Plant and Soil

, Volume 405, Issue 1–2, pp 357–370 | Cite as

Plant-associated microbiomes in arid lands: diversity, ecology and biotechnological potential

  • Asma Soussi
  • Raoudha Ferjani
  • Ramona Marasco
  • Amel Guesmi
  • Hanene Cherif
  • Eleonora Rolli
  • Francesca Mapelli
  • Hadda Imene Ouzari
  • Daniele Daffonchio
  • Ameur CherifEmail author
Regular Article



Aridification is a worldwide serious threat directly affecting agriculture and crop production. In arid and desert areas, it has been found that microbial diversity is huge, built of microorganisms able to cope with the environmental harsh conditions by developing adaptation strategies. Plants growing in arid lands or regions facing prolonged abiotic stresses such as water limitation and salt accumulation have also developed specific physiological and molecular stress responses allowing them to thrive under normally unfavorable conditions.


Under such extreme selection pressures, special root-associated bacterial assemblages, endowed with capabilities of plant growth promotion (PGP) and extremophile traits, are selected by the plants. In this review, we provide a general overview on the microbial diversity in arid lands and deserts versus specific microbial assemblages associated with plants. The ecological drivers that shape this diversity, how plant-associated microbiomes are selected, and their biotechnological potential are discussed.


Selection and recruitment of the plant associated bacterial assemblages is mediated by the combination of the bio-pedo-agroclimatic conditions and the plant species or varieties. Diversity and functional redundancy of these associated PGPR makes them very active in supporting plant improvement, health and resistance to drought, salt and related stresses. Implementing proper biotechnological applications of the arid and desert-adapted PGPR constitute the challenge to be raised.


Plant associated microbiome Arid land Extreme environments Drought Salinity Plant Growth Promoting Rhizobacteria Sustainable agriculture Biotechnology 



The authors thank for financial support the European Union in the ambit of project BIODESERT (EU FP7-CSA-SA REGPOT-2008-2, grant agreement no. 245746), and the Tunisian Ministry of Higher Education and Scientific research in the ambit of the laboratory projects LR MBA206 and LR11ES31.


  1. Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54(10):876–886. doi: 10.1139/w08-081 CrossRefPubMedGoogle Scholar
  2. Afzal M, Khan QM, Sessitsch A (2014) Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117c:232–242. doi: 10.1016/j.chemosphere.2014.06.078 CrossRefGoogle Scholar
  3. Ait Kaki A, Kacem Chaouche N, Dehimat L, Milet A, Youcef-Ali M, Ongena M, Thonart P (2013) Biocontrol and plant growth promotion characterization of Bacillus species isolated from Calendula officinalis rhizosphere. Indian J Microbiol 53(4):447–452. doi: 10.1007/s12088-013-0395-y CrossRefPubMedPubMedCentralGoogle Scholar
  4. Almaghrabi OA, Massoud SI, Abdelmoneim TS (2013) Influence of inoculation with plant growth promoting rhizobacteria (PGPR) on tomato plant growth and nematode reproduction under greenhouse conditions. Saudi J Biol Sci 20(1):57–61. doi: 10.1016/j.sjbs.2012.10.004 CrossRefPubMedGoogle Scholar
  5. An S, Couteau C, Luo F, Neveu J, DuBow MS (2013) Bacterial diversity of surface sand samples from the Gobi and Taklamaken deserts. Microb Ecol 66(4):850–860. doi: 10.1007/s00248-013-0276-2 CrossRefPubMedGoogle Scholar
  6. Appuhn A, Joergensen RG (2006) Microbial colonization of roots as a function of plant species. Soil Biol Biochem 38:1040–1051CrossRefGoogle Scholar
  7. Backhaus S, Wiehl D, Beierkuhnlein C, Jentsch A, Wellstein C (2014) Warming and drought do not influence the palatability of Quercus pubescens willd leaves of four European provenances. Arthropod Plant Interact 8(4):329–337. doi: 10.1007/s11829-014-9313-4 Google Scholar
