. Exopolysaccharide production by drought tolerant Bacillus spp. and effect on soil aggregation under drought stress. J. Microbiol. Biotechnol. Food Sci. 4: 51-57. https://doi.org/10.15414/jmbfs.2014.4.1.51-57
  74. Timmusk S, Abd El-Daim IA, Copolovici L, Tanilas T, Kannaste A, Behers L, et al. 2014. Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9: e96086. https://doi.org/10.1371/journal.pone.0096086
  75. Gontia-Mishra I, Sapre S, Sharma A. Tiwari S. 2016. Amelioration of drought tolerance in wheat by the interaction of plantgrowthpromoting rhizobacteria. Plant Biol.18: 992-1000. https://doi.org/10.1111/plb.12505
  76. Camaille M, Fabre N, Clement C, Ait Barka E. 2021.Advances in wheat physiology in response to drought and the role of plant growth promoting rhizobacteria to trigger drought tolerance. Microorganisms 9: 687. https://doi.org/10.3390/microorganisms9040687
  77. FAO, ITPS, GSBI, CBD and EC. 2020. State of knowledge of soil biodiversity - Status, challenges and potentialities, Report 2020. Rome, FAO.
  78. Deng J, Orner EP, Chau JF, Anderson EM, Kadilak AL, Rubinstein RL, et al. 2015. Synergistic effects of soil microstructure and bacterial EPS on drying rate in emulated soil micromodels. Soil Biol. Biochem. 83: 116-124. https://doi.org/10.1016/j.soilbio.2014.12.006
  79. Ma Y, Dias MC, Freitas H. 2020. Drought and salinity stress responses and microbe-induced tolerance in plants. Front. Plant Sci. 11: 591911. https://doi.org/10.3389/fpls.2020.591911
  80. Parida S K, and Das A B. 2005. Salt tolerance and salinity effects on plants. Ecotoxicol. Environ. Safety 60: 324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010
  81. Gupta B, Huang B. 2014. Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int. J. Genomics 2014: 701596. https://doi.org/10.1155/2014/701596
  82. Qurashi AW, Sabri AN. 2012a. Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz. J. Microbiol. 43: 1183-1191. https://doi.org/10.1590/S1517-83822012000300046
  83. Minah B, Hazarin Subair F. 2015. Isolation and Screening bacterial exopolysaccharide (EPS) from potato rhizosphere in highland and the potential as a producer indole acetic acid (IAA). Procedia Food Sci. 3: 74-81. https://doi.org/10.1016/j.profoo.2015.01.007
  84. Tewari S, Arora NK. 2014a. Multifunctional exopolysaccharides from Pseudomonas aeruginosa PF23 involved in plant growth stimulation, biocontrol and stress amelioration in sunflower under saline conditions. Curr. Microbiol. 69: 484-494. https://doi.org/10.1007/s00284-014-0612-x
  85. Singh RP, Jha PN.2016. A halotolerant bacterium Bacillus licheniformis HSW-16 augments induced systemic tolerance to salt stress in wheat plant (Triticum aestivum). Front. Plant Sci. 7: 1890. https://doi.org/10.3389/fpls.2016.01890
  86. Pawar ST, Amarsinh A. Bhosale, Trishala B. Gawade, Nale TR. 2013. Isolation, screening and optimization of exopolysaccharide producing bacterium from saline soil. J. Microbiol. Biotechnol. Res. 3: 24-31.
  87. Choudhary DK, Kasotia A, Jain S, Vaishnav A, Kumari S, Sharma KP, et al. 2015. Bacterial-mediated tolerance and resistance to plants under abiotic and biotic stress. J. Plant Growth Regul. 35: 276-300. https://doi.org/10.1007/s00344-015-9521-x
  88. Ashraf M, Berge SH, Mahmood OT. 2004. Inoculating wheat seedling with exopolysaccharides-producing bacteria restrict sodium uptake and stimulates plant growth under salt stress. Biol. Fertil Soils 40: 157-162.
  89. Arora M, Kaushik A, Rani N, Kaushik CP. 2010. Effect of cyanobacterial exopolysaccharides on salt stress alleviation and seed germination. J. Environ. Biol. 31: 701-704.
