Advertisement

Endophytic Bacteria in Tree Shoot Tissues and Their Effects on Host

  • Anna Maria Pirttilä
Chapter
Part of the Forestry Sciences book series (FOSC, volume 86)

Abstract

Shoot endophytic bacteria have mainly been isolated during plant tissue culture started from shoot tips (buds) or embryos. With methods such as in situ hybridization and transmission electron microscopy, endophytic bacteria have been localized in buds, seeds, and flowers of forest trees. By GFP tagging of endophytic bacteria, colonization of tree seedlings has been observed. It is still unknown whether shoot-associated bacteria are transmitted to new trees via seeds, although many results point to this direction. Interactions between the plant and endophytic bacteria in the shoots likely differ to some extent from those in the roots. Shoot endophytic bacteria share some mechanisms of plant growth promotion with the root endophytes, such as the ability of producing plant growth hormones. In addition, some shoot endophytes may affect plant growth through production of adenine derivatives or bacterial photosynthesis. An interesting new mechanism of enhancing host growth is suggested for intracellular bacteria that can act directly through production of nucleomodulins, eukaryotic transcription factors, encoded in the bacterial genome. This mechanism was identified through genome sequencing of a shoot endosymbiont. Therefore, we can expect further interesting discoveries in the future on shoot endophytes of forest trees.

