Rhizosphere biology and crop productivity—a review

M. Watt; J. A. Kirkegaard; J. B. Passioura

doi:10.1071/SR05142

REVIEW (Open Access)

Previous Next Contents Vol 44(4)

Rhizosphere biology and crop productivity—a review

M. Watt ^A ^B , J. A. Kirkegaard ^A and J. B. Passioura ^A

+ Author Affiliations

- Author Affiliations

^A CSIRO Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia.

^B Corresponding author. Email: michelle.watt@csiro.au

Australian Journal of Soil Research 44(4) 299-317 https://doi.org/10.1071/SR05142
Submitted: 15 September 2005 Accepted: 18 April 2006 Published: 27 June 2006

Abstract

There is great potential to use the wide genotypic and agronomically induced diversity of root systems and their exuded chemicals to influence rhizosphere biology to benefit crop production. Progress in the areas of pathogens and symbionts in this regard is clear. Further progress, especially related to interactions with non-pathogenic organisms, will rely on an appreciation of the properties of rhizospheres in the field: the spatial and temporal boundaries of these rhizospheres, and the effects of structural, chemical, and physical soil heterogeneity in which the roots and associated microorganisms exist and function. We consider the rhizosphere environment within Australian cropping systems in relation to the likely success of biological interventions, and provide 3 case studies that highlight the need to characterise the rhizosphere and the microbial interactions therein to capture agronomic benefits. New techniques are available that allow direct visualisation and quantification of rhizosphere processes in field conditions. These will no doubt help develop better genetic and agronomic approaches. Future success, as with those in the past, will rely on integrating interventions related to rhizosphere biology with other management constraints of specific farming systems.

Additional keywords: roots, exudates, soil, microorganisms, agronomy, genetics.

Acknowledgments

This review, and much of the research reported, were supported by the Grains Research and Development Corporation (GRDC) of Australia. We are grateful to Margaret McCully for stimulating research on field-grown roots at CSIRO, Plant Industry, and in Australia via Root and Rhizosphere Workshops. We also thank Rosemary White and the CSIRO Plant Industry Microscopy Centre, and Geoff Howe and the Ginnindera Research Station staff for experimental support. We are grateful to Linda Magee for Figs 2d, 3b, and c and the reference section, to Julianne Lilley for the annual temperature analysis from APSIM in Fig. 3a, and to Alan Richardson for valuable suggestions on the manuscript.

References

Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59, 143–169.
| PubMed |

Angus JF (2001) Nitrogen supply and demand in Australian agriculture. Australian Journal of Experimental Agriculture 41, 277–288.
| Crossref | GoogleScholarGoogle Scholar |

Angus JF, Gardner PA, Kirkegaard JA, Desmarchelier JM (1994) Biofumigation: Isothiocyanates released from Brassica roots inhibit the growth of the take-all fungus. Plant and Soil 162, 107–112.
| Crossref | GoogleScholarGoogle Scholar |

Angus JF, van Herwaarden AF, Howe GN (1991) Productivity and break crop effect of winter-growing oilseeds. Australian Journal of Experimental Agriculture 31, 669–677.
| Crossref | GoogleScholarGoogle Scholar |

Azcón R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytologist 87, 677–685.
| Crossref |

Bais HP, Park S, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends in Plant Science 9, 26–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM (2005) Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434, 217–221.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Barnett SJ, Roget DK, Ryder MH (2006) Suppression of Rhizoctonia solani AG-8 induced disease on wheat by the interaction between Pantoea, Exiguobacterium, and Microbacteria. Australian Journal of Soil Resaerch 44, 331–342.

Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil 256, 67–83.
| Crossref | GoogleScholarGoogle Scholar |

Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist 157, 465–473.
| Crossref | GoogleScholarGoogle Scholar |

Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N, Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: New perspectives for studying microbial communities. Molecular Plant-Microbe Interactions 13, 1170–1176.
| PubMed |

Boelens J, Vande Woestyne M, Verstraete W (1994) Ecological importance of motility for the plant growth-promoting rhizopseudomonas strain ANP15. Soil Biology and Biochemistry 26, 269–277.
| Crossref | GoogleScholarGoogle Scholar |

Borneman J (1999) Culture-independent identification of microorganisms that respond to specified stimuli. Applied and Environmental Microbiology 65, 3398–3400.
| PubMed |

Bouvier T, Del Giorgio PA (2003) Factors influencing the detection of bacterial cells using fluorescence in situ hybridization (FISH): a quantitative review of published reports. FEMS Microbiology Ecology 44, 3–15.
| Crossref | GoogleScholarGoogle Scholar |

Bowen GD (1980) Misconceptions, concepts and approaches in rhizosphere biology. In ‘Contemporary microbial ecology’. (Eds DC Ellwood, JN Hedger, MJ Latham, JM Lynch, JH Slater) pp. 283–304. (Academic Press: New York)

Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbial and Molecular Biology Reviews 69, 155–194.
| Crossref | GoogleScholarGoogle Scholar |

Brockwell J, Bottomley PJ, Thies JE (1995) Manipulation of rhizobia microflora for improving legume productivity and soil fertility: A critical assessment. Plant and Soil 174, 143–180.
| Crossref | GoogleScholarGoogle Scholar |

Burke DW, Miller DE, Barker AW (1980) Effects of soil temperature on growth of beans in relation to soil compaction and fusarium root rot. Phytopathology 70, 1047–1049.

Camper AK, Hayes JT, Sturman PJ, Jones WL, Cunningham AB (1993) Effects of motility and adsorption rate coefficient on transport of bacteria through saturated porous media. Applied and Environmental Microbiology 59, 3455–3462.
| PubMed |

Chan KY, Heenan DP (1996) The influence of crop rotation on soil structure and soil physical properties under conventional tillage. Soil and Tillage Research 37, 113–125.
| Crossref | GoogleScholarGoogle Scholar |

Chan KY, Mead JA, Roberts WP (1987) Poor early growth and yield of wheat under direct drilling. Australian Journal of Agricultural Research 38, 791–800.

Cockroft B, Olsson KA (2000) Degradation of soil structure due to coalescence of aggregates in no-till, no-traffic beds in irrigated crops. Australian Journal of Soil Research 38, 61–70.
| Crossref | GoogleScholarGoogle Scholar |

Cohen Y, Tadmor NH (1969) Effects of temperature on the elongation of seedling roots of some grasses and legumes. Crop Science 9, 189–192.

Connell P , Hooper S (2002) Report of the Australian Agricultural and Grazing Industry Survey of Grain Farms. ABARE, Canberra.

Cresswell HP, Kirkegaard JA (1995) Subsoil amelioration by plant roots – the process and the evidence. Australian Journal of Soil Research 33, 221–239.
| Crossref | GoogleScholarGoogle Scholar |

Darrah PR (1991) Models of the rhizosphere. I. Microbial population dynamics around a root releasing soluble and insoluble carbon. Plant and Soil 133, 187–199.
| Crossref | GoogleScholarGoogle Scholar |

Darrah PR (1998) Interactions between root exudates, mineral nutrition and plant growth. In ‘Inherent variation in plant growth. Physiological mechanisms and ecological consequences’. (Eds H Lambers, H Poorter, MMI Van Vuuren) pp. 159–181. (Backhuys Publishers: The Netherlands)

Darwent MJ, Paterson E, McDonald AJS, Tomos AD (2003) Biosensor reporting of root exudation from Hordeum vulgare in relation to shoot nitrate concentration. Journal of Experimental Botany 54, 325–334.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Davies SL, Peoples MB (2003) Identifying potential approaches to improve the reliability of terminating a lucerne pasture before cropping: a review. Australian Journal of Experimental Agriculture 43, 429–447.
| Crossref | GoogleScholarGoogle Scholar |

