Skip to main content
SpringerLink
Log in

Bacteria in the plant tissue culture environment

  • Review
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 21:41–48

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Arshad M, Frankenberger WT (1991) Microbial production of plant hormones. Plant Soil. doi:10.1007/BF00011893

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Bergey DH, Krieg NR, Holt JG (1984) Bergey’s manual of systematic bacteriology. Williams & Wilkins, Baltimore

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 307–335

    Google Scholar 

  • Burlak OP, de Vera J-P, Yatsenko V, Kozyrovska NO (2013) Putative mechanisms of bacterial effects on plant photosystem under stress. Biopolym Cell 29:3–10

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carletti S, Llorente B, Caceres E, Tandecarz J (1998) Jojoba inoculation with Azospirillum brasilense stimulates in vitro root formation. Plant Tissue Cult Biotechnol 4:165–174

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cassells AC (1991) Problems in tissue culture: culture contamination. In: Debergh PC, Zimmerman RH (eds) Micropropagation: technology and application. Kluwer Academic Publishers, Dordrecht, pp 31–44

    Chapter  Google Scholar 

  • 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 1–13

    Chapter  Google Scholar 

  • 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 223–238

    Google Scholar 

  • 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 35–50

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Digat B, Brochard P, Hermelin V, Tozet M (1987) Interest of bacterized synthetic substrates MILCAP® for in vitro culture. Acta Hortic 212:375–378

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dunaeva S, Osledkin Y (2015) Bacterial microorganisms associated with the plant tissue culture: identification and possible role. Agric Biol 50:3–15

    Google Scholar 

  • 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 28–30

  • 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 155–160

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 42:23–46

    Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 233–242

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Herman E (1987) Toward control of micropropagation contamination. Agricell Rep 9:33–35

    Google Scholar 

  • Herman E (1990) Non-axenic plant tissue culture: possibilities and opportunities. Acta Hortic 280:233–238

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 66:81–92

    Article  Google Scholar 

  • 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 50:354–359

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klocke E, Abel S, Weinzierl K (2012) The “hidden” endophytes in protoplast cultures-a critical thinking about. Current aspects of European endophyte research

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 479:373–380

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 219–224

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Larraburu EE, Carletti SM, Cáceres EAR, Llorente BE (2007) Micropropagation of photinia employing rhizobacteria to promote root development. Plant Cell Rep 26:711–717

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 13:139–183

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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) 50:209–216

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 54:73–77

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 87:223–230

    Article  CAS  Google Scholar 

  • Orlikowska T, Nowak J, Ogórek L (2017) Burkholderia phytofirmans PsJN promotes in vitro rooting and acclimatization of Helleborus. Acta Hortic (in press)

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 43:614–622

    Article  CAS  Google Scholar 

  • 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 51–55

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Partida-Martinez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100. doi:10.3389/fpls.2011.00100

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 66:3073–3077

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 95:47–55

    Article  CAS  Google Scholar 

  • Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140:1255–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 103–113

    Chapter  Google Scholar 

  • Poppenberger B, Leonhardt W, Redl H (2002) Latent persistence of Agrobacterium vitis in micropropagated Vitis vinifera. VITIS-J Grapevine Res 41:113–114

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 103:121–133

    Article  PubMed  Google Scholar 

  • Rames E, Hamili E, Kurtböke I (2009) Bacterially-induced growth promotion of micropropagated ginger. Acta Hortic 829:155–159

    Article  Google Scholar 

  • Reed BM, Tanprasert P (1995) Detection and control of bacterial contaminants of plant tissue cultures. A review of recent literature. Plant Tissue Cult Biotechnol 1:137–142

    Google Scholar 

  • Reed BM, Buckley PM, DeWilde TN (1995) Detection and eradication of endophytic bacteria from micropropagated mint plants. In Vitro Cell Dev Biol-Plant 31:53–57

    Article  Google Scholar 

  • 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 233–236

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 10:9631–9646

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Saravanakumar D (2012) Rhizobacterial ACC deaminase in plant growth and stress amelioration. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin, pp. 187–210

    Chapter  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 61–96

    Chapter  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    Article  CAS  PubMed  Google Scholar 

  • Stead D, Elphinstone J, Weller S, Smith N, Hennesy J (2000) Modern methods for characterizing, identifying and detecting bacteria associated with plants. Acta Hortic 530:45–55

    Article  CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 233–236

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Thomas P (2004a) A three-step screening procedure for detection of covert and endophytic bacteria in plant tissue cultures. Curr Sci (Banglore) 87:67–72

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tsao C-W, Postman JD, Reed BM (2000) Virus infections reduce in vitro multiplication of “Malling Landmark” raspberry. In Vitro Cell Dev Biol Plant 36:65–68

    Article  Google Scholar 

  • Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209. doi:10.1186/gb-2013-14-6-209

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ueno K, Shetty K (1997) Effect of selected polysaccharide-producing soil bacteria on hyperhydricity control in oregano tissue cultures. Appl Environ Microbiol 63:767–770

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 33:441–445

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 337–360

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson D (1995) Endophyte: The evolution of a term, and clarification of its use and definition. Oikos 73:274–276. doi:10.2307/3545919

    Article  Google Scholar 

  • 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 4:948–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 41:595–604

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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 233–236

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Research Institute of Horticulture, Skierniewice, Poland

    Teresa Orlikowska & Katarzyna Nowak

  2. Department of Horticulture, Oregon State University and U S Department of Agriculture, Corvallis, OR, USA

    Barbara Reed

Authors
  1. Teresa Orlikowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katarzyna Nowak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara Reed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Barbara Reed.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Orlikowska, T., Nowak, K. & Reed, B. Bacteria in the plant tissue culture environment. Plant Cell Tiss Organ Cult 128, 487–508 (2017). https://doi.org/10.1007/s11240-016-1144-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-016-1144-9

Keywords

Search

Navigation