Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 128, Issue 3, pp 487–508 | Cite as

Bacteria in the plant tissue culture environment



Bacteria and plants are joined in various symbiotic relationships that have developed over millennia and have influenced the evolution of both groups. Bacteria inhabit the surfaces of most plants and are also present inside many plant organs. These bacteria may have positive, neutral or negative impacts on their plant hosts. Probiotic effects may improve plant nutrition or increase resistance to biotic and abiotic stresses. Conversely pathogenic bacteria may kill or reduce the vigor of plant hosts. In addition some bacteria inhabit plants and profit from excess metabolites or shelter while not injuring the plant. Micropropagation of plants is based on the stimulation of organogenesis or embryogenesis from explants that are superficially decontaminated and placed into a sterile environment. If successful, this process removes bacteria from surfaces, but those inhabiting inner tissues and organs are usually not affected by these steriliants. In vitro conditions are designed for optimal plant growth and development, however these conditions are also often ideal for bacterial multiplication. The presence of bacteria in the in vitro environment was almost universally considered negative for plant culture, but more recently this view has been questioned. Certain bacteria appear to have a beneficial effect on the explants in culture; increasing multiplication and rooting, increasing explant quality, and organo- and embryogenesis of recalcitrant genotypes. The most important role of beneficial bacteria for micropropagated plants is likely to be during acclimatization, when growth is resumed under natural conditions. This review includes the role of bacterial interactions in plants, especially those grown in vitro.


Beneficial bacteria Biotization Burkholderia Contamination Stress Symbiosis 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aballay E, Mårtensson A, Persson P (2011) Screening of rhizosphere bacteria from grapevine for their suppressive effect on Xiphinema index Thorne & Allen on in vitro grape plants. Plant Soil 347:313–325. doi: 10.1007/s11104-011-0851-6 CrossRefGoogle Scholar
  2. Abdi G, Salehi H, Khosh-Khui M (2008) Nano silver: a novel nanomaterial for removal of bacterial contaminants in valerian (Valeriana officinalis L.) tissue culture. Acta Physiol Plant 30:709–714. doi: 10.1007/s11738-008-0169-z CrossRefGoogle Scholar
  3. Abreu-Tarazi MF, Navarrete AA, Andreote FD, Almeida CV, Tsai SM, Almeida M (2010) Endophytic bacteria in long-term in vitro cultivated “axenic” pineapple microplants revealed by PCR–DGGE. World J Microbiol Biotechnol 26:555–560. doi: 10.1007/s11274-009-0191-3 CrossRefGoogle Scholar
  4. Ali B, Hasnain S (2007) Efficacy of bacterial auxin on in vitro growth of Brassica oleracea L. World J Microbiol Biotechnol 23:779–784. doi: 10.1007/s11274-006-9297-z CrossRefGoogle Scholar
  5. Ali S, Charles TC, Glick BR (2014a) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167. doi: 10.1016/j.plaphy.2014.04.003 PubMedCrossRefGoogle Scholar
  6. Ali S, Duan J, Charles TC, Glick BR (2014b) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198. doi: 10.1016/j.jtbi.2013.10.007 PubMedCrossRefGoogle Scholar
  7. Alvarez AM (2004) Integrated approaches for detection of plant pathogenic bacteria and diagnosis of bacterial diseases. Annu Rev Phytopathol 42:339–366. doi: 10.1146/annurev.phyto.42.040803.140329 PubMedCrossRefGoogle Scholar
  8. Andreote FD, da Rocha UN, Araújo WL, Azevedo JL, van Overbeek LS (2010) Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum). Antonie Van Leeuwenhoek 97:389–399. doi: 10.1007/s10482-010-9421-9 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Andressen D, Manoochehri I, Carletti S, Llorente B, Tacoronte M, Vielma M l (2009) Optimization of the in vitro proliferation of jojoba (Simmondsia chinensis (Link)Schn.) by using rotable central composite design and inoculation with rhizobacteria. Bioagro 21:41–48Google Scholar
  10. Ardanov P, Leonid O, Iryna Z, Natalia K, Maria PA (2011) Endophytic bacteria enhancing growth and disease resistance of potato (Solanum tuberosum L.). Biol Control 56:43–49. doi: 10.1016/j.biocontrol.2010.09.014 CrossRefGoogle Scholar
  11. Ardanov P, Sessitsch A, Häggman H, Kozyrovska N, Pirttilä AM (2012) Methylobacterium-induced endophyte community changes correspond with protection of plants against pathogen attack. PLoS ONE 7:e46802. doi: 10.1371/journal.pone.0046802 PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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. doi: 10.1007/s11104-007-9233-5 CrossRefGoogle Scholar
  13. Arshad M, Frankenberger WT (1991) Microbial production of plant hormones. Plant Soil. doi: 10.1007/BF00011893 Google Scholar
  14. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512. doi: 10.1074/jbc.M112.433300 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Balla I, Vértesy J, Köves-Péchy K, Vörös I, Bujtás Z, Bíró B (1998) Acclimation results of micropropagated black locust (Robina pseudoacacia L.) improved by symbiotic micro-organisms. Plant Cell Tissue Organ Cult 52:113–115. doi: 10.1023/A:1005974024515 CrossRefGoogle Scholar
  16. Barka EA, Belarbi A, Hachet C, Nowak J, Audran J-C (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett. doi: 10.1111/j.1574-6968.2000.tb09087.x PubMedGoogle Scholar
  17. Barka EA, Gognies S, Nowak J, Audran J, Belarbi A (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote grapevine growth. Biol Control. doi: 10.1016/S1049-9644(02)00034-8 Google Scholar
  18. Barka EA, Nowak J, Clément S (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Env Microbiol. doi: 10.1128/AEM.01047-06 Google Scholar
