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Bacterial Endophytes in Plant Tissue Culture: Mode of Action, Detection, and Control

Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1815)

Abstract

Endophytic bacteria have been increasingly in the focus of research projects during the last decade. This has changed the view on bacteria in plant tissue culture and led to the differentiation between artificially introduced contaminations and naturally occurring endophytes with neutral, negative, or positive impact on the plant propagation process. This review chapter gives an overview on recent findings about the impact that bacteria have on the plant physiology in general and during micropropagation. Additionally, methods for the detection and identification of bacteria in plant tissue are described and, finally, suggestions of how to deal with bacterial endophytes in in vitro culture are given.

Key words

Bacteria Contamination Culture-dependent Culture-independent Endophytes Identification Micropropagation Plant growth promotion Quantification 

References

  1. 1.
    Hardoim PR, van Overbeek LS, Berg G et al (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    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. https://doi.org/10.1016/j.tim.2008.07.008 CrossRefPubMedGoogle Scholar
  3. 3.
    De Bary A (1866) Morphologie und Physiologie der Pilze, Flechten und Myxomyceten. Handb der Physiol Bot 2:335Google Scholar
  4. 4.
    Carroll GC (1986) Biology of endophytism in plants with particular reference to woody perennials. In: Fokkema N, J van den Heuvel (eds) Microbiol. Phyllosph. Cambridge University Press, pp 205–222Google Scholar
  5. 5.
    Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews J, Hirano S (eds) Microb. Ecol. leaves. Springer, New York, pp 179–197. https://doi.org/10.1007/978-1-4612-3168-4_9 CrossRefGoogle Scholar
  6. 6.
    Koskimäki JJ, Pirttilä M, Ihantola E-L et al (2015) The intracellular scots pine shoot symbiont Methylobacterium extorquens DSM13060 aggregates round the host nucleus and encodes eucaryote-like proteins. MBio 6:e00039–e00015. https://doi.org/10.1128/mBio.00039-15 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117. https://doi.org/10.1264/jsme2.23.109 CrossRefPubMedGoogle Scholar
  8. 8.
    Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS One 6:e20396. https://doi.org/10.1371/journal.pone.0020396 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Glassner H, Zchori-Fein E, Yaron S et al (2017) Bacterial niches inside seeds of Cucumis melo L. Plant Soil 422:1–13. https://doi.org/10.1007/s11104-017-3175-3 CrossRefGoogle Scholar
  10. 10.
    Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. https://doi.org/10.1146/annurev-genet-110410-132549 CrossRefPubMedGoogle Scholar
  11. 11.
    Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. https://doi.org/10.1016/j.soilbio.2009.11.024 CrossRefGoogle Scholar
  12. 12.
    Yanni YG, Rizk RY, El-Fattah FKA et al (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. Trifolii with rice roots. Funct Plant Biol 28:845–870CrossRefGoogle Scholar
  13. 13.
    Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443. https://doi.org/10.1016/j.pbi.2011.04.004 CrossRefPubMedGoogle Scholar
  14. 14.
    Pirttilä AM, Laukkanen H, Pospiech H et al (2000) Detection of intracellular bacteria in the buds of scotch pine (Pinus sylvestris L.) by in situ hybridization. Appl Environ Microbiol 66:3073–3077. https://doi.org/10.1128/AEM.66.7.3073-3077.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Kukkurainen S, Leino A, Vähämiko S et al (2004) Occurrence and location of endophytic bacteria in garden and wild strawberry. Hortscience 39:1–5Google Scholar
  16. 16.
    Compant S, Kaplan H, Sessitsch A et al (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93. https://doi.org/10.1111/j.1574-6941.2007.00410.x CrossRefPubMedGoogle Scholar
  17. 17.
    Carroll G (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:2–9. https://doi.org/10.2307/1943154 CrossRefGoogle Scholar
  18. 18.
    Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Interact 19:827–837. https://doi.org/10.1094/MPMI-19-0827 CrossRefPubMedGoogle Scholar
  19. 19.
    Promputtha I, Lumyong S, Dhanasekaran V et al (2007) A phylogenetic evaluation of whether endophytes become saprotrophs at host senescence. Microb Ecol 53:579–590. https://doi.org/10.1007/s00248-006-9117-x CrossRefPubMedGoogle Scholar
  20. 20.
    Kozyrovska N (2013) Crosstalk between endophytes and a plant host within information processing networks. Biopolym Cell 29:234–243CrossRefGoogle Scholar
  21. 21.
    Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68. https://doi.org/10.1006/jtbi.1997.0532 CrossRefPubMedGoogle Scholar
  22. 22.
    Compant S, Duffy B, Nowak J et al (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. https://doi.org/10.1128/AEM.71.9.4951 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150. https://doi.org/10.1094/MPMI-06-11-0179 CrossRefPubMedGoogle Scholar
  24. 24.
    Ryan RP, Germaine K, Franks A et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x CrossRefPubMedGoogle Scholar
  25. 25.
    Kaymak HC (2010) Potential of PGPR in agricultural innovations. In: Maheshwari DK (ed) Plant growth heal. promot. bact. Springer-Verlag, Heidelberg, pp 45–79. https://doi.org/10.1007/978-3-642-13612-2_3 CrossRefGoogle Scholar
  26. 26.
    Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. https://doi.org/10.1111/j.1574-6976.2007.00072.x CrossRefPubMedGoogle Scholar
  27. 27.
    Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2005) Auxin production by bacteria associated with orchid roots. Microbiology 74:46–53. https://doi.org/10.1007/s11021-005-0027-6 CrossRefGoogle Scholar
  28. 28.
    Ali B, Sabri AN, Ljung K, Hasnain S (2009) Auxin production by plant associated bacteria: impact on endogenous IAA content and growth of Triticum aestivum L. Lett Appl Microbiol 48:542–547. https://doi.org/10.1111/j.1472-765X.2009.02565.x CrossRefPubMedGoogle Scholar
  29. 29.
    Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS One 3:e2702. https://doi.org/10.1371/journal.pone.0002702 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18. https://doi.org/10.3109/10408419509113531 CrossRefPubMedGoogle Scholar
  31. 31.
    Salomon MV, Bottini R, de Souza Filho GA et al (2013) 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(4):359–374. https://doi.org/10.1111/ppl.12117 CrossRefPubMedGoogle Scholar
  32. 32.
    Belimov AA, Dodd IC, Safronova VI et al (2014) Abscisic acid metabolizing rhizobacteria decrease ABA concentrations in planta and alter plant growth. Plant Physiol Biochem 74:84–91. https://doi.org/10.1016/j.plaphy.2013.10.032 CrossRefPubMedGoogle Scholar
  33. 33.
    Wang XM, Yang B, Ren CG et al (2015) Involvement of abscisic acid and salicylic acid in signal cascade regulating bacterial endophyte-induced volatile oil biosynthesis in plantlets of Atractylodes lancea. Physiol Plant 153:30–42. https://doi.org/10.1111/ppl.12236 CrossRefPubMedGoogle Scholar
  34. 34.
    Ali S, Charles TC, Glick BR (2012) Delay of flower senescence by bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate deaminase. J Appl Microbiol 113:1139–1144. https://doi.org/10.1111/j.1365-2672.2012.05409.x CrossRefPubMedGoogle Scholar
  35. 35.
    Hilda R, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–355CrossRefGoogle Scholar
  36. 36.
    Faleiro AC, Pereira TP, Espindula E et al (2013) Real time PCR detection targeting nifA gene of plant growth promoting bacteria Azospirillum brasilense strain FP2 in maize roots. Symbiosis 61:125–133. https://doi.org/10.1007/s13199-013-0262-y CrossRefGoogle Scholar
  37. 37.
    Herman EB (1990) Non-axenic plant tissue culture: possibilities and opportunities. Acta Hortic 280:233–238. https://doi.org/10.17660/ActaHortic.1990.280.40 CrossRefGoogle Scholar
  38. 38.
    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 Plant 32:51–56. https://doi.org/10.1007/BF02823014 CrossRefGoogle Scholar
  39. 39.
    Leifert C, Ritchie J, Waites W (1991) Contaminants of plant-tissue and cell cultures. World J Microbiol Biotechnol 7:452–469. https://doi.org/10.1007/BF00303371 CrossRefPubMedGoogle Scholar
  40. 40.
    Liu T-H a, Hsu N-W, Wu R-Y (2005) Control of leaf-tip necrosis of micropropagated ornamental statice by elimination of endophytic bacteria. In Vitro Cell Dev Biol Plant 41:546–549. https://doi.org/10.1079/IVP2005673 CrossRefGoogle Scholar
  41. 41.
    Leifert C, Cassells A (2001) Microbial hazards in plant tissue and cell cultures. In Vitro Cell Dev Biol Plant 37:133–138. https://doi.org/10.1079/IVP2000129 CrossRefGoogle Scholar
  42. 42.
