Journal of Life Science (생명과학회지)

Korean Society of Life Science (한국생명과학회)
권호 표지
DOI QR코드

DOI QR Code

Current Perspectives on the Effects of Plant Growth-promoting Rhizobacteria

식물생장촉진 근권미생물의 영향에 대한 연구 현황 및 전망

  • Le, Thien Tu Huynh (Department of Applied Bioscience, Graduate School of Natural Science, Dong-A University) ;
  • Jun, Sang Eun (Department of Molecular Genetics, College of Natural Resources and Life Science, Dong-A University) ;
  • Kim, Gyung-Tae (Department of Applied Bioscience, Graduate School of Natural Science, Dong-A University)
  • Received : 2019.11.06
  • Accepted : 2019.11.21
  • Published : 2019.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

The rhizosphere is the active zone where plant roots communicate with the soil microbiome, each responding to the other's signals. The soil microbiome within the rhizosphere that is beneficial to plant growth and productivity is known as plant growth-promoting rhizobacteria (PGPR). PGPR take part in many pivotal plant processes, including plant growth, development, immunity, and productivity, by influencing acquisition and utilization of nutrient molecules, regulation of phytohormone biosynthesis, signaling, and response, and resistance to biotic- and abiotic-stresses. PGPR also produce secondary compounds and volatile organic compounds (VOCs) that elicit plant growth. Moreover, plant roots exude attractants that cause PGPR to aggregate in the rhizosphere zone for colonization, improving soil properties and protecting plants against pathogenic factors. The interactions between PGPR and plant roots in rhizosphere are essential and interdependent. Many studies have reported that PGPR function in multiple ways under the same or diverse conditions, directly and indirectly. This review focuses on the roles and strategies of PGPR in enhancing nutrient acquisition by nutrient fixation/solubilization/mineralization, inducing plant growth regulators/phytohormones, and promoting growth and development of root and shoot by affecting cell division, elongation, and differentiation. We also summarize the current knowledge of the effects of PGPR and the soil microbiota on plants.

근권은 식물 뿌리와 토양 미생물이 서로의 신호를 주고 받으며 끊임없이 상호반응하는 역동적인 장소이다. 근권 주위에서 식물의 생장과 생산성에 유익한 토양 미생물을 식물생장촉진근권미생물(Plant Growth Promoting Rhizobacteria, PGPR)이라 칭하며, 이 PGPR은 식물 전 생장기간동안 생물학적 및 비생물학적 스트레스에 대한 저항성, 식물 호르몬 조절, 영양분의 흡수와 이용 등에 영향을 끼침으로써 식물의 생장과 발달, 면역, 생산력 등 중요한 생명 과정에 관여한다. 그리고, PGPR은 식물 생장을 유도하는 2차 대사산물이나 휘발성 유기 화합물을 생산하고, 식물의 뿌리 역시 식물 유해한 인자 혹은 병원성 인자에 대항하여 자신을 보호하거나 토양 성질 개선을 위해, PGPR을 유인하고 정착시키기 위한 물질을 생산, 분비한다. 그러므로, 식물과 PGPR 사이의 상호작용은 필수적이면서도 상호의존적이다. 현재까지, PGPR에 대한 많은 연구는 직간접적 개념에 대하여 공통적 또는 다양한 조건들에서 여러 방식으로 PGPR의 기능을 밝히는 방향으로 전개되어 왔다. 본 총설에서는 세포분열과 팽창, 분화에 의한 식물의 생장과 발달의 촉진, 식물생장조절인자와 호르몬의 유도, 영양물질의 고정, 용해, 무기화를 촉진하기 위한 PGPR의 역할과 전략을 소개하였다. 또한 PGPR와 토양 미생물군의 효과에 대한 현재까지의 연구 정보를 요약하였다.

Keywords

References

  1. Abaid-Ullah, M., Hassan, M. N., Jamil, M., Brader, G., Shah, M. K., Sessitsch, A. and Hafeez, F. Y. 2015. Plant growth promoting rhizobacteria: an alternate way to improve yield and quality of wheat (Triticum aestivum). Int. J. Agric. Biol. 17, 51-60.
  2. Ahemad, M. 2012. Implications of bacterial resistance against heavy metals in bioremediation: a review. J. Inst. Integr. Omics Appl. Biotechnol. 3, 39-46.