  19. Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770. doi: 10.1016/S0734-9750(98)00003-2 CrossRefGoogle Scholar
  20. Bashan Y, de-Bashan LE, Prabhu SR, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33. doi: 10.1007/s11104-013-1956-x CrossRefGoogle Scholar
  21. Bensalim S, Nowak J, Asiedu SK (1998) A plant growth promoting rhizobacterium and temperature effects on performance of 18 clones of potato. Am J Potato Res. doi: 10.1007/BF02895849 Google Scholar
  22. Berg G, 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. doi: 10.1111/j.1574-6941.2009.00654.x PubMedCrossRefGoogle Scholar
  23. Berg G, Grube M, Schloter M, Smalla K (2014) Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol 5:148. doi: 10.3389/fmicb.2014.00148 PubMedPubMedCentralGoogle Scholar
  24. Bergey DH, Krieg NR, Holt JG (1984) Bergey’s manual of systematic bacteriology. Williams & Wilkins, BaltimoreGoogle Scholar
  25. Bhawana, Stubblefield JM, Newsome AL, Cahoon AB (2015) Surface decontamination of plant tissue explants with chlorine dioxide gas. In Vitro Cell Dev Biol 51:214–219. doi: 10.1007/s11627-014-9659-4 CrossRefGoogle Scholar
  26. Bordiec S, Paquis S, Lacroix H, Dhondt S, Ait Barka E, Kauffmann S, Jeandet P, Mazeyrat-Gourbeyre F, Clement C, Baillieul F, Dorey S (2011) Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J Exp Bot 62:595–603. doi: 10.1093/jxb/erq291 PubMedCrossRefGoogle Scholar
  27. Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503. doi: 10.1007/s00253-004-1696-1 PubMedCrossRefGoogle Scholar
  28. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37. doi: 10.1016/j.copbio.2013.09.012 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Buckley PM, DeWilde TN, Reed BM (1995) Characterization and identification of bacteria isolated from micropropagated mint plants. In Vitro Cell Dev Biol 31:58–64. doi: 10.1007/BF02632229 CrossRefGoogle Scholar
  30. Bunn E, Tan B (2002) Microbial contaminants in plant tissue culture propagation. In: Sivasithamparama K, Dixon KW, Barrett RL (eds) Microorganisms in plant conservation and biodiversity. Springe, Dordrecht, pp 307–335Google Scholar
  31. Burlak OP, de Vera J-P, Yatsenko V, Kozyrovska NO (2013) Putative mechanisms of bacterial effects on plant photosystem under stress. Biopolym Cell 29:3–10CrossRefGoogle Scholar
  32. Burns JA, Schwarz OJ (1996) Bacterial stimulation of adventitious rooting on in vitro cultured slash pine (Pinus elliottii Engelm.) seedling explants. Plant Cell Rep 15:405–408. doi: 10.1007/BF00232064 PubMedCrossRefGoogle Scholar
  33. Cain CC, Henry AT, Waldo RH, Casida LJ, Falkinham JO (2000) Identification and characteristics of a novel Burkholderia strain with broad-spectrum antimicrobial activity. Appl Environ Microbiol 66:4139–4141. doi: 10.1128/AEM.66.9.4139-4141.2000 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Carletti S, Llorente B, Caceres E, Tandecarz J (1998) Jojoba inoculation with Azospirillum brasilense stimulates in vitro root formation. Plant Tissue Cult Biotechnol 4:165–174Google Scholar
  35. Carvalho TLG, Ballesteros HGF, Thiebaut F, Ferreira PCG, 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. doi: 10.1007/s11103-016-0435-1 PubMedCrossRefGoogle Scholar
  36. Cassells AC (1991) Problems in tissue culture: culture contamination. In: Debergh PC, Zimmerman RH (eds) Micropropagation: technology and application. Kluwer Academic Publishers, Dordrecht, pp 31–44CrossRefGoogle Scholar
  37. Cassells AC (1997) Pathogen and microbial contamination management in micropropagation—an overview. In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Kluwer Academic Publishers, Dordrecht, pp 1–13CrossRefGoogle Scholar
  38. Cassells AC (2011) Detection and elimination of microbial endophytes and prevention of contamination in plant tissue culture. In: Trigiano RN, Gray DJ (eds) Plant tissue culture, development, and biotechnology. CRC Press, Boca Raton, pp 223–238Google Scholar
  39. Cassells AC, Doyle BM (2006) Pathogen and biological contamination management. In: Loyola-Vargas FM, Vazquez-Flota F (eds) Plant methods in molecular biology: plant cell culture protocols, 2nd edn, vol 318. Humana Press Inc., Totowa, pp 35–50Google Scholar
  40. Cassells AC, Tahmatsidou V (1996) The influence of local plant growth conditions on non-fastidious bacterial contamination of meristem-tips of Hydrangea cultured in vitro. Plant Cell Tissue Organ Cult 47:15–26. doi: 10.1007/BF02318961 CrossRefGoogle Scholar
  41. Chandra S, Bandopadhyay R, Kumar V, Chandra R (2010) Acclimatization of tissue cultured plantlets: from laboratory to land. Biotechnol Lett 32:1199–1205. doi: 10.1007/s10529-010-0290-0 PubMedCrossRefGoogle Scholar
  42. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl Env Microbiol. doi: 10.1128/AEM.71.9.4951-4959.2005 Google Scholar
  43. Compant S, Kaplan H, Sessitsch A, Nowak J, Ait Barka E, Clement C (2008a) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93. doi: 10.1111/j.1574-6941.2007.00410.x PubMedCrossRefGoogle Scholar
  44. Compant S, Nowak J, Coenye T, Clement C, Ait Barka E (2008b) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607. doi: 10.1111/j.1574-6976.2008.00113.x PubMedCrossRefGoogle Scholar
  45. Compant S, Mitter B, Colli-Mull JG, Gangl 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. doi: 10.1007/s00248-011-9883-y PubMedCrossRefGoogle Scholar
  46. Compant S, Brader G, Muzammil S, Sessitsch A, Lebrihi A, Mathieu F (2013) Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. Biocontrol 58:435–455. doi: 10.1007/s10526-012-9479-6 CrossRefGoogle Scholar
  47. Conn KL, Lazarovits G, Nowak J (1997) A gnotobiotic bioassay for studying interactions between potatoes and plant growth-promoting rhizobacteria. Can J Microbiol 43:801–808. doi: 10.1139/m97-117 CrossRefGoogle Scholar
