Abstract
Plant–microbe and soil interactions are one of the oldest muse for multi-disciplinary researchers. Plant growth promoting microorganisms influence the host physiology by secreting regulatory chemical signals in the vicinity of plant roots and play a key role in the enhancement of plant growth and expansion. The present review deals with the in-depth understanding of steps involved in host tissues colonization by bacterial endophytes. The molecular insights of these events, particularly for endophytic bacteria, are poorly documented till date. The endophytic bacteria must coexist with the host plant and capable of colonizing the internal plant tissues without being recognized as a pathogen. A proper understanding of exchange of signals between the host plant and bacterial communities is required which may facilitate the development of new strategies to promote beneficial interactions between them. This knowledge can be instrumental in agricultural practices as well as for phytoremediation of pollutants. Keeping these facts in mind, the present review attempts to explore the systematic understanding of steps involved and molecular insights of plant colonization events by endophytic bacteria. We conclude that molecular mechanisms and factors affecting endophytic bacterial colonization deserve more research attention in order to exploit their beneficial aspects for sustainable agriculture and environment.
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References
Ahemad M, Khan MS (2010) Influence of selective herbicides on plant growth promoting traits of phosphate solubilizing Enterobacter asburiae strain PS2. Res J Microbiol 5:849–857
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20
Alavi P, Müller M, Cardinale M, Zachow C, Sanchez MB, Martínez JL, Berg G (2013) The DSF quorum sensing system controls the positive influence of Stenotrophomonas maltophila on plants. PloS One 8:e67103
Ali S, Trevor CC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160167
Antunes LCM, Ferreira RBR, Buckner MMC, Finlay BB (2010) Quorum sensing in bacterial virulence. Microbiology 156:2271–2282
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in the rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Balsanelli E, Serrato RV, de Baura VA, Sassaki G, Yates MG, Rigo LU, Pedrosa FO, de Souza EM, Monteiro RA (2010) Herbaspirillum seropedicae rfbB and rfbC genes are required for maize colonization. Environ Microbiol 12:2233–2244
Balsanelli E, Tuleski TR, de Baura VA, Yates MG, Chubatsu LS, de Oliveira Pedrosa F, de Souza EM, Monteiro RA (2013) Maize root lectins mediate the interaction with Herbaspirillum seropedicae via N-acetyl glucosamine residues of lipopolysaccharides. PloS One 10:e77001. https://doi.org/10.1371/journal.pone
Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth promoting rhizobacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250
Berendsen RL, van Verk MC, Stringlis IA, Zamioudis C, Tommassen J, Pieterse CMJ, Bakker PAHM (2015) Unearthing the genomes of plant-beneficial Pseudomonas model strains WCS358, WCS374 and WCS417. BMC Genom 16:539
Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Bilal R, Rasul G, Arshad M, Malik K (1993) Attachment, colonization and proliferation of Azospirillum brasilense and Enterobacter spp. on root surface of grasses. World J Microbiol Biotechnol 9:63–69
Bloemberg GV, Lugtenberg B (2001) Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol. https://doi.org/10.1016/S1369-5266(00)00183-7
Böhm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2-fixing endophzyte Azoarcus sp. strain BH72. Mol Plant-Microbe Interact 20:526–533
Burdman GI, Dixon DG, Glick BR (2000) Plant growth promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46:237–245
Carvalho TL, Ballesteros HG, Thiebaut F, Ferreira PC, Hemerly AS (2016) Nice to meet you: genetic, epigenetic and metabolic controls of plant perception of beneficial associative and endophytic diazotrophic bacteria in non-leguminous plants. Plant Mol Biol 90:561–574
Cazorla FM, Romero D, Perez-Garcıa A, Lugtenberg BJ, deVicente Ad, Bloemberg G (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103:1950–1959
Cecagno R, Fritsch TE, Schrank IS (2014) The plant growth-promoting bacteria Azospirillum amazonense: genomic versatility and phytohormone pathway. BioMed Research Int. https://doi.org/10.1155/2015/898592
Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278
Chu W, Zhou S, Zhu W, Zhuang X (2014) Quorum quenching bacteria Bacillus sp. QSI-1 protect zebrafish (Danio rerio) from Aeromonas hydrophila infection. Sci Rep 4:5446
Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clément C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93
Compant S, Cle´ment C, Sessitsch A (2010) A plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Compant S, Mitter M, Colli-Mull JG, Gang H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197
Compant S, Saikkonen K, Mitter M, Campisano A, Mercado-Blanco J (2016) Editorial special issue: soil, plants and endophytes. Plant Soil 405:1–11
Coutinho BG, Licastro D, Mendonca-Previato L, Cámara M, Venturi V (2015) Plant-influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol Plant-Microbe Interact 28:10–21
Croes CL, Moens S, van Bastelaere E, Vanderleyden J, Michieles KW (1993) The polar flagellum mediates Azospirillum brasiliense adsorption on wheat roots. J Gen Microbiol 139:2261–2269
Czaban J, Gajda A, Wróblewska B (2007) The motility of bacteria from rhizosphere and different zones of winter wheat roots. Polish J Environ Stud 16:301–308
Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legume transcend antimicrobial definitions of phytoalexins. Physiol Mol Plant Pathol 49:1–20
Dary M, Chamber-Pe´rez MA, Palomares AJ, Pajuelo E (2010) ‘‘In situ’’ phytostabilisation of heavy metal polluted soils using Lupinus luteus inoculated with metal resistant plant-growth promoting rhizobacteria. J Hazard Mater 177:323–330
de Laurentis VL, De Bortoli SA, Polanczyk RA, Lessandra MV, Veiga ACP, De Bortoli CP, Volpe HX (2014a) Kluyvera ascorbata: a plant growth-promoting bacteria (PGPB) to manage plutella xylostella (L. 1758) (Lepidoptera: plutellidae). Int J Res Agri Sci 1:340–343
de Laurentis VL, De Bortoli SA, Polanczyk RA, Vacari AM, Veiga ACP, De Bortoli CP, Volpe HXL (2014b) Kluyvera ascorbata: a plant growth-promoting bacteria (PGPB) to manage Plutella xylostella (lepidoptera: plutellidae). Int J Res Agri Sci 5:340–343
de Weert S, Vermeiren H, Mulders IH, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15:1173–1180
de Weert S, Dekkers LC, Bitter W, Tuinman S, Wijfjes AH, Boxtel RV, Lutenberg BJJ (2006) The two-component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane. FEMS Microbiol Ecol 58:205–213
Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci 97:3526–3531
Dong YH, Gusti AR, Zhang Q, Xu JL (2002) Identification of quorum quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759
Dong Y, Iniguez AL, Triplett EW (2003) Quantitative assessments of the host range and strain specificity of endophytic colonization by Klebsiella pneumoniae 342. Plant Soil 257:49–59
Dörr J, Hurek T, Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol Microbiol 30:7–17
Downing KJ, Thomson JA (2000) Introduction of the Serratia marcescens chiA gene into an endophytic Pseudomonas fluorescens for the biocontrol of phytopathogenic fungi. Can J Microbiol 46:363–369
Duffy BK, Defago G (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65:2429–2438
Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36(3):232–244
Eastman EW, Weselowski B, Nathoo N, Yuan ZC (2014) Complete genome sequence of Paenibacillus polymyxa CR1, a plant growth-promoting bacterium isolated from the corn rhizosphere exhibiting potential for biocontrol, biomass degradation, and biofuel production. Genome Announc. https://doi.org/10.1128/genomeA.01218-13
Espinosa-Urgel M, Kolter R, Ramos JL (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology 148:341–343
Fan X, Yang R, Qiu S, Cai X, Zou H, Hu F (2016) The endo-β-1,4-glucanase of Bacillus amyloliquefaciens is required for optimum endophytic colonization of plants. J Microbiol Biotechnol 26:946–952
Frey-Klett P, Burlinson P, Deveau A, Barret M, Tarkka M, Sarniguet A (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75:583–609
Fuentes-Ramı́rez LE, Caballero-Mellado J, Sepúlveda J, Martı́nez-Romero E (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Ecol 29:117–128
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Hindawi Publishing Corporation, Scientifica. https://doi.org/10.6064/2012/96340
Gough C, Galera C, Vasse J, Webster G, Cocking EC, Denarie J (1997) Specific flavonoids promote intercellular colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS 571. Mol Plant-Microbe Interact 10:560–567
Gray KM, Garey JR (2001) The evolution of bacterial LuxI and LuxR quorum sensing regulators. Microbiology 147:2379–2387
Gupta G, Panwar J, Akhtar MS, Jha PN (2012) Endophytic nitrogen-fixing bacteria as biofertilizer (2012). In: Lichtfouse E (ed) sustainable agriculture reviews, https://doi.org/10.1007/978-94-007-5449-2_8. Springer Science Business Media, Dordrecht
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 7:096–102. https://doi.org/10.4172/1948-5948.1000188
Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93
Hallmann JA, Quadt-Hallmann WF, Mahaffee Kloepper JW (1997) Endophytic bacteria in agricultural crops. Can J Microbiol 43:895–914
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within Plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320
Heeb S, Haas D (2001) Regulatory roles of the GacS/GacA two-compound system in plant-associated and other Gram-negative bacteria. Mol Plant-Microbe Interact 14:1351–1363
Hiltner L (1904) Iiber neuere Erfahrungen und unter besonderer berucksichtingung der grundunging und brache. Arb Dtsch Landw Ges 98:59–78
Hinsa SM, O’Toole GA (2006) Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD. Microbiology 152:1375–1383
Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178
Ijaz A, Shabir G, Khan QM, Afzal M (2015) Enhanced remediation of sewage effluent by endophyte-assisted floating treatment wetlands. Ecol Eng 84:58–66
Ijaz A, Imran A, Haq MA, Khan QM, Afzal M (2016) Phytoremediation recent advances in plant-endophytic synergistic interactions. Plant Soil 405:179–195
Iniguez AL, Dong Y, Carter HD, Ahmer BMM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant-Microbe Interact 18:169–178
James EK, Olivares FL (1998) Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119
James EK, Olivares FL, de Oliveira ALM, dos Reis Jr FB, da Silva LG, Reis VM (2001) Further observations on the interaction between sugar cane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J Exp Bot 52:747–760
Jha PN, Kumar A (2007) Endophytic colonization of Typha australis by a plant growth-promoting bacterium Klebsiella oxytoca strain GR-3. J Appl Microbiol 103:1311–1320
Jha P, Panwar J, Jha PN (2015) Secondary plant metabolites and root exudates: guiding tools for polychlorinated biphenyl biodegradation. Int J Environ Sci Technol 12:789–802
Jiang C, Sheng X, Qian M, Wang Q (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal polluted soil. Chemosphere 72:157–164
Jida M, Assefa F (2012) Phenotypic diversity and plant growth promoting characteristics of Mesorhizobium species isolated from chickpea (Cicer arietinum L.) growing areas of Ethiopia. Afr J Biotechnol 29:7483–7493
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kaira GS, Dhakar K, Pandey A (2015) A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range. AMB Express 5:1
Kang BG, Kim WT, Yun HS, Chang SC (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183
Khammas K, Kaiser P (1991) Characterization of a pectinolytic activity in Azospirillum irakense. In: Polsinelli M, Materassi R, Vincenzini M (eds) Nitrogen fixation. Developments in plant and soil sciences, vol 48. Springer, Dordrecht, pp 205–209
Kloepper JW (1993) Plant growth-promoting rhizobacteria as biological control agents. In: Metting FB Jr (ed) Soil microbial ecology-applications in agricultural and environmental management. Marcel Dekker, New York, pp 255–274
Kloepper JW, Leong J, Teintz M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth promoting rhizobacteria. Nature 286:885
Kumar KV, Singh N, Behl HM, Srivastava S (2008) Influence of plant growth promoting bacteria and its mutant on heavy metal toxicity in Brassica juncea grown in fly ash amended soil. Chemosphere 72:678–683
Li L, Jiao Z, Hale L, Wu W, Guo Y (2014) Disruption of gene pqqA or pqqB reduces plant growth promotion activity and biocontrol of crown gall disease by Rahnella aquatilis HX2. PlosOne. https://doi.org/10.1371/journal.pone.0115010
Liu H, He Y, Jiang H, Peng H, Huang X, Zhang X, Thomashow LS, Xu Y (2007) Characterization of a phenazine producing strain Pseudomonas chlororaphis GP72 with broad spectrum antifungal activity from green pepper rhizosphere. Curr Microbiol 54:302–306
Lledó S, Rodrigo S, Poblaciones MJ, Santamaria O (2016) Biomass yield, nutritive value and accumulation of minerals in Trifolium subterraneumas affected by fungal endophytes. Plant Soil. https://doi.org/10.1007/s11104-015-2596-0
Lopez-Gomez M, Sandal N, Stougaard J, Boller T (2012) Interplay of flg22-induced defense responses and nodulation in Lotus japonicus. J Exp Bot 63:393–401
Lugtenberg BJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by pseudomonas. Annu Rev Phytopathol 39:461–490
Ma Y, Rajkumar M, Luo Y, Freitas H (2011a) Inoculation of endophytic bacteria on host and non-host plants-effects on plant growth and Ni uptake. J Hazard Mater 195:230–237
Ma Y, Rajkumar M, Vicente JA, Freitas H (2011b) Inoculation of Ni-resistant plant growth promoting bacterium Psychrobacter sp. strain SRS8 for the improvement of nickel phytoextraction by energy crops. Int J Phytoremediation 13:126–139
