Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Microbiome of Halophytes: Diversity and Importance for Plant Health and Productivity

  • Mukhtar, Salma (Department of Biological Sciences, Forman Christian College (A Chartered University)) ;
  • Malik, Kauser Abdulla (Department of Biological Sciences, Forman Christian College (A Chartered University)) ;
  • Mehnaz, Samina (Department of Biological Sciences, Forman Christian College (A Chartered University))
  • Received : 2018.04.30
  • Accepted : 2018.10.24
  • Published : 2019.03.28
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Abstract

Saline soils comprise more than half a billion hectares worldwide. Thus, they warrant attention for their efficient, economical, and environmentally acceptable management. Halophytes are being progressively utilized for human benefits. The halophyte microbiome contributes significantly to plant performance and can provide information regarding complex ecological processes involved in the osmoregulation of halophytes. Microbial communities associated with the rhizosphere, phyllosphere, and endosphere of halophytes play an important role in plant health and productivity. Members of the plant microbiome belonging to domains Archaea, Bacteria, and kingdom Fungi are involved in the osmoregulation of halophytes. Halophilic microorganisms principally use compatible solutes, such as glycine, betaine, proline, trehalose, ectoine, and glutamic acid, to survive under salinity stress conditions. Plant growth-promoting rhizobacteria (PGPR) enhance plant growth and help to elucidate tolerance to salinity. Detailed studies of the metabolic pathways of plants have shown that plant growth-promoting rhizobacteria contribute to plant tolerance by affecting the signaling network of plants. Phytohormones (indole-3-acetic acid and cytokinin), 1-aminocyclopropane-1-carboxylic acid deaminase biosynthesis, exopolysaccharides, halocins, and volatile organic compounds function as signaling molecules for plants to elicit salinity stress. This review focuses on the functions of plant microbiome and on understanding how the microorganisms affect halophyte health and growth.

Keywords

References

  1. Rengsamy P. 2002. Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust. J. Exp. Agr. 42: 351-361. https://doi.org/10.1071/EA01111
  2. Bui EN. 2013. Soil salinity: a neglected factor in plant ecology and biogeography. J. Arid. Environ. 92: 14-25. https://doi.org/10.1016/j.jaridenv.2012.12.014
  3. Nassar IN, Horton R. 1999. Salinity and compaction effects on soil water evaporation and water and solute distributions. Soil Sci. Soc. Am. J. 63: 752-758. https://doi.org/10.2136/sssaj1999.634752x
  4. Munns R. 2005. Genes and salt tolerance: bringing them together. New Phytol. 167: 645-663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
  5. Flowers TJ, Colmer TD. 2015. Plant salt tolerance: adaptations in halophytes. Ann. Bot. 115: 327-331. https://doi.org/10.1093/aob/mcu267
  6. Parida AK, Das AB. 2005. Salt tolerance and salinity effects on plants: A review. Ecotoxicol. Environ. Saf. 60: 324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010
  7. Qureshi AS, McCornick PG, Qadir M, Aslam M. 2008. Managing salinity and waterlogging in the Indus Basin of Pakistan. Agri. Water Manag. 95: 1-10. https://doi.org/10.1016/j.agwat.2007.09.014
  8. Khan MA. 2003. Halophytes of Pakistan: Distribution and Ecology. pp. 167-188. In H. Lieth and M. Moschenko. Cash Crop Halophytes: Recent Studies: 10 years after the Al-Ain meeting (Tasks for Vegetation Science, 38). Kluwer Academic Press, Netherlands.
  9. Ashraf MY, Naveed NH, Ashraf M, Akram NA. 2009. Salt-induced some biochemical changes in germinating seeds of three rice cultivars. Agrochimica 308-321.
  10. Ahmad I, Hussain M, Ahmad MSA, Ashraf MY, Ahmad R, Asghar M. 2009. Spatio-temporal variations in physiochemical attributes of Adiantum capillus veneris from soone valley of Salt Range (Pakistan). Pak. J. Bot. 40: 1387-1398.
  11. Bauder JW, Brock TA. 2001. Irrigation water quality, soil amendment and crop effects on sodium leaching. Arid Land Res. Manag. 15: 101-113. https://doi.org/10.1080/15324980151062724
  12. Olsen GJ, Woese CR, Overbeek RC. 1994. The winds of (evolutionary) change: breathing new life into microbiology. J. Bacteriol. 176: 1-6. https://doi.org/10.1128/jb.176.1.1-6.1994
  13. Pitman MG, Lauchi A. 2002. pp. 3-20. Global impact of salinity and agricultural ecosystems in Salinity: Environment - Plants - Molecules. eds A. Lauchi and U. Luttage (Amsterdam: Kluwer Academic Publishers).