    Orlikowska T, Nowak K, Reed B (2017) Bacteria in the plant tissue culture environment. Plant Cell Tissue Org 128:487–508. https://doi.org/10.1007/s11240-016-1144-9 CrossRefGoogle Scholar
  43. 43.
    Thomas P, Swarna GK, Roy PK, Patil P (2008) Identification of culturable and originally non-culturable endophytic bacteria isolated from shoot tip cultures of banana cv. Grand Naine. Plant Cell Tissue Org 93:55–63. https://doi.org/10.1007/s11240-008-9341-9 CrossRefGoogle Scholar
  44. 44.
    Dias ACF, Costa FEC, Andreote FD et al (2008) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195. https://doi.org/10.1007/s11274-008-9878-0 CrossRefGoogle Scholar
  45. 45.
    Abreu-Tarazi MF, Navarrete AA, Andreote FD et al (2010) Endophytic bacteria in long-term in vitro cultivated “axenic” pineapple microplants revealed by PCR-DGGE. World J Microbiol Biotechnol 26:555–560. https://doi.org/10.1007/s11274-009-0191-3 CrossRefGoogle Scholar
  46. 46.
    Lucero ME, Unc A, Cooke P et al (2011) Endophyte microbiome diversity in micropropagated Atriplex canescens and Atriplex torreyi var griffithsii. PLoS One 6:e17693. https://doi.org/10.1371/journal.pone.0017693 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Jimtha JC, Smitha PV, Anisha C et al (2014) Isolation of endophytic bacteria from embryogenic suspension culture of banana and assessment of their plant growth promoting properties. Plant Cell Tissue Org 118:57–66. https://doi.org/10.1007/s11240-014-0461-0 CrossRefGoogle Scholar
  48. 48.
    Izumi H, Anderson IC, Killham K, Moore ERB (2008) Diversity of predominant endophytic bacteria in European deciduous and coniferous trees. Can J Microbiol 54:173–179. https://doi.org/10.1139/W07-134 CrossRefPubMedGoogle Scholar
  49. 49.
    Ulrich K, Stauber T, Ewald D (2008) Paenibacillus—a predominant endophytic bacterium colonising tissue cultures of woody plants. Plant Cell Tissue Org 93:347–351. https://doi.org/10.1007/s11240-008-9367-z CrossRefGoogle Scholar
  50. 50.
    Zaspel I, Ulrich A, Boine B, Stauber T (2008) Occurrence of culturable bacteria living in micropropagated black locust cultures (Robinia pseudoacacia L.). Eur J Hortic Sci 73:231–235Google Scholar
  51. 51.
    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 22:1032–1037. https://doi.org/10.1094/MPMI-22-8-1032 CrossRefPubMedGoogle Scholar
  52. 52.
    Donnarumma F, Capuana M, Vettori C et al (2011) Isolation and characterisation of bacterial colonies from seeds and in vitro cultures of Fraxinus spp. from Italian sites. Plant Biol 13:169–176. https://doi.org/10.1111/j.1438-8677.2010.00334.x CrossRefPubMedGoogle Scholar
  53. 53.
    Pohjanen J, Koskimäki JJ, Sutela S et al (2014) Interaction with ectomycorrhizal fungi and endophytic methylobacterium affects nutrient uptake and growth of pine seedlings in vitro. Tree Physiol 34:993–1005. https://doi.org/10.1093/treephys/tpu062 CrossRefPubMedGoogle Scholar
  54. 54.
    Quambusch M, Brümmer J, Haller K et al (2016) Dynamics of endophytic bacteria in plant in vitro culture: quantification of three bacterial strains in Prunus avium in different plant organs and in vitro culture phases. Plant Cell Tissue Org 126:305–317. https://doi.org/10.1007/s11240-016-0999-0 CrossRefGoogle Scholar
  55. 55.
    Quambusch M, Pirttilä AM, Tejesvi MV et al (2014) Endophytic bacteria in plant tissue culture: differences between easy- and difficult-to-propagate Prunus avium genotypes. Tree Physiol 34:524–533. https://doi.org/10.1093/treephys/tpu027 CrossRefPubMedGoogle Scholar
  56. 56.
    Pirttilä AM, Podolich O, Koskimäki JJ et al (2008) Role of origin and endophyte infection in browning of bud-derived tissue cultures of scots pine (Pinus sylvestris L.). Plant Cell Tissue Org 95:47–55. https://doi.org/10.1007/s11240-008-9413-x CrossRefGoogle Scholar
  57. 57.