Maldonado-González Schiliro E, Prieto P, Mercado-Blanco J (2015) Endophytic colonization and biocontrol performance of Pseudomonas fluorescens PICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility. Environ Microbiol 17:3139–3153
Mark GL, Dow JM, Kiely PD, Higgins H, Haynes J, Baysse C, Abbas A, Foley T, Franks A, Morrissey J, O’Gara F (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci USA 102:17454–17459
Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollès G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci USA 100:1444–1449
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
Meneses CH, Rouws LF, Simoes-Araujo JL, Vidal MS, Baldani JI (2011) Exopolysaccharide production is required for biofilm formation and plant colonization by the nitrogen-fixing endophyte Gluconacetobacter diazotrophicus. Microbe Interact 24:1448–1458
Meneses C, Gonçalves T, Alquéres S, Rouws L, Serrato R, Vidal M, Baldani JI (2017) Gluconacetobacter diazotrophicus exopolysaccharide protects bacterial cells against oxidative stress in vitro and during rice plant colonization. Plant Soil 416:133–147
Miché L, Battistoni F, Gemmer S, Belghazi M, Reinhold-Hurek B (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant Microbe 19:502–511
Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414
Noordman WH, Reissbrodt R, Bongers RS, Rademaker ILW, Bockelmann W, Smit G (2006) Growth stimulation of Brevibacterium sp. by siderophores. J Appl Microbiol 101:637–646
O’Toole GA (2016) Classic spotlight: quorum sensing and the multicellular life of unicellular organisms. J Bacteriol 198:601. https://doi.org/10.1128/JB.00956-15
O’Callaghan KJ, Stone PJ, Hu X, Griffiths DW, Davey MR, Cocking EC (2000) Effects of glucosinolates and flavonoids on colonization of the roots of Brassica napus by Azorhizobium caulinodans ORS571. Appl Environ Microbiol 66:2185–2191
Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, Colauto NB, Fernandez MA, Fungaro MHP, Grisard EC, Hungria M et al (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7:e100206
Pérez-Donoso AG, Sun Q, Roper MC, Greve LC, Kirkpatrick B, Labavitch JM (2010) Cell wall-degrading enzymes enlarge the pore size of intervessel pit membranes in healthy and Xylella fastidiosa-infected grapevines. Plant Physiol 152:1748–1759
Pétriacq P, Williams A, Cotton A, McFarlane AE, Rolfe SA, Ton J (2017) Metabolite profiling of non-sterile rhizosphere soil. Plant J 92(1):147–162
Pierson EA, Wood DW, Cannon JA, Blachere FM, Pierson LS III (1998) Interpopulation signaling via N-acyl-homoserine lactones among bacteria in the wheat rhizosphere. Mol Plant-Microbe Interact 11:1078–1084
Podile AR, Vukanti RVNR Sravani, Kalam S, Dutta S, Durgeshwar P, Rao VP (2014) Root colonization and quorum sensing are the driving forces of plant. Proc Indian Natl Sci Acad 80:407–413
Preston GM, Bertrand N, Rainey PB (2001) Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol 41:999–1014
Prieto P, Schilirò E, Maldonado-González MM, Valderrama R, Barroso-Albarracín JB, Mercado-Blanco J (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb Ecol 62:435–445
Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie Van Leeuwenhoek 81:537–547
Rajkumar M, Nagendran R, Kui JL, Wang HL, Sung ZK (2006) Influence of plant growth promoting bacteria and Cr(VI) on the growth of Indian mustard. Chemosphere 62:741–748
Rajwar A, Sahgal M, Johri BN (2013) Legume- Rhizobia symbiosis and interactions in agroecosystems. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Fundamentals and Advances. https://doi.org/10.1007/978-81-322-1287-4
Ramírez-Mata A, Lopez-Lara LI, Xiqui-Vázquez ML, Jijon-Moreno S, Romero-Osorio A, Baca BE (2016) The cyclic-di-GMP diguanylate cyclase CdgA has a role in biofilm formation and exopolysaccharide production in Azospirillum brasilense. Res Microbiol 167:190–201
Ramos HJ, Roncato-Maccari LD, Souza EM, Soares-Ramos JR, Hungria M, Pedrosa FO (2002) Monitoring Azospirillum-wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J Biotechnol 97:243–252
Reinhold Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14(4):435–443
Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144
Reinhold-Hurek B, Maes T, Gemmer S, Van Montagu M, Hurek T (2006) An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus sp. strain BH72. Mol Plant-Microbe Interact 19:181–188
Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S, Dhakephalkar PK, Chopade BA (2011) Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J Microbiol Biotechnol 21:556–566
Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interaction with hosts. Mol Plant-Microbe Interact 19:827–837