  14. Podell S, Ugalde JA, Narasingarao P, Banfield JF, Heidelberg KB, Allen EE. 2013. Assembly-driven community genomics of a hypersaline microbial ecosystem. PLoS One 8: e61692. https://doi.org/10.1371/journal.pone.0061692
  15. Smith DL, Subramanian S, Lamont JR, Bywater-Ekegard M. 2015b. Signaling in the phytomicrobiome: breadth and potential. Front. Plant Sci. 6: 709. https://doi.org/10.3389/fpls.2015.00709
  16. Upadhyay SK, Singh DP. 2015. Effect of salt-tolerant plant growth promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol. 17: 288-293. https://doi.org/10.1111/plb.12173
  17. Ruppel S, Franken P, Witzel K. 2013. Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct. Plant Biol. 40: 940-951. https://doi.org/10.1071/FP12355
  18. Khan MY, Zahir ZA, Asghar HN, Waraich EA. 2017. Preliminary investigations on selection of synergistic halotolerant plant growth promoting rhizobacteria for inducing salinity tolerance in wheat. Pak. J. Bot. 49: 1541-1551.
  19. Mukhtar S, Mirza MS, Awan HA, Maqbool A, Mehnaz S, Malik KA. 2016. Microbial diversity and metagenomic analysis of the rhizosphere of Para Grass (Urochloa mutica) growing under saline conditions. Pak. J. Bot. 48: 779-791.
  20. Rodriguez H, Fraga R. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319-339. https://doi.org/10.1016/S0734-9750(99)00014-2
  21. Gray EJ, Smith DL. 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
  22. Singh RP, Jha PN. 2016. Alleviation of salinity-induced damage on wheat plant by an ACC deaminase-producing halophilic bacterium Serratia sp SL-12 isolated from a salt lake. Symbiosis 69: 101-111. https://doi.org/10.1007/s13199-016-0387-x
  23. Lindow SE, Brandl MT. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69: 1875-1883. https://doi.org/10.1128/AEM.69.4.1875-1883.2003
  24. Bodenhausen N, Horton MW, Bergelson J. 2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8: e56329. https://doi.org/10.1371/journal.pone.0056329
  25. Vokou D, Vareli K, Zarali E, Karamanoli K, Constantinidou HI, Monokrousos N, et al. 2012. Exploring biodiversity in the bacterial community of the Mediterranean phyllosphere and its relationship with airborne bacteria. Microb. Ecol. 64: 714-724. https://doi.org/10.1007/s00248-012-0053-7
  26. Mukhtar S, Ishaq A, Hassan S, Mehnaz S, Mirza MS, Malik KA. 2017. Comparison of microbial communities associated with halophyte (Salsola stocksii) and non-halophyte (Triticum aestivum) using culture-independent approaches. Pol. J. Microbiol. 66: 375-386. https://doi.org/10.5604/01.3001.0010.4875
  27. Gonzalez AJ, Larraburu EE, Llorente BE. 2015. Azospirillum brasilense increased salt tolerance of jojoba during in vitro rooting. Ind. Crop Prod. 76: 41-48. https://doi.org/10.1016/j.indcrop.2015.06.017
  28. Goswami D, Thakker JN, Dhandhukia PC. 2016. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cog. Food Agri. 2: 11275.
