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RESEARCH ARTICLE
Contents Vol 60(2)

Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere

P. R. Harvey A C , R. A. Warren A and S. Wakelin B
+ Author Affiliations
- Author Affiliations

A CSIRO Entomology, PMB 2, Glen Osmond, SA 5064, Australia.

B CSIRO Land and Water, PMB 2, Glen Osmond, SA 5064, Australia.

C Corresponding author. Email: Paul.Harvey@csiro.au

Crop and Pasture Science 60(2) 144-151 https://doi.org/10.1071/CP08084
Submitted: 30 March 2008  Accepted: 2 October 2008   Published: 27 February 2009

Abstract

Phosphate anions in soil solution are extremely reactive and may be rapidly immobilised in the soil through precipitation and adsorption reactions, resulting in sparingly soluble forms of phosphorus (P) that are essentially unavailable to plants. This low P-fertiliser efficiency is often offset through high application rates, which are economically and environmentally unsustainable and not an available option for organic producers. Microorganisms play a fundamental role in the biogeochemical cycling of inorganic and organic P in the rhizosphere and detritusphere. Free-living rhizosphere microbes can directly increase the availability of phosphate to plant roots via mechanisms associated with solubilisation and mineralisation of P from inorganic and organic forms of total soil P. These include releasing organic anions, H+ ions, phosphatases, and cation chelating compounds into the rhizosphere. Many soil-borne microbes also increase P availability indirectly by producing phytohormones that increase root density and function. There is increasing interest worldwide in the use of rhizosphere microorganisms as inoculants to increase P availability for agricultural production. Recent research has focussed on developing actively sporulating Penicillium fungi known to express mechanisms to enhance P mobilisation and therefore, considered to be a key component of the mycoflora involved in P cycling in soils. Penicillium species do not exhibit specific plant or soil associations and have a broad agro-ecological range, indicating their potential to be developed as inoculants for a range of plant production systems. Successful adoption of microbial inoculants requires a thorough understanding of their rhizosphere ecology, genetic stability, and the mechanisms associated with enhancing P availability in soils and plant-growth promotion. This will provide a better understanding of which inoculants to use under particular agro-ecological conditions for increased efficacy and consistent performance.


References


Achouak W, Thiéry JM, Roubaud P, Heulin T (2000) Impact of crop management on intraspecific diversity of Pseudomonas corrugata in bulk soil. FEMS Microbiology Ecology 31, 11–19.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295-22. Applied and Environmental Microbiology 65, 2926–2933.
|  CAS | PubMed |
open url image1

Anderson G (1980) Assessing organic phosphorus in soils. In ‘The role of phosphorus in agriculture’. (Eds FE Khasawneh, EC Sample, EJ Kamprath) pp. 411–432. (American Society of Agronomy: Madison, WI)

Anderson IC, Cairney JWG (2004) Diversity and ecology of soil fungal communities: increasing understanding through the application of molecular techniques. Environmental Microbiology 6, 769–779.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Anstis ST (2004) Penicillium radicum: Studies on the mechanisms of plant growth promotion in wheat. PhD Thesis, Adelaide University, Australia.

Asea PEA, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilisation by two Penicillium species in solution culture and soil. Soil Biology & Biochemistry 20, 459–464.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant and Soil 287, 51–58.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Babu-Khan S, Yeo TC, Martin WL, Duron MR, Rogers RD, Goldstein AH (1995) Cloning of a mineral phosphate-solubiliizing gene from Pseudomonas cepacia. Applied and Environmental Microbiology 61, 972–978.
|  CAS | PubMed |
open url image1

Beckie HJ, Schlechte D, Moulin AP, Gleddie SC, Pulkinen DA (1998) Response of alfalfa to inoculation with Penicillium bilaii (Provide). Canadian Journal of Plant Science 78, 91–102. open url image1

Bertrand I, Holloway RE, Armstrong RD, McLaughlin MG (2003) Chemical characteristics of phosphorus in alkaline soils from southern Australia. Australian Journal of Soil Research 41, 61–76.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bowen GD, Rovira AD (1991) The rhizosphere: the hidden half of the hidden half. In ‘Plant roots: the hidden half’. (Eds Y Waisel, A Eshel, U Kafkafi) pp. 641–669. (Marcel Dekker: New York)

Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Advances in Agronomy 66, 1–102.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Chambers JW, Yeomans JC (1990) The influence of PB-50 (Penicillium bilaji inoculant) on yield and phosphorus uptake by wheat. Proceedings of the Annual Manitoba Society of Soil Science 33, 283–293. open url image1

Costa R, Falcão Salles J, Berg G, Smalla K (2006) Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environmental Microbiology 8, 2136–2149.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dalal RC (1977) Soil organic phosphorus. Advances in Agronomy 29, 85–117. open url image1

de la Fuente JM, Ramírez-Rodrígez V, Cabrera-Ponce JL, Herera-Estrella L (1997) Aluminium tolerance in transgenic plants by alteration of citrate synthesis. Science 276, 1566–1568.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Delhaize E, Ryan PR, Hocking PJ, Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations and citrate efflux from tobacco (Nicotiana tabacum L.) roots. Plant and Soil 248, 137–144.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Downey J, van Kessel C (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji. Biology and Fertility of Soils 10, 194–196. open url image1

Edel V, Steinberg C, Gautheron N, Alabouvette C (1997) Populations of non-pathogenic Fusarium oxysporum associated with roots of four plant species compared to soil populations. Phytopathology 87, 693–697.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Edel-Hermann V, Gautheron N, Alabouvette C, Steinberg C (2008) Fingerprinting methods to approach multitrophic interactions among microflora and microfauna communities in soil. Biology and Fertility of Soils 44, 975–984.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

El-Tarabily KA, Nassar AH, Sivasithamparam K (2008) Promotion of growth of bean (Phaseolus vulgaris L.) in a calacareous soil by a phosphate-solubilizing, rhizosphere-competent isolate of Micromonospora endolithica. Applied Soil Ecology 39, 161–171.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Foster R (1986) The ultrastructure of the rhizoplane and the rhizosphere. Annual Review of Phytopathology 24, 211–234.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Fromin N, Achouak W, Thiéry JM, Heulin T (2001) The genotypic diversity of Pseudomonas brassicacearum populations isolated from roots of Arabidopsis thaliana: influence of plant genotype. FEMS Microbiology Ecology 37, 21–29.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gadd GM (1999) Fungal production of citric and oxalic acid: importance in metal speciation, physiology and biogeochemical processes. Advances in Microbial Physiology 41, 47–92.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Gerretsen FC (1948) The influence of microorganisms on the phosphate intake by the plant. Plant and Soil 1, 51–81.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gleddie SC (1993) Response of pea and lentil to inoculation with the phosphate-solubilizing fungus Penicillium bilaii (PROVIDE™). In ‘Proceedings of the Soils and Crops Workshop’. Saskatoon, Saskatchewan. pp. 47–52.

Gulden RH, Vessey JK (2000) Penicillium bilaii inoculation increases root hair production in field pea. Canadian Journal of Plant Science 80, 801–804. open url image1

Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant and Soil 245, 83–93.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Harvey PR, Butterworth PJ, Hawke BG, Pankhurst CE (2001a) Genetic and pathogenic variation among cereal, medic and sub-clover isolates of Pythium irregulare. Mycological Research 105, 85–93.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Harvey PR, Langridge P, Marshall DR (2001b) Genetic drift and host-mediated selection cause genetic differentiation among Gaeumannomyces graminis populations infecting cereals in southern Australia. Mycological Research 105, 927–935.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Harvey PR, Warren RA, Achouak W, Ryder MH (2005) Geographic differentiation of Pseudomonas brassicacearum populations and bio-control of take-all disease of wheat and Pythium root rot of canola. Shandong Science 18, 50–61. open url image1

Haugland RA, Varma M, Wymer LJ, Vesper SJ (2004) Quantitative PCR analysis of selected Aspergillus, Penicillium and Paecilomyces species. Systematic and Applied Microbiology 27, 198–210.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hawes MC, Brigham LA, Woo HH, Wen F (1996) Root border cells. In ‘Biology of plant–microbe interactions’. (Eds G Stacey, B Mallin, P Gresshoff) pp. 509–514. (International Society for Molecular Plant-Microbe Interactions: St Paul, MN)