  3. Ahemad, M. and Khan, M. S. 2010d. Phosphate-solubilizing and plant growth promoting Pseudomonas aeruginosa PS1 improves greengram performance in quizalafop-p-ethyl and clodinafop amended soil. Arch. Environ. Contam. Toxicol. 58, 361-372. https://doi.org/10.1007/s00244-009-9382-z
  4. Ahemad, M. and Khan, M. S. 2012a. Effect of fungicides on plant growth promoting activities of phosphate solubilizing Pseudomonas putida isolated from mustard (Brassica compestris) rhizosphere. Chemosphere 86, 945-950. https://doi.org/10.1016/j.chemosphere.2011.11.013
  5. Ahemad, M. and Kibret, M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. J. King Saud Univ. Sci. 26, 1-20. https://doi.org/10.1016/j.jksus.2013.05.001
  6. Albacete, A., Ghanem, M. E., Martinez-Andujar, C., Acosta, M., Sanchez-Bravo, J., Martinez, V., Lutts, S., Dodd, I. C. and Perez-Alfocea, F. 2008. Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 59, 4119-4131. https://doi.org/10.1093/jxb/ern251
  7. Alves, B. J. R., Boddey, R. M. and Urquiaga, S. 2004. The success of Biological Nitrogen Fixation (BNF) in soybean in Brazil. Plant Soil. 252, 1-9. https://doi.org/10.1023/A:1024191913296
  8. Ammari, T. and Mengel, K. 2006. Total soluble Fe in soil solutions of chemically different soils. Geoderma 136, 876-885. https://doi.org/10.1016/j.geoderma.2006.06.013
  9. Anand, K., Kumari, B. and Mallick, M. A. 2016. Phosphate solubilizing microbes: An effective and alternative approach as biofertilizers. Int. J. Pharm. Pharm. Sci. 8, 37-40. https://doi.org/10.22159/ijpps.2016.v8i9.11466
  10. Arkhipova, T., Veselov, S., Melentiev, A., Martynenko, E. and Kudoyarova, G. 2005. Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil. 272, 201-209. https://doi.org/10.1007/s11104-004-5047-x
  11. Arora, N. K., Tewari, S. and Singh, R. 2013. Multifaceted plant-associated microbes and their mechanisms diminish the concept of direct and indirect PGPRs, pp. 411-449. In: Arora, N. K. (ed) Plant microbe symbiosis: fundamentals and advances. Springer, New Delhi, India.
  12. Arshad, M. and Frankenberger, W. T. 1998. Plant growth-regulating substances in the rhizosphere: Microbial production and functions. Adv. Agron. 62, 46-151.
  13. Bahadur, I., Maurya, B. R., Meena, V. S., Saha, M., Kumar, A. and Aeron, A. 2017. Mineral release dynamics of tricalcium phosphate and waste muscovite by mineral-solubilizing rhizobacteria (MSR) isolated from Indo-Gangetic Plain (IGP) of India. Geomicrobiol. J. 34, 454-466. https://doi.org/10.1080/01490451.2016.1219431
  14. Bailly, A. and Weisskopf, L. 2012. The modulating effect of bacterial volatiles on plant growth: current knowledge and future challenges. Plant Signal. Behav. 7, 79-85. https://doi.org/10.4161/psb.7.1.18418
  15. Belimov, A. A., Dodd, I. C., Hontzeas, N., Theobald, J. C., Safronova, V. I. and Davies, W. J. 2009. Rhizosphere bacteria containing ACC deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol. 181, 413-423. https://doi.org/10.1111/j.1469-8137.2008.02657.x
  16. Belimov, A. A., Kunakova, A. M., Safronova, V. I., Stepanok, V. V., Iudkin, L. Iu., Alekseev, Iu. V. and Kozhemiakov, A. P. 2004. Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiologia 73, 99-106.
