Suppression of Rhizoctonia solani AG-8 induced disease on wheat by the interaction between Pantoea, Exiguobacterium, and Microbacteria
Stephen J. Barnett A B C , David K. Roget A and Maarten H. Ryder AA CSIRO Land and Water, PMB 2, Glen Osmond, SA 5064, Australia.
B South Australian Research and Development Institute, Field Crops Pathology Unit, GPO Box 397, Adelaide, SA 5001, Australia.
C Corresponding author. Email: barnett.steve2@saugov.sa.gov.au
Australian Journal of Soil Research 44(4) 331-342 https://doi.org/10.1071/SR05113
Submitted: 12 August 2005 Accepted: 19 April 2006 Published: 27 June 2006
Abstract
Rhizoctonia solani AG-8 is a major wheat root pathogen; however, soils can become suppressive to the expression of disease under intensive cropping with retention of crop residues. This is in part due to the action of soil microorganisms. A step-wise approach was used to determine which microorganisms contributed to suppression of R. solani induced disease in a disease-suppressive soil. Using wheat-soil-pathogen bioassays it was determined that the interaction between 3 phylogenetically diverse groups of bacteria, Pantoea agglomerans, Exiguobacterium acetylicum, and Microbacteria (family Microbacteriaceae), was a major contributor to disease suppression. Inoculation of a sterilised soil with the combination of these groups resulted in greatly increased seedling shoot dry weight and reduced infection compared with diseased control plants with no bacterial inoculation, or inoculated with individual types of bacteria. These groups, however, did not reduce levels of pathogen DNA, although inoculation with suppressive soil (at 10% w/w) did reduce pathogen DNA. Root associated P. agglomerans and E. acetylicum promoted the growth of infected wheat plants and soil associated Microbacteria reduced root infection by R. solani.
Additional keywords: disease suppression, Exiguobacterium acetylicum, Microbacterium, Pantoea agglomerans, rhizosphere interactions.
Acknowledgments
The authors thank the Grains Research and Development Corporation, Australia, for financial support for S.J.B. through a Post Doctoral Fellowship (BAR01), B. Hawke for assistance with FAME profiles, P. Harvey for advice on the molecular component, and K. Ophel-Keller and A. Mckay for estimation of R. solani DNA.
Amellal N,
Bartoli F,
Villemin G,
Talouzte A, Heulin T
(1999) Effects of inoculation of EPS-producing Pantoea agglomerans on wheat rhizosphere aggregation. Plant and Soil 211, 93–101.
| Crossref | GoogleScholarGoogle Scholar |
Barnett SJ,
Alami Y,
Singleton I, Ryder MH
(1999b) Diversification of Pseudomonas corrugata 2140 produces new phenotypes altered in GC-FAME, BIOLOG, and in vitro inhibition profiles and taxonomic identification. Canadian Journal of Microbiology 45, 287–298.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Barnett SJ,
Singleton I, Ryder MH
(1999a) Spatial variation in populations of Pseudomonas corrugata 2140 and pseudomonads on take-all diseased and healthy root systems of wheat. Soil Biology and Biochemistry 31, 633–636.
| Crossref | GoogleScholarGoogle Scholar |
Becker DM,
Kinkel LL, Schottel JL
(1997) Evidence for interspecies communication and its potential role in pathogen suppression in a naturally occuring disease suppressive soil. Canadian Journal of Microbiology 43, 985–990.
Behrendt U,
Ulrich A, Schumann P
(2001) Description of Microbacterium foliorum sp. nov., and Microbacterium phyllosphaerae sp. nov., isolated from the phyllosphere of grasses and the surface litter after mulching the sward, and reclassification of Aureobacterium resistens (Funke et al. 1998) as Microbacterium resistens comb. nov. International Journal of Systematic and Evolutionary Microbiology 51, 1267–1276.
| PubMed |
Caldwell DE,
Wolfaardt GM,
Korber DR, Lawrence JR
(1997) Do bacterial communities transcend Darwinism. Advances in Microbial Ecology 15, 105–191.
Castejón-Muñoz M, Oyarzun PJ
(1995) Soil receptivity to Fusarium solani f. sp. pisi and biocontrol of root rot of pea. European Journal of Plant Pathology 101, 35–49.
| Crossref | GoogleScholarGoogle Scholar |
Cook RJ, Rovira AD
(1976) The role of bacteria in the biological control of Gaeumannomyces graminis by suppressive soils. Soil Biology and Biochemistry 8, 269–273.
| Crossref | GoogleScholarGoogle Scholar |
Duijff BJ,
Recorbet G,
Bakker PAHM,
Loper JE, Lemanceau P
(1999) Microbial antagonism at the root level is involved in the suppression of Fusarium wilt by the combination of non-pathogenic Fusarium oxysporum Fo47 and Pseudomonas Putida WCS358. Phytopathology 89, 1073–1079.