Hocking AD, Whitelaw M, Harden TJ (1998) Penicillium radicum sp. nov. from the rhizosphere of Australian wheat. Mycological Research 102, 801–806.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Holford ICR (1997) Soil phosphorus, its measurements and its uptake by plants. Australian Journal of Soil Research 35, 227–239.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Illmer P, Schinner F (1995) Solubilization of calcium-phosphates—solubilisation mechanisms. Soil Biology & Biochemistry 27, 257–263.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere microorganisms and plant phosphorus uptake. In ‘Phosphorus, agriculture and the environment’. (Eds JT Sims, AN Sharpley) pp. 437–494. (American Society for Agronomy: Madison, WI)

Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant and Soil 205, 25–44.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Koyama H, Kawamura A, Kihara T, Hara T, Tikita E, Shibata D (2000) Over expression of mitochondrial citrate synthetase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant & Cell Physiology 41, 1030–1037.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kucey RMN (1983) Phosphate-solubilizing bacteria and fungi in various cultivated and virgin Alberta soils. Canadian Journal of Soil Science 63, 671–678.
|  CAS |
open url image1

Kucey RMN (1987) Increased phosphorus uptake by wheat and field beans inoculated with a phosphorus-solubilizing Penicillium bilaji strain and with vesicular-arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 53, 2699–2703.
|  CAS | PubMed |
open url image1

Kucey RMN (1988) Effect of Penicillium bilaji on solubility and uptake of P and micronutrients from soil by wheat. Canadian Journal of Soil Science 68, 261–270.
|  CAS |
open url image1

Kucey RMN, Janzen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Advances in Agronomy 42, 199–228.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kucey RMN, Leggett ME (1989) Increased yields and phosphorus uptake by Westar canola (Brassica napus L.) inoculated with a phosphate-solubilizing isolate of Penicillium bilaji. Canadian Journal of Soil Science 69, 425–432. open url image1

Latour X, Corberand T, Laguerre G, Allard F, Lemanceau P (1996) The composition of fluorescent pseudomonad population associated with roots is influenced by plant and soil type. Applied and Environmental Microbiology 62, 2449–2456.
|  CAS | PubMed |
open url image1

Lemanceau P, Corberand T, Gardan L, Latour X, Laguerre G, Boeufgras J-M, Alabouvette C (1995) Effects of two plant species, flax (Linum usitatissimum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Applied and Environmental Microbiology 61, 1004–1012.
|  CAS | PubMed |
open url image1

López-Bucio J, de la Vega OM, Guevara-Garcia A, Herera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnology 18, 450–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lukow T, Dunfield PF, Liesak W (2000) Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiology Ecology 32, 241–247.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lung S, Chan W, Yip WK, Wang L, Yeung EC, Lim BL (2005) Secretion of beta-propeller phytase from tobacco and Arabidopsis roots enhances phosphorus utilisation. Plant Science 169, 341–349.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Mazzola M, Gu Y-H (2000) Impact of wheat cultivation on microbial communities from replant soils and apple growth in greenhouse trials. Phytopathology 90, 114–119.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

McLaughlin MJ, Baker TG, James TR, Rundle JA (1990) Distribution of forms of phosphorus and aluminium in acidic topsoils under pastures in south-eastern Australia. Australian Journal of Soil Research 28, 371–385.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Naef A, Senatore M, Defago G (2006) A microsatellite based method for quantification of fungi in decomposing plant material elucidates the role of Fusarium graminearum DON production in the saprophytic competition with Trichoderma atroviride in maize tissue microcosoms. FEMS Microbiology Ecology 55, 211–220.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martínez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubiliizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biology & Biochemistry 33, 103–110.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rashid A, Ryan J (2004) Micronutrient constraints to crop production in soils with Mediterranean-type characteristics: a review. Journal of Plant Nutrition 27, 959–975.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rice WA, Lupwayi NZ, Olsen PE, Schlechte D, Gleddie SC (2000) Field evaluation of dual inoculation of alfalfa with Sinorhizobium meliloti and Penicillium bilaii. Canadian Journal of Plant Science 80, 303–308. open url image1

Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Australian Journal of Plant Physiology 28, 897–906. open url image1

Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas spp. that utilise inositol phosphates. Canadian Journal of Microbiology 43, 509–516.
|  CAS | PubMed |
open url image1