  48. de Almeida CV, Andreote FD, Yara R, Tanaka FAO, Azevedo JL, de Almeida M (2009) Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J Microbiol Biotechnol 25:1757–1764. doi: 10.1007/s11274-009-0073-8 CrossRefGoogle Scholar
  49. 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 25:189–195. doi: 10.1007/s11274-008-9878-0 CrossRefGoogle Scholar
  50. Digat B, Brochard P, Hermelin V, Tozet M (1987) Interest of bacterized synthetic substrates MILCAP® for in vitro culture. Acta Hortic 212:375–378CrossRefGoogle Scholar
  51. Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694. doi: 10.1111/j.1365-3040.2009.02028.x PubMedCrossRefGoogle Scholar
  52. Duffy EM, Hurley EM, Cassells AC (1999) Weaning performance of potato microplants following bacterization and mycorrhization. Potato Res 42:521–527. doi: 10.1007/BF02358168 CrossRefGoogle Scholar
  53. Dunaeva S, Osledkin Y (2015) Bacterial microorganisms associated with the plant tissue culture: identification and possible role. Agric Biol 50:3–15Google Scholar
  54. Efremova N, Welters P, Lührs R (2012) Protoplast cultures as a source to determine the spectrum of endophytes. Current aspects of European endophyte research. COST Action FA 1103 Endophytes Biotechnol Agric Workshop vol 11, pp 28–30Google Scholar
  55. Falkiner F (1997) Antibiotics in plant tissue culture and micropropagation—what are we aiming at? In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Kluwer Academic Publishers, Dordrecht, pp 155–160CrossRefGoogle Scholar
  56. Fang J-Y, Hsu Y-R (2012) Molecular identification and antibiotic control of endophytic bacterial contaminants from micropropagated Aglaonema cultures. Plant Cell Tissue Organ Cult 110:53–62. doi: 10.1007/s11240-012-0129-6 CrossRefGoogle Scholar
  57. Faria DC, Dias ACF, Melo IS, de Carvalho Costa FE (2013) Endophytic bacteria isolated from orchid and their potential to promote plant growth. World J Microbiol Biotechnol 29:217–221. doi: 10.1007/s11274-012-1173-4 PubMedCrossRefGoogle Scholar
  58. Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens L, Clément C, Fontaine F, Ait Barka E (2012) Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant–Microbe Interact MPMI 25:496–504. doi: 10.1094/MPMI-09-11-0245 PubMedCrossRefGoogle Scholar
  59. Fletcher J, Leach JE, Eversole K, Tauxe R (2013) Human pathogens on plants: designing a multidisciplinary strategy for research. Phytopathology 103:306–315. doi: 10.1094/PHYTO-09-12-0236-IA PubMedCrossRefGoogle Scholar
  60. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46CrossRefGoogle Scholar
  61. Frommel MI, Nowak J, Lazarovits G (1991) Growth enhancement and developmental modification of in vitro grown potato (Solanum tuberosum spp. tuberosum) as affected by a nonfluorescent Pseudomonas sp. Plant Physiol. doi: 10.1104/pp.96.3.928 PubMedPubMedCentralGoogle Scholar
  62. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609. doi: 10.1111/1365-2435.12042 CrossRefGoogle Scholar
  63. Goellner K, Conrath U (2008) Priming: it’s all the world to induced disease resistance. In: Collinge DB, Munk L, Cooke BM (eds) Sustainable disease management in a European context. Springer, Dordrecht, pp 233–242CrossRefGoogle Scholar
  64. Gonzalez AJ, Larraburu EE, Llorente BE (2015) Azospirillum brasilense increased salt tolerance of jojoba during in vitro rooting. Ind Crops Prod 76:41–48. doi: 10.1016/j.indcrop.2015.06.017 CrossRefGoogle Scholar
  65. González-Olmedo JL, Fundora Z, Molina LA, Abdulnour J, Desjardins Y, Escalona M (2005) New contributions to propagation of pineapple (Ananas comosus L. Merr) in temporary immersion bioreactors. In Vitro Cell Dev Biol 41:87–90. doi: 10.1079/IVP2004603 CrossRefGoogle Scholar
  66. Gopinath S, Kumaran KS, Sundararaman M (2015) A new initiative in micropropagation: airborne bacterial volatiles modulate organogenesis and antioxidant activity in tobacco (Nicotiana tabacum L.) callus. In Vitro Cell Dev Biol 51:514–523. doi: 10.1007/s11627-015-9717-6 CrossRefGoogle Scholar
  67. Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240. doi: 10.1007/s11274-010-0572-7 CrossRefGoogle Scholar
  68. Guglielmetti S, Basilico R, Taverniti V, Arioli S, Piagnani C, Bernacchi A (2013) Luteibacter rhizovicinus MIMR1 promotes root development in barley (Hordeum vulgare L.) under laboratory conditions. World J Microbiol Biotechnol 29:2025–2032. doi: 10.1007/s11274-013-1365-6 PubMedCrossRefGoogle Scholar
  69. Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. doi: 10.1016/j.tim.2008.07.008 PubMedCrossRefGoogle Scholar
  70. Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD (2011) Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol 77:154. doi: 10.1111/j.1574-6941.2011.01092.x PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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. doi: 10.1128/MMBR.00050-14 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Herman E (1987) Toward control of micropropagation contamination. Agricell Rep 9:33–35Google Scholar
  73. Herman E (1990) Non-axenic plant tissue culture: possibilities and opportunities. Acta Hortic 280:233–238CrossRefGoogle Scholar
  74. Jaizme-Vega M del C, Rodríguez-Romero, A S, Guerra MSP (2004) Potential use of rhizobacteria from the Bacillus genus to stimulate the plant growth of micropropagated bananas. Fruits 59:83–90. doi: 10.1051/fruits:2004008 CrossRefGoogle Scholar
  75. James M, Blagden T, Moncrief I, Burans JP, Schneider K, Fletcher J (2014) Validation of real-time PCR assays for bioforensic detection of model plant pathogens. J Forensic Sci 59:463–469. doi: 10.1111/1556-4029.12321 PubMedCrossRefGoogle Scholar
  76. Kaluzna M, Mikicińsk A, Sobiczewski P, Zawadzka M, Zenkteler E, Orlikowska T (2013) Detection, isolation, and preliminary characterization of bacteria contaminating plant tissue cultures. Acta Agrobot 66:81–92CrossRefGoogle Scholar