  90. Ha-Tran DM, Nguyen TTM, Hung SH, Huang E, Huang CC. 2021. Roles of plant growth-promoting Rhizobacteria (PGPR) in stimulating salinity stress defense in plants: a review. Int. J. Mol. Sci. 22: 3154. https://doi.org/10.3390/ijms22063154
  91. Yasmeen T, Ahmad A, Arif MS, Mubin M, Rehman K, Shahzad SM, et al. 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
  92. Bhat MA, Kumar V, Bhat MA, Wani IA, Dar FL, Farooq I, et al. 2020. Mechanistic Insights of the interaction of Plant Growth-Promoting Rhizobacteria (PGPR) with plant roots toward enhancing plant productivity by alleviating salinity stress. Front. Microbiol. 20: 1952.
  93. Lloret J, Wulff BB, Rubio JM, Downie J A, Bonilla I, Rivilla R. 1998. Exopolysaccharide II production is regulated by salt in the halotolerant strain Rhizobium meliloti EFB1. Appl. Environ. Microbiol. 64: 1024-1028. https://doi.org/10.1128/AEM.64.3.1024-1028.1998
  94. Atouei M T, Pourbabaee A A, Shorafa M. 2019. Alleviation of salinity stress on some growth parameters of wheat by exopolysaccharide-producing bacteria. Ir. J. Sci. Technol. Trans. A. 43: 2725-2733. https://doi.org/10.1007/s40995-019-00753-x
  95. Chu TN, Tran BTH, Van Bui L, Hoang MTT. 2019. Plant growth-promoting rhizobacterium Pseudomonas PS01 induces salt tolerance in Arabidopsis thaliana. BMC Res. Notes 12: 11 https://doi.org/10.1186/s13104-019-4046-1
  96. Wang J, Song L, Gong X, Xu J, Li M. 2020. Functions of jasmonic acid in plant regulation and response to abiotic stress. Int. J. Mol. Sci. 21: 1446. https://doi.org/10.3390/ijms21041446
  97. Sultana S, Paul SC, Parveen S, Alam S, Rahman N, Jannat B, et al. 2020. Isolation and identification of salt-tolerant plant-growth-promoting rhizobacteria and their application for rice cultivation under salt stress. Can. J. Microbiol. 66: 144-160. https://doi.org/10.1139/cjm-2019-0323
  98. Liu X, Luo Y, Li Z, Wang J, Wei G. 2017. Role of exopolysaccharide in salt stress resistance and cell motility of Mesorhizobium alhagi CCNWXJ12-2T. Appl. Microbiol. Biotechnol. 101: 2967-2978. https://doi.org/10.1007/s00253-017-8114-y
  99. Abd El-Ghany, Mona FA Attia, Magdy. 2020. Effect of exopolysaccharide-producing bacteria and melatonin on faba bean production in saline and non-saline soil agronomy. 10: 316. https://doi.org/10.3390/agronomy10030316
  100. Nunkaew T, Kantachote D, Nitoda T, Kanzaki H, Ritchie RJ. 2015. Characterization of exopolymeric substances from selected Rhodopseudomonas palustris strains and their ability to adsorb sodium ions. Carbohydr. Polym. 22: 115: 334-41. https://doi.org/10.1016/j.carbpol.2014.08.099
  101. Amna Xia Y, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, et al. 2020. Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol. Biochem. 151: 1640-1649.
  102. Oosten V, Stasio MJ. Cirillo ED, Silletti V, Ventorino S, Pepe V, Raimondi O, Maggio G A. 2018. Root inoculation with Azotobacter chroococcum 76A enhances tomato plants adaptation to salt stress under low N conditions. BMC Plant Biol. 18: 205. https://doi.org/10.1186/s12870-018-1411-5
  103. Mohammad A F. 2018. Effectiveness of exopolysaccharides and biofilm forming plant growth promoting rhizobacteria on salinity tolerance of faba bean (Vicia faba L.). Afr. J. Microbiol. Res. 12: 399-404. https://doi.org/10.5897/AJMR2018.8822
  104. Kumari P and Khanna V. 2015. ACC-deaminase and EPS production by salt tolerant rhizobacteria augment growth in chickpea under salinity stress. Int. J. Bio-resource Stress Manage. 6: 558-565. https://doi.org/10.5958/0976-4038.2015.00084.6
  105. Yang A, Akhtar SS, Iqbal S, Amjad M, Naveed M, Zahir ZA, et al. 2016. Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Funct. Plant Biol. 43: 632-642. https://doi.org/10.1071/FP15265
  106. Bano A and Fatima M. 2009. Salt tolerance in Zea mays(L). following inoculation with Rhizobium and Pseudomonas. Biol. Fertil. Soils 45: 405-413. https://doi.org/10.1007/s00374-008-0344-9
  107. Ashraf M, Ahmad MSA, Ozturk M, Aksoy A. 2012. Crop improvement through different means. In Ashraf et al. (eds.), pp. 1-15. Crop Production for Agricultural Improvement, Springer.