  29. Shi W, Takano T, Liu S. 2012. Isolation and characterization of novel bacterial taxa from extreme alkali-saline soil. World J. Microbiol. Biotechnol. 28: 2147-2157. https://doi.org/10.1007/s11274-012-1020-7
  30. Mukhtar S, Mirza BS, Mehnaz S, Mirza MS, Mclean J, Kauser AM. 2018. Impact of soil salinity on the structure and composition of rhizosphere microbiome. World J. Microbiol. Biotechnol. 34: 136. https://doi.org/10.1007/s11274-018-2509-5
  31. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK, Vivanco JM. 2013. Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS One 8: e55731. https://doi.org/10.1371/journal.pone.0055731
  32. Browne P, Rice O, Miller SH, Burke J, Dowling DN, Morrissey JP, et al. 2009. Superior inorganic phosphate solubilization is linked to phylogeny within the Pseudomonas fluorescens complex. Appl. Soil. Ecol. 43: 131-138. https://doi.org/10.1016/j.apsoil.2009.06.010
  33. Dimkpa CO, Zeng J, McLean JE, Britt DW, Zhan J, Anderson AJ. 2012. Production of indole-3-acetic acid via the indole-3-acetamide pathway in the plant-beneficial bacterium Pseudomonas chlororaphis O6 is inhibited by ZnO nanoparticles but enhanced by CuO nanoparticles. Appl. Environ. Microbiol. 78: 1404-1410. https://doi.org/10.1128/AEM.07424-11
  34. Susilowati DN, Sudiana IM, Mubarik NR, Suwanto A. 2015. Species and functional diversity of rhizobacteria of rice plant in the coastal soils of Indonesia. Indones. J. Agric. Sci. 16: 39-51. https://doi.org/10.21082/ijas.v16n1.2015.p39-50
  35. Glick BR. 2012. Plant growth-promoting bacteria: mechanisms and applications. Hindawi Pub. Corpor. Sci. 2012: 23-30.
  36. Ahemad M, 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
  37. Kuan KB, Othman R, Rahim AK, Shamsuddin ZH. 2016. Plant growth-promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilisation of maize under greenhouse conditions. PLos One 11: e0152478. https://doi.org/10.1371/journal.pone.0152478
  38. Martinez-Hidalgo P, Hirsch AM. 2017. The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes 1: 70-82. https://doi.org/10.1094/PBIOMES-12-16-0019-RVW
  39. Jaisingh R, Kumar A, Dhiman M. 2016. Isolation and characterization of PGPR from rhizosphere of Sesame indicum L. Int. J. Adv. Res. Biol. Sci. 3: 238-244. https://doi.org/10.22192/ijarbs.2016.03.09.032
  40. Mukhtar S, Mirza MS, Mehnaz S, Mirza BS, Malik KA. 2018. Diversity of Bacillus-like bacterial community in the rhizospheric and nonrhizospheric soil of halophytes (Salsola stocksii and Atriplex amnicola) and characterization of osmoregulatory genes in halophilic Bacilli. Can. J. Microbiol. 64: 567-579. https://doi.org/10.1139/cjm-2017-0544
  41. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V. 2015. Plant growth promoting rhizobacteria (pgpr): Current and future prospects for development of sustainable agriculture. J. Microbiol. Biochem. Technol. 7: 96-102.
  42. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, et al. 2009. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. USA 106: 16428-16433. https://doi.org/10.1073/pnas.0905240106
  43. Knief C, Delmotte N, Chaffron S, Stark M, Innerebner G, Wassmann R, et al. 2012. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6: 1378-1390. https://doi.org/10.1038/ismej.2011.192
  44. Daesik K, Sojung K, Sunghyun K, Jeongbin P, Jin-Soo K. 2016. Genome-wide target specificities of CRISPR-Cas9 nucleases revealed by multiplex digenomic sequencing. Gen. Res. 26: 406-415. https://doi.org/10.1101/gr.199588.115
  45. Muller T, Ruppel S. 2014. Progress in cultivation-independent phyllosphere microbiology. FEMS Microbiol. Ecol. 87: 2-17. https://doi.org/10.1111/1574-6941.12198
  46. Laforest-Lapointe I, Messier C, Kembel SW. 2016. Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4: 27-32. https://doi.org/10.1186/s40168-016-0174-1
  47. Vorholt JA. 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10: 828-840. https://doi.org/10.1038/nrmicro2910
  48. Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA. 2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Gen. 10: e1004283. https://doi.org/10.1371/journal.pgen.1004283
  49. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
  50. DasSarma S, DasSarma P. 2015. Halophiles and their enzymes: negativity put to good use. Curr. Opin. Microbiol. 25: 120-126. https://doi.org/10.1016/j.mib.2015.05.009
  51. Bestvater T, Louis P, Galinski EA. 2008. Heterologous ectoine production in Escherichia coli: by-passing the metabolic bottleneck. Saline Systems 4: 12. https://doi.org/10.1186/1746-1448-4-12
  52. Ventosa A, Marquez MC, Sanchez-Porro C, de la Haba R. 2012. Taxonomy of halophilic archaea and bacteria. pp. 59-80. In Vreeland R.H. (ed) Advances in Understanding the Biology of Halophilic Microorganisms. Springer, Dordrecht.