Dong Z, Wu L, Kettlewell B, Caldwell CD, Layzell DB (2003) Hydrogen fertilization of soils – is this a benefit of legumes in rotation? Plant, Cell & Environment 26, 1875–1879.
| Crossref | GoogleScholarGoogle Scholar |

Doube BM , Brown GG (1998) Life in a complex community: functional interactions between earthworms, organic matter, microorgansims and plants. In ‘Earthworm ecology’. (Ed. CA Edwards) pp. 179–211. (St Lucie Press: Boca Raton, FL)

Doube BM, Buckerfield JC, Kirkegaard JA (1994) Short-term effects of tillage and stubble management on earthworm populations in cropping systems in southern New South Wales. Australian Journal of Agricultural Research 45, 1587–1600.
| Crossref | GoogleScholarGoogle Scholar |

Duineveld BM, van Veen JA (1999) The number of bacteria in the rhizosphere during plant development: relating colony-forming units to different reference units. Biology and Fertility of Soils 28, 285–291.
| Crossref | GoogleScholarGoogle Scholar |

Elliott LF, Lynch JM (1985) Plant growth-inhibitory pseudomonads colonizing winter wheat (Triticum aestivum L.) roots. Plant and Soil 84, 57–65.
| Crossref | GoogleScholarGoogle Scholar |

Evans LT (1998) ‘Feeding the ten billion: plants and population growth.’ (Cambridge University Press: Cambridge, UK)

Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84, 827–837.

Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition in wheat and barley cultivars. Plant and Soil 191, 181–188.
| Crossref | GoogleScholarGoogle Scholar |

Garbeva P, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annual Review of Phytopathology 42, 243–270.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant and Soil 218, 159–171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Gerhardson B, Alström S, Ramert B (1985) Plant reactions to inoculation of roots with fungi and bacteria. Phytopathologische Zeitschrift 114, 108–117.

Gill JS, Hunt S, Sivasithamparam K, Smettem KRJ (2004) Root growth altered by compaction of a sandy loam soil affects severity of rhizoctonia root rot of wheat seedlings. Australian Journal of Experimental Agriculture 44, 595–599.
| Crossref | GoogleScholarGoogle Scholar |

Gilligan CA (1980) Dynamics of root colonization by the take-all fungus, Gaeumannomyces graminis. Soil Biology and Biochemistry 12, 507–512.
| Crossref | GoogleScholarGoogle Scholar |

Gochnauer MB, McCully ME, Labbe H (1989) Different populations of bacteria associated with sheathed and bare regions of roots of field-grown maize. Plant and Soil 114, 107–120.
| Crossref | GoogleScholarGoogle Scholar |

Gochnauer MB, Sealey LJ, Mccully ME (1990) Do detached root-cap cells influence bacteria associated with maize roots? Plant, Cell & Environment 13, 793–801.
| Crossref |

Graham JH (2000) Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. In ‘Current advances in mycorrhizae research’. (Eds GK Podila, DD Douds) pp. 111–126. (APS Press: St Paul, MN)

Graham JH (2001) What do root pathogens see in mycorrhizas? New Phytologist 149, 357–359.
| Crossref | GoogleScholarGoogle Scholar |

Greaves MP, Darbyshire JF (1972) The ultrastructure of the mucilaginous layer on plant roots. Soil Biology and Biochemistry 4, 443–449.
| Crossref | GoogleScholarGoogle Scholar |

Grose MJ, Gilligan CA, Spencer D, Goddard BVD (1996) Spatial heterogeneity of soil water around single roots: use of CT-scanning to predict fungal growth in the rhizosphere. New Phytologist 133, 261–272.
| Crossref |

Gupta VVSR (1994) The impact of soil and crop management practice on the dynamics of soil microfauna and mesofauna. In ‘Soil biota. Management in sustainable farming systems’. (Eds CE Pankhurst, BM Doube, VVSR Gupta, PR Grace) pp. 107–124. (CSIRO Publishing: Melbourne)