Elliott ML, Des Jardin EA
(1999) Comparison of media and diluents for enumeration of aerobic bacteria from bermuda grass golf course putting greens. Journal of Microbiological Methods 34, 193–202.
| Crossref | GoogleScholarGoogle Scholar |
Elsherif M, Grossmann F
(1994) Comparative investigations on the antagonistic activity of flourescent pseudomonads against Gaeumannomyces graminis var. tritici in vitro and in vivo. Microbiological Research 149, 371–377.
Farrow JAE,
Wallbanks S, Collins MD
(1994) Phylogenetic interrelationships of the round-spore-forming Bacilli containing cell walls based on lysine and the non-spore-forming genera Caryophanon, Exiguobacterium, Kurthia and Planococcus. International Journal of Systematic Bacteriology 44, 74–82.
| PubMed |
Fukui R,
Fukui H, Alvarez AM
(1999) Comparisons of single versus multiple bacterial species on biological control of anthurium blight. Phytopathology 89, 366–373.
Haahtela K,
Laakso T,
Nurmiaho EL, Korhonen TK
(1988) Effects of inoculation of Poa pratensis and Triticum aestivum with root-associated, N2-fixing Klebsiella, Enterobacter and Azospirillum. Plant and Soil 106, 239–248.
| Crossref | GoogleScholarGoogle Scholar |
Hollaway GJ,
Gillings MR, Fahy PC
(1997) Use of fatty acid profiles and repetitive element polymerase chain reaction (PCR) to assess the genetic diversity of Pseudomonas syringae pv. pisi and Pseudomonas syringae pv. syringae isolated from field peas in Australia. Australasian Plant Patholology 26, 98–108.
| Crossref | GoogleScholarGoogle Scholar |
James FC, McCulloch CE
(1990) Multivariate analysis in ecology and systematics: panacea or Pandora’s box. Annual Review of Ecology and Systematics 21, 129–166.
Joseph SJ,
Hugenholtz P,
Sangwan CA, Janssen PH
(2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Applied and Environmental Microbiology 69, 7210–7215.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim KY,
McDonald GA, Jordan D
(1997) Solubilization of hydroxyapatite by Enterobacter agglomerans and cloned Escherichia coli in culture medium. Biology and Fertility of Soils 24, 347–352.
| Crossref | GoogleScholarGoogle Scholar |
Landa BB,
Mavrodi DM,
Thomashow LS, Weller DM
(2003) Interactions between strains of 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens in the rhizosphere of wheat. Phytopathology 93, 982–994.
Legard DE,
McQuilken MP,
Whipps JM,
Fenlon JS,
Fermor TR,
Thompson IP,
Bailey MJ, Lynch JM
(1994) Studies of the seasonal changes in the wheat microbial populations on the phyllosphere of spring wheat as a prelude to the release of a genetically modified microorganism. Agriculture, Ecosystems & Environment 50, 87–101.
| Crossref | GoogleScholarGoogle Scholar |
Lemanceau P,
Corberand T,
Gardan L,
Latour X,
Laguerre G,
Boeufgras JM, Alabouvette C
(1995) Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Applied and Environmental Microbiology 61, 1004–1012.
| PubMed |
Lucas P,
Smiley RW, Collins HP
(1993) Decline of Rhizoctonia root rot on wheat in soils infested with Rhizoctonia solani AG 8. Phytopathology 83, 260–265.
MacNish GC
(1988) Changes in take-all (Gaeumannomyces graminis var. tritici), Rhizoctonia root rot (Rhizoctonia solani) and soil pH in continuous wheat with annual applications of nitrogenous fertiliser in Western Australia. Australian Journal of Experimental Agriculture 28, 333–341.
| Crossref | GoogleScholarGoogle Scholar |
Madsen EL
(1998) Epistemology of environmental microbiology. Environmental Science & Technology 32, 429–439.
| Crossref | GoogleScholarGoogle Scholar |
Mahaffee WF, Kloepper JW
(1997) Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microbial Ecology 34, 210–223.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McKellar ME, Nelson EB
(2003) Compost-induced suppression of Pythium damping-off is mediated by fatty-acid-metabolizing seed-colonising microbial communities. Applied and Environmental Microbiology 69, 452–460.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Molin J, Molin S
(2000) Complex adaptive systems ecology. Advances in Microbial Ecology 16, 233–275.
Orozco-Medina C,
Meada MAM, Lopez CA
(2002) Effect of aerobic Gram-positive heterotrophic bacteria associated with Artemia franciscana cysts on the survival and development of its larvae. Aquaculture 213, 15–29.
| Crossref | GoogleScholarGoogle Scholar |
Oyarzun PJ,
Gerlagh M, Zadoks JC
(1998) Factors associated with soil receptivity to some fungal root rot pathogens of peas. Applied Soil Ecology 10, 151–169.
| Crossref | GoogleScholarGoogle Scholar |
Pumphrey FV,
Wilkins DE,
Hane DC, Smiley RW
(1987) Influence of tillage and nitrogen fertiliser on Rhizoctonia root rot (bare patch) of winter wheat. Plant Disease 71, 125–127.