  8. Bae H, Sicher RC, Kim MS, Kim S-H, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60(11):3279–3295CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bashan Y, de-Bashan LE (2010) Microbial populations of arid lands and their potential for restoration of deserts. In: Soil biology and agriculture in the tropics. Springer, 109–137Google Scholar
  10. Bashan Y, Salazar BG, Moreno M, Lopez BR, Linderman RG (2012) Restoration of eroded soil in the Sonoran Desert with native leguminous trees using plant growth-promoting microorganisms and limited amounts of compost and water. J Environ Manag 102:26–36. doi: 10.1016/j.jenvman.2011.12.032 CrossRefGoogle Scholar
  11. Begley M, Gahan CG, Hill C (2002) Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl Environ Microbiol 68(12):6005–6012CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099CrossRefPubMedPubMedCentralGoogle Scholar
  13. Boor KJ (2006) Bacterial stress responses: what doesn’t kill them can make then stronger. PLoS Biol 4 (1). doi:  10.1371/journal.pbio.0040023
  14. Borin S, Ventura S, Tambone F, Mapelli F, Schubotz F, Brusetti L, Scaglia B, D’Acqui LP, Solheim B, Turicchia S, Marasco R, Hinrichs KU, Baldi F, Adani F, Daffonchio D (2010) Rock weathering creates oases of life in a High Arctic desert. Environ Microbiol 12(2):293–303. doi: 10.1111/j.1462-2920.2009.02059 CrossRefPubMedGoogle Scholar
  15. Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244(2):341–345. doi: 10.1016/j.femsle.2005.02.008 CrossRefPubMedGoogle Scholar
  16. Cassells A, Rafferty-McArdle S (2012) Priming of Plant Defenses by PGPR against Fungal and Bacterial Plant Foliar Pathogens. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin Heidelberg, 1–26. doi:  10.1007/978-3-642-23465-1_1
  17. Cavaglieri LOJ, Etcheverry M (2009) Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiol Res 164:391–399CrossRefPubMedGoogle Scholar
  18. Chanal A, Chapon V, Benzerara K, Barakat M, Christen R, Achouak W, Barras F, Heulin T (2006) The desert of Tataouine: an extreme environment that hosts a wide diversity of microorganisms and radiotolerant bacteria. Environ Microbiol 8(3):514–525. doi: 10.1111/j.1462-2920.2005.00921.x CrossRefPubMedGoogle Scholar
  19. Chanway CP (1997) Inoculation of tree roots with plant growth promoting soil bacteria: an emerging technology for reforestation. For Sci 43(1):99–112Google Scholar
  20. Colica G, Li H, Rossi F, Li D, Liu Y, De Philippis R (2014) Microbial secreted exopolysaccharides affect the hydrological behavior of induced biological soil crusts in desert sandy soils. Soil Biol Biochem 68:62–70. doi: 10.1016/j.soilbio.2013.09.017 CrossRefGoogle Scholar
  21. Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71(9):4951–4959. doi: 10.1128/aem.71.9.4951-4959.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21(1):1–18CrossRefPubMedGoogle Scholar
  23. Couillerot O, Prigent‐Combaret C, Caballero‐Mellado J, Moënne‐Loccoz Y (2009) Pseudomonas fluorescens and closely‐related fluorescent pseudomonads as biocontrol agents of soil‐borne phytopathogens. Lett Appl Microbiol 48(5):505–512CrossRefPubMedGoogle Scholar
  24. Daffonchio D, Hirt H, Berg G (2015) Plant-Microbe Interactions and Water Management in Arid and Saline Soils. In: Lugtenberg B (ed) Principles of Plant-Microbe Interactions. Springer International Publishing, 265–276. doi:  10.1007/978-3-319-08575-3_28
  25. Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Annu Rev Microbiol 61:401–422CrossRefPubMedGoogle Scholar
  26. De Freitas JR, Germida JJ (1992) Growth promotion of winter wheat by fluorescent pseudomonads under growth chamber conditions. Soil Biol Biochem 24(11):1127–1135. doi: 10.1016/0038-0717(92)90063-4 CrossRefGoogle Scholar