Gupta VVSR , Roget DK , Coppi JA (2004) Identification of a previously unrecognized biological constraint to yield in sequential wheat crops. In ‘Proceedings of the 3rd Australasian Soilborne Disease Symposium’. Adelaide. (Eds K Ophel Keller, B Hall) pp. 13–14. (SARDI: Adelaide)

Hansel CM, Fendorf S, Sutton S, Newville M (2001) Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science & Technology 35, 3863–3868.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogenity arising from root-mediated physical and chemical processes. New Phytologist 168, 293–303.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Hodda M , Stewart E , FitzGibbon F , Reid I , Longstaff BC , Packer I (1997) The identification of free-living soil-dwelling nematode assemblages as indicators of sustainable soil use. RIRDC Project Report CSE-73A, Canberra.

Huisman OC (1982) Interrelations of root growth dynamics to epidemiology of root-invading fungi. Annual Review of Phytopathology 20, 303–327.
| Crossref | GoogleScholarGoogle Scholar |

Husain SS, McKeen WE (1963) Interactions between strawberry roots and Rhizoctonia fragariae. Phytopathology 53, 541–545.

Iijima M, Griffiths B, Bengough AG (2000) Sloughing of cap cells and carbon exudation from maize seedling roots in compacted sand. New Phytologist 145, 477–482.
| Crossref | GoogleScholarGoogle Scholar |

Jaeger C, Lindow S, Miller S, Clark E, Firestone M (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Applied and Environmental Microbiology 65, 2685–2690.
| PubMed |

Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria and Verrucomicrobia. Applied and Environmental Microbiology 68, 2391–2396.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Johnson MJ, Lee KY, Scow KM (2003) DNA fingerprinting reveals links among agricultural crops, soil properties, and the composition of soil microbial communities. Geoderma 114, 279–303.
| Crossref | GoogleScholarGoogle Scholar |

Johnson SN, Read DB, Gregory PJ (2004) Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecological Entomology 29, 117–122.
| Crossref | GoogleScholarGoogle Scholar |

Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459–480.
| Crossref | GoogleScholarGoogle Scholar |

Joseph CA, Phillips DA (2003) Metabolites from soil bacteria affect plant water relations. Plant Physiology and Biochemistry 41, 189–192.
| Crossref | GoogleScholarGoogle Scholar |

Keel C, Schnider U, Maurhofer M, Voisard C, Laville J, Burger U, Wirthner P, Haas D, Defago G (1992) Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Molecular Plant-Microbe Interactions 5, 4–13.

Khan DF , Herridge DF , Schwenke GD , Chen D , Peoples MB (2001) The application of ¹⁵N-shoot labelling techniques to field-grown crops to study the decomposition and fate of shoot or root residue N in a legume-cereal rotation. In ‘11th Nitrogen Workshop Book of Abstracts’. pp. 121–122. (INRA: France)

Kirkegaard JA (1995) A review of trends in wheat yield responses to conservation cropping in Australia. Australian Journal of Experimental Agriculture 35, 835–848.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA, Gardner PA, Angus JF, Koetz E (1994) Effect of Brassica break crops on the growth and yield of wheat. Australian Journal of Agricultural Research 45, 529–545.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA , Gardner PA , Desmarchelier JM , Angus JF (1993) Biofumigation – using Brassica species to control pests and diseases in horticulture and agriculture. In ‘Proceedings of the 9th Australian Research Assembly on Brassicas’. Wagga Wagga, NSW. (Eds N Wratten, R Mailer) pp. 77–82. (NSW Agriculture)

Kirkegaard JA, Howe GN, Mele P (1999a) Enhanced accumulation of mineral-N following canola. Australian Journal of Experimental Agriculture 39, 587–593.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA , Howe GN , Simpfendorfer S , Angus JF , Gardner PA , Hutchinson P (2001) Poor wheat yield response to conservation cropping—causes and consequences during 10 years of the Harden tillage trial. In ‘Proceedings of the 10th Australian Agronomy Conference’. Hobart, Tas. (The Australian Agronomy Society)