  108. Nawaz MS, Arshad A, Rajput L, Fatima K, Ullah S, Ahmad M, et al. 2020. Growth-stimulatory effect of quorum sensing signal molecule N-Acyl-Homoserine lactone-producing multi-trait Aeromonas spp. on wheat genotypes under salt stress. Front. Microbiol. 29: 11:553621. https://doi.org/10.3389/fmicb.2020.553621
  109. Chibuike GU, Obiora SC 2014. Heavy metal polluted soils: effect on plants and bioremediation methods. Appl. Environ. Soil Sci. 2014: 1-12. https://doi.org/10.1155/2014/752708
  110. Adrees M, Ali S, Rizwan M, Zia-Ur-Rehman M, Ibrahim M, Abbas F, et al. 2015. Mechanisms of silicon-mediated alleviation of heavy metal toxicity in plants: a review. Ecotoxicol. Environ. Saf. 119: 186-97. https://doi.org/10.1016/j.ecoenv.2015.05.011
  111. Violante A, Cozzolino V, PerelomovL, Caporale AG, Pigna M. 2010. Mobility and bioavailability of heavy metals and metalloids in soil environments. J. Soil. Sci. Plant Nutr. 10: 268-292.
  112. Mishra J, Singh R, Arora N K. 2017. Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front. Microbiol. 8: 1706. https://doi.org/10.3389/fmicb.2017.01706
  113. Ayangbenro AS, Babalola OO. 2017. A New strategy for heavy metal polluted environments: a review of microbial biosorbents. Int. J. Environ. Res. Public Health 14: 94. https://doi.org/10.3390/ijerph14010094
  114. Dobrowolski R, Szczes A, Czemierska M, Jarosz-Wikolazka A. 2017. Studies of cadmium (II), lead (II), nickel (II), cobalt (II) and chromium (VI) sorption on extracellular polymeric substances produced by Rhodococcus opacus and Rhodococcus rhodochrous. Bioresour. Technol. 225: 113-120. https://doi.org/10.1016/j.biortech.2016.11.040
  115. Karthik C, Elangovan N, Kumar TS, Govindharaju S, Barathi S, Oves M, et al. 2017. Characterization of multifarious plant growth promoting traits of rhizobacterial strain AR6 under Chromium (VI) stress. Microbiol. Res. 204: 65-71. https://doi.org/10.1016/j.micres.2017.07.008
  116. Zainab N, Bashir Ud Din A, Muhammad Tariq Javed M, Siddique Afridi M, Tehmeena Mukhtar, Kamran Muhammad Aqeel, et al. 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
  117. Jittawuttipoka T, Planchon M, Spalla O, Benzerara K, Guyot F, Cassier-Chauvat C , et al. 2013. Multidisciplinary evidences that synechocystis PCC6803 exopolysaccharides operate in cell sedimentation and protection against salt and metal stresses. PLoS One 8: e55564. https://doi.org/10.1371/journal.pone.0055564
  118. Kalita D, Joshi SR. 2017. Study on bioremediation of Lead by exopolysaccharide producing metallophilic bacterium isolated from extreme habitat. Biotechnol. Rep. 16: 48-57. https://doi.org/10.1016/j.btre.2017.11.003
  119. Getahun A, Muleta D, Assefa F, Kiros S. 2020. Plant growth-promoting rhizobacteria isolated from degraded habitat enhance drought tolerance of acacia (Acacia abyssinica Hochst. ex Benth.) seedlings. Int. J. Microbiol. 2020: 8897998.
