Plant and Soil

, Volume 295, Issue 1–2, pp 115–125 | Cite as

Decreasing prevalence of rhizosphere IAA producing and seedling root growth promoting bacteria with barley development irrespective of protozoan grazing regime

  • Mette Vestergård
  • Lisa Bjørnlund
  • Frédéric Henry
  • Regin Rønn
Regular Article

Abstract

Barley was grown in soil with either bacteria and a mixed protozoan community (Mixed protozoa) or bacteria and a single vahlkampfiid amoebal species (Single amoeba). We assessed the influence of plant age (day 29, 43 and 57 after sowing) on two aspects of rhizosphere bacterial functioning: (1) the proportion of indole-3-acetic acid (IAA) producing bacteria and (2) the effect of mixed rhizosphere bacterial assemblages on barley seedling root growth in an agar based assay. The proportion of IAA producers was significantly lower at day 57 than at day 29 and 43, and mixed bacterial assemblages extracted from rhizospheres of 29 days old plants were significantly less harmful to seedling growth than bacterial assemblages from older plants. Hence both assays indicated that bacterial communities from rhizospheres of older plants were less beneficial for root growth than bacterial communities from younger plants. Genetic fingerprinting of rhizosphere bacterial communities was compared by use of length heterogeneity polymerase chain reaction (LH-PCR). This analysis showed a clear succession from the inoculum bacterial community with a rather low diversity to a community with much higher diversity at day 29. However, diversity did not change after day 29, and no relationship between protozoan treatment nor plant age and genetic fingerprinting was found.