  17. Berendsen, R. L., Pieterse, C. M. and Bakker, P. A. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478-486. https://doi.org/10.1016/j.tplants.2012.04.001
  18. Berg, G. and Smalla, K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1-13. https://doi.org/10.1111/j.1574-6941.2009.00654.x
  19. Bhattacharyya, P. N. and Jha, D. K. 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28, 1327-1350. https://doi.org/10.1007/s11274-011-0979-9
  20. Bishopp, A., Mahonen, A. P. and Helariutta, Y. 2006. Signs of change: Hormone receptors that regulate plant development. Development 133, 1857-1869. https://doi.org/10.1242/dev.02359
  21. Bomke, C. and Tudzynski, B. 2009. Diversity, regulation and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70, 1876-1893. https://doi.org/10.1016/j.phytochem.2009.05.020
  22. Borrell, A. K., Hammer, G. L. and Henzell, R. G. 2000. Does maintaining green leaf area in sorghum improve yield under drought? II. Dry matter production and yield. Crop Sci. 40, 1037-1048. https://doi.org/10.2135/cropsci2000.4041037x
  23. Bottini, R., Cassan, F. and Piccoli, P. 2004. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 65, 497-503. https://doi.org/10.1007/s00253-004-1696-1
  24. Cassan, F., Vanderleyden, J. and Spaepen, S. 2014. Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J. Plant Growth Regul. 33, 440-459. https://doi.org/10.1007/s00344-013-9362-4
  25. Chen, Y. P., Rekha, P. D., Arun, A. B., Shen, F. T., Lai, W. A. and Young, C. C. 2006. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl. Soil Ecol. 34, 33-41. https://doi.org/10.1016/j.apsoil.2005.12.002
  26. Cohen, A. C., Bottini, R. and Piccoli, P. N. 2008. Azospirillum brasilense Sp245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul. 54, 97-103. https://doi.org/10.1007/s10725-007-9232-9
  27. Cohen, A. C., Travaglia, C. N., Bottini, R. and Piccoli, P. N. 2009. Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87, 455-462. https://doi.org/10.1139/B09-023
  28. Cohen, A. C., Bottini, R., Pontin, M., Berli, F. J., Moreno, D., Boccanlandro, H., Travaglia, C. N. and Piccoli, P. N. 2015. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol. Plant. 153, 79-90. https://doi.org/10.1111/ppl.12221
  29. Conrath, U., Beckers, G. J. M., Flors, V., Garcia-Agustin, P., Jakab, G. and Mauch, F. 2006. Priming: getting ready for battle. Mol. Plant Microbe. Interact. 19, 1062-1071. https://doi.org/10.1094/MPMI-19-1062
  30. Crowley, D. E. 2006 Microbial Siderophores in the Plant Rhizosphere, pp 169-198. In: Barton L.L. and Abadia J. (eds), Iron Nutrition in Plants and Rhizospheric Microorganisms. Springer Publisher: Dordrecht, The Netherland.
  31. Dakora, F., Matiru, V. and Kanu, A. 2015. Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants. Front. Plant Sci. 6, 700. https://doi.org/10.3389/fpls.2015.00700
  32. Das, A. J., Kumar, M. and Kumar, R. 2013. Plant growth promoting rhizobacteria (PGPR): An alternative of chemical fertilizer for sustainable, environment friendly agriculture. Res. J. Agric. For. Sci. 1, 21-23.
  33. Davies, P. J. 2010. Introduction, pp. 1-35. In: Davies, P. J. (ed.), Plant hormones: Biosynthesis, signal transduction, action! revised 3rd edition. Springer Publisher: Dordrecht, The Netherland.
  34. Deka, H., Deka, S. and Baruah, C. 2015. Plant growth promoting rhizobacteria for value addition: mechanism of action, pp 305-321. In: Egamberdieva, D., Shrivastava, S., Varma, A. (Eds.), Plant-Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants. Springer International Publishing, Cham, New York, U. S. A.
  35. Dobbelaere, S., Vanderleyden, J. and Okon, Y. 2003. Plant growth promoting effects of diazotrophs in the rhizosphere. Crit. Rev. Plant Sci. 22, 107-149. https://doi.org/10.1080/713610853
  36. Dodd, I. C., Zinovkina, N. Y., Safronova, V. I. and Belimov, A. A. 2010. Rhizobacterial mediation of plant hormone status. Ann. Appl. Biol. 157, 361-379. https://doi.org/10.1111/j.1744-7348.2010.00439.x
  37. Duca, D., Lorv, J., Patten, C. L., Rose, D. and Glick, B. R. 2014. Indole-3-acetic acid in plant-microbe interactions. Antonie van Leeuwenhoek 106, 85-125. https://doi.org/10.1007/s10482-013-0095-y
  38. Egamberdieva, D. and Lugtenberg, B. 2014. Use of Plant Growth-Promoting Rhizobacteria to Alleviate Salinity Stress in Plants, pp 73-96. In: Miransari, M. (ed) Use of Microbes for the Alleviation of Soil Stresses, Volume 1. Springer Publisher: New York, U. S. A.