Kirkegaard JA, Munns R, James RA, Gardner PA, Angus JF (1995) Reduced growth and yield of wheat with conservation cropping. 2. Soil biological factors limit growth under direct drilling. Australian Journal of Agricultural Research 46, 75–88.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA, Munns R, James RA, Neate SM (1999b) Does water and phosphorus uptake limit leaf growth of Rhizoctonia-infected wheat seedlings? Plant and Soil 209, 157–166.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA, Sarwar M, Wong PTW, Mead A, Howe G, Newell M (2000) Field studies on the biofumigation of take-all by Brassica break crops. Australian Journal of Agricultural Research 51, 445–456.
| Crossref | GoogleScholarGoogle Scholar |

Kirkegaard JA, Simpfendorfer S, Holland J, Bambach R, Moore KJ, Rebetzke GJ (2004) Effect of previous crops on crown rot and yield of durum and bread wheat in northern NSW. Australian Journal of Agricultural Research 55, 321–334.
| Crossref | GoogleScholarGoogle Scholar |

Leach LD (1947) Growth rates of host and pathogen as factors determining the severity of preemergence damping-off. Journal of Agricultural Research 75, 161–179.

Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytologist 168, 189–204.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Letey J, Sojka RE, Upchurch DR, Cassel DK, Olson KR, Payne WA, Petrie SE, Price GH, Reginato RJ, Scott HD, Smethurst PJ, Triplett GB (2003) Deficiencies in the soil quality concept and its application. Journal of Soil and Water Conservation 58, 180–187.

Liljeroth E, Burgers SLGE, van Veen JA (1991) Changes in bacterial populations along roots of wheat (Triticum aestivum L.) seedlings. Biology and Fertility of Soils 10, 276–280.
| Crossref | GoogleScholarGoogle Scholar |

Longstaff BC , Greenslade PJM , Colloff M , Reid I , Hart P , Packer I (1999) The impact of soil tillage practice on soil fauna in the NSW wheatbelt. RIRDC Report 99/18, Canberra.

Lyon D , Bruce SE , Vyn T , Peterson G (2004) Achievements and future challenges in conservation tillage. In ‘Proceedings of the 4th International Crop Science Congress’. Brisbane, Qld. www.cropscience.org.au

Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biology and Biochemistry 33, 1437–1445.
| Crossref | GoogleScholarGoogle Scholar |

Matiru VN, Dakora FD (2005) The rhizosphere signal molecule lumichrome alters seedling development in both legumes and cereals. New Phytologist 166, 439–444.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Matthiessen JN, Warton B, Shackleton MA (2004) The importance of plant maceration and water addition in achieving high Brassica-derived isothiocyanate levels in soil. Agroindustria 3, 277–280.

Mazzola M, Funnell DL, Raaijmakers JM (2004) Wheat cultivar-specific selection of 2,4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microbial Ecology 48, 338–348.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

McCully ME (1999) Roots in soil: Unearthing the complexities of roots and their rhizospheres. Annual Review of Plant Physiology and Plant Molecular Biology 50, 695–718.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

McCully ME (2001) Niches for bacterial endophytes in crop plants: a plant biologist’s view. Australian Journal of Plant Physiology 28, 983–990.

McCully ME, Canny MJ (1985) Localisation of translocated 14C in roots and root exudates of field-grown maize. Physiologia Plantarum 65, 380–392.
| Crossref |

McNeill A , Unkovich M , Zhu C , Pinchand T (1999) The N benefit from above-ground and below-ground legume crop residues. In ‘Proceedings of the 12th Australian Nitrogen Fixation Conference’. Wagga Wagga, NSW. (The Australian Society for Nitrogen Fixation)

Merbach W, Mirus E, Knof G, Remus R, Ruppel S, Russow R, Gransee A, Schulze J (1999) Release of carbon and nitrogen compounds by plant roots and their possible ecological importance. Journal of Plant Nutrition and Soil Science 162, 373–383.
| Crossref | GoogleScholarGoogle Scholar |

Miki NK, Clarke KJ, McCully ME (1980) A histological and histochemical comparison of the mucilages on the root tips of several grasses. Canadian Journal of Botany 58, 2581–2593.