  27. De-Bashan LE, Hernandez JP, Nelson KN, Bashan Y, Maier RM (2010) Growth of quailbush in acidic, metalliferous desert mine tailings: effect of Azospirillum brasilense Sp6 on biomass production and rhizosphere community structure. Microb Ecol 60(4):915–927. doi: 10.1007/s00248-010-9713-7 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Deivanai S, Bindusara AS, Prabhakaran G, Bhore SJ (2014) Culturable bacterial endophytes isolated from Mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in Rice. J Nat Sci Biol Med 5(2):437–444. doi: 10.4103/0976-9668.136233 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Desai S, Grover M, Amalraj EL, Kumar GP, Ahmed SKM (2012) Exploiting Plant Growth Promoting Rhizomicroorganisms for Enhanced Crop Productivity. In: Satyanarayana T, Johri BN (eds) Microorganisms in Sustainable Agriculture and Biotechnology. Springer, Netherlands, 227–241. doi:  10.1007/978-94-007-2214-9_12
  30. Dias ACF, Costa FEC, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, Araújo WL, Azevedo JL, Melo IS (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25(2):189–195. doi: 10.1007/s11274-008-9878-0 CrossRefGoogle Scholar
  31. DiRuggiero J, Wierzchos J, Robinson CK, Souterre T, Ravel J, Artieda O, Souza-Egipsy V, Ascaso C (2013) Microbial colonization of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert. Biogeosciences 10(4):2439–2450. doi: 10.5194/bg-10-2439-2013 CrossRefGoogle Scholar
  32. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179(2):318–333CrossRefPubMedGoogle Scholar
  33. Duineveld BM, Rosado AS, van Elsas JD, van Veen JA (1998) Analysis of the dynamics of bacterial communities in the rhizosphere of the chrysanthemum via denaturing gradient gel electrophoresis and substrate utilization patterns. Appl Environ Microbiol 64(12):4950–4957PubMedPubMedCentralGoogle Scholar
  34. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36(2–3):184–189. doi: 10.1016/j.apsoil.2007.02.005 CrossRefGoogle Scholar
  35. El-Sayed WS, Akhkha A, El-Naggar MY, Elbadry M (2014) In vitro antagonistic activity, plant growth promoting traits and phylogenetic affiliation of rhizobacteria associated with wild plants grown in arid soil. Frontiers in microbiology 5Google Scholar
  36. Etesami H, Mirsyed Hosseini H, Alikhani HA (2014) In planta selection of plant growth promoting endophytic bacteria for rice (Oryza sativa L.). J Soil Sci Plant Nutr 14:491–503Google Scholar
  37. Falcäo LL, Silva-Werneck JO, Vilarinho BR, da Silva JP, Pomella AWV, Marcellino LH (2014) Antimicrobial and plant growth-promoting properties of the cacao endophyte Bacillus subtilis ALB629. J Appl Microbiol 116(6):1584–1592. doi: 10.1111/jam.12485 CrossRefPubMedGoogle Scholar
  38. Ferjani R, Marasco R, Rolli E, Cherif H, Cherif A, Gtari M, Boudabous A, Daffonchio D, Ouzari H-I (2015) The date palm tree rhizosphere is a niche for plant growth promoting bacteria in the oasis ecosystem. BioMed Res Int. doi: 10.1155/2015/153851 PubMedPubMedCentralGoogle Scholar
  39. Forchetti G, Masciarelli O, Alemano S, Alvarez D, Abdala G (2007) Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl Microbiol Biotechnol 76(5):1145–1152CrossRefPubMedGoogle Scholar
  40. Gabriele W, Regine N, Horst B (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67(12):5849–5854CrossRefGoogle Scholar
  41. Garbeva P, Van Elsas JD, Van Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32CrossRefGoogle Scholar
  42. Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2, 4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57(2):302–310CrossRefPubMedGoogle Scholar
  43. Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65(2–3):93–106. doi: 10.1016/S0378-4290(99)00080-5 CrossRefGoogle Scholar
  44. Hallmann J, Quadt-Hallmann A, Mahaffee W, Kloepper J (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43(10):895–914CrossRefGoogle Scholar
  45. Haney CH, Samuel BS, Bush J, Ausubel FM (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nature PlantsGoogle Scholar
  46. Jorquera MA, Shaharoona B, Nadeem SM, de la Luz MM, Crowley DE (2012) Plant growth-promoting rhizobacteria associated with ancient clones of creosote bush (Larrea tridentata). Microb Ecol 64(4):1008–1017. doi: 10.1007/s00248-012-0071-5 CrossRefPubMedGoogle Scholar