    Ardanov P, Sessitsch A, Häggman H et al (2012) Methylobacterium-induced endophyte community changes correspond with protection of plants against pathogen attack. PLoS One 7:e46802. https://doi.org/10.1371/journal.pone.0046802 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Tsavkelova EA, Egorova MA, Leontieva MR et al (2016) Dendrobium nobile Lindl. Seed germination in co-cultures with diverse associated bacteria. Plant Growth Regul 80:79–91. https://doi.org/10.1007/s10725-016-0155-1 CrossRefGoogle Scholar
  59. 59.
    Wang X, Yam TW, Meng Q et al (2016) The dual inoculation of endophytic fungi and bacteria promotes seedlings growth in Dendrobium catenatum (Orchidaceae) under in vitro culture conditions. Plant Cell Tissue Org 126:523–531. https://doi.org/10.1007/s11240-016-1021-6 CrossRefGoogle Scholar
  60. 60.
    Kulkarni AA, Kelkar SM, Watve MG, Krishnamurthy KV (2007) Characterization and control of endophytic bacterial contaminants in in vitro cultures of Piper spp., Taxus baccata subsp. wallichiana, and Withania somnifera. Can J Microbiol 53:63–74. https://doi.org/10.1139/w06-106 CrossRefPubMedGoogle Scholar
  61. 61.
    Cassells AC, Harmey MA, Carney BF et al (1988) Problems posed by culturable bacterial endophytes in the establishment of axenic cultures of Pelargonium domesticum: the use of Xanthomonas pelargonii-specific ELISA, DNA probes and culture indexing in the screening of antibiotic treated and untreated donor plants. Acta Hortic 225:153–161. https://doi.org/10.17660/ActaHortic.1988.225.16 CrossRefGoogle Scholar
  62. 62.
    Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  63. 63.
    Keller ERJ, Blattner FR, Fritsch R et al (2012) The genus Allium in the Gatersleben plant collections - progress in germplasm preservation, characterization and phylogenetic analysis. In: Acta Hortic. International Society for Horticultural Science (ISHS), Leuven, Belgium, pp 273–287. https://doi.org/10.17660/ActaHortic.2012.969.36 CrossRefGoogle Scholar
  64. 64.
    Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of “unculturable” bacteria. FEMS Microbiol Lett 309:1–7. https://doi.org/10.1111/j.1574-6968.2010.02000.x CrossRefPubMedGoogle Scholar
  65. 65.
    Aoi Y, Kinoshita T, Hata T et al (2009) Hollow-fiber membrane chamber as a device for in situ environmental cultivation. Appl Environ Microbiol 75:3826–3833. https://doi.org/10.1128/AEM.02542-08 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Zhang D, Berry JP, Zhu D et al (2015) Magnetic nanoparticle-mediated isolation of functional bacteria in a complex microbial community. ISME J 9:603–614. https://doi.org/10.1038/ismej.2014.161 CrossRefPubMedGoogle Scholar
  67. 67.
    Eevers N, Gielen M, Sánchez-López A et al (2015) Optimization of isolation and cultivation of bacterial endophytes through addition of plant extract to nutrient media. Microb Biotechnol 8:707–715. https://doi.org/10.1111/1751-7915.12291 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Middlebrook G, Cohn ML (1958) Bacteriology of tuberculosis: laboratory methods. AJPH 48:844–853Google Scholar
  69. 69.
    Van Overbeek LS, Van Vuurde J, Van Elsas JD (2006) Application of molecular fingerprinting techniques to explore the diversity of bacterial endophytic communities. Microb Root Endophytes 9:337–354. https://doi.org/10.1007/3-540-33526-9_19 CrossRefGoogle Scholar
  70. 70.
    Smalla K, Oros-Sichler M, Milling A et al (2007) Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: do the different methods provide similar results? J Microbiol Methods 69:470–479. https://doi.org/10.1016/j.mimet.2007.02.014 CrossRefPubMedGoogle Scholar
  71. 71.
    Shen SY, Fulthorpe R (2015) Seasonal variation of bacterial endophytes in urban trees. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.00427 CrossRefGoogle Scholar
  72. 72.
    Garbeva P, Van Overbeek LS, van Vuurde JWL et al (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383. https://doi.org/10.1007/s002480000096 CrossRefPubMedGoogle Scholar
  73. 73.