Miller HJ., Liljeroth E, Henken G, van Veen JA (1990) Fluctuations in the fluorescent pseudomonad and actinomycete populations of the rhizosphere and rhizoplane during the growth of spring wheat. Canadian Journal of Microbiology 36, 254–258.

Morra MJ, Kirkegaard JA (2002) Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biology and Biochemistry 34, 1683–1690.
| Crossref | GoogleScholarGoogle Scholar |

Nagahashi G, Douds DD (2004) Isolated root caps, border cells, and mucilage from host roots stimulate hyphal branching of the arbuscular mycorrhizal fungus, Gigaspora gigantea. Mycological Research 108, 1079–1088.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Neal JL, Larson RI, Atkinson TG (1973) Changes in rhizosphere populations of selected physiological groups of bacteria related to substitution of specific pairs of chromosomes in spring wheat. Plant and Soil 39, 209–212.
| Crossref | GoogleScholarGoogle Scholar |

Nelson DR, Mele PM (2006) The impact of crop residue amendments and lime on microbial community structure and nitrogen-fixing bacteria in the wheat rhizosphere. Australian Journal of Soil Research 44, 319–329.

Newman EI, Watson A (1977) Microbial abundance in the rhizosphere: A computer model. Plant and Soil 48, 17–56.
| Crossref | GoogleScholarGoogle Scholar |

van Noordwijk M, de Ruiter PC, Zwart KB, Bloem J, Moore JC, van Faassen HG, Burgers SLGE (1993) Synlocation of biological activity, roots, cracks and recent organic inputs in a sugar beet field. Geoderma 56, 265–276.
| Crossref | GoogleScholarGoogle Scholar |

O’Connell KP, Goodman RM, Handelsman J (1996) Engineering the rhizosphere: expressing a bias. Trends in Biotechnology 170, 6–10.

Olsson S, Persson P (1999) The composition of bacterial populations in soil fractions differing in their degree of adherence to barley roots. Applied Soil Ecology 12, 205–215.
| Crossref | GoogleScholarGoogle Scholar |

Pahlavian AM, Silk WK (1988) Effect of temperature on spatial and temporal aspects of growth in the primary maize root. Plant Physiology 87, 529–532.
| PubMed |

Pankhurst CE, McDonald HJ, Hawke BG, Kirby CA (2002) Effect of tillage and stubble management on chemical and microbiological properties, and the development of suppression towards cereal root disease, in soils from two sites in NSW, Australia. Soil Biology and Biochemistry 34, 833–840.
| Crossref | GoogleScholarGoogle Scholar |

Pierret A, Moran CJ, Pankhurst CE (1999) Differentiation of soil properties related to the spatial association of wheat roots and soil macropores. Plant and Soil 211, 51–58.
| Crossref | GoogleScholarGoogle Scholar |

Pietikäinen J, Pettersson M, Baath E (2005) Comparison of temperature effects on soil respiration and bacterial and fungal growth rates. FEMS Microbiology Ecology 52, 49–58.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Prosser JI (2002) Molecular and functional diversity in soil micro-organisms. Plant and Soil 244, 9–17.
| Crossref | GoogleScholarGoogle Scholar |

Refshauge S, Watt M, McCully ME, Huang CX (2006) Frozen in time: A new method using cryo-SEM to visualise root-fungal interactions. New Phytologist In press ,
| Crossref | GoogleScholarGoogle Scholar |

Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytologist 168, 305–312.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Rumberger A, Marschner P (2003) 2-phenylethylisothiocyanate concentration and microbial community composition in the rhizosphere of canola. Soil Biology and Biochemistry 35, 445–452.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant and Soil 250, 225–239.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and Soil 244, 263–271.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, van Herwaarden AF, Angus JF, Kirkegaard JA (2005) Colonisation by arbuscular mycorrhizal fungi is associated with reductions in biomass of wheat in a low-P soil under field conditions. Plant and Soil 270, 275–286.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Kirkegaard JA, Angus JF (2006) Nitrogen mineralisation in relation to previous crops and pasture. Australian Journal of Soil Research 44, 367–377.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, McCully ME, Huang CX (2003) Location and quantification of phosphorus and other elements in fully-hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytologist 160, 429–441.
| Crossref | GoogleScholarGoogle Scholar |