  47. Klay I, Pirrello J, Riahi L, Bernadac A, Cherif A, Bouzayen M, Bouzid S (2014) Ethylene response factor Sl-ERF. B. 3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. The Scientific World Journal 2014Google Scholar
  48. Koberl M, Muller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 6(9), e24452. doi: 10.1371/journal.pone.0024452 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant-Microbe Interact 17(1):6–15. doi: 10.1094/MPMI.2004.17.1.6 CrossRefPubMedGoogle Scholar
  50. Kumar A, Maurya BR, Raghuwanshi R (2014) Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatalysis and Agricultural Biotechnology (0). doi:  10.1016/j.bcab.2014.08.003
  51. Latour X, Corberand T, Laguerre G, Allard F, Lemanceau P (1996) The composition of fluorescent pseudomonad populations associated with roots is influenced by plant and soil type. Appl Environ Microbiol 62(7):2449–2456PubMedPubMedCentralGoogle Scholar
  52. Laukkanen H, Soini H, Kontunen-Soppela S, Hohtola A, Viljanen M (2000) A mycobacterium isolated from tissue cultures of mature Pinus sylvestris interferes with growth of Scots pine seedlings. Tree Physiol 20:915–920CrossRefPubMedGoogle Scholar
  53. Lazarovits G, Nowak J (1997) Rhizobacteria for improvement of plant growth and establishment. Hortic Sci 32(2):188–192Google Scholar
  54. Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, der Lelie D (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21(6):583–606CrossRefGoogle Scholar
  55. Lopez B, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the southern Sonoran Desert. Arch Microbiol 193(7):527–541. doi: 10.1007/s00203-011-0695-8 CrossRefPubMedGoogle Scholar
  56. Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60(1):157–166CrossRefPubMedGoogle Scholar
  57. Mapelli F, Marasco R, Balloi A, Rolli E, Cappitelli F, Daffonchio D, Borin S (2012) Mineral-microbe interactions: biotechnological potential of bioweathering. J Biotechnol 157(4):473–481. doi: 10.1016/j.jbiotec.2011.11.013 CrossRefPubMedGoogle Scholar
  58. Mapelli F, Marasco R, Rolli E, Barbato M, Cherif H, Guesmi A, Ouzari I, Daffonchio D, Borin S (2013) Potential for plant growth promotion of Rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed research international 2013Google Scholar
  59. Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One 7(10), e48479. doi: 10.1371/journal.pone.0048479 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Marasco R, Rolli E, Fusi M, Cherif A, Abou-Hadid A, El-Bahairy U, Borin S, Sorlini C, Daffonchio D (2013a) Plant growth promotion potential is equally represented in diverse grapevine root-associated bacterial communities from different biopedoclimatic environments. BioMed Res Int 2013Google Scholar
  61. Marasco R, Rolli E, Vigani G, Borin S, Sorlini C, Ouzari H, Zocchi G, Daffonchio D (2013b) Are drought-resistance promoting bacteria cross-compatible with different plant models? Plant Signal Behav 8 (10). doi:  10.4161/psb.26741
  62. McCully M (2005) The rhizosphere: the key functional unit in plant/soil/microbial interactions in the field. Implications for the understanding of allelopathic effects. In: Proceedings of the 4th World Congress on Allelopathy, 2005. 21–26Google Scholar
  63. Melnick RL, Bailey BA, Backman PA (2013) Bacterial endophytes of perennial crops for management of plant disease. In: Bacteria in Agrobiology: Disease Management. Springer, 49-76Google Scholar
  64. Müller H, Berg C, Landa B, Auerbach B, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Frontiers in Microbiology 6. doi: 10.3389/fmicb.2015.00138
  65. Muñoz Z, Moret A, Garcés S (2009) Assessment of chitosan for inhibition of Colletotrichum sp. on tomatoes and grapes. Crop Prot 28(1):36–40. doi: 10.1016/j.cropro.2008.08.015 CrossRefGoogle Scholar
  66. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32(2):429–448. doi: 10.1016/j.biotechadv.2013.12.005 CrossRefPubMedGoogle Scholar