  77. Kalyaeva M, Ivanova E, Doronina N, Zakharchenko NS, Trotsenko YA, Buryanov YI (2003) The effect of aerobic methylotrophic bacteria on in vitro morphogenesis of soft wheat (Triticum aestivum). Russ J Plant Physiol 50:354–359CrossRefGoogle Scholar
  78. Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6:151. doi: 10.3389/fpls.2015.00151 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kim S, Lowman S, Hou G, Nowak J, Flinn B, Mei C (2012) Growth promotion and colonization of switchgrass (Panicum virgatum) cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnol Biofuels 5:37. doi: 10.1186/1754-6834-5-37 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Klocke E, Abel S, Weinzierl K (2012) The “hidden” endophytes in protoplast cultures-a critical thinking about. Current aspects of European endophyte researchGoogle Scholar
  81. Knief C (2014) Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front Plant Sci 5:216. doi: 10.3389/fpls.2014.00216 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kohmura H, Yanagawa T, Tanaka M (1999) An efficient micropropagation system using disinfectant incorporated medium and film culture vessel for in vitro plant regeneration of asparagus. Acta Hortic 479:373–380CrossRefGoogle Scholar
  83. Kurepin LV, Park JM, Lazarovits G, Bernards MA (2015) Burkholderia phytofirmans-induced shoot and root growth promotion is associated with endogenous changes in plant growth hormone levels. Plant Growth Regul 75:199–207. doi: 10.1007/s10725-014-9944-6 CrossRefGoogle Scholar
  84. Langens-Gerrits M, Albers M, De Klerk G-J (1997) Hot-water treatment before tissue culture reduces initial contamination in Lilium and Acer. In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Springer, Dordrecht, pp 219–224CrossRefGoogle Scholar
  85. Lara-Chavez A, Lowman S, Kim S, Tang Y, Zhang J, Udvardi M, Nowak J, Flinn B, Mei C (2015) Global gene expression profiling of two switchgrass cultivars following inoculation with Burkholderia phytofirmans strain PsJN. J Exp Bot 66:4337–4350. doi: 10.1093/jxb/erv096 PubMedCrossRefGoogle Scholar
  86. Larraburu EE, Llorente BE (2015) Azospirillum brasilense enhances in vitro rhizogenesis of Handroanthus impetiginosus (pink lapacho) in different culture media. Ann For Sci 72:219–229. doi: 10.1007/s13595-014-0418-9 CrossRefGoogle Scholar
  87. Larraburu EE, Carletti SM, Cáceres EAR, Llorente BE (2007) Micropropagation of photinia employing rhizobacteria to promote root development. Plant Cell Rep 26:711–717PubMedCrossRefGoogle Scholar
  88. Larraburu EE, Apóstolo NM, Llorente BE (2010) Anatomy and morphology of photinia (Photinia × fraseri Dress) in vitro plants inoculated with rhizobacteria. Trees 24:635–642. doi: 10.1007/s00468-010-0433-x CrossRefGoogle Scholar
  89. Lata H, Li XC, Silva B, Moraes RM, Halda-Alija L (2006) Identification of IAA-producing endophytic bacteria from micropropagated Echinacea plants using 16 S rRNA sequencing. Plant Cell Tissue Organ Cult 85:353–359. doi: 10.1007/s11240-006-9087-1 CrossRefGoogle Scholar
  90. Leifert C, Morris CE, Waites WM (1994) Ecology of microbial saprophytes and pathogens in tissue culture and field-grown plants: reasons for contamination problems in vitro. Crit Rev Plant Sci 13:139–183CrossRefGoogle Scholar
  91. Lowman JS, Lava-Chavez A, Kim-Dura S, Flinn B, Nowak J, Mei C (2015) Switchgrass field performance on twosSoils as affected by bacterization of seedlings with Burkholderia phytofirmans Strain PsJN. BioEnergy Res 8:440–449. doi: 10.1007/s12155-014-9536-3 CrossRefGoogle Scholar
  92. Lucero ME, Unc A, Cooke P, Dowd S, Sun S (2011) Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS ONE 6:e17693. doi: 10.1371/journal.pone.0017693 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ludwig-Müller J (2015a) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37:1325–1334. doi: 10.1007/s10529-015-1814-4 PubMedCrossRefGoogle Scholar
  94. Ludwig-Müller J (2015b) Bacteria and fungi controlling plant growth by manipulating auxin: balance between development and defense. J Plant Physiol 172:4–12. doi: 10.1016/j.jplph.2014.01.002 PubMedCrossRefGoogle Scholar
  95. Ma Y, Rajkumar M, Luo Y, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237. doi: 10.1016/j.jhazmat.2011.08.034 PubMedCrossRefGoogle Scholar
  96. Madmony A, Chernin L, Pleban S, Peleg E, Riov J (2005) Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol (Praha) 50:209–216CrossRefGoogle Scholar
  97. Marino G, Altan AD, Biavati B (1996) The effect of bacterial contamination on the growth and gas evolution of in vitro cultured apricot shoots. In Vitro Cell Dev Biol 32:51–56. doi: 10.1007/BF02823014 CrossRefGoogle Scholar
  98. Marino G, Gaggìa F, Baffoni L, Toniolo C, Nicoletti M (2015) Antimicrobial activity of Melia azedarach fruit extracts for control of bacteria in inoculated in-vitro shoots of “MRS 2/5” plum hybrid and calla lily and extract influence on the shoot cultures. Eur J Plant Pathol 141:505–521. doi: 10.1007/s10658-014-0559-6 CrossRefGoogle Scholar
  99. Meldau DG, Long HH, Baldwin IT (2012) A native plant growth promoting bacterium, Bacillus sp. B55, rescues growth performance of an ethylene-insensitive plant genotype in nature. Front Plant Sci 3:112. doi: 10.3389/fpls.2012.00112 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100. doi: 10.1126/science.1203980 PubMedCrossRefGoogle Scholar
  101. Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, Normand P, Malik KA (2001) Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant Soil 237:47–54. doi: 10.1023/A:1013388619231 CrossRefGoogle Scholar