  39. Etesami, H., Emami, S. and Alikhani, H. A. 2017. Potassium solubilizing bacteria (KSB): Mechanisms, promotion of plant growth, and future prospects ­ A review. J. Soil Sci. Plant Nutr. 17, 897-911. https://doi.org/10.4067/S0718-95162017000400005
  40. Galland, M., Gamet, L., Varoquaux, F., Touraine, B., Touraine, B. and Desbrosses, G. 2012. The ethylene pathway contributes to root hair elongation induced by the beneficial bacteria Phyllobacterium brassicacearum STM196. Plant Sci. 190, 74-81. https://doi.org/10.1016/j.plantsci.2012.03.008
  41. Ghosh, S. and Basu, P. S. 2006. Production and metabolism of indole acetic acid in roots and root nodules of Phaseolus mungo. Microbiol. Res. 161, 362-366. https://doi.org/10.1016/j.micres.2006.01.001
  42. Glick, B. R., Penrose, D. M. and Li, J. P. 1998. A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J. Theor. Biol. 190, 63-68. https://doi.org/10.1006/jtbi.1997.0532
  43. Glick, B. R. 2012. Plant Growth-Promoting Bacteria: Mechanisms and Applications. Scientifica (Cairo) 2012, 963401.
  44. Gontia-Mishra, I., Sapre, S., Sharma, A. and Tiwari, S. 2016. Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J. Plant Growth Regul. 35, 1000-1012. https://doi.org/10.1007/s00344-016-9598-x
  45. Gouws, L. M., Botes, E., Wiese, A. J., Trenkamp, S., Torres-Jerez, I., Tang, Y., Hills, P. N., Usadel, B., Lloyd, J. R., Fernie, A. R., Kossmann, J. and van der Merwe, M. J. 2012. The plant growth-promoting substance, lumichrome, mimics starch, and ethylene-associated symbiotic responses in lotus and tomato roots. Front. Plant Sci. 3, 120. https://doi.org/10.3389/fpls.2012.00120
  46. Govindarajan, M., Balandreau, J., Kwon, S. W., Weon, H. Y. and Lakshminarasimhan, C. 2008. Effects of the inoculation of Burkholderia vietnamensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb. Ecol. 55, 21-37. https://doi.org/10.1007/s00248-007-9247-9
  47. Gray, E. J. and Smith, D. L. 2005. Intracellular and extracellular PGPR: commonalities and distinctions in the plant bacterium signaling processes. Soil Biol. Biochem. 37, 395-412. https://doi.org/10.1016/j.soilbio.2004.08.030
  48. Gupta, G., Parihar, S. S., Ahirwar, N. K., Snehi, S. K. and Singh, V. 2015. Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. Microb. Biochem. Technol. 7, 96-102.
  49. Gupta, A., Meyer, J. M. and Goel, R. 2002. Development of heavy metal-resistant mutants of phosphate solubilizing Pseudomonas sp. NBRI 4014 and their characterization. Curr. Microbiol. 45, 323-327. https://doi.org/10.1007/s00284-002-3762-1
  50. Gutierrez-Manero, F. J., Ramos-Solano, B., Probanza, A., Mehouachi, J., Tadeo, F. R. and Talon, M. 2001. The plant-growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol. Plant. 111, 206-211. https://doi.org/10.1034/j.1399-3054.2001.1110211.x
  51. Ham, B. K., Chen, J., Yan, Y. and Lucas, W. J. 2018. Insights into plant phosphate sensing and signaling. Curr. Opin. Biotechnol. 49, 1-9. https://doi.org/10.1016/j.copbio.2017.07.005
  52. Iqbal, A. and Hasnain, S. 2013. Aeromonas punctata PNS-1: a promising candidate to change the root morphogenesis of Arabidopsis thaliana in MS and sand system. Acta Physiol. Plant. 35, 657-665. https://doi.org/10.1007/s11738-012-1106-8
  53. James, E. K., Gyaneshwar, P., Mathan, N., Barraquio, W. L., Reddy, P. M., Iannetta, P. P. M., Olivares, F. L. and Ladha, J. K. 2002. Infection and colonization of rice seedlings by the plant growth promoting bacterium Herbaspirillum seropedicae Z67. Mol. Plant Microbe. Interact. 15, 894-906. https://doi.org/10.1094/MPMI.2002.15.9.894
  54. Jameson, P. 2000. Cytokinins and auxins in plant-pathogens interactions-an overview. Plant Growth Regul. 32, 369-380. https://doi.org/10.1023/A:1010733617543
  55. Jha, C. K. and Saraf, M. 2015. Plant growth promoting rhizobacteria (PGPR): a review. E3 J. Agric. Res. Dev. 5, 108-119.