  67. Nagy ML, Perez A, Garcia-Pichel F (2005) The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54(2):233–245. doi: 10.1016/j.femsec.2005.03.011 CrossRefPubMedGoogle Scholar
  68. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270(45):26723–26726CrossRefPubMedGoogle Scholar
  69. Neilson JW, Quade J, Ortiz M, Nelson WM, Legatzki A, Tian F, LaComb M, Betancourt JL, Wing RA, Soderlund CA, Maier RM (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles: Life Under Extreme Cond 16(3):553–566. doi: 10.1007/s00792-012-0454-z CrossRefGoogle Scholar
  70. Othman AA, Amer WM, Fayez M, Hegazi N (2004) Rhizosheath of Sinai desert plants is a potential repository for associative diazotrophs. Microbiol Res 159(3):285–293CrossRefPubMedGoogle Scholar
  71. Park MS, Jung SR, Lee MS, Kim KO, Do JO, Lee KH, Kim SB, Bae KS (2005) Isolation and characterization of bacteria associated with two sand dune plant species, Calystegia soldanella and Elymus mollis. J Microbiol-Seoul- 43(3):219Google Scholar
  72. Paula MA, Urquiaga S, Siqueira JO, Döbereiner J (1992) Synergistic effects of vesicular-arbuscular mycorrhizal fungi and diazotrophic bacteria on nutrition and growth of sweet potato (Ipomoea batatas). Biol Fertil Soils 14(1):61–66. doi: 10.1007/BF00336304 CrossRefGoogle Scholar
  73. Pirttilä AM, Laukkanen H, Pospiech H, Myllylä R, Hohtola A (2000) Detection of intracellular bacteria in the buds of Scotch Pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077CrossRefPubMedPubMedCentralGoogle Scholar
  74. Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10(8):551–562. doi: 10.1038/nrmicro2831 CrossRefPubMedGoogle Scholar
  75. Qin S, Xing K, Jiang J-H, Xu L-H, Li W-J (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic Actinobacteria. Appl Microbiol Biotechnol 89(3):457–473CrossRefPubMedGoogle Scholar
  76. Raddadi N, Cherif A, Daffonchio D, Fava F (2013) Halo-alkalitolerant and thermostable cellulases with improved tolerance to ionic liquids and organic solvents from Paenibacillus tarimensis isolated from the Chott El Fejej, Sahara desert, Tunisia. Bioresour Technol 150:121–128. doi: 10.1016/j.biortech.2013.09.089 CrossRefPubMedGoogle Scholar
  77. Recep K, Fikrettin S, Erkol D, Cafer E (2009) Biological control of the potato dry rot caused by Fusarium species using PGPR strains. Biol Control 50(2):194–198CrossRefGoogle Scholar
  78. Requena N, Jimenez I, Toro M, Barea JM (1997) Interactions between plant-growth promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136:667–677CrossRefGoogle Scholar
  79. Rhoden SA, Garcia A, Santos E, Silva MC, Azevedo JL, Pamphile JA (2015) Phylogenetic analysis of endophytic bacterial isolates from leaves of the medicinal plant Trichilia elegans A. Juss. (Meliaceae). Genet Mol Res 14(1):1515–1525. doi: 10.4238/2015.February.20.7 CrossRefPubMedGoogle Scholar
  80. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Funct Plant Biol 28(9):897–906CrossRefGoogle Scholar
  81. Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321(1–2):305–339CrossRefGoogle Scholar
  82. Rodríguez‐Díaz M, Rodelas‐Gonzalés B, Pozo‐Clemente C, Martínez‐Toledo MV, González‐López J (2008) A review on the taxonomy and possible screening traits of plant growth promoting rhizobacteria. Plant-Bacteria Interactions: Strategies and Techniques to Promote Plant Growth: 55–80Google Scholar
  83. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19(8):827–837CrossRefPubMedGoogle Scholar
  84. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278(1):1–9. doi: 10.1111/j.1574-6968.2007.00918.x CrossRefPubMedGoogle Scholar
  85. Saharan B, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30Google Scholar
  86. Salles JF, Van Veen JA, Van Elsas JD (2004) Multivariate analyses of Burkholderia species in soil: effect of crop and land use history. Appl Environ Microbiol 70(7):4012–4020CrossRefPubMedPubMedCentralGoogle Scholar