  102. Mitter B, Petric A, Shin MW, Chain PSG, Hauberg-Lotte L, Reinhold-Hurek B, Nowak J, Sessitsch A (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120. doi: 10.3389/fpls.2013.00120 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Miyazaki J, Tan BH, Errington SG (2010) Eradication of endophytic bacteria via treatment for axillary buds of Petunia hybrida using Plant Preservative Mixture (PPMTM). Plant Cell Tissue Organ Cult 102:365–372. doi: 10.1007/s11240-010-9741-5 CrossRefGoogle Scholar
  104. Montañez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28. doi: 10.1016/j.apsoil.2012.02.009 CrossRefGoogle Scholar
  105. Muganu M, Paolocci M, Bignami C, Di Mattia E (2015) Enhancement of adventitious root differentiation and growth of in vitro grapevine shoots inoculated with plant growth promoting rhizobacteria. VITIS-J Grapevine Res 54:73–77Google Scholar
  106. Müller P, Döring M (2009) Isothermal DNA amplification facilitates the identification of a broad spectrum of bacteria, fungi and protozoa in Eleutherococcus sp. plant tissue cultures. Plant Cell Tissue Organ Cult 98:35–45. doi: 10.1007/s11240-009-9536-8 CrossRefGoogle Scholar
  107. Murthy BNS, Vettakkorumakankav NN, KrishnaRaj S, Odumeru J, Saxena PK (1999) Characterization of somatic embryogenesis in Pelargonium × hortorum mediated by a bacterium. Plant Cell Rep 18:607–613. doi: 10.1007/s002990050630 CrossRefGoogle Scholar
  108. Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014a) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131. doi: 10.1007/s10725-013-9874-8 CrossRefGoogle Scholar
  109. Naveed M, Mitter B, Reichenauer TG, Wieczorek K, Sessitsch A (2014b) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot 97:30–39. doi: 10.1016/j.envexpbot.2013.09.014 CrossRefGoogle Scholar
  110. Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2014c) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50:249–262. doi: 10.1007/s00374-013-0854-y CrossRefGoogle Scholar
  111. Norman DJ, Alvarez AM (1994) Latent infections of in vitro anthurium caused by Xanthomonas campestris pv. dieffenbachiae. Plant Cell Tissue Organ Cult 39:55–61. doi: 10.1007/BF00037592 CrossRefGoogle Scholar
  112. Nowak J (1998) Benefits of in vitro “biotization” of plant tissue cultures with microbial inoculants. In Vitro Cell Dev Biol 34:122–130. doi: 10.1007/BF02822776 CrossRefGoogle Scholar
  113. Nowak J, Shulaev V (2003) Priming for transplant stress resistance in in vitro propagation. In Vitro Cell Dev Biol 39:107–124. doi: 10.1079/IVP2002403 CrossRefGoogle Scholar
  114. Nowak J, Bensalim S, Smith CD, Dunbar C, Asiedu SK, Madani A, Lazarovits G, Northcott D, Sturz AV (1999) Behaviour of plant material issued from in vitro tuberization. Potato Res 42:505–519. doi: 10.1007/BF02358167 CrossRefGoogle Scholar
  115. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Micro 11:252–263. doi: 10.1038/nrmicro2990 CrossRefGoogle Scholar
  116. Orlikowska T, Zawadzka M, Zenkteler E, Sobiczewski P (2012) Influence of the biocides PPMtm and Vitrofural on bacteria isolated from contaminated plant tissue cultures and on plant microshoots grown on various media. J Hortic Sci Biotechnol 87:223–230CrossRefGoogle Scholar
  117. Orlikowska T, Nowak J, Ogórek L (2017) Burkholderia phytofirmans PsJN promotes in vitro rooting and acclimatization of Helleborus. Acta Hortic (in press)Google Scholar
  118. Owen D, Williams AP, Griffith GW, Withers PJA (2015) Use of commercial bio-inoculants to increase agricultural production through improved phosphorous acquisition. Appl Soil Ecol 86:41–54. doi: 10.1016/j.apsoil.2014.09.012 CrossRefGoogle Scholar
  119. Păcurar DI, Thordal-Christensen H, Păcurar ML, Pamfil D, Botez C, Bellini C (2011) Agrobacterium tumefaciens: From crown gall tumors to genetic transformation. Physiol Mol Plant Pathol 76:76–81. doi: 10.1016/j.pmpp.2011.06.004 CrossRefGoogle Scholar
  120. Pandey A, Palni LMS, Bag N (2000) Biological hardening of tissue culture raised tea plants through rhizosphere bacteria. Biotechnol Lett 22:1087–1091. doi: 10.1023/A:1005674803237 CrossRefGoogle Scholar
  121. Panicker B, Thomas P, Janakiram T, Venugopalan R, Narayanappa SB (2007) Influence of cytokinin levels on in vitro propagation of shy suckering chrysanthemum Arka Swarna and activation of endophytic bacteria. In Vitro Cell Dev Biol 43:614–622CrossRefGoogle Scholar
  122. Panigrahi S, Aruna Lakshmi K, Venkateshwarulu Y, Umesh N (2015) Biohardening of micropropagated plants with PGPR and endophytic bacteria enhances the protein content. In: Biotechnology and bioforensics, forensic and medical bioinformatics. pp 51–55Google Scholar
  123. Park JM, Lazarovits G (2014) Involvement of hexokinase1 in plant growth promotion as mediated by Burkholderia phytofirmans. Can J Microbiol 60:343–354. doi: 10.1139/cjm-2014-0053 PubMedCrossRefGoogle Scholar
  124. Parray JA, Kamili AN, Reshi ZA, Quadri RA, Jan S (2015) Interaction of rhizobacterial strains for growth improvement of Crocus sativus L. under tissue culture conditions. Plant Cell Tissue Organ Cult (PCTOC) 121:325–334. doi: 10.1007/s11240-014-0703-1 CrossRefGoogle Scholar
  125. Partida-Martinez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100. doi: 10.3389/fpls.2011.00100 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801. doi: 10.1128/AEM.68.8.3795-3801.2002 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Pillay VK, Nowak J (1997) Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can J Microbiol 43:354–361. doi: 10.1139/m97-049 CrossRefGoogle Scholar
  128. 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 66:3073–3077PubMedPubMedCentralCrossRefGoogle Scholar
  129. Pirttilä AM, Podolich O, Koskimäki JJ, Hohtola E, Hohtola A (2008) Role of origin and endophyte infection in browning of bud-derived tissue cultures of Scots pine (Pinus sylvestris L.). Plant Cell Tissue Organ Cult 95:47–55CrossRefGoogle Scholar
  130. Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140:1255–1278PubMedPubMedCentralCrossRefGoogle Scholar