  120. 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. https://doi.org/10.3389/fmicb.2019.01207
  121. Ali J, Ali F, Ahmad I, Rafique M, Munis MFH, Hassan SW, et al. 2020. Mechanistic elucidation of germination potential and growth of Sesbania sesban seedlings with Bacillus anthracis PM21 under heavy metals stress: an in vitro study. Ecotoxicol. Environ. Saf. 208: 111769.
  122. Thijs S, Sillen W, Weyens N, Vangronsveld J. 2017. Phytoremediation: 2017. State-of-the-art and a key role for the plant microbiome in future trends and research prospects. Int. J. Phytoremed. 19: 23-38. https://doi.org/10.1080/15226514.2016.1216076
  123. Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP. 2016. Potential biotechnological strategies for the clean up of heavy metals and metalloids Front. Plant Sci. 7: 303. https://doi.org/10.3389/fpls.2016.00303
  124. Teixeira EI, Fischer G, Velthuizen HV, Walter C, Ewert F. 2013 Global hot spots of heat stress on agricultural crops due to climate change. Agric. Meteorol. 170: 206-215. https://doi.org/10.1016/j.agrformet.2011.09.002
  125. FAO (2017). Water Scarcity - One of the greatest challenges of our time. Food and Agriculture Organization of the United Nations.
  126. Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, et al. 2017. Crop production under drought and heat stress: plant responses and management options. Front. Plant Sci. 8: 1147. https://doi.org/10.3389/fpls.2017.01147
  127. Kumar S, Thakur P, Kaushal N, Malik J. A Gaur P, Nayyar H. 2013. Effect of varying high temperatures during reproductive growth on reproductive function, oxidative stress and seed yield in chickpea genotypes differing in heat sensitivity. Arch. Agronomy Soil Sci. 59: 823-843. https://doi.org/10.1080/03650340.2012.683424
  128. Devasirvatham V, Gaur PM, Mallikarjuna N, Tokachichu RN, Trethowan, RM, Tan DK. 2012. Effect of high temperature on the reproductive development of chickpea genotypes under controlled environments. Funct. Plant Biol. 39: 1009-1018. https://doi.org/10.1071/FP12033
  129. Kaur R, Bains TS, Bindumadhava H, Nayyar H. 2015. Responses of mungbean (Vigna radiata L.) genotypes to heat stress: effects on reproductive biology, leaf function and yield traits. Sci. Hortic. 197: 527-541. https://doi.org/10.1016/j.scienta.2015.10.015
  130. Prasad PV V, Djanaguiraman M, Perumal R, Ciampitti IA. 2015. Impact of high temperature stress on floret fertility and individual grain weight of grain sorghum: sensitive stages and thresholds for temperature and duration. Front. Plant Sci. 6: 1-11. https://doi.org/10.3389/fpls.2015.00001
  131. Farooq M, Bramley H, Palta JA, Siddique KHM. 2011. Heat stress in wheat during reproductive and grain-filling phases. CRC Crit. Rev. Plant Sci. 30: 491-507. https://doi.org/10.1080/07352689.2011.615687
  132. Sita K, Sehgal A, Kumar J, Kumar S, Singh S, Siddique KH, et al. 2017. Identification of high-temperature tolerant lentil (Lens culinaris Medik.) genotypes through leaf and pollen traits. Front. Plant Sci. 8: 1-26.
  133. Bramhachari PV, Nagaraju GP, Kariali E. 2018. Current perspectives on rhizobacterial-EPS interactions in alleviation of stress responses: novel strategies for sustainable agricultural productivity. In Role of Rhizospheric Microbes in Soil; Springer: Singapore. 2018: 33-55.