  56. Kamran, S., Shahid, I., Baig, D. N., Rizwan, M., Malik, K. A. and Mehnaz, S. 2017. Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front. Microbiol. 8, 2593. https://doi.org/10.3389/fmicb.2017.02593
  57. Kang, S. M., Khan, A. L., Hamayun, M., Hussain, J., Joo, G. J., You, Y. H., Kim, J. G. and Lee, I. J. 2012. Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. J. Microbiol. 50, 902-909. https://doi.org/10.1007/s12275-012-2273-4
  58. Kang, S. M., Radhakrishnan, R., Khan, A. L., Kim, M. J., Park, J. M., Kim, B. R., Shin, D. H. and Lee, I. J. 2014. Gibberellin secreting rhizobacterium, Pseudomonas putida H-2-3 modulates the hormonal and stress physiology of soybean to improve the plant growth under saline and drought conditions. Plant Physiol. Biochem. 84, 115-124. https://doi.org/10.1016/j.plaphy.2014.09.001
  59. Kang, S. M., Khan, A. L., Waqas, M., You, Y. H., Kim, J. H., Kim, J. G., Hamayun, M. and Lee, I. J. 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. https://doi.org/10.1080/17429145.2014.894587
  60. Khan, A. L., Waqas, M., Hussain, J., Al-Harrasi, A., Hamayun, M. and Lee, I. J. 2015. Phytohormones enabled endophytic fungal symbiosis improve aluminum phyto extraction in tolerant Solanum lycopersicum: an example of Penicillium janthinellum LK5 and comparison with exogenous $GA_3$. J. Hazard Mater. 295, 70-78. https://doi.org/10.1016/j.jhazmat.2015.04.008
  61. Khan, M. S., Zaidi, A., Wani, P. A. and Oves, M. 2009. Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ. Chem. Lett. 7, 1-19. https://doi.org/10.1007/s10311-008-0155-0
  62. Khan, W., Prithiviraj, B. and Smith, D. L. 2008. Nod factor [Nod Bj V (C18:1, MeFuc)] and lumichrome enhance photosynthesis and growth of corn and soybean. J. Plant Physiol. 165, 1342-1351. https://doi.org/10.1016/j.jplph.2007.11.001
  63. Kim, J. and Rees, D. C. 1994. Nitrogenase and biological nitrogen fixation. Biochemistry 33, 389-397. https://doi.org/10.1021/bi00168a001
  64. Kloepper, J. W., Schroth, M. N. and Miller, T. D. 1980. Effects of rhizosphere colonization by plant growth promoting rhizobacteria on potato plant development and yield. Phytopathology 70, 1078-1082. https://doi.org/10.1094/Phyto-70-1078
  65. Kumar, A., Kumar, A. and Pratush, A. 2014. Molecular diversity and functional variability of environmental isolates of Bacillus species. Springerplus 3, 312. https://doi.org/10.1186/2193-1801-3-312
  66. Kumar, A., Singh, V., Singh, M., Singh, P. P., Singh, S. K., Singh, P. K. and Pandey, K. D. 2016b. Isolation of plant growth promoting rhizobacteria and their impact on growth and curcumin content in Curcuma longa L. Biocatal. Agric. Biotechnol. 8, 1-7. https://doi.org/10.1016/j.bcab.2016.07.002
  67. Li, M., Guo, R., Yu, F., Chen, X., Zhao, H., Li, H. and Wu, J. 2018. Indole-3-acetic Acid biosynthesis pathways in the plant-beneficial bacterium Arthrobacter pascens ZZ21. Int. J. Mol. Sci. 19, 443. https://doi.org/10.3390/ijms19020443
  68. Chen, L., Dodd, I. C., Theobald, J. C., Belimov, A. A. and Davies, W. J. 2013. The rhizobacterium Variovorax paradoxus 5C-2, containing ACC deaminase, promotes growth and development of Arabidopsis thaliana via an ethylene-dependent pathway. J. Exp. Bot. 64, 1565-1573. https://doi.org/10.1093/jxb/ert031
  69. Liu, D., Lian, B. and Dong, H. 2012. Isolation of Paenibacillus sp. and assessment of its potential for enhancing mineral weathering. Geomicrobiol. J. 29, 413-421. https://doi.org/10.1080/01490451.2011.576602
  70. Llorente, B. E., Alasia, M. A. and Larraburu, E. E. 2016. Biofertilization with Azospirillum brasilense improves in vitro culture of Handroanthus ochraceus, a forestry, ornamental and medicinal plant. N. Biotechnol. 33, 32-40. https://doi.org/10.1016/j.nbt.2015.07.006
  71. Lopez-Bucio, J., Campos-Cuevas, J. C., Hernandez-Calderon, E., Velasquez-Becerra, C., Farias-Rodriguez, R., Macias-Rodriguez, L. I. and Valencia-Cantero, E. 2007. Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol. Plant Microbe Interact. 20, 207-217. https://doi.org/10.1094/MPMI-20-2-0207