Abbreviations

TEM

Transmission electron microscopy

PHB

Polyhydroxybutyrate

GFP

Green fluorescent protein

IAA

Indole-acetic acid

NGS

Next-generation sequencing

DMHF

2,5-dimethyl-4-hydroxy-2H-furan-3-one

BphP

Bacteriophytochrome

ACC

Aminocyclopropane-1-carboxylate

FISH

Fluorescent in situ hybridization

References

  1. Ali S, Charles TC, Glick BR (2012) Delay of flower senescence by bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate deaminase. J Appl Microbiol 113:1139–1144CrossRefPubMedGoogle Scholar
  2. Alibrandi P, Cardinale M, Rahman MM et al (2017) The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacterium spp. and Staphylococcus spp. with potential plant-growth promoting activities. Plant Soil: 1–19Google Scholar
  3. Anand R, Grayston S, Chanway C (2013) N2-fixation and seedling growth promotion of lodgepole pine by endophytic Paenibacillus polymyxa. Microb Ecol 66:369–374CrossRefPubMedGoogle Scholar
  4. Baldani JI, Caruso L, Baldani VLD et al (1997) Recent advances in BNF with non legume plants. Soil Biol Biochem 29:911–922CrossRefGoogle Scholar
  5. Bandara WMMS, Seneviratne G, Kulasooriya SA (2006) Interactions among endophytic bacteria and fungi: effects and potentials. J Biosci 31:645–650CrossRefPubMedGoogle Scholar
  6. Basile DV, Basile MR, Li QY et al (1985) Vitamin B12-stimulated growth and development of Jungermannia leiantha Grolle and Gymnocolea inflata (Huds.) Dum. (Hepaticae). Bryologist 88:77–81CrossRefGoogle Scholar
  7. Baumann TW, Schulthess BH, Linden A et al (1994) Structure and metabolism of t-β-D-glucopyranosyladenine. The product of a cytokinin-sparing reaction? Phytochemistry 36:537–542CrossRefGoogle Scholar
  8. Beckers B, De Beeck MO, Weyens N et al (2017) Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees. Microbiome 5:25CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503CrossRefPubMedGoogle Scholar
  10. Cankar K, Kraigher H, Ravnikar M et al (2005) Bacterial endophytes from seed of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345CrossRefPubMedGoogle Scholar
  11. Carrell AA, Frank AC (2014) Pinus flexilis and Picea engelmannii share a simple and consistent needle endophyte microbiota with a potential role in nitrogen fixation. Front Microbiol 5:333CrossRefPubMedPubMedCentralGoogle Scholar
  12. Compant S, Mitter B, Colli-Mull JG et al (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 62:188–197CrossRefGoogle Scholar
  13. Croft MT, Lawrence AD, Raux-Deery E et al (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93CrossRefPubMedGoogle Scholar
  14. Dalla Santa OR, Hernández RF et al (2004) Azospirillum sp. inoculation in wheat, barley and oats seeds greenhouse experiments. Braz Arch Biol Technol 47:843–850CrossRefGoogle Scholar
  15. Doty SL, Oakley B, Xin G et al (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47:23–33CrossRefGoogle Scholar
  16. Eichel J, González JC, Hotze M et al (2008) Vitamin-B12-independent methionine synthase from a higher plant (Catharanthus roseus): Molecular characterization, regulation, heterologous expression, and enzyme properties. Eur J Biochem 230:1053–1058CrossRefGoogle Scholar
  17. Fall R (1996) Cycling of methanol between plants, methylotrophs and the atmosphere. In: Lidstrom ME, Tabita FR (eds) Microbial Growth on C1 Compounds. Kluwer Academic Publishers, Dordrecht, pp 343–350CrossRefGoogle Scholar
  18. Fall R, Benson AA (1996) Leaf methanol—the simplest natural product from plants. Trends Plant Sci 1:296–301CrossRefGoogle Scholar
  19. Ferreira A, Quecine MC, Lacava PT et al (2008) Diversity of endophytic bacteria from Eucalyptus species seed and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287:8–14CrossRefPubMedGoogle Scholar
  20. Frank AC (2011) The Genomes of endophytic bacteria. In: Pirttilä AM, Frank AC (eds) Endophytes of forest trees: biology and applications, vol 80, 1st edn. Springer Forestry Sciences, pp. 107–136CrossRefGoogle Scholar
  21. Freyermuth SK, Long RLG, Mathur S et al (1996) Metabolic aspects of plant interaction with commensal methylotrophs. In: Lidstrom ME, Tabita RF (eds) Microbial growth on C1 compounds. Kluwer Academic Publishers, Dordrecht, pp 277–284CrossRefGoogle Scholar
  22. George EF, Sherrington PD (1984) Plant propagation by tissue culture methods. Handbook and directory of commercial laboratories. Eastern Press, ReadingGoogle Scholar
  23. Giraud E, Hannibal L, Fardoux J et al (2000) Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc Natl Acad Sci 97:14795–14800CrossRefPubMedGoogle Scholar
  24. Giraud E, Fardoux J, Fourrier N et al (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417:202–205CrossRefPubMedGoogle Scholar
  25. Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 25:1–7CrossRefGoogle Scholar
  26. Gout E, Aubert S, Bligny R et al (2000) Metabolism of methanol in plant cells. Carbon-13 nucleic magnetic resonance studies. Plant Physiol 123:287–296CrossRefPubMedPubMedCentralGoogle Scholar
  27. Holland MA (1997) Occam’s razor applied to hormonology. Are cytokinins produced by plants? Plant Physiol 115:865–868CrossRefPubMedPubMedCentralGoogle Scholar
  28. Holland MA, Polacco JC (1994) PPFMs and other covert contamination: is there more to plant physiology than just plant? Annu Rev Plant Phys Plant Mol Biol 45:197–209CrossRefGoogle Scholar