    Weinert N, Meincke R, Gottwald C et al (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75:3859–3865. https://doi.org/10.1128/AEM.00414-09 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Videira SS, Pereira e Silva MDC, Souza Galisa P et al (2013) Culture-independent molecular approaches reveal a mostly unknown high diversity of active nitrogen-fixing bacteria associated with Pennisetum purpureum—a bioenergy crop. Plant Soil 373:737–754. https://doi.org/10.1007/s11104-013-1828-4 CrossRefGoogle Scholar
  75. 75.
    Marques JM, da Silva TF, Vollu RE et al (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88:424–435. https://doi.org/10.1111/1574-6941.12313 CrossRefPubMedGoogle Scholar
  76. 76.
    Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73:127–141CrossRefGoogle Scholar
  77. 77.
    Knief C (2014) Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front Plant Sci 5:216. https://doi.org/10.3389/fpls.2014.00216 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Van Tongeren SP, Degener JE, Harmsen HJM (2011) Comparison of three rapid and easy bacterial DNA extraction methods for use with quantitative real-time PCR. Eur J Clin Microbiol Infect Dis 30:1053–1061. https://doi.org/10.1007/s10096-011-1191-4 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Rantakokko-Jalava K, Jalava J (2002) Optimal DNA isolation method for detection of bacteria in clinical specimens by broad-range PCR. J Clin Microbiol 40:4211–4217. https://doi.org/10.1128/JCM.40.11.4211 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Maropola MKA, Ramond JB, Trindade M (2015) Impact of metagenomic DNA extraction procedures on the identifiable endophytic bacterial diversity in Sorghum bicolor (L. Moench). J Microbiol Methods 112:104–117. https://doi.org/10.1016/j.mimet.2015.03.012 CrossRefPubMedGoogle Scholar
  81. 81.
    Clarridge JE (2004) Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17:840–862. https://doi.org/10.1128/CMR.17.4.840 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Woo PCY, Lau SKP, Teng JLL et al (2008) Then and now: use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clin Microbiol Infect 14:908–934. https://doi.org/10.1111/j.1469-0691.2008.02070.x CrossRefPubMedGoogle Scholar
  83. 83.
    Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. https://doi.org/10.1093/nar/gkt1244 CrossRefPubMedGoogle Scholar
  84. 84.
    Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219 CrossRefGoogle Scholar
  85. 85.
    Nesme X, Normand P (2004) Easy individual community typing by rDNA ITS1 analysis. In: Kowalchuk GA, de Bruijn FJ, Head IM et al Mol. Microb. Ecol. Man., 2nd ed. Kluwer Academic Publishers, Dordrecht, pp 671–688Google Scholar
  86. 86.
    Weisburg WG, Barns SM, Pelletier DA et al (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703. https://doi.org/10.1128/jb.173.2.697-703.1991 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263. https://doi.org/10.1007/s002480000087 CrossRefPubMedGoogle Scholar
  88. 88.
    Rasche F, Velvis H, Zachow C et al (2006) Impact of transgenic potatoes expressing anti-bacterial agents on bacterial endophytes is comparable with the effects of plant genotype, soil type and pathogen infection. J Appl Ecol 43:555–566. https://doi.org/10.1111/j.1365-2664.2006.01169.x CrossRefGoogle Scholar
  89. 89.
    Sun L, Qiu F, Zhang X et al (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb Ecol 55:415–424. https://doi.org/10.1007/s00248-007-9287-1 CrossRefPubMedGoogle Scholar
  90. 90.
    Rasche F, Trondl R, Naglreiter C et al (2006) Chilling and cultivar type affect the diversity of bacterial endophytes colonizing sweet pepper (Capsicum anuum L.). Can J Microbiol 52:1036–1045. https://doi.org/10.1139/w06-059 CrossRefPubMedGoogle Scholar
  91. 91.
    Arenz BE, Schlatter DC, Bradeen JM, Kinkel LL (2015) Blocking primers reduce co-amplification of plant DNA when studying bacterial endophyte communities. J Microbiol Methods 117:1–3. https://doi.org/10.1016/j.mimet.2015.07.003 CrossRefPubMedGoogle Scholar
  92. 92.
    Ruppel S, Rühlmann J, Merbach W (2006) Quantification and localization of bacteria in plant tissues using quantitative real-time PCR and online emission fingerprinting. Plant Soil 286:21–35. https://doi.org/10.1007/s11104-006-9023-5 CrossRefGoogle Scholar
  93. 93.