  134. Ali SZ, Sandhya V, Grover M., Linga VR, Bandi V. 2011. Effect of inoculation with a thermo-tolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J. Plant. Interact. 6: 239-246. https://doi.org/10.1080/17429145.2010.545147
  135. Mukhtar T, Rehman S, Smith D, Sultan T, Seleiman M, Alsadon A, et al. 2020. Mitigation of heat stress in Solanum lycopersicum L. by ACC-deaminase and exopolysaccharide. Producing Bacillus cereus: effects on biochemical profiling. Sustainability 12: 2159. https://doi.org/10.3390/su12062159
  136. Parsell DA, Lindquist S. 1993. The function of heat shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27: 437-496. https://doi.org/10.1146/annurev.ge.27.120193.002253
  137. Nandal K, Sehrawat AR, Yadav AS, Vashishat RK, Boora KS. 2005. High temperature-induced changes in exopolysaccharides, lipopolysaccharides, and protein profile of heat-resistant mutants of Rhizobium sp. (Cajanus). Microbiol. Res. 160: 367 - 373. https://doi.org/10.1016/j.micres.2005.02.011
  138. Nguyena HT, Razafindralambo H, Blecker C, N'Yapoa C, Thonart P, Delvignea F. 2014. Stochastic exposure to sub-lethal high temperature enhances exopolysaccharides (EPS) excretion and improves Bifidobacterium bifidum cell survival to freeze-drying. Biochem. Eng. J. 88: 85-94. https://doi.org/10.1016/j.bej.2014.04.005
  139. Bensalim, S, Nowak J, Asiedu SK. 1998 A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am. J. Pot. Res. 75: 145-152. https://doi.org/10.1007/BF02895849
  140. Abd El-Daim I A, Bejai S, Fridborg I. Meijer J. 2018. Identifying potential molecular factors involved in Bacillus amyloliquefaciens 5113 mediated abiotic stress tolerance in wheat. Plant Biol. 20: 271-279. https://doi.org/10.1111/plb.12680
  141. Shin DJ, Yoo SJ, Hong JK, Weon HY, Song J, Sang MK. 2019. Effect of Bacillus aryabhattai H26-2 and B. siamensis H30-3 on Growth promotion and alleviation of heat and drought stresses in Chinese cabbage. Plant Pathol. J. 35: 178-187. https://doi.org/10.5423/PPJ.NT.08.2018.0159
  142. Ogden AJ, McAleer JM, Kahn ML. 2019. Characterization of the Sinorhizobium meliloti HslUV and ClpXP protease systems in freeliving and symbiotic states. J. Bacteriol. 201: e00498-18.
  143. Nishihata S, Kondo T, Tanaka K. et al. 2018. Bradyrhizobium diazoefficiens USDA110 PhaR functions for pleiotropic regulation of cellular processes besides PHB accumulation. BMC Microbiol. 18: 156. https://doi.org/10.1186/s12866-018-1317-2
  144. Mishra PK, Bisht SC, Ruwari P, Selvakumar G, Joshi GK, Bisht JK, et al. 2018. Alleviation of cold stress in inoculated wheat (Triticum aestivum L.) seedlings with psychrotolerant Pseudomonads from NW Himalayas. Arch Microbiol. 193: 497-513. https://doi.org/10.1007/s00203-011-0693-x
  145. Zubair M, Hanif A, Farzand A, Sheikh T, Khan A R, 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 7: 337. https://doi.org/10.3390/microorganisms7090337
  146. Ait Barka E, Nowak J, Clement C. 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth promoting Rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72: 7246-7252. https://doi.org/10.1128/AEM.01047-06
  147. Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clement C, et al. 2012. Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol. Plant Microbe Interact. 25: 496-504. https://doi.org/10.1094/MPMI-09-11-0245
  148. Wang C, Wang C, Gao YL, Wang Y-P, Guo J-H. 2016. A Consortium of three plant growth-promoting Rhizobacterium strains acclimates Lycopersicon esculentum and confers a better tolerance to chilling stress. J. Plant Growth Regul. 35: 54-64. https://doi.org/10.1007/s00344-015-9506-9
  149. Abd El-Daim IA, Bejai S, Meijer J. 2019. Bacillus velezensis 5113 Induced metabolic and molecular reprogramming during abiotic stress tolerance in wheat. Sci. Rep. 9: 16282. https://doi.org/10.1038/s41598-019-52567-x

Cited by

  1. Microbial Derived Compounds Are a Promising Approach to Mitigating Salinity Stress in Agricultural Crops vol.12, 2021, https://doi.org/10.3389/fmicb.2021.765320
  2. The Regulatory Functions of σ54 Factor in Phytopathogenic Bacteria vol.22, pp.23, 2021, https://doi.org/10.3390/ijms222312692