Skip to main content
SpringerLink
Log in

Dendrobium nobile Lindl. seed germination in co-cultures with diverse associated bacteria

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The conservation of orchids is challenging due to their strong biotic relations and tiny seeds, requiring mycorrhiza for germination. This is aggravated when tropical plants are maintained in artificial conditions of greenhouses. We aimed to select the plant growth promoting rhizobacteria (PGPR) for orchid seed germination, to study plant–microbial interactions, and to determine whether there is any specificity between two species of Dendrobium plants in choosing bacterial partners. By the isolation of rhizoplane and endophytic rhizobacteria from Dendrobium moschatum roots, the known PGPR (Azospirillum, Enterobacter, Streptomyces) and less popular (Roseomonas, Agrococcus) strains were tested for the production of biologically active auxin. The bacterization of another orchid, D. noblie, with several newly selected strains and previously isolated ones (Mycobacterium sp., Bacillus pumilus) revealed that the orchids did not express evident specificity in relations with favorable bacteria, but refused to establish associations with Streptomyces and Azospirillum. Endophytic Agrococcus and Sphingomonas strains showed significant promotion of orchid germination. Mycobacterium and B. pumilus were also stable in their positive influence on the acceleration of D. noblie seed development. The active colonization of the seed surface and the inner tissues by associated bacteria was observed under electron microscopy. The analysis of orchid–bacteria relations was made. Altogether, the data shows that selection provides a good strategy for choosing the active strains for orchid seeds’ bacterization, since not all known PGPR are useful and successful in building associative frameworks with orchid seeds. The stable activity of the strains guarantees their long-term and effective application in orchid in vitro biotechnology.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20

    Article  Google Scholar 

  • Apine OA, Jadhav JP (2011) Optimization of medium for indole-3-acetic acid production using Pantoea agglomerans strain PVM. J Appl Microbiol 110:1235–1244

    Article  CAS  PubMed  Google Scholar 

  • Baldotto LEB, Olivares FL (2008) Phylloepiphytic interaction between bacteria and different plant species in a tropical agricultural system. Can J Microbiol 54:918–931

    Article  CAS  PubMed  Google Scholar 

  • Beauregard PB, Chaib Y, Vlamakis H, Losick R, Koltera R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci 110:E1621–E1630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrendt U, Schumann P, Ulrich A (2008) Agrococcus versicolor sp. nov., an actinobacterium associated with the phyllosphere of potato plants. Int J Syst Evol Microbiol 58:2833–2838

    Article  CAS  PubMed  Google Scholar 

  • Bharucha U, Patel K (2008) Optimization of indole acetic acid production by Pseudomonas putida UB1 and its effect as plant growth-promoting rhizobacteria on mustard (Brassica nigra). Agric Res 2:215–221

    Article  Google Scholar 

  • Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744

    Article  CAS  PubMed  Google Scholar 

  • Cassán F, Perrig D, Sgroy V, Luna V (2014) Basic and technological aspects of phytohormone production by microorganisms: Azospirillum sp. as a model of plant growth promoting rhizobacteria. In: Maheshwari DK (ed) Bacteria in agrobiology. Plant nutrient management. Springer, Berlin, pp 141–182

    Google Scholar 

  • De Melo Pereira GV, Magalhães KT, Lorenzetii ER, Souza TP, Schwan RF (2012) A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microb Ecol 63:405–417

    Article  PubMed  Google Scholar 

  • Doty S, Oakley B, Xin G, Kang JW, Singleton G, Khan Z, Vajzovic A, Staley JT (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis 47:23–33

    Article  CAS  Google Scholar 

  • Faria DC, Dias AC, 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

    Article  PubMed  Google Scholar 

  • Galdiano Júnior RF, Pedrinho EAN, Castellane TCL, Lemos EGM (2011) Auxin-producing bacteria isolated from the roots of Cattleya walkeriana, an endangered Brazilian orchid, and their role in acclimatization. Rev Bras Ciência Solo 35:729–737