Richardson AE, Hadobas PA, Hayes JE (2001a) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. The Plant Journal 25, 641–649.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Richardson AE, Hadobas PA, Hayes JE, O’Hara CP, Simpson RJ (2001b) Utilisation of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil microorganisms. Plant and Soil 229, 47–56.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilisation and its potential applications for improving plant growth-promoting bacteria. Plant and Soil 287, 15–21.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Sanyal SK, De Datta SK (1991) Chemistry of phosphorus transformations in soil. Advances in Soil Science 16, 1–50.
|  CAS |
open url image1

Seeling B, Jungk A (1996) Utilization of organic phosphorus in calcium chloride extracts of soil by barley plants and hydrolysis by acid and alkaline phosphatases. Plant and Soil 178, 179–184.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Smith SE, Read DJ (1997) ‘Mycorrhizal symbiosis.’ (Academic Press: San Diego, CA)

Tang J, Leung A, Leung C, Lim BL (2006) Hydrolysis of precipitated Phytate by three distinct families of phytases. Soil Biology and Biochemistry 38, 1316–1324.
|  CAS | Crossref |
open url image1

Tunney H, Carton OT, Brookes PC, Johnson AE (1997) ‘Phosphorus loss from soil to water.’ (CAB International: Oxford, UK)

Turner BL, Paphazy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 449–469.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Tye AJ, Siu KY, Leung YC, Lim BL (2002) Molecular cloning and the biochemical characterisation of two novel phytases from B. subtilis 168 and B. licheniformis. Applied Microbiology and Biotechnology 59, 190–197.
|  CAS | PubMed |
open url image1

Ullah AH, Sethumadhavan K, Mullaney EJ, Ziegelhoffer T, Austin-Phillips S (2002) Cloned and expressed fungal phyA gene in Alfalfa produces a stable phytase. Biochemical and Biophysical Research Communications 290, 1343–1348.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Van Veen JA, Leonard S, van Overbeek LS, Van Elsas JD (1997) Fate and activity of micro-organisms introduced into soil. Microbiology and Molecular Biology Reviews 61, 121–135.
|  CAS | PubMed |
open url image1

Vessey JK, Heisinger KG (2001) Effect of Penicillium bilaii inoculation and phosphorus fertilization on root and shoot parameters of field grown pea. Canadian Journal of Plant Science 81, 361–366. open url image1

Wakelin S, Colloff M, Harvey PR, Marschner P, Gregg AL, Rogers SL (2007a) The effects of stubble retention and nitrogen application on microbial community structure and functional gene abundance under irrigated maize. FEMS Microbiology Ecology 59, 661–670.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wakelin SA, Gupta VVSR, Harvey PR, Ryder MH (2007b) The effect of Penicillium fungi on plant growth and P mobilisation in neutral to alkaline soils from southern Australia. Canadian Journal of Microbiology 53, 106–115.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004b) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biology and Fertility of Soils 40, 36–43.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wakelin SA, Warren RA, Ryder MH (2004a) Effect of soil properties on growth promotion of wheat by Penicillium radicum. Australian Journal of Soil Research 42, 897–904.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Advances in Agronomy 69, 99–151.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Whitelaw MA, Harden TJ, Bender GL (1997) Plant growth promotion of wheat inoculated with Penicillium radicum sp. nov. Australian Journal of Soil Research 35, 291–300.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biology & Biochemistry 31, 655–665.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Xiao K, Harrison MJ, Wang ZY (2005) Transgenic expression of a novel M. truncatula phytase gene results in improved acquisition of organic phosphorus by Arabidopsis. Planta 222, 27–36.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Xu J (2006) microbial ecology in the age of genomics and metagenomics: concepts, tools and recent advances. Molecular Ecology 15, 1713–1731.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Yadav RS, Tarafdar JC (2003) Phytase and phosphatase producing fungi in arid and semi-arid soils and their efficiency in hydrolyzing different organic P compounds. Soil Biology & Biochemistry 35, 745–751.
| Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Yergeau E, Filion M, Vujanovic V, St-Arnaud M (2005) A PCR-denaturing gradient gel electrophoresis approach to assess Fusarium diversity in asparagus. Journal of Microbiological Methods 60, 143–154.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1