  131. Podolich O, Laschevskyy V, Ovcharenko L, Kozyrovska N, Pirttilä AM (2009) Methylobacterium sp. resides in unculturable state in potato tissues in vitro and becomes culturable after induction by Pseudomonas fluorescens IMGB163. J Appl Microbiol 106:728–737. doi: 10.1111/j.1365-2672.2008.03951.x PubMedCrossRefGoogle Scholar
  132. Pohjanen J, Koskimaki J, Pirttilä A (2014) Interaction of meristem-associated endophytic bacteria. In: Verma YC, Gange AC (eds) Advances in endophytic research. Springer, New Delhi, pp 103–113CrossRefGoogle Scholar
  133. Poppenberger B, Leonhardt W, Redl H (2002) Latent persistence of Agrobacterium vitis in micropropagated Vitis vinifera. VITIS-J Grapevine Res 41:113–114Google Scholar
  134. Poupin MJ, Timmermann T, Vega A, Zuñiga A, González B (2013) Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS ONE 8:e69435. doi: 10.1371/journal.pone.0069435 PubMedPubMedCentralCrossRefGoogle Scholar
  135. Quambusch M, Pirttilä AM, Tejesvi MV, Winkelmann T, Bartsch M (2014) Endophytic bacteria in plant tissue culture: differences between easy- and difficult-to-propagate Prunus avium genotypes. Tree Physiol 34:524–533. doi: 10.1093/treephys/tpu027 PubMedCrossRefGoogle Scholar
  136. Rakotoniriana EF, Rafamantanana M, Randriamampionona D, Rabemanantsoa C, Urveg-Ratsimamanga S, El Jaziri M, Munaut F, Corbisier A-M, Quetin-Leclercq J, Declerck S (2013) Study in vitro of the impact of endophytic bacteria isolated from Centella asiatica on the disease incidence caused by the hemibiotrophic fungus Colletotrichum higginsianum. Antonie Van Leeuwenhoek 103:121–133PubMedCrossRefGoogle Scholar
  137. Rames E, Hamili E, Kurtböke I (2009) Bacterially-induced growth promotion of micropropagated ginger. Acta Hortic 829:155–159CrossRefGoogle Scholar
  138. Reed BM, Tanprasert P (1995) Detection and control of bacterial contaminants of plant tissue cultures. A review of recent literature. Plant Tissue Cult Biotechnol 1:137–142Google Scholar
  139. Reed BM, Buckley PM, DeWilde TN (1995) Detection and eradication of endophytic bacteria from micropropagated mint plants. In Vitro Cell Dev Biol-Plant 31:53–57CrossRefGoogle Scholar
  140. Reed BM, Mentzer J, Tanprasert P, Yu X (1997) Internal bacterial contamination of micropropagated hazelnut: identification and antibiotic treatment. In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Kluwer Academic Publishers, Dordrecht, pp 233–236Google Scholar
  141. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis ML, Gandolfi C, Casati E, Previtali F, Gerbino R, Pierotti Cei F, Borin S, Sorlini C, Zocchi G, Daffonchio D (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331. doi: 10.1111/1462-2920.12439 PubMedCrossRefGoogle Scholar
  142. Rosenberg E, Sharon G, Atad I, Zilber-Rosenberg I (2010) The evolution of animals and plants via symbiosis with microorganisms. Environ Microbiol Rep 2:500–506. doi: 10.1111/j.1758-2229.2010.00177.x PubMedCrossRefGoogle Scholar
  143. Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant–Microbe Interact MPMI 19:827–837. doi: 10.1094/MPMI-19-0827 PubMedCrossRefGoogle Scholar
  144. Rout ME, Chrzanowski TH, Westlie TK, DeLuca TH, Callaway RM, Holben WE (2013) Bacterial endophytes enhance competition by invasive plants. Am J Bot 100:1726–1737. doi: 10.3732/ajb.1200577 PubMedCrossRefGoogle Scholar
  145. Rowntree JK (2006) Development of novel methods for the initiation of in vitro bryophyte cultures for conservation. Plant Cell Tissue Organ Cult 87:191–201. doi: 10.1007/s11240-006-9154-7 CrossRefGoogle Scholar
  146. Ruiz S, Adriano L, Ovando I, Navarro C, Salvador M (2011) Biofertilization of micropropagated Agave tequilana: Effect on plant growth and production of hydrolytic enzymes. Afr J Biotechnol 10:9631–9646CrossRefGoogle Scholar
  147. Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A (2008) Enhanced micropropagation response and biocontrol effect of Azospirillum brasilense Sp245 on Prunus cerasifera L. clone Mr.S 2/5 plants. J Biotechnol 134:312–319. doi: 10.1016/j.jbiotec.2008.01.020 PubMedCrossRefGoogle Scholar
  148. Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648. doi: 10.1007/s10295-007-0240-6 PubMedCrossRefGoogle Scholar
  149. Salomon MV, Bottini R, de Souza Filho GA, Cohen AC, Moreno D, Gil M, Piccoli P (2014) Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses, induce abscisic acid accumulation and synthesis of defense-related terpenes in in vitro cultured grapevine. Physiol Plant 151:359–374. doi: 10.1111/ppl.12117 PubMedCrossRefGoogle Scholar
  150. Santhanam R, Baldwin IT, Groten K (2015) In wild tobacco, Nicotiana attenuata, variation among bacterial communities of isogenic plants is mainly shaped by the local soil microbiota independently of the plants’ capacity to produce jasmonic acid. Commun Integr Biol 8:e1017160. doi: 10.1080/19420889.2015.1017160 PubMedPubMedCentralCrossRefGoogle Scholar
  151. Santoro MV, Cappellari LR, Giordano W, Banchio E (2015) Plant growth-promoting effects of native Pseudomonas strains on Mentha piperita (peppermint): an in vitro study. Plant Biol 17:1218–1226. doi: 10.1111/plb.12351 PubMedCrossRefGoogle Scholar
  152. Saravanakumar D (2012) Rhizobacterial ACC deaminase in plant growth and stress amelioration. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin, pp. 187–210CrossRefGoogle Scholar
  153. Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: proposal for division of this genus into the amended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Front Genet 5:429. doi: 10.3389/fgene.2014.00429 PubMedPubMedCentralCrossRefGoogle Scholar
  154. Scherling C, Ulrich K, Ewald D, Weckwerth W (2009) A metabolic signature of the beneficial interaction of the endophyte Paenibacillus sp. isolate and in vitro-grown poplar plants revealed by metabolomics. Mol Plant–Microbe Interact MPMI 22:1032–1037. doi: 10.1094/MPMI-22-8-1032 PubMedCrossRefGoogle Scholar