    Article  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Habibi S, Djedidi S, Prongjunthuek K, Mortuza Md, Ohkama-Ohtsu N, Sekimoto H, Yokoyoma T (2014) Physiological and genetic characterization of rice nitrogen fixer PGPR isolated from rhizosphere soils of different crops. Plant Soil 379:51–66

    Article  CAS  Google Scholar 

  • James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PP, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microb Interact 15:894–906

    Article  CAS  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and l-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256

    Article  CAS  PubMed  Google Scholar 

  • Kefeli VI, Kutacek M (1977) Phenolic substances and their possible role in plant growth regulation. Plant Growth Regul 6:181–188

    Article  Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee IJ (2014) Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J Microbiol 52:689–695

    Article  CAS  PubMed  Google Scholar 

  • Knudson L (1922) Nonsymbiotic germination of orchid seeds. Bot Gazette 73:1–25

    Article  Google Scholar 

  • Kolomeitseva GL, Tsavkelova EA, Gusev EM, Malina NE (2002) On symbiosis of orchids and active isolate of the bacterium Bacillus pumilus in culture in vitro. Bull GBS Russ Acad Sci 183:117–126 (in Russian with English abstract)

    Google Scholar 

  • Kublanov IV, Perevalova AA, Slobodkina GB, Lebedinsky AV, Bidzhieva SK, Kolganova TV, Kaliberda EN, Rumsh LD, Haertlé T, Bonch-Osmolovskaya EA (2009) Biodiversity of thermophilic prokaryotes with hydrolytic activities in hot springs of Uzon Caldera, Kamchatka (Russia). Appl Environ Microbiol 75:286–291

    Article  CAS  PubMed  Google Scholar 

  • Lange A, Moreira FMS (2002) Detecção de Azospirillum amazonense em raízes e rizosfera de Orchidaceae e de outras famílias vegetais. R Bras Ci Solo 26:529–533

    Article  Google Scholar 

  • Liu F, Ying G-G, Tao R, Zhao J-L, Yang J-F, Zhao L-F (2009) Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environ Pollut 157:1636–1642

    Article  CAS  PubMed  Google Scholar 

  • Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol 64:795–799

    CAS  PubMed  PubMed Central  Google Scholar 

  • McInroy JA, Kloepper JW (1995) Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil 173:337–342

    Article  CAS  Google Scholar 

  • Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335

    Article  PubMed  Google Scholar 

  • Meuwley P, Pilet PE (1991) Local treatment with indole-3-acetic acid induces differential growth responses in Zea mays L. roots. Planta 185:58–64

    Google Scholar 

  • Morris CE, Monier JM (2003) The ecological significance of biofilm formation by plant-associated bacteria. Annu Rev Phytopathol 41:429–453

    Article  CAS  PubMed  Google Scholar 

  • Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer, Dordrecht, pp 1–27

    Google Scholar 

  • Oleskin AV, Bottvinko IV, Tsavkelova EA (2000) Colonial organization and intercellular communication of microorganisms. Microbiology 69:309–327

    Article  CAS  PubMed  Google Scholar 

  • Opriş O, Copaciu F, Soran ML, Ristoiu D, Niinemets Ü, Copolovici L (2013) Influence of nine antibiotics on key secondary metabolites and physiological characteristics in Triticum aestivum: leaf volatiles as a promising new tool to assess toxicity. Ecotoxicol Environ Safe 87:70–79

    Article  Google Scholar 

  • Passari AK, Mishra VK, Saikia R, Gupta VK, Singh BP (2015) Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Front Microbiol. doi:10.3389/fmicb.2015.00273

    PubMed  PubMed Central  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indole acetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinaudi L, Giordano W (2010) An integrated view of biofilm formation in rhizobia. FEMS Microbiol Lett 304:1–11

    Article  CAS  PubMed  Google Scholar 

  • Roberts DL, Dixon KW (2008) Orchids. Curr Biol 18:R325–R329

    Article  CAS  PubMed  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    Article  CAS  PubMed  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 21:1–30

    Google Scholar 

  • Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 4:239–249

    Article  Google Scholar 

  • Shahab S, Ahmed N, Khan NS (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agric Res 4:1312–1316