  53. Boutaiba S, Hacene H, Bidle KA, Maupin-Furlow JA. 2011. Microbial diversity of the hypersaline Sidi Ameur and Himalatt salt lakes of the Algerian Sahara. J. Arid. Environ. 75: 909-916. https://doi.org/10.1016/j.jaridenv.2011.04.010
  54. Dang H, Zhu H, Wang J, Li T. 2009. Extracellular hydrolytic enzyme screening of culturable heterotrophic bacteria from deep-sea sediments of the Southern Okinawa Trough. World J. Microbiol. Biotechnol. 25: 71-79. https://doi.org/10.1007/s11274-008-9865-5
  55. DasSarma S, Arora P. 2001. A general review on Halophiles. In Encyclopedia of life sciences. Nature publishing group/www.els.net
  56. Spring S, Ludwig W, Marquez MC, Ventosa A, Schleifer KH. 1996. Halobacillus gen. nov., with descriptions of Halobacillus litoralis sp. nov. and Halobacillus trueperi sp. nov., and transfer of Sporosarcina halophila to Halobacillus halophilus comb. nov. Int. J. Syst. Bacteriol. 46: 492-496. https://doi.org/10.1099/00207713-46-2-492
  57. Sanchez-Porro C, Martin S, Mellado E, Ventosa A. 2003. Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J. Appl. Microbiol. 94: 295-300. https://doi.org/10.1046/j.1365-2672.2003.01834.x
  58. Anton J, Oren A, Benlloch S, Rodriguez-Valera F, Amann R, Rossello-Mora R. 2002. Salinibacter ruber gen. nov., sp. nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int. J. Syst. Evol. Microbiol. 52: 485-491. https://doi.org/10.1099/00207713-52-2-485
  59. Kim YG, Choi DH, Hyun S, Cho BC. 2007. Oceanobacillus profundus sp. nov., isolated from a deep-sea sediment core. Int. J. Syst. Evol. Microbiol. 57: 409-413. https://doi.org/10.1099/ijs.0.64375-0
  60. Yoon JH, Kang SJ, Oh TK. 2007. Reclassification of Marinococcus albus Hao et al. 1985 as Salimicrobium album gen. nov., comb. nov. and Bacillus halophilus Ventosa et al. 1990 as Salimicrobium halophilum comb. nov., and description of Salimicrobium luteum sp. nov. Int. J. Syst. Evol. Microbiol. 57: 2406-2411. https://doi.org/10.1099/ijs.0.65003-0
  61. Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, et al. 1992. Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbondegrading marine bacterium. Int. J. Syst. Bacteriol. 42: 568-576. https://doi.org/10.1099/00207713-42-4-568
  62. Heyndrickx M, Lebbe L, Kersters K, De Vos P, Forsyth G, Logan NA. 1998. Virgibacillus: a new genus to accommodate Bacillus pantothenticus (Proom and Knight 1950). Emended description of Virgibacillus pantothenticus. Int. J. Syst. Evol. Microbiol. 48: 99-106.
  63. Sorokin DY, Tindall BJ. 2006. The status of the genus name Halovibrio Fendrich 1989 and the identity of the strains Pseudomonas halophila DSM 3050 and Halomonas variabilis DSM 3051. Request for an opinion. Int. J. Syst. Evol. Microbiol. 56: 487-489. https://doi.org/10.1099/ijs.0.63965-0
  64. Amoozegar MA, Schumann P, Hajighasemi M, Fatemi AZ, Karbalaei-Heidari HR. 2008. Salinivibrio proteolyticus sp. nov., a moderately halophilic and proteolytic species from a hypersaline lake in Iran. Int. J. Syst. Evol. Microbiol. 58: 1159-1163. https://doi.org/10.1099/ijs.0.65423-0
  65. Biswas J, Paul AK. 2013. Production of extracellular enzymes by halophilic bacteria isolated from solar salterns. Int. J. Appl. Biol. Pharma. Technol. 4: 30-36.