  155. Segers P, Vancanneyt M, Pot B, Torck U, Hoste B, Dewettinck D, Falsen E, Kersters K, De Vos P (1994) Classification of Pseudomonas diminuta Leifson and Hugh 1954 and Pseudomonas vesicularis Busing, Döll, and Freytag 1953 in Brevundimonas gen. nov. as Brevundimonas diminuta comb. nov. and Brevundimonas vesicularis comb. nov, respectively. Int J Syst Bacteriol 44:499–510. doi: 10.1099/00207713-44-3-499 PubMedCrossRefGoogle Scholar
  156. Senthilkumar M, Madhaiyan M, Sundaram SP, Sangeetha H, Kannaiyan S (2008) Induction of endophytic colonization in rice (Oryza sativa L.) tissue culture plants by Azorhizobium caulinodans. Biotechnol Lett 30:1477–1487. doi: 10.1007/s10529-008-9693-6 PubMedCrossRefGoogle Scholar
  157. Senthilkumar M, Anandham R, Madhaiyan M, Venkateshwarulu V, Sa T (2011) Endophytic bacteria: perspectives and applications in agricultural crop production. In: Maheshwari DK (ed) Bacteria in agrobiology:crop ecosystems. Springer, Berlin, Heidelberg, pp 61–96CrossRefGoogle Scholar
  158. Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol. doi: 10.1099/ijs.0.63149-0 PubMedGoogle Scholar
  159. Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant–Microbe Interact MPMI 25:28–36. doi: 10.1094/MPMI-08-11-0204 PubMedCrossRefGoogle Scholar
  160. Sharma VK, Nowak J (1998) Enhancement of verticillium wilt resistance in tomato transplants by in vitro co-culture of seedlings with a plant growth promoting rhizobacterium (Pseudomonas sp. strain PsJN). Can J Microbiol 44:528–536. doi: 10.1139/w98-017 CrossRefGoogle Scholar
  161. Shetty K, Curtis OF, Levin RE, Witkowsky R, Ang W (1995) Prevention of vitrification associated with in vitro shoot culture of oregano (Origanum vulgare) by Pseudomonas spp. J Plant Physiol 147:447–451. doi: 10.1016/S0176-1617(11)82181-4 CrossRefGoogle Scholar
  162. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefGoogle Scholar
  163. Stead D, Elphinstone J, Weller S, Smith N, Hennesy J (2000) Modern methods for characterizing, identifying and detecting bacteria associated with plants. Acta Hortic 530:45–55CrossRefGoogle Scholar
  164. Su F, Jacquard C, Villaume S, Michel J, Rabenoelina F, Clement C, Barka EA, Dhondt-Cordelier S, Vaillant-Gaveau N (2015) Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci 6:810. doi: 10.3389/fpls.2015.00810 PubMedPubMedCentralGoogle Scholar
  165. Su F, Gilard F, Guérard F, Citerne S, Clément C, Vaillant-Gaveau N, Dhondt-Cordelier S (2016) Spatio-temporal responses of arabidopsis leaves in photosynthetic performance and metabolite contents to Burkholderia phytofirmans PsJN. Front Plant Sci 7:403. doi: 10.3389/fpls.2016.00403 PubMedPubMedCentralGoogle Scholar
  166. Suada EP, Jasim B, Jimtha CJ, Gayatri GP, Radhakrishnan EK, Remakanthan A (2015) Phytostimulatory and hardening period-reducing effects of plant-associated bacteria on micropropagated Musa acuminata cv. Grand Naine. In Vitro Cell Dev Biol 51:682–687. doi: 10.1007/s11627-015-9721-x CrossRefGoogle Scholar
  167. Suarez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonca-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266. doi: 10.1007/s00248-011-9929-1 PubMedCrossRefGoogle Scholar
  168. Sunayana MR, Sasikala C, Ramana CV (2005) Rhodestrin: A novel indole terpenoid phytohormone from Rhodobacter sphaeroides. Biotechnol Lett 27:1897–1900. doi: 10.1007/s10529-005-3900-5 PubMedCrossRefGoogle Scholar
  169. Szendrák E, Read P, Yang G (1997) Prevention and elimination of contamination for in vitro culture of several woody species. In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Kluwer Academic Publishers, Dordrecht, pp 233–236CrossRefGoogle Scholar
  170. Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clement C, Barka EA (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol Plant–Microbe Interact MPMI 25:241–249. doi: 10.1094/MPMI-05-11-0124 PubMedCrossRefGoogle Scholar
  171. Thomas P (2004a) A three-step screening procedure for detection of covert and endophytic bacteria in plant tissue cultures. Curr Sci (Banglore) 87:67–72Google Scholar
  172. Thomas P (2004b) Isolation of Bacillus pumilus from in vitro grapes as a long-term alcohol-surviving and rhizogenesis inducing covert endophyte. J Appl Microbiol 97:114–123. doi: 10.1111/j.1365-2672.2004.02279.x PubMedCrossRefGoogle Scholar
  173. Thomas P (2011) Intense association of non-culturable endophytic bacteria with antibiotic-cleansed in vitro watermelon and their activation in degenerating cultures. Plant Cell Rep 30:2313–2325. doi: 10.1007/s00299-011-1158-z PubMedCrossRefGoogle Scholar
  174. Thomas P, Sekhar AC (2014) Live cell imaging reveals extensive intracellular cytoplasmic colonization of banana by normally non-cultivable endophytic bacteria. AoB Plants. doi: 10.1093/aobpla/plu002 PubMedPubMedCentralGoogle Scholar
  175. Thomas P, Prabhakara BS, Pitchaimuthu M (2006) Cleansing the long-term micropropagated triploid watermelon cultures from covert bacteria and field testing the plants for clonal fidelity and fertility during the 7–10 year period in vitro. Plant Cell Tissue Organ Cult 85:317–329. doi: 10.1007/s11240-006-9083-5 CrossRefGoogle Scholar
  176. Thomas P, Kumari S, Swarna GK, Gowda TKS (2007) Papaya shoot tip associated endophytic bacteria isolated from in vitro cultures and host-endophyte interaction in vitro and in vivo. Can J Microbiol 53:380–390. doi: 10.1139/W06-141 PubMedCrossRefGoogle Scholar
  177. Thomas J, Ajay D, Raj Kumar R, Mandal AKA (2010) Influence of beneficial microorganisms during in vivo acclimatization of in vitro-derived tea (Camellia sinensis) plants. Plant Cell Tissue Organ Cult 101:365–370. doi: 10.1007/s11240-010-9687-7 CrossRefGoogle Scholar