    Google Scholar 

  • Shekhovtsova N, Marakaev O, Pervushina K, Osipov G (2013) The underground organ microbial complexes of moorland spotted orchid Dactylorhiza maculata (L.) Soó (Orchidaceae). Adv Biosci Biotechnol 4:35–42

    Article  Google Scholar 

  • Shokri D, Emtiazi G (2010) Indole-3-acetic acid (IAA) production in symbiotic and non-symbiotic nitrogen-fixing bacteria and its optimization by Taguchi design. Curr Microbiol 61:217–225

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    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 

  • Teixeira da Silva JA, Tsavkelova EA, Zeng S, Ng TB, Parthibhan S, Dobránszki J, Cardoso JC, Rao MV (2015) Symbiotic in vitro seed propagation of Dendrobium: fungal and bacterial partners and their influence on plant growth and development. Planta 242:1–22

    Article  CAS  PubMed  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2004) Bacteria associated with the roots of epiphytic orchids. Microbiology 73:710–715

    Article  CAS  Google Scholar 

  • Tsavkelova EA, Klimova SIu, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use, a review. Appl Biochem Microbiol 2:117–126

    Article  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AI (2007a) Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res 162:69–76

    Article  CAS  PubMed  Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Klimova SY, Shestakov AI, Botina SG, Netrusov AI (2007b) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664

    Article  CAS  PubMed  Google Scholar 

  • Videira SS, De Araujo JLS, da Rodrigues LS, Baldani VL, Baldani JI (2009) Occurrence and diversity of nitrogen-fixing Sphingomonas bacteria associated with rice plants grown in Brazil. FEMS Microbiol Lett 293:11–19

    Article  CAS  PubMed  Google Scholar 

  • Wang Xu, Ryu D, Houtkooper RH, Auwerx J (2015) Antibiotic use and abuse: a threat to mitochondria and chloroplasts with impact on research, health, and environment. BioEssays 37:1045–1053

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson KG, Dixon KW, Sivasithamparam K (1989) Interaction of soil bacteria, mycorrhizal fungi and orchid seed in relation to germination of Australian orchids. New Phytol 112:429–435

    Article  Google Scholar 

  • Wilkinson KG, Dixon KW, Sivasithamparam K, Ghisalberti EL (1994) Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid-associated bacteria. Plant Soil 159:291–295

    Article  CAS  Google Scholar 

  • Yang S, Zhang X, Cao Z, Zhao K, Wang S, Chen M, Hu X (2014) Growth-promoting Sphingomonas paucimobilis ZJSH1 associated with Dendrobium officinale through phytohormone production and nitrogen fixation. Microb Biotechnol 7:611–620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Mr. Paul Girling for grammatically editing the manuscript. This study was partially supported by the Russian Science Foundation grant (project #14-50-00029).

Author information

Authors and Affiliations

  1. Department of Microbiology, Biological Faculty, Lomonosov Moscow State University, 1-12 Lenin’s Hills, Moscow, Russia, 119234

    Elena A. Tsavkelova, Maria A. Egorova, Maria R. Leontieva & Alexander I. Netrusov

  2. Department of Biotechnology, Biological Faculty, Lomonosov Moscow State University, 1-12 Lenin’s Hills, Moscow, Russia, 119234

    Sophie G. Malakho

  3. The Stock Greenhouse of the The Tsitsin Main Botanical Garden RAS, Botanicheskaya Street 4, Moscow, Russia, 127276

    Galina L. Kolomeitseva

Authors
  1. Elena A. Tsavkelova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria A. Egorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria R. Leontieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sophie G. Malakho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Galina L. Kolomeitseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexander I. Netrusov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elena A. Tsavkelova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 327 kb)

Supplementary material 2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsavkelova, E.A., Egorova, M.A., Leontieva, M.R. et al. Dendrobium nobile Lindl. seed germination in co-cultures with diverse associated bacteria. Plant Growth Regul 80, 79–91 (2016). https://doi.org/10.1007/s10725-016-0155-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-016-0155-1

Keywords

Search

Navigation