  66. Koh HW, Song HS, Song U, Yim KJ, Roh SW, Park SJ. 2015. Halolamina sediminis sp. nov., an extremely halophilic archaeon isolated from solar salt. Int. J. Syst. Evol. Microbiol. 65: 2479-2484. https://doi.org/10.1099/ijs.0.000287
  67. Xin H, Itoh T, Zhou P, Suzuki K, Kamekura M, Nakase T. 2000. Natrinema versiforme sp. nov., an extremely halophilic archaeon from Aibi salt lake, Xinjiang, China. Int. J. Syst. Evol. Microbiol. 50: 1297-1303. https://doi.org/10.1099/00207713-50-3-1297
  68. Xue Y, Fan H, Ventosa A, Grant WD, Jones BE, Cowan DA, et al. 2005. Halalkalicoccus tibetensis gen. nov., sp. nov., representing a novel genus of haloalkaliphilic archaea. Int. J. Syst. Evol. Microbiol. 55: 2501-2505. https://doi.org/10.1099/ijs.0.63916-0
  69. Beneduzi A, Ambrosini A, Passaglia LMP. 2012. Plant growth promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet. Mol. Biol. 35: 1044-1051. https://doi.org/10.1590/S1415-47572012000600020
  70. Mehnaz S, Baig DN, Lazarovits G. 2010. Genetic and phenotypic diversity of plant growth promoting rhizobacteria isolated from sugarcane plants growing in Pakistan. J. Microbiol. Biotechnol. 20: 1614-1623. https://doi.org/10.4014/jmb.1005.05014
  71. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA. 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2: 587. https://doi.org/10.1186/2193-1801-2-587
  72. Janssen J, Weyens N, Croes S, Beckers B, Meiresonne L, Van Peteghem P, et al. 2015. Phytoremediation of metal contaminated soil using willow: exploiting plant-associated bacteria to improve biomass production and metal uptake. Int. J. Phytoremediation 17: 1123-1136. https://doi.org/10.1080/15226514.2015.1045129
  73. Weyens N, Beckers B, Schellingen K, Ceulemans R, Van der Lelie D, Newman L, et al. 2015. The potential of the Ni-resistant TCE degrading Pseudomonas putida W619-TCE to reduce phytotoxicity and improve phytoremediation efficiency of poplar cuttings on A Ni-TCE Co-contamination. Int. J. Phytoremediation 17: 40-48. https://doi.org/10.1080/15226514.2013.828016
  74. Dodd IC, Perez-Alfocea F. 2012. Microbial amelioration of crop salinity stress. J. Exp. Bot. 63: 3415-3428. https://doi.org/10.1093/jxb/ers033
  75. 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. https://doi.org/10.1002/jobm.201200778
  76. Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR. 2007. Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292: 305-315. https://doi.org/10.1007/s11104-007-9233-5
  77. Ilangumaran G, Smith DL. 2017. Plant growth promoting Rhizobacteria in Amelioration of salinity stress: A systems biology perspective. Front. Plant Sci. 8: 1768. https://doi.org/10.3389/fpls.2017.01768
  78. Shen X, Hu H, Peng H, Wang W, Zhang X. 2013. Comparative genomic analysis of four representative plant growth-promoting rhizobacteria in Pseudomonas. BMC Genomics 14: 271. https://doi.org/10.1186/1471-2164-14-271
  79. Delbarre-Ladrat C, Sinquin C, Lebellenger L, Zykwinska A, Colliec-Jouault S. 2014. Exopolysaccharides produced by marine bacteria and their applications as glycosaminoglycan-like molecules. Front. Chem. 2: 85.
  80. Llamas I, Amjres H, Mata JA, Quesada E, Bejar V. 2012. The potential biotechnological applications of the exopolysaccharide produced by the halophilic bacterium Halomonas almeriensis. Molecules 17: 7103-7120. https://doi.org/10.3390/molecules17067103
  81. Abd_Allah EF, Alqarawi AA, Hashem A, Radhakrishnan R, Asma A, Al-Huqail AA, et al. 2018. Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defence mechanisms. J. Plant Interact. 13: 37-44. https://doi.org/10.1080/17429145.2017.1414321
  82. Oren A. 2015. Halophilic microbial communities and their environments. Curr. Opin. Microbiol. 33: 119-124.
  83. Kumar V, Saxena J, Tiwari SK. 2016. Description of a halocin-producing Haloferax larsenii ha1 isolated from pachpadra salt lake in rajasthan. Arch. Microbiol. 198: 181-192. https://doi.org/10.1007/s00203-015-1175-3
  84. Besse A, Peduzzi J, Rebuffat S, Carre-Mlouka A. 2015. Antmicrobial peptides and proteins in the face of extremes: lessons from archaeocins. Biochimie 118: 344-355. https://doi.org/10.1016/j.biochi.2015.06.004
  85. Meknaci R, Lopes P, Servy C, LeCaer JP, Andrieu JP, Hacene H, et al. 2014. Agar-supported cultivation of Halorubrum sp. SSR and production of halocin C8 on the scale-up prototype Platex. Extremophiles 18: 1049-1055. https://doi.org/10.1007/s00792-014-0682-5
  86. Subramanian S, Souleimanov A, Smith DL. 2016. Proteomic studies on the effects of lipo-chitooligosaccharide and thuricin 17 under unstressed and salt stressed conditions in Arabidopsis thaliana. Front. Plant Sci. 7: 1314.