  29. Ivanova EG, Doronina NV, Shepelyakovskaya AO et al (2000) Facultative and obligate aerobic methylobacteria synthesize cytokinins. Mikrobiologiya 69:764–769Google Scholar
  30. Ivanova EG, Doronina NV, Trotsenko YA (2001) Aerobic methylobacteria are capable of synthesizing auxins. Microbiologiya 70:452–458Google Scholar
  31. Ivanova EG, Fedorov DN, Doronina NV et al (2006) Production of vitamin B12 in aerobic methylotrophic bacteria. Microbiologiya 75:494–496Google Scholar
  32. Ivanova EG, Pirttilä AM, Fedorov DNF et al (2008) Association of methylotrophic bacteria with plants: metabolic aspects. In: Sorvari S, Pirttilä AM (eds) Prospects and applications for plant associated microbes. A laboratory manual, Part A: bacteria. Biobien Innovations, Turku, Finland, pp. 225–231Google Scholar
  33. Kalyaeva MA, Zakharchenko NS, Doronina NV et al (2001) Plant growth and morphogenesis in vitro is promoted by associative methylotrophic bacteria. Russ J Plant Physiol 48:514–517CrossRefGoogle Scholar
  34. Kamoun R, Lepoivre P, Boxus P (1998) Evidence for the occurrence of endophytic prokaryotic contaminants in micropropagated plantlets of Prunus cerasus cv. ‘Montgomery’. Plant Cell Tissue Org Cult 52:57–59CrossRefGoogle Scholar
  35. Keppler F, Boros M, Frankenberg C et al (2009) Methane formation in aerobic environments. Env Chem 6:459–465CrossRefGoogle Scholar
  36. Koenig RL, Morris RO, Polacco JC (2002) tRNA is the source of low-level trans-zeatin production in Methylobacterium spp. J Bacteriol 184:1832–1842CrossRefPubMedPubMedCentralGoogle Scholar
  37. Koopman V, Kutschera U (2005) In vitro regeneration of sunflower plants: effects of a Methylobacterium strain on organ development. J Appl Bot Food Qual 79:59–62Google Scholar
  38. Koskimäki JJ, Nylund S, Suorsa M et al (2010) Mycobacterial endophytes are enriched during micropropagation of Pogonatherum paniceum. Env Microbiol Rep 2:619–624CrossRefGoogle Scholar
  39. Koskimäki JJ, Pirttilä AM, Ihantola, E-L et al (2015) The intracellular Scots pine shoot symbiont Methylobacterium extorquens DSM13060 aggregates around the host nucleus and encodes eukaryote-like proteins. mBio 6(2): e00039-15CrossRefPubMedPubMedCentralGoogle Scholar
  40. Koskimäki JJ, Kajula M, Hokkanen J et al (2016) Methyl-esterified 3-hydroxybutyrate oligomers protect bacteria from hydroxyl radicals. Nat Chem Biol 12:332–338CrossRefPubMedGoogle Scholar
  41. Koutsompogeras P, Kyriacou A, Zabetakis I (2007) The formation of 2,5-dimethyl-4-hydroxy-2H-furan-3-one by cell free extracts of Methylobacterium extorquens and strawberry (Fragaria × ananassa cv. Elsanta). Food Chem 104:1654–1661CrossRefGoogle Scholar
  42. Laukkanen H, Soini H, Kontunen-Soppela S et al (2000) A mycobacterium isolated from tissue cultures of mature Pinus sylvestris interferes with growth of Scots pine seedlings. Tree Physiol 20:915–920CrossRefPubMedGoogle Scholar
  43. Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone mnipulations do not result in common growth responses. PLoS ONE 3:e2702CrossRefPubMedPubMedCentralGoogle Scholar
  44. Madmony A, Chernin L, Pleban S et al (2005) Enterobacter cloacae, an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol 50:209–216CrossRefGoogle Scholar
  45. Miguel PS, de Oliveira MN, Delvaux JC et al (2016) Diversity and distribution of the endophytic bacterial community at different stages of Eucalyptus growth. Antonie van Leeuwenhoek 109: 755–771CrossRefPubMedGoogle Scholar
  46. Moore FP, Barac T, Borremans B et al (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556CrossRefPubMedGoogle Scholar
  47. Moritz T, Sundberg B (1996) Endogenous cytokinins in the vascular cambial region of Pinus sylvestris during activity and dormancy. Physiol Plant 98:693–698CrossRefGoogle Scholar
  48. Moyes AB, Kueppers LM, Pett-Ridge J et al (2016) Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer. New Phytol 210:657–668CrossRefPubMedGoogle Scholar
  49. Murthy BNS, Vettakkorumakankav NN, KrishnaRaj S et al (1999) Characterization of somatic embryogenesis in Pelargonium × hortorum mediated by a bacterium. Plant Cell Rep 18:607–613CrossRefGoogle Scholar
  50. Nasopoulou C, Pohjanen J, Koskimäki JJ et al (2014) Localization of strawberry (Fragaria x ananassa) and Methylobacterium extorquens genes of strawberry flavour biosynthesis in strawberry tissue by in situ hybridization. J Plant Physiol 171:1099–1105CrossRefPubMedGoogle Scholar
  51. Nemecek-Marshall M, MacDonald RC, Franzen JJ et al (1995) Methanol emission from leaves (enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development). Plant Physiol 108:1359–1368CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nonomura AM, Benson AA (1991) The path of carbon in photosynthesis: improved crop yields with methanol. PNAS 89:9794–9798CrossRefGoogle Scholar
  53. Nishio N, Tanaka M, Matsuno R et al (1977) Production of vitamin B12 by methanol-utilizing bacteria, Pseudomonas AM-1 and Microcyclus eburneus. Ferment Technol 55:200–203Google Scholar
  54. Pham NT, Meier-Dinkel A, Höltken AM et al (2017) Endophytic bacterial communities in in vitro shoot cultures derived from embryonic tissue of hybrid walnut (Juglans × intermedia). Plant Cell Tiss Organ Cult 130:153–165CrossRefGoogle Scholar