Keywords

Bacterial metabolites Flagellates LH-PCR Plant deleterious bacteria PGPR 

References

  1. Ashgar HN, Zahir ZA, Arshad M, Khaliq A (2002) Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils 35:231–237CrossRefGoogle Scholar
  2. Åström B, Gustafsson A, Gerhardson B (1993) Characteristics of a plant deleterious rhizosphere pseudomonad and its inhibitory metabolite(s). J Appl Bacteriol 74:20–28Google Scholar
  3. Barbieri P, Galli E (1993) Effect of wheat root development of inoculation with an Azospirillum brasiliense mutant with altered indole-3- acetic acid production. Res Microbiol 144:69–75PubMedCrossRefGoogle Scholar
  4. Bjørnlund L, Mørk S, Vestergård M, Rønn R (2006) Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley. Biol Fertil Soils 43:1–11CrossRefGoogle Scholar
  5. Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34:1709–1715CrossRefGoogle Scholar
  6. Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538PubMedGoogle Scholar
  7. Bååth E, Olsson S, Tunlid A (1988) Growth of bacteria in rhizoplane and rhizosphere of rape seedlings. FEMS Microbiol Ecol 53:355–360CrossRefGoogle Scholar
  8. Campbell R, Greaves MP (1990) Anatomy and community structure of the rhizosphere. In: Lynch JM (ed) The Rhizosphere. John Wiley & Sons, Chichester, pp 11–34Google Scholar
  9. Chakrabarti T, Doy CH, Subrahmanyam NC (1978) The analysis of barley genomes. I: The problem that the DNA of bacteria may contribute to the DNA in extracts of barley tissues derived from germinated seeds. Barley Genetics Newsletter 8:25–28Google Scholar
  10. Christensen S, Bjørnlund L, Vestergård M (2007) Decomposer biomass in the rhizosphere to assess rhizodeposition. Oikos 116:65–74CrossRefGoogle Scholar
  11. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17:181–187CrossRefGoogle Scholar
  12. Curl EA, Truelove B (1986) The rhizosphere. Springer-Verlag, BerlinGoogle Scholar
  13. Darbyshire JF, Wheatley RE, Greaves MP, Inkson RHE (1974) A rapid micromethod for estimating bacterial and protozoan populations in soil. Rev Écol Biol Sol 11:465–475Google Scholar
  14. Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasiliense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164CrossRefGoogle Scholar
  15. Frankenberger WT, Arshad M (1995) Phytohormones in soils. Microbial production and function. Marcel Dekker, Inc., New YorkGoogle Scholar
  16. Frederickson JK, Elliott LF (1985) Effects on winter wheat seedling growth by toxin-producing rhizobacteria. Plant Soil 83:399–409CrossRefGoogle Scholar
  17. Fægri A, Torsvik VL, Goksöyr J (1977) Bacterial and fungal activities in soil: Separation of bacteria and fungi by a rapid fractionated centrifugation technique. Soil Biol Biochem 9:105–112CrossRefGoogle Scholar
  18. Glick BR, Changping L, Ghosh S, Dumbroff EB (1997) Early development of Canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239CrossRefGoogle Scholar
  19. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68CrossRefGoogle Scholar
  20. Gregory PJ, Atwell BJ (1991) The fate of carbon in pulse-labelled crops of barley and wheat. Plant Soil 136:205–213CrossRefGoogle Scholar
  21. Griffiths BS (1990) A comparison of microbial-feeding nematodes and protozoa in the rhizosphere of different plants. Biol Fertil Soils 9:83–88CrossRefGoogle Scholar
  22. Griffiths BS, Bonkowski M, Dobson G, Caul S (1999) Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43:297–304Google Scholar
  23. Hankes LV, Riesen WH, Henderson LM, Elvehjem CA (1948) Liberation of amino acids from raw and heated casein by acid and enzyme hydrolysis. J Biol Chem 176:467–476Google Scholar
  24. Henry F, Nguyen C, Paterson E, Sim A, Robin C (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth? Plant Soil 269:181–191CrossRefGoogle Scholar
  25. Jensen B (1993) Rhizodeposition by 14CO2-pulse-labelled spring barley grown in small field plots on sandy loam. Soil Biol Biochem 25:1553–1559CrossRefGoogle Scholar
  26. Kandeler E, Marschner P, Tscherko D, Gahoonia TS, Nielsen NE (2002) Microbial community composition and functional diversity in the rhizosphere of maize. Plant Soil 238:301–312CrossRefGoogle Scholar
  27. Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie van Leeuwenhoek 81:509–520PubMedCrossRefGoogle Scholar
  28. Krasnoff SB, Lobkovsky EB, Wach MJ, Loria R, Gibson DM (2005) Chemistry and phytotoxicity of thaxtomin A alkyl esters. J Agric Food Chem 53:9446–9451PubMedCrossRefGoogle Scholar
  29. Liu WT, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522PubMedGoogle Scholar
  30. Lottmann J, Heuer H, Smalla K, Berg G (1999) Influence of transgenic T4-lysozyme-producing potato plants on potentially beneficial plant-associated bacteria. FEMS Microbiol Ecol 29:365–377CrossRefGoogle Scholar