  87. Sandhya V, Ali SZ, Venkateswarlu B, Reddy G, Grover M (2010) Effect of osmotic stress on plant growth promoting Pseudomonas spp. Arch Microbiol 192(10):867–876. doi: 10.1007/s00203-010-0613-5 CrossRefPubMedGoogle Scholar
  88. Saul-Tcherkas V, Steinberger Y (2011) Soil microbial diversity in the vicinity of a Negev Desert Shrub—Reaumuria negevensis. Microb Ecol 61(1):64–81. doi: 10.1007/s00248-010-9763-x CrossRefPubMedGoogle Scholar
  89. Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85(2):371–381CrossRefPubMedGoogle Scholar
  90. Shelef O, Helman Y, Friedman ALL, Behar A, Rachmilevitch S (2013) Tri-party underground symbiosis between a weevil, bacteria and a desert plant. PloS One 8 (11). doi:  10.1371/journal.pone.0076588
  91. Shukla KP, Sharma S, Singh NK, Singh V, Tiwari K, Singh S (2013) Nature and role of root exudates: efficacy in bioremediation. Afr J Biotechnol 10(48):9717–9724CrossRefGoogle Scholar
  92. Siddiqui ZA (2006) PGPR: prospective biocontrol agents of plant pathogens. In: PGPR: biocontrol and biofertilization. Springer, 111–142Google Scholar
  93. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31(4):425–448CrossRefPubMedGoogle Scholar
  94. Strobel G (2007) Plant‐Associated Microorganisms (Endophytes) as a new source of bioactive natural products. Med Plant Biotechnol: From Basic Res Ind Appl 49–72Google Scholar
  95. Ulrich K, Ulrich A, Ewald D (2008) Paenibacillus - a predominant endophytic bacterium colonizing tissue cultures of woody plants. Plant Cell Tissue Organ Cult 93:347–351CrossRefGoogle Scholar
  96. Van Loon L, Bakker P, Pieterse C (1997) Mechanisms of PGPR-induced resistance against pathogensGoogle Scholar
  97. Van Overbeek L, Van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296CrossRefPubMedGoogle Scholar
  98. Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7(12), e52565. doi: 10.1371/journal.pone.0052565 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Whitford WG (2002) Ecology of desert systems. Academic PressGoogle Scholar
  100. Xia Y, Greissworth E, Mucci C, Williams MA, De Bolt S (2013) Characterization of culturable bacterial endophytes of switchgrass (Panicum virgatum L.) and their capacity to influence plant growth. GCB Bioenergy 5(6):674–682CrossRefGoogle Scholar
  101. Xu Y, Rossi F, Colica G, Deng S, De Philippis R, Chen L (2013) Use of cyanobacterial polysaccharides to promote shrub performances in desert soils: a potential approach for the restoration of desertified areas. Biol Fertil Soils 49(2):143–152CrossRefGoogle Scholar
  102. Yanxia Xu GW, Jian J, Junjie L, Qiuying Z, Xiaobing L (2009) Bacterial communities in soybean rhizosphere in response to soil type, soybean genotype, and their growth stage. Soil Biol Biochem 41:919–925CrossRefGoogle Scholar
  103. Zahran H.H (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 968–989Google Scholar
  104. Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374(1–2):689–700CrossRefGoogle Scholar
  105. Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68(5):2198–2208CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Asma Soussi
    • 1
  • Raoudha Ferjani
    • 2
  • Ramona Marasco
    • 1
  • Amel Guesmi
    • 2
  • Hanene Cherif
    • 2
  • Eleonora Rolli
    • 3
  • Francesca Mapelli
    • 3
  • Hadda Imene Ouzari
    • 2
  • Daniele Daffonchio
    • 1
    • 3
  • Ameur Cherif
    • 4
    Email author
  1. 1.Biological and Environmental Sciences and Engineering DivisionKing Abdullah University of Science and TechnologyThuwalKingdom of Saudi Arabia
  2. 2.Laboratory of Microorganisms and Active Biomolecules, Faculty of Sciences of TunisUniversity of Tunis El ManarTunisTunisia
  3. 3.Department of Food Environmental and Nutritional SciencesUniversità degli Studi di MilanoMilanoItaly
  4. 4.Higher Institute of Biotechnology, LR11-ES31 Biotechnology and Bio-Geo Resources ValorizationUniversity of ManoubaArianaTunisia

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