  178. Trivedi P, Pandey A (2007) Biological hardening of micropropagated Picrorhiza kurrooa Royel ex Benth., an endangered species of medical importance. World J Microbiol Biotechnol 23:877–878. doi: 10.1007/s11274-006-9293-3 CrossRefGoogle Scholar
  179. Tsao C-W, Postman JD, Reed BM (2000) Virus infections reduce in vitro multiplication of “Malling Landmark” raspberry. In Vitro Cell Dev Biol Plant 36:65–68CrossRefGoogle Scholar
  180. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. doi: 10.1186/gb-2013-14-6-209 PubMedPubMedCentralCrossRefGoogle Scholar
  181. Ueno K, Shetty K (1997) Effect of selected polysaccharide-producing soil bacteria on hyperhydricity control in oregano tissue cultures. Appl Environ Microbiol 63:767–770PubMedPubMedCentralGoogle Scholar
  182. Ueno K, Cheplick S, Shetty K (1998) Reduced hyperhydricity and enhanced growth of tissue culture-generated raspberry (Rubus sp.) clonal lines by Pseudomonas sp. isolated from oregano. Process Biochem 33:441–445CrossRefGoogle Scholar
  183. Ulrich K, Stauber T, Ewald D (2008) Paenibacillus—a predominant endophytic bacterium colonising tissue cultures of woody plants. Plant Cell Tissue Organ Cult 93:347–351. doi: 10.1007/s11240-008-9367-z CrossRefGoogle Scholar
  184. Vacheron J, Desbrosses G, Bouffaud M-L, Touraine B, Moenne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dye F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. doi: 10.3389/fpls.2013.00356 PubMedPubMedCentralCrossRefGoogle Scholar
  185. Vereecke D, Burssens S, Simón-Mateo C, Inzé D, Van Montagu M, Goethals K, Jaziri M (2000) The Rhodococcus fascians-plant interaction: morphological traits and biotechnological applications. Planta 210:241–251. doi: 10.1007/PL00008131 PubMedCrossRefGoogle Scholar
  186. Vestberg M, Cassells A (2009) The use of AMF and PGPR inoculants singly and combined to promote microplant establishment, growth and health. In: Varma A, Kharkwal AC (eds) Fungi symbiotic, biology soil. Springer, Berlin, pp 337–360CrossRefGoogle Scholar
  187. Vettori L, Russo A, Felici C, Fiaschi G, Morini S, Toffanin A (2010) Improving micropropagation: effect of Azospirillum brasilense Sp245 on acclimatization of rootstocks of fruit tree. J Plant Interact 5:249–259. doi: 10.1080/17429145.2010.511280 CrossRefGoogle Scholar
  188. Wang B, Mei C, Seiler JR (2015) Early growth promotion and leaf level physiology changes in Burkholderia phytofirmans strain PsJN inoculated switchgrass. Plant Physiol Biochem PPB 86:16–23. doi: 10.1016/j.plaphy.2014.11.008 PubMedCrossRefGoogle Scholar
  189. Weilharter A, Mitter B, Shin MV, Chain PSG, Nowak J, Sessitsch A (2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol 193:3383–3384. doi: 10.1128/JB.05055-11 PubMedPubMedCentralCrossRefGoogle Scholar
  190. Wilson D (1995) Endophyte: The evolution of a term, and clarification of its use and definition. Oikos 73:274–276. doi: 10.2307/3545919 CrossRefGoogle Scholar
  191. Xie X, Zhang H, Pare PW (2009) Sustained growth promotion in arabidopsis with long-term exposure to the beneficial soil bacterium Bacillus subtilis (GB03). Plant Signal Behav 4:948–953PubMedPubMedCentralCrossRefGoogle Scholar
  192. Yang Y-S, Wada K, Goto M, Futsuhara Y (1991) In vitro formation of nodular calli in soybean (Glycine max L.) induced by cocultivated Pseudomonas maltophilia. Jpn J Breed 41:595–604CrossRefGoogle Scholar
  193. Young L-S, Hameed A, Peng S-Y, Shan Y-H, Wu S-P (2013) Endophytic establishment of the soil isolate Burkholderia sp. CC-Al74 enhances growth and P-utilization rate in maize (Zea mays L.). Appl Soil Ecol 66:40–47. doi: 10.1016/j.apsoil.2013.02.001 CrossRefGoogle Scholar
  194. Zakharchenko NS, Kochetkov VV, Buryanov YI, Boronin AM (2011) Effect of rhizosphere bacteria Pseudomonas aureofaciens on the resistance of micropropagated plants to phytopathogens. Appl Biochem Microbiol 47:661. doi: 10.1134/S0003683811070118 CrossRefGoogle Scholar
  195. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ (2013) Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria. Plant Physiol 162:304–318. doi: 10.1104/pp.112.212597 PubMedPubMedCentralCrossRefGoogle Scholar
  196. Zawadzka M, Trzciński P, Nowak K, Orlikowska T (2014) The impact of three bacteria isolated from contaminated plant cultures on in vitro multiplication and rooting of microshoots of four ornamental plants. J Hortic Res 21:41. doi: 10.2478/johr-2013-0020 Google Scholar
  197. Zenkteler E, Wlodarczak K, Klosowska M (1997) The application of antibiotic and sulphonamide for eliminating Bacillus cereus during the micropropagation of infected Dieffenbachia picta Schott. In: Cassells AC (ed) Pathogen and microbial contamination management in micropropagation. Kluwer Academic Publishers, Dordrecht, pp 233–236Google Scholar
  198. Zhao S, Wei H, Lin C-Y, Zeng Y, Tucker MP, Himmel ME, Ding S-Y (2016) Burkholderia phytofirmans inoculation-induced changes on the shoot cell anatomy and iron accumulation reveal novel components of arabidopsis-endophyte Interaction that can benefit downstream biomass deconstruction. Front Plant Sci 7:24. doi: 10.3389/fpls.2016.00024 PubMedPubMedCentralGoogle Scholar
  199. Ziemienowicz A (2014) Agrobacterium-mediated plant transformation: factors, applications and recent advances. Biocatal Agric Biotechnol 3:95–102. doi: 10.1016/j.bcab.2013.10.004 Google Scholar
  200. Zúñiga A, Poupin MJ, Donoso R, Ledger T, Guiliani N, Gutierrez RA, Gonzalez B (2013) Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol Plant–Microbe Interact MPMI 26:546–553. doi: 10.1094/MPMI-10-12-0241-R PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2016

Authors and Affiliations

  • Teresa Orlikowska
    • 1
  • Katarzyna Nowak
    • 1
  • Barbara Reed
    • 2
  1. 1.Research Institute of HorticultureSkierniewicePoland
  2. 2.Department of HorticultureOregon State University and U S Department of AgricultureCorvallisUSA

Personalised recommendations