  87. Vurukonda SS, Vardharajula S, Shrivastava M, SkZ A. 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol. Res. 184: 13-24. https://doi.org/10.1016/j.micres.2015.12.003
  88. Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Pare PW. 2008. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 21: 737-744. https://doi.org/10.1094/MPMI-21-6-0737
  89. Zhuo C, Ma Z, Zhu L, Xiao X, Xie Y, Zhu J, et al. 2016. Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int. J. Mol. Sci. 17: 976. https://doi.org/10.3390/ijms17060976
  90. Aslam R, Bostan N, Maria M, Safdar W. 2011. A critical review on halophytes: salt tolerant plants. J. Med. Plant Res. 5: 7108-7118.
  91. Apse MP, Blumwald E. 2002. Engineering salt tolerance in plants. Curr. Opin. Biotechnol. 13: 146-150. https://doi.org/10.1016/S0958-1669(02)00298-7
  92. Chen H, An R, Tang JH, Cui XH, Hao FS, Chen J, Wang XC. 2007. Over-expression of a vacuolar $Na^+$/$H^+$ antiporter gene improves salt tolerance in an upland rice. Mol. Breed. 19: 215-225. https://doi.org/10.1007/s11032-006-9048-8
  93. Nuccio ML, Russel BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD. 1998. The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J. 16: 487-498. https://doi.org/10.1046/j.1365-313x.1998.00316.x
  94. Flowers TJ, Colmer TD. 2015. Plant salt tolerance: adaptations in halophytes. Ann. Bot. 115: 327-331. https://doi.org/10.1093/aob/mcu267
  95. Maurel P. 1997. Aquaporins and water permeability of plant membranes. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48: 399-429. https://doi.org/10.1146/annurev.arplant.48.1.399
  96. Dou DL, Zhou JM. 2005. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12: 484-495. https://doi.org/10.1016/j.chom.2012.09.003
  97. Bittel P, Robatzek S. 2007. Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr. Opin. Plant. Biol. 10: 335-341. https://doi.org/10.1016/j.pbi.2007.04.021
  98. Bari R, Jones J. 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69: 473-488. https://doi.org/10.1007/s11103-008-9435-0
  99. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, et al. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959-962. https://doi.org/10.1038/nature00841
  100. Akiyama K, Hayashi H. 2006. Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann. Bot. 97: 925-931. https://doi.org/10.1093/aob/mcl063
  101. Hassan S, Mathesius U. 2012. The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J. Exp. Bot. 63: 3429-3444. https://doi.org/10.1093/jxb/err430
  102. Bednarek P, Osbourn A. 2009. Plant-microbe interactions: chemical diversity in plant defense. Science 324: 746-748. https://doi.org/10.1126/science.1171661
  103. Bressan M, Roncato MA, Bellvert F, Comte G, Haichar FEZ, Achouak W, et al. 2009. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J. 3: 1243-1257. https://doi.org/10.1038/ismej.2009.68
  104. Osbourn AE, Clarke BR, Lunness P, Scott PR, Daniels MJ. 1994. An oat species lacking avenacin is susceptible to infection by Gaeumannomyces-graminis vartritici. Physiol. Mol. Plant. Pathol. 45: 457-467. https://doi.org/10.1016/S0885-5765(05)80042-6
  105. Carter JP, Spink J, Cannon PF, Daniels MJ, Osbourn AE. 1999. Isolation, characterization, and avenacin sensitivity of a diverse collection of cereal root-colonizing fungi. Appl. Environ. Microbiol. 65: 3364-3372. https://doi.org/10.1128/AEM.65.8.3364-3372.1999
  106. Cotta SR, Dias ACF, Marriel IE, Gomes EA, van Elsas JD, Seldin L. 2013. Temporal dynamics of microbial communities in the rhizosphere of two genetically modified (GM) maize hybrids in tropical agrosystems. Antonie Van Leeuwenhoek 103: 589-601. https://doi.org/10.1007/s10482-012-9843-7

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