  72. Lynch, J. and Whipps, J. 1990. Substrate flow in the rhizosphere. Plant Soil 129, 1-10. https://doi.org/10.1007/BF00011685
  73. Manjili, F. A., Sedghi, M. and Pessarakli, M. 2012. Effects of phytohormones on proline content and antioxidant enzymes of various wheat cultivars under salinity stress. J. Plant Nutr. 35, 1098-1111. https://doi.org/10.1080/01904167.2012.671411
  74. Manjunath, M., Prasanna, R., Sharma, P., Nain, L. and Singh, R. 2011. Developing PGPR consortia using novel genera Providencia and Alcaligenes along with cyanobacteria for wheat. Arch. Agron. Soil Sci. 57, 873-887. https://doi.org/10.1080/03650340.2010.499902
  75. Manulis, S., Haviv-Chesner, A., Brandl, M. T., Lindow, S. E. and Barash, I. 1998. Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol. Plant Microbe Interact. 11, 634-642. https://doi.org/10.1094/MPMI.1998.11.7.634
  76. Martinez-Viveros, O., Jorquera, M. A., Crowley, D. E., Gajardo, G. M. L. M. and Mora, M. L. 2010. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J. Soil Sci. Plant Nutr. 10, 293-319.
  77. Matiru, V. N. and Dakora, F. D. 2005a. The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytol. 166, 439-444. https://doi.org/10.1111/j.1469-8137.2005.01344.x
  78. Mayak, S., Tirosh, T. and Glick, B. R. 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and peppers. Plant Sci. 166, 525-530. https://doi.org/10.1016/j.plantsci.2003.10.025
  79. Minerdi, D., Bossi, S., Maffei, M. E., Gullino, M. L. and Garibaldi, A. 2011. Fusarium oxysporum and its bacterial consortium promote lettuce growth and expansion A5 gene expression through microbial volatile organic compound (MVOC) emission. FEMS Microbiol. Ecol. 76, 342-351. https://doi.org/10.1111/j.1574-6941.2011.01051.x
  80. Mohapatra, P. K., Panigrahi, R. and Turner, N. C. 2011. Chapter five - Physiology of spikelet development on the rice panicle: is manipulation of apical dominance crucial for grain yield improvement? Adv. Agron. 110, 333-360. https://doi.org/10.1016/B978-0-12-385531-2.00005-0
  81. Morgan, P. W. and Drew, M. C. 1997. Ethylene and plant responses to stress. Physiol. Plant. 100, 620-630. https://doi.org/10.1111/j.1399-3054.1997.tb03068.x
  82. Nambara, E. and Marion-Poll, A. 2005. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 56, 165-185. https://doi.org/10.1146/annurev.arplant.56.032604.144046
  83. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O. and Jones, J. D. G. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-443. https://doi.org/10.1126/science.1126088
  84. Negi, S., Sukumar, P., Liu, X., Cohen, J. D. and Muday, C. K. 2010. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J. 61, 3-15. https://doi.org/10.1111/j.1365-313X.2009.04027.x
  85. Nett, R. S., Montanares, M., Marcassa, A., Lu, X., Nagel, R., Charles, T. C., Hedden, P., Rojas, M. C. and Peters, R. J. 2017. Elucidation of gibberellin biosynthesis in bacteria reveals convergent evolution. Nat. Chem. Biol. 13, 69-74. https://doi.org/10.1038/nchembio.2232
  86. Ortiz-Castro, R., Martinez-Trujillo, M. and Lopez-Bucio, J. 2008. N-Acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ. 31, 1497-1509. https://doi.org/10.1111/j.1365-3040.2008.01863.x
  87. Ortiz-Castro, R., Diaz-Perez, C., Martinez-Trujillo, M., del Rio, R. E., Campos-Garcia, J. and Lopez-Bucio, J. 2011. Transkingdom signaling based on bacterial cyclodipeptides with auxin activity in plants. Proc. Natl. Acad. Sci. USA. 108, 7253-7258. https://doi.org/10.1073/pnas.1006740108
  88. Oteino, N., Lally, R. D., Kiwanuka, S., Lloyd, A., Ryan, D., Germaine, K. J. and Dowling, D. N. 2015. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front. Microbiol. 6, 745. https://doi.org/10.3389/fmicb.2015.00745
  89. Pahari, A. and Mishra, B. B. 2017. Antibiosis of siderophore producing bacterial isolates against phytopathogens and their effect on growth of okra. Int. J. Curr. Microbiol. App. Sci. 6, 1925-1929. https://doi.org/10.20546/ijcmas.2017.608.227