Ryan MH, Norton RM, Kirkegaard JA, McCormick KM, Knights SE, Angus JF (2002) Increasing mycorrhizal colonisation does not improve growth and nutrition of wheat on Vertosols in south-eastern Australia. Australian Journal of Agricultural Research 53, 1173–1181.
| Crossref | GoogleScholarGoogle Scholar |

Sarwar M, Kirkegaard JA, Wong PTW, Desmarchelier JM (1998) Biofumigation potential of brassicas. III. In vitro toxicity of isothiocyanates to soil-borne fungal pathogens. Plant and Soil 201, 103–112.
| Crossref | GoogleScholarGoogle Scholar |

Schönhammer A, Fischbeck G (1987) Investigations on cereal crop rotations and monocultures. III Changes in soil properties. Bayerisches Landwirtschaftliches Jahrbuch 64, 681–694.

Schroth MN, Hildebrand DC (1964) Influence of plant exudates on root-infecting fungi. Annual Review of Phytopathology 2, 101–132.
| Crossref | GoogleScholarGoogle Scholar |

Scott EM, Rattray EAS, Prosser JI, Killham K, Glover LA, Lynch JM, Bazin MJ (1995) A mathematical model for dispersal of bacterial inoculants colonizing the wheat rhizosphere. Soil Biology and Biochemistry 27, 1307–1318.
| Crossref | GoogleScholarGoogle Scholar |

Sharma A, Sahgal M, Johri BN (2003) Microbial communication in the rhizosphere: operation of quorum sensing. Current Science 85, 1164–1172.

Simons M, van der Bij AJ, Brand I, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Molecular Plant-Microbe Interactions 9, 600–607.
| PubMed |

Simpfendorfer S, Kirkegaard JA, Heenan DP, Wong PTW (2001) Involvement of root inhibitory Pseudomonas spp. in the poor early growth of direct drilled wheat: studies in intact cores. Australian Journal of Agricultural Research 52, 845–853.
| Crossref | GoogleScholarGoogle Scholar |

Simpfendorfer S, Kirkegaard JA, Heenan DP, Wong PTW (2002) Reduced early growth of direct drilled wheat in southern New South Wales—role of root inhibitory pseudomonads. Australian Journal of Agricultural Research 53, 323–331.
| Crossref | GoogleScholarGoogle Scholar |

Sivasithamparam K, Parker CA (1979) Rhizosphere micro-organisms of seminal and nodal roots of wheat grown in pots. Soil Biology and Biochemistry 11, 155–160.
| Crossref | GoogleScholarGoogle Scholar |

Smiley RW, Wilkins DE (1992) Impact of sulfonylurea herbicides on Rhizoctonia root rot, growth, and yield of winter wheat. Plant Disease 76, 399–404.

Smith BJ, Kirkegaard JA (2002) In vitro inhibition of soil microorganisms by 2-phenylethyl isothiocyanate. Plant Pathology 51, 585–593.
| Crossref | GoogleScholarGoogle Scholar |

Smith BJ, Kirkegaard JA, Howe GN (2004) Impacts of Brassica break crops on soil biology and yield of following wheat crops. Australian Journal of Agricultural Research 55, 1–11.
| Crossref | GoogleScholarGoogle Scholar |

Smith BJ , Sarwar M , Wong PTW , Kirkegaard JA (1999) Suppression of cereal pathogens by canola root tissues in soil. In ‘Proceedings of the 10th International Rapeseed Congress’. Canberra, ACT. (Eds PA Salisbury, TD Potter, G McDonald, AG Green) (CD-ROM)