Rainey PB,
Bailey MJ, Thompson IP
(1994) Phenotypic and genotypic diversity of fluorescent pseudomonads isolated from field-grown sugar beet. Microbiology 140, 2315–2331.
| PubMed |
Reddy MS,
Hynes RK, Lazarovits G
(1994) Relationship between in vitro growth inhibition of pathogens and suppression of preemergence damping-off and postemergence root rot of white bean seedlings in the greenhouse by bacteria. Canadian Journal of Microbiology 40, 113–119.
Roget DK
(1995) Decline in root rot (Rhizoctonia solani AG-8) in wheat in a tillage and rotation experiment at Avon, South Australia. Australian Journal of Experimental Agriculture 35, 1009–1013.
| Crossref | GoogleScholarGoogle Scholar |
Roget DK
(2001) Prediction modelling of soilborne plant diseases. Australasian Plant Pathology 30, 85–89.
| Crossref | GoogleScholarGoogle Scholar |
Ross IL,
Alami Y,
Harvey PR,
Achouak W, Ryder MH
(2000) Genetic diversity and biological control activity of novel species of closely related pseudomonads isolated from wheat field soils in South Australia. Applied and Environmental Microbiology 66, 1609–1616.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rovira AD
(1986) Influence of crop rotation and tillage on Rhizoctonia bare patch of wheat. Phytopathology 76, 669–673.
Shipton PJ,
Cook RJ, Sitton JW
(1973) Occurrence and transfer of a biological factor in soil that suppresses take-all of wheat in eastern Washington. Phytopathology 63, 511–517.
Simon A, Ridge EH
(1974) The use of ampicillin in a simplified selective media for the reisolation of fluorescent pseudomonads. Journal of Applied Bacteriology 37, 459–460.
| PubMed |
Simon A, Sivasithamparam K
(1988) Interactions among Gaeumannomyces graminis var. tritici, Trichoderma koningii, and soil bacteria. Canadian Journal of Microbiology 34, 871–876.
Stockwell VO,
Hohnson KB,
Sugar D, Loper JE
(2002) Antibiosis contributes to biological control of fire blight by Pantoea agglomerans strain Eh252 in orchards. Phytopathology 92, 1202–1209.
Sturz AV, Kimpinski J
(2004) Endoroot bacteria derived from marigolds (Tagetes spp.) can decrease soil population densities of root-lesion nematodes in the potato root zone. Plant and Soil 262, 241–249.
| Crossref | GoogleScholarGoogle Scholar |
Teixidó N,
Usall J,
Palou L,
Asensio A,
Numes C, Viñas I
(2001) Improved control of green and blue moulds of oranges by combining Pantoea agglomerans (CPA-2) and sodium bicarbonate. European Journal of Plant Pathology 107, 685–694.
| Crossref |
Tonso NL,
Matheson VG, Holben WE
(1995) Polyphasic characterisation of a suite of bacterial isolates capable of degrading 2,4-D. Microbial Ecology 30, 3–24.
| Crossref | GoogleScholarGoogle Scholar |
Versalovic J,
Schneider M,
de Bruijn F, Lupski R
(1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cellular Biology 5, 25–40.
Weaver PK,
Wall JD, Gest H
(1975) Characterisation of Rhodopseudomonas capsulata. Archives of Microbiology 105, 207–216.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weisburg WG,
Barns SM,
Pelletier DA, Lane DJ
(1991) 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173, 697–703.
| PubMed |
Werker AR,
Gilligan CA, Hornby D
(1991) Analysis of disease-progress curves for take-all in consecutive crops of winter wheat. Plant Pathology 40, 8–24.
Whisson DL,
Herdina PH, Francis L
(1995) Detection of Rhizoctonia solani AG-8 in soil using a specific DNA probe. Mycological Research 99, 1299–1302.
Wiseman BM,
Neate SM,
Ophel Keller K, Smith SE
(1996) Suppression of Rhizoctonia solani anastomosis group 8 in Australia and its biological nature. Soil Biology and Biochemistry 28, 727–732.
| Crossref | GoogleScholarGoogle Scholar |
Yang H,
Ryder MH, Tang W
(2005a) Characterisation and identification of Trichoderma isolates from a South Australian soil suppressive to Rhizoctonia solani on wheat. Shandong Science 18, 36–49.
Yang H,
Ryder MH, Tang W
(2005b) Isolation and biocontrol potential of bacteria and actinomycetes from soils suppressive to Rhizoctonia bare-patch disease in South Australia. Shandong Science 18, 68–77.
Zinniel DK,
Lambrecht P,
Harris NB,
Feng Z,
Kuczmarski D,
Higley P,
Ishimaru CA,
Arunakumari A,
Barletta RG, Vidaver AK
(2002) Isolation and characterisation of endophytic colonizing bacteria from agronomic crops and prairie plants. Applied and Environmental Microbiology 68, 2198–2208.
| Crossref | GoogleScholarGoogle Scholar | PubMed |