  31. Magurran AE (2003) Measuring biological diversity. Blackwell Science Ltd, MaldenGoogle Scholar
  32. Marschner P, Yang C-H, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445CrossRefGoogle Scholar
  33. Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208CrossRefGoogle Scholar
  34. Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. Cv. Jemalong line J5. New Phytol 170:165–175PubMedCrossRefGoogle Scholar
  35. Murase J, Noll M, Frenzel P (2006) Impact of protists on the activity and structure of the bacterial community in a rice field soil. Appl Environ Microbiol 72:5436–5444PubMedCrossRefGoogle Scholar
  36. Olsen RA, Bakken LR (1987) Viability of soil bacteria: optimization of the plate-counting technique. Microb Ecol 13:59–74CrossRefGoogle Scholar
  37. Page FC (1988) A new key to freshwater and soil gymnamoebae. Freshwater Biological Association, AmblesideGoogle Scholar
  38. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environl Microbiol 68:3795–3801CrossRefGoogle Scholar
  39. Picard C, Bosco M (2003) Soil antimony pollution and plant growth stage affect the biodiversity of auxin-producing bacterial isolated from the rhizosphere of Achillea agaretum L. FEMS Microbiol Ecol 46:73–80CrossRefGoogle Scholar
  40. Priemé A, Sitaula JIB, Klemedtsson ÅK, Bakken LR (1996) Extraction of methane-oxidizing bacteria from soil particles. FEMS Microbiol Ecol 21:59–68CrossRefGoogle Scholar
  41. de Ridder-Duine AS, Kowalchuk GA, Gunnewiek PJAK, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol& Biochem 37:349–357CrossRefGoogle Scholar
  42. Ritchie NJ, Schutter ME, Dick RP, Myrold DD (2000) Use of Length Heterogeneity PCR and Fatty Acid Methyl Ester profiles to characterize microbial communities in soil. Appl Environ Microbiol 66:1668–1675PubMedCrossRefGoogle Scholar
  43. Rovira AD, Newman EI, Bowen HJ, Campbell R (1974) Quantitative assessment of the rhizoplane microflora by direct microscopy. Soil Biol Biochem 6:211–216CrossRefGoogle Scholar
  44. Rønn R, Ekelund F, Christensen S (1995) Optimizing soil extract and broth media for MPN-enumeration of naked amobae and heterotrophic flagellates in soil. Pedobiologia 39:10–19Google Scholar
  45. Rønn R, McCaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environl Microbiol 68:6094–6105CrossRefGoogle Scholar
  46. de Salamone IEG, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411CrossRefGoogle Scholar
  47. Schippers B, Bakker AW, Bakker PAHM, van Peer R (1990) Beneficial and deleterious effects of HCN-producing pseudomonads on rhizosphere interactions. Plant Soil 129:75–83CrossRefGoogle Scholar
  48. Swinnen J (1994) Rhizodeposition and turnover of root–derived organic material in barley and wheat under conventional and integrated management. Agric Ecosyst Environ 51:115–128CrossRefGoogle Scholar
  49. Swinnen J, van Veen JA, Merckx R (1995) Carbon fluxes in the rhizosphere of winter wheat and spring barley with conventional vs integrated farming. Soil Biol Biochem 27:811–820CrossRefGoogle Scholar
  50. Techau MEC, Bjørnlund L, Christensen S (2004) Simulated herbivory effects on rhizosphere organisms in pea (Pisum sativum) depended on phosphate. Plant Soil 264:185–194CrossRefGoogle Scholar
  51. Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852CrossRefGoogle Scholar
  52. Vestergård M, Bjørnlund L, Christensen S (2004) Aphid effects on rhizosphere microorganisms and microfauna depend more on barley growth phase than on soil fertilization. Oecologia 141:84–93PubMedCrossRefGoogle Scholar
  53. Weisskopf L, Fromin N, Tomasi N, Aragno M, Martinoia E (2005) Secretion activity of white lupin’s cluster roots influences bacterial abundance, function and community structure. Plant Soil 268:181–194CrossRefGoogle Scholar
  54. Wilmotte A, Vanderauwera G, Dewachter R (1993) Structure of the 16S ribosomal-RNA of the thermophilic cyanobacterium Chlorogloeopsis HTF (‘Mastigocladus laminosus HTF’) strain PCC7518, and phylogenetic analysis. FEBS Letter 317:96–100CrossRefGoogle Scholar
  55. Wolsing M, Priemé A (2004) Observation of high seasonal variation in community structure of denitrifying bacteria in arable soil receiving artificial fertilizer and cattle manure by determining T-RFLP of nir gene fragments. FEMS Microbiol Ecol 48:261–271CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Mette Vestergård
    • 1
  • Lisa Bjørnlund
    • 2
  • Frédéric Henry
    • 1
  • Regin Rønn
    • 1
  1. 1.Section of Terrestrial Ecology, Department of BiologyUniversity of CopenhagenCopenhagen KDenmark
  2. 2.Section of Genetics and Microbiology, Department of Ecology, Faculty of Life SciencesUniversity of CopenhagenFrederiksberg CDenmark

Personalised recommendations