    Andreote F, Azevedo J, Araújo W (2009) Assessing the diversity of bacterial communities associated with plants. Braz J Microbiol 40:417–432. https://doi.org/10.1590/S1517-83822009000300001 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Lacava PT, Li WB, Araújo WL et al (2006) Rapid, specific and quantitative assays for the detection of the endophytic bacterium Methylobacterium mesophilicum in plants. J Microbiol Methods 65:535–541. https://doi.org/10.1016/j.mimet.2005.09.015 CrossRefPubMedGoogle Scholar
  95. 95.
    Peralta KD, Araya T, Valenzuela S et al (2012) Production of phytohormones, siderophores and population fluctuation of two root-promoting rhizobacteria in Eucalyptus globulus cuttings. World J Microbiol Biotechnol 28:2003–2014. https://doi.org/10.1007/s11274-012-1003-8 CrossRefPubMedGoogle Scholar
  96. 96.
    Alvarez AM (2004) Integrated approaches for detection of plant pathogenic bacteria and diagnosis of bacterial diseases. Annu Rev Phytopathol 42:339–366. https://doi.org/10.1146/annurev.phyto.42.040803.140329 CrossRefPubMedGoogle Scholar
  97. 97.
    Lo Piccolo S, Ferraro V, Alfonzo A et al (2010) Presence of endophytic bacteria in Vitis vinifera leaves as detected by fluorescence in situ hybridization. Ann Microbiol 60:161–167. https://doi.org/10.1007/s13213-010-0023-6 CrossRefGoogle Scholar
  98. 98.
    Cardinale M, Grube M, Erlacher A et al (2015) Bacterial networks and co-occurrence relationships in the lettuce root microbiota. Environ Microbiol 17:239–252. https://doi.org/10.1111/1462-2920.12686 CrossRefPubMedGoogle Scholar
  99. 99.
    Armanhi JSL, de Souza RSC, de Araujo LM et al (2016) Multiplex amplicon sequencing for microbe identification in community- based culture collections. Sci Rep 6:1–9. https://doi.org/10.1038/srep29543 CrossRefGoogle Scholar
  100. 100.
    van der Heijden MGA, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14:1–9. https://doi.org/10.1371/journal.pbio.1002378 CrossRefGoogle Scholar
  101. 101.
    Mbah EI, Wakil SM (2012) Elimination of bacteria from in vitro yam tissue cultures using antibiotics. J Plant Pathol 94:53–58. https://doi.org/10.4454/jpp.fa.2012.023 CrossRefGoogle Scholar
  102. 102.
    Fang JY, Hsu YR (2012) Molecular identification and antibiotic control of endophytic bacterial contaminants from micropropagated Aglaonema cultures. Plant Cell Tissue Org 110:53–62. https://doi.org/10.1007/s11240-012-0129-6 CrossRefGoogle Scholar
  103. 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 Org 102:365–372. https://doi.org/10.1007/s11240-010-9741-5 CrossRefGoogle Scholar
  104. 104.
    George MW, Tripepi RR (2001) Plant preservative MixtureTM can affect shoot regeneration from leaf explants of chrysanthemum, European birch, and rhododendron. Hortscience 36:768–769Google Scholar
  105. 105.
    Bartsch M, Mahnkopp F, Winkelmann T (2014) In vitro propagation of Dionaea muscipula Ellis. Prop Ornam Plants 14:117–124Google Scholar
  106. 106.
    Luna C, Acevedo R, Collavino M et al (2013) Endophytic bacteria from Ilex paraguariensis shoot cultures: localization, characterization, and response to isothiazolone biocides. In Vitro Cell Dev Biol Plant 49:326–332. https://doi.org/10.1007/s11627-013-9500-5 CrossRefGoogle Scholar
  107. 107.
    Marino BG, Gaggìa F (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. https://doi.org/10.1007/s10658-014-0559-6 CrossRefGoogle Scholar
  108. 108.
    Boine B, Naujoks G, Stauber T (2008) Investigations on influencing plant-associated bacteria in tissue cultures of black locust (Robinia pseudoacacia L.). Plant Cell Tissue Org 94:219–223. https://doi.org/10.1007/s11240-008-9395-8 CrossRefGoogle Scholar
  109. 109.
    Matyjaszczyk E (2015) Products containing microorganisms as a tool in integrated pest management and the rules of their market placement in the European Union. Pest Manag Sci 71:1201–1206. https://doi.org/10.1002/ps.3986 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Abteilung WaldgenressourcenNordwestdeutsche Forstliche VersuchsanstaltHann. MündenGermany
  2. 2.Institut für Gartenbauliche ProduktionssystemeLeibniz Universität HannoverHannoverGermany

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