Steed GR , Ellington A , Pratley JE (1993) Conservation tillage in the south-eastern Australian wheat-sheep belt. In ‘Conservation tillage in temperate agroecosystems’. (Ed. MR Carter) pp. 231–251. (Lewis Publishers: Boca Raton, FL)

Steidle A, Sigl K, Schuhegger R, Ihring A, Schmid M, Gantner S, Stoffels M, Riedel K, Givskov M, Hartmann A, Langebartels C, Eberl L (2001) Visualization of N-acylhomoserine lactone-mediated cell–cell communication between bacteria colonizing the tomato rhizosphere. Applied and Environmental Microbiology 67, 5761–5770.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Stewart A (2001) Commercial biocontrol—reality or fantasy? Australasian Plant Pathology 30, 127–131.
| Crossref | GoogleScholarGoogle Scholar |

Stirzaker RJ, Passioura JB, Wilms Y (1996) Soil structure and plant growth: Impact of bulk density and biopores. Plant and Soil 185, 151–162.
| Crossref | GoogleScholarGoogle Scholar |

Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviours in associated bacteria. Molecular Plant-Microbe Interactions 13, 637–648.
| PubMed |

Thompson JP (1987) Decline of vesicular-arbuscular mycorrhizas in long fallow disorder of field crops and its expression in phosphorus deficiency in sunflower. Australian Journal of Agricultural Research 38, 847–867.
| Crossref | GoogleScholarGoogle Scholar |

Thompson JP , Owen KJ , Clewett TG (2001) Pre-cropping with canola decreases vesicular-arbuscular mycorrhiza and growth of wheat in low P soil. In ‘Proceedings of the 2nd Australasian Soil-Borne Root Disease Symposium’. Lorne, Vic. pp. 150–151.

Wang Y-J, Leadbetter JR (2005) Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Applied and Environmental Microbiology 71, 1291–1299.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Watt M, Hugenholtz P, White R, Vinall K (2006a) Numbers and locations of native bacteria on field grown wheat roots quantified by fluorescence in situ hybridization (FISH). Environmental Microbiology 8, 871–884.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Watt M, Kirkegaard JA, Rebetzke GJ (2005) A wheat genotype developed for rapid leaf growth copes well with the physical and biological constraints of unploughed soil. Functional Plant Biology 32, 695–706.
| Crossref | GoogleScholarGoogle Scholar |

Watt M, McCully ME, Canny MJ (1994) Formation and stabilisation of maize rhizosheaths: Effect of soil water content. Plant Physiology 106, 179–186.
| PubMed |

Watt M, McCully ME, Jeffree CE (1993) Plant and bacterial mucilages of the maize rhizosphere: Comparison of their soil binding properties and histochemistry in a model system. Plant and Soil 151, 151–165.
| Crossref | GoogleScholarGoogle Scholar |

Watt M, McCully ME, Kirkegaard JA (2003) Soil strength and rate of rot elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat. Functional Plant Biology 30, 483–491.
| Crossref | GoogleScholarGoogle Scholar |

Watt M, Silk WK, Passioura JP (2006b) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97, 839–855.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

West ES (1952) A study of the annual soil temperature wave. Australian Journal of Scientific Research 5, 303–314.
| PubMed |

Wheal MS, Rengel Z, Graham RD (1998) Chlorsulfuron reduces extension of wheat root tips in low-zinc solution culture. Annals of Botany 81, 385–389.
| Crossref | GoogleScholarGoogle Scholar |

Williams CH , Andrew CS (1970) Mineral Nutrition of Pastures. In ‘Australian grasslands’. (Ed. RM Moore) pp. 321–338. (ANU Press: Canberra)

Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biology and Fertility of Soils 31, 249–253.
| Crossref | GoogleScholarGoogle Scholar |

Zelenev VV, van Bruggen AHC, Semenov AM (2000) ‘BACWAVE’, a spatial-temporal model for travelling waves of bacterial populations in response to a moving carbon source in soil. Microbial Ecology 40, 260–272.
| PubMed |