  90. Parmar, P. and Sindhu, S. S. 2013. Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J. Microbiol. Res. 3, 25-31.
  91. Patten, C. J., Blakney, A. J. C. and Coulson, T. J. D. 2013. Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Crit. Rev. Microbiol. 39, 395-415. https://doi.org/10.3109/1040841X.2012.716819
  92. Pierik, R., Tholde D., Poorter H., Visser E. J. W. and Voesenek, L. A. C. J. 2006. The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci. 11, 176-183. https://doi.org/10.1016/j.tplants.2006.02.006
  93. Poupin, M. J., Timmermann, T., Vega, A., Zuniga, A. and Gonzalez, B. 2013. Effects of the plant growth-promoting Bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS One 8, e69435. https://doi.org/10.1371/journal.pone.0069435
  94. Poupin, M. J., Greve, M., Carmona, V. and Pinedo, I. 2016. A complex molecular interplay of auxin and ethylene signaling pathways is involved in Arabidopsis growth promotion by Burkholderia phytofirmans PsJN. Front. Plant Sci. 7, 492.
  95. Rajkumar, M., Ae, N., Prasad, M. N. V. and Freitas, H. 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28, 142-149. https://doi.org/10.1016/j.tibtech.2009.12.002
  96. Raymond, J., Siefert, J. L., Staples, C. R. and Blankenship, R. E. 2004. The natural history of nitrogen fixation. Mol. Biol. Evol. 21, 541- 554. https://doi.org/10.1093/molbev/msh047
  97. Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Wei, H. X., Pare, P. W. and Kloepper, J. W. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. USA. 100, 4927-4932. https://doi.org/10.1073/pnas.0730845100
  98. Sakakibara, H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 57, 431-449. https://doi.org/10.1146/annurev.arplant.57.032905.105231
  99. Schulz, B. and Boyle, C. 2006. What are Endophytes?, pp. 1-13. In: Schulz B. J. E., Boyle C. J. C. and Sieber T. N. (eds), Microbial Root Endophytes. Soil Biology, vol 9. Springer, Berlin, Heidelberg.
  100. Setiawati, T. C. and Mutmainnah, L. 2016. Solubilization of Potassium containing mineral by microorganisms from sugarcane rhizosphere. Agri. Sci. Procedia 9, 108-117.
  101. Shahzad, R., Waqas, M., Khan, A. L., Asaf, S., Khan, M. A., Kang, S. M., Yun, B. W. and Lee, I. J. 2016. Seed-borne endophytic Bacillus amyloliquefaciens RWL-1 produces gibberellins and regulates endogenous phytohormones of Oryza sativa. Plant Physiol. Biochem. 106, 236-243. https://doi.org/10.1016/j.plaphy.2016.05.006
  102. Shaikh, S., Wani, S. and Sayyed, R. 2018. Impact of Interactions between Rhizosphere and Rhizobacteria: A Review. J. Bacteriol. Mycol. 5, 1058.
  103. Sharp, R. E. and Le Noble, M. E. 2002. ABA, ethylene and the control of shoot and root growth under water stress. J. Exp. Bot. 53, 33-37. https://doi.org/10.1093/jexbot/53.366.33
  104. Shilev, S. 2013. Soil rhizobacteria regulating the uptake of nutrients and undesirable elements by plants, pp 147-150. In: Arora, N. K. (ed), Plant microbe symbiosis: fundamentals and advances. Springer, New Delhi, India.
  105. Simon, L., Bousquet, J., Levesque, R. C. and Lalonde, M. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67-69. https://doi.org/10.1038/363067a0
  106. Singh, B., Natesan, S. K. A., Singh, B. K. and Usha, K. 2005. Improving zinc efficiency of cereals under zinc deficiency. Curr. Sci. 88, 36-44.
  107. Singh, M., Kumar, A., Singh, R. and Pandey, K. D. 2017a. Endophytic bacteria: a new source of bioactive compounds. 3 Biotech. 7, 315.