  55. 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 66:3073–3077CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pirttilä AM, Laukkanen H, Hohtola A (2002) Chitinase production in pine callus (Pinus sylvestris L.): a defense reaction against endophytes? Planta 214:848–852CrossRefPubMedGoogle Scholar
  57. Pirttilä AM, Pospiech H, Laukkanen H et al (2003) Two endophytic fungi in different tissues of Scots pine buds (Pinus sylvestris L.). Microbial Ecol 45:53–62CrossRefGoogle Scholar
  58. Pirttilä AM, Joensuu P, Pospiech P et al (2004) Endophytic products affect morphology and mitigate browning of callus cultures of Scots pine (Pinus sylvestris L.). Physiol Plant 121:305–312CrossRefPubMedGoogle Scholar
  59. Pirttilä AM, Pospiech H, Laukkanen H et al (2005) Seasonal variation in location and population structure of endophytes in buds of Scots pine. Tree Physiol 25:289–297CrossRefPubMedGoogle Scholar
  60. Pirttilä AM, Hohtola A, Ivanova EG et al (2008) Identification and localization of methylotrophic plant-associated bacteria. In: Sorvari S, Pirttilä AM (eds) Prospects and applications for plant associated microbes. A laboratory manual, Part A: bacteria. Biobien Innovations, Turku, Finland. pp. 218–224Google Scholar
  61. Pirttilä AM (2011) Colonization of Tree Shoots by Endophytic Fungi. In: Pirttilä AM, Sorvari S (eds) Prospects and applications for plant-associated microbes. A laboratory manual, Part B: fungi. BioBien Innovations, Turku, Finland, pp. 93–95Google Scholar
  62. Podolich O, Laschevskyy V, Ovcharenko L et al (2009) Methylobacterium sp. resides in unculturable state in potato tissues in vitro and becomes culturable after induction by Pseudomonas fluorescens IMGB163. J Appl Microbiol 106:728–737CrossRefPubMedGoogle Scholar
  63. Pohjanen J, Koskimäki JJ, Sutela S et al (2014) The interaction with ectomycorrhizal fungi and endophytic Methylobacterium affects the nutrient uptake and growth of pine seedlings in vitro. Tree Physiol 34:993–1005CrossRefPubMedGoogle Scholar
  64. 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 34:524–533CrossRefPubMedGoogle Scholar
  65. 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 Tiss Organ Cult 126:305–317CrossRefGoogle Scholar
  66. Ramírez I, Dorta F, Espinoza V et al (2006) Effects of foliar and root applications of methanol on the growth of arabidopsis, tobacco, and tomato plants. J Plant Growth Regul 25:30–44CrossRefGoogle Scholar
  67. Reed BM, Mentzer J, Tanprasert P et al (1998) Internal bacterial contamination of micropropagated hazelnut: identification and antibiotic treatment. Plant Cell Tiss Org Cult 52:67–70CrossRefGoogle Scholar
  68. Río-Álvarez I, Rodríguez-Herva JJ, Martínez PM et al (2014) Light regulates motility, attachment and virulence in the plant pathogen Pseudomonas syringae pv tomato DC3000. Environ Microbiol 16:2072–2085CrossRefPubMedGoogle Scholar
  69. Scherling C, Ulrich K, Ewald D et al (2009) 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 22:1032–1037CrossRefPubMedGoogle Scholar
  70. Skoog F, Armstrong DJ (1970) Cytokinins. Annu Rev Plant Physiol 21:359–384CrossRefGoogle Scholar
  71. Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131–136CrossRefPubMedGoogle Scholar
  72. Taghavi A, Garafola C, Monchy S et al (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl Environ Microbiol 75:748–757CrossRefPubMedGoogle Scholar
  73. Toraya T, Yongsmith B, Tanaka A, Fukui S (1975) Vitamin B12 production by a methanol-utilizing bacterium. Appl Microbiol 30:477–479PubMedPubMedCentralGoogle Scholar
  74. Ulrich K, Ulrich A, Ewald D (2008) Paenibacillus- a predominant endophytic bacterium colonizing tissue cultures of woody plants. Plant Cell Tiss Organ Cult 93:347–351CrossRefGoogle Scholar
  75. Van Aken B, Peres CM, Doty SL et al (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoides x nigra DN34). Int J Syst Evol Microbiol 54:1191–1196CrossRefPubMedGoogle Scholar
  76. Visser C, Murthy BNS, Odumeru J et al (1994) Modulation of somatic embryogenesis in hypocotyl cultures of geranium (Pelargonium × hortorum Bailey) cv. Ringo Rose by a bacterium. In Vitro Cell Dev Biol 30P:140–143CrossRefGoogle Scholar
  77. Wu L, McGrane RS, Beattie GA (2013) Light regulation of swarming motility in Pseudomonas syringae integrates signaling pathways mediated by a bacteriophytochrome and a LOV protein. mBio 4: e00334–00313CrossRefGoogle Scholar
  78. Xing K, Bian GK, Qin S et al (2012) Kibdelosporangium phytohabitans sp. nov., a novel endophytic actinomycete isolated from oil-seed plant Jatropha curcas L. containing 1-aminocyclopropane-1-carboxylic acid deaminase. Antonie Van Leeuwenhoek 101:433–441CrossRefPubMedGoogle Scholar
  79. Yrjälä K, Mancano G, Fortelius C et al (2010) The incidence of Burkholderia in epiphytic and endophytic bacterial cenoses in hybrid aspen grown on sandy peat. Boreal Environ Res 15:81–96Google Scholar
  80. Zabetakis I (1997) Enhancement of flavour biosynthesis from strawberry (Fragaria × ananassa) callus cultures by Methylobacterium species. Plant Cell Tiss Org Cult 50:179–183CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Ecology and GeneticsUniversity of OuluOuluFinland

Personalised recommendations