Sang-Mi Yu, Lee YH (2013) Plant growth promoting rhizobacterium Proteus vulgaris JBLS202 stimulates the seedling growth of Chinese cabbage through indole emission. Plant Soil 370:485–495
Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798
Serrato RV, Sassaki GL, Cruz LM, Carlson RW, Muszyński A, Monteiro RA, Pedrosa FO, Souza EM, Iacomini M (2010) Chemical composition of lipopolysaccharides isolated from various endophytic nitrogen-fixing bacteria of the genus Herbaspirillum. Can J Microbiol 56:342–347
Sevilla M, Kennedy C (2000) Genetic analysis of nitrogen fixation and plant-growth-stimulating properties of Acetobacter diazotrophicus, an endophyte of sugar cane. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Horizon Scientific Press, UK, pp 737–760
Shatrupa R, Jyoti S, Rahul SR, Hrikesh BS, Surendra S (2018) Endophytic bacteria: anessential requirement of phyto nutrition. Nutri FoodSci Int J 5(2):555657. https://doi.org/10.19080/NFSIJ.2018.05.555657
Singh RK, Malik N, Singh S (2013) Impact of rhizobial inoculation and nitrogen utilization in plant growth promotion of maize (Zea mays L.) Nusantara. Bioscience 5:8–14
Slininger PJ, Shea-Wilbur MA (1995) Liquid-culture pH, temperature, and carbon (not nitrogen) source regulate phenazine productivity of the take-all biocontrol agent Pseudomonas fluorescens. Appl Microbiol Biotechnol 43:388–392
Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–235
Sprent JI, de Faria SM (1988) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157–165
Studer SV, Schwartzman JA, Ho JS, Geske GD, Blackwell HE, Ruby EG (2014) Non-native acylated homoserine lactones reveal that LuxIR quorum sensing promotes symbiont stability. 16:2623–2634
Suzuki W, Sugawara M, Miwa K, Morikawa M (2014) Plant growth-promoting bacterium Acinetobacter calcoaceticus P23 increases the chlorophyll content of the monocot Lemna minor (duckweed) and the dicot Lactuca sativa (lettuce). J Biosci Bioeng 118:41–44
Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting bacterium Enterobacter sp. 638. Plos Genet 13(6):943. https://doi.org/10.1371/journal.pgen.1000943
Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71:7292–7300
Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2005) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664
Van Overbeek LS, Saikkonen K (2016) Impact of bacterial-fungal interactions on the colonization of the endosphere. Trends Plant Sci 21:230–242
VanHook AM (2016) Host exploits bacterial quorum sensing. Sci Signal 424:ec90
Veselova MA, Klein SH, Bass IA, Lipasova VA, Metlitskaya AZ, Ovadis MI, Chernin LS, Khmel IA (2008) Quorum sensing systems of regulation, synthesis, synthesis of phenazine antibiotics and antifungal activity in rhizospheric bacterium Pseudomonas chlororaphis 449. Russ J Genet 44:1400–1408
Vivas A, Biró B, Ruíz-Lozano JM, Barea JM, Azcón R (2006) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn toxicity. Chemosphere 62:1523–1533
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51. https://doi.org/10.1104/pp.102.019661132:44-51
Wani P, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267
Webster G, Gough C, Vasse J, Batchelor CA, O’Callaghan KJ, Kothari SL, Davey MR, Dènariè J, Cocking EC (1997) Interactions of rhizobia with rice and wheat. Plant Soil 194:115–122
Wei HL, Zhang LQ (2006) Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie Van Leeuwenhoek 89:267–280
Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhang W, Yao Z, Li H et al (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci USA 105:7564–7569
Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997
Zhang Z, Pierson LS III (2001) A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production in Pseudomonas aureofaciens. Appl Environ Microbiol 67:4305–4315
Zhu X, Ni X, Liu J, Gao YZ (2014) Application of endophytic bacteria to reduce persistent organic pollutants contamination in plants. Clean-Soil Air Water 42:306–310
Acknowledgements
Prameela Jha is thankful to financial support provided by DST, India under the scheme WOS-A (DST No. SR/WOS-A/LS-275/2011) PJ, PNJ and JP thank Birla Institute of Technology and Science, Pilani, India for providing logistic supports.
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Jha, P., Panwar, J. & Jha, P.N. Mechanistic insights on plant root colonization by bacterial endophytes: a symbiotic relationship for sustainable agriculture. Environmental Sustainability 1, 25–38 (2018). https://doi.org/10.1007/s42398-018-0011-5
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DOI: https://doi.org/10.1007/s42398-018-0011-5