  108. Singh, S. and Prasad, S. M. 2014. Growth, photosynthesis and oxidative responses of Solanum melongena L. seedlings to cadmium stress: mechanism of toxicity amelioration by kinetin. Sci. Hortic. 176, 1-10. https://doi.org/10.1016/j.scienta.2014.06.022
  109. Singh, V. K., Singh, A. K. and Kumar, A. 2017b. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech. 7, 255. https://doi.org/10.1007/s13205-017-0896-1
  110. Spaepen, S., Vanderleyden, J. and Remans, R. 2007. Indole-3-acetic acid in microbial and microorganism plant signaling. FEMS Microbiol. Rev. 31, 425-448. https://doi.org/10.1111/j.1574-6976.2007.00072.x
  111. Torres, A. R., Kaschuk, G., Saridakis, G. P. and Hungria, M. 2012. Genetic variability in Bradyrhizobium japonicum strains nodulating soybean Glycine max (L.) Merrill. World J. Microbiol. Biotechnol. 28, 1831-1835. https://doi.org/10.1007/s11274-011-0964-3
  112. Uren, N. C. 2000. Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants, pp. 1-21. In: Pinton, R., Varanini, Z. and Nannipieri, P. (eds.), The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface, second edition. CRC Press: Boca Raton, FL, U. S. A.
  113. Vacheron, J., Desbrosses, G., Bouffaud, M. L., Touraine, B., Moenne-Loccoz, Y., Muller, D., Legendre, L., Wisniewski-Dye, F. and Prigent-Combaret, C. 2013. Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 4, 356. https://doi.org/10.3389/fpls.2013.00356
  114. Whipps, J. M. 2001. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487-511. https://doi.org/10.1093/jxb/52.suppl_1.487
  115. Xu, J., Li, X. L. and Luo, L. 2012. Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl. Environ. Microbiol. 78, 8056-8061. https://doi.org/10.1128/AEM.01276-12
  116. You, Y. H., Yoon, H., Kang, S. M., Shin, J. H., Choo, Y. S, Lee, I. J., Lee, J. M. and Kim, J. G. 2012. Fungal diversity and plant growth promotion of endophytic fungi from six halophytes in Suncheon Bay. J. Microbiol. Biotechnol. 22, 1549-1556. https://doi.org/10.4014/jmb.1205.05010
  117. Zahran, H. H. 2001. Rhizobia from wild legumes: diversity, taxonomy, ecology, nitrogen fixation and biotechnology. J. Biotechnol. 91, 143-153. https://doi.org/10.1016/S0168-1656(01)00342-X
  118. Zaidi, A., Ahmad, E., Khan, M. S., Saif, S. and Rizvi, A. 2015. Role of plant growth promoting rhizobacteria in sustainable production of vegetables: current perspective. Sci. Hortic. 193, 231-239. https://doi.org/10.1016/j.scienta.2015.07.020
  119. Zaidi, A. and Khan, M. S. 2005. Interactive effect of rhizospheric microorganisms on growth, yield and nutrient uptake of wheat. J. Plant Nutr. 28, 2079-2092. https://doi.org/10.1080/01904160500320897
  120. Zamioudis, C., Mastranesti, P., Dhonukshe, P., Blilou, I. and Pieterse, C. M. J. 2013. Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol. 162, 304-318. https://doi.org/10.1104/pp.112.212597
  121. Zhang, H., Kim, M. S., Krishnamachari, V., Payton, P., Sun, Y., Grimson, M., Farag, M. A., Ryu, C. M., Allen, R., Melo, I. S. and Pare, P. W. 2007. Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226, 839-851. https://doi.org/10.1007/s00425-007-0530-2
  122. Zhang, A., Zhao, G., Gao, T., Wang, W., Li, J., Zhang, S. and Zhu, B. 2013. Solubilization of insoluble potassium and phosphate by Paenibacillus kribensis CX-7: a soil microorganism with biological control potential. Afri. J. Microbiol. Res. 7, 41-47. https://doi.org/10.5897/AJMR12.1485
  123. Zhang, C. and Kong, F. 2014. Isolation and identification of potassium-solubilizing bacteria from tobacco rhizo-spheric soil and their effect on tobacco plants. Appl. Soil. Ecol. 82, 18-25. https://doi.org/10.1016/j.apsoil.2014.05.002
  124. Zhao, Q., Zhang, C., Jia, Z., Huang, Y., Li, H. and Song, S. 2015. Involvement of calmodulin in regulation of primary root elongation by N-3-oxo-hexanoyl homoserine lactone in Arabidopsis thaliana. Front. Plant Sci. 5, 1-11.