The root–microbe–soil interface: new tools for sustainable plant production

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Ever increasing global food production targets continue to be met through advances in such diverse fields as plant breeding, mineral fertilizer/pesticide chemistry and agricultural engineering. Commercialisation of developments in these and emergent biotechnologies, such as transgenics, and their successful incorporation into modern agricultural practice have helped to deliver the necessary increases in crop yield and productivity. Yet high levels of plant diversity and productivity are maintained in native grassland and tropical or boreal forest ecosystems in the absence of major human intervention. When viewed from an above-ground ecophysiological perspective, the reasons for this apparent paradox have remained enigmatic even after decades of investigation. However, answers are now being uncovered through the study of associations between plant roots and key members of the soil microbiota, namely, bacteria, fungi and microfauna (Watkinson, 1998; Copley, 2000; Bradford et al., 2002).

Progress at relevant scales

Reviews in this issue not only highlight the diversity of plant–soil–microbe combinations and root associations under investigation, but also showcase rapid advances being made at gene, organismal and ecosystem scales (see also other related New Phytologist features: Martin, 2001; Sprent, 2002). Bever (pp. 465–473) presents a detailed analysis of empirical studies to further support his earlier proposal on the roles of host–microbe specificity- and microbial community-linked feedback mechanisms in controlling plant diversity and productivity. Both positive and negative feedback has been identified but underlying mechanisms still need to be elucidated for a better prediction of outcomes in different plant and soil microbial community settings. Organic nutrient (particularly nitrogen and phosphorus) mobilising activities of root symbiotic mycorrhizal fungi are of critical importance (Smith & Read, 1997; Leake, 2001; Lilleskov & Bruns, 2001; Cairney & Ashford, 2002). In this issue this is further emphasised by Read & Perez-Moreno (pp. 475–492) in a review of the predominating mycorrhizal symbioses of plants that are found in mineral nutrient limited grassland, heathland and forest ecosystems. In particular, Northern boreal forests that represent a major atmospheric carbon sink thrive in recalcitrant ligno-cellulose and mycorrhizal fungi rich soils (Hogberg & Hogberg, 2002). The established view that clear-cut wood harvesting has a detrimental impact on mycorrhizal fungal communities and subsequent forest regeneration is now revised by Jones et al. (pp. 399–422) following their re-evaluation of earlier data and examination of more recent targeted studies.

Soil fungi that attack plant roots (e.g. Rhizoctonia and Fusarium spp.) represent economically important phytopathogens in agriculture and forestry. Suppressive soils that support crop production in the presence of root pathogenic Fusarium oxysporum are often found to be enriched in nonpathogenic F. oxysporum strains (Fravel et al. pp. 493–502). Control mechanisms include niche and nutrient competition and activation of induced systemic resistance in plants. These beneficial properties of nonpathogenic strains present an alternative, more environmentally friendly, route for nonpesticide disease control as microbial biological control agents. Fluorescent pseudomonads are near ubiquitous members of the soil bacterial community and, similarly, include species comprising antagonistic and beneficial populations. The latter and strains of other beneficial soil bacterial species that have been found to promote plant growth are collectively termed plant growth promoting rhizobacteria (PGPR). Specific inoculant strains (e.g. atmospheric nitrogen fixers and fungal antagonists) are already in commercial production. Chin-a-Woeng et al. (pp. 503–523) now present an in-depth update on current understanding of the molecular basis for PGPR activity in Pseudomonas spp., with a strong focus on rhizosphere induction, biosynthesis and mode of action of antifungal phenazines produced by these bacteria.

The presence of enriched soil bacterial communities in the rhizosphere, often organised in intimately structured biofilms, provides ideal conditions for horizontal gene transfer (HGT) between co-occurring bacterial species. Driving forces, mechanisms, mobilizing vectors and frequencies of HGT in rhizosphere bacterial communities are the main subjects of discussion in the review by van Elsas et al. (pp. 525–537). Most intriguingly, putative bacterial capture of plant DNA in the rhizosphere is also suggested from recent studies. If plant-to-microbe HGT were proved to be more widespread than previously thought, this phenomenon would have a major impact on current thinking regarding plant–bacterial coevolution and below-ground gene flow.

Multitrophic associations demand greater multidisciplinary investigation

A common recommendation expressed in these reviews is the need for integrative experiments that re-evaluate earlier targeted data under more relevant nonreductionist conditions. This is an unavoidable but logical conclusion when considering the complexity of interactions involving diverse plant and microbial taxa in as many soil types. What was earlier considered an impossible task, and thus the main argument for reductionism, is now being seen as an achievable proposition. The paradigm shift in thinking follows great strides in methodological development in such diverse areas as genomics, proteomics, bioinformatics, microscopy, isotope chemistry, plant growth chamber design, ecological modelling and bio- and remote-sensing.

Our present understanding of bacterial community functioning in structured biofilms is a relevant case in point. The composition, spatial organisation, stability and dynamics, and activities (e.g. synergistic antibiotic resistance) of biofilms were originally characterised using standard bacteriological, molecular and microscopical techniques together with those of the physical sciences, particularly surface and fluid mechanics (Costerton et al., 1995; Dunne, 2002). As discussed by Chin-a-Woeng et al. bacterial biofilms also develop on root surfaces, and the molecular events regulating biofilm development via the universal – cell density dependent (quorum sensing) – production of a diverse array of signal molecules has now been elucidated using advanced molecular techniques. The functioning of biofilms in density dependant production of, for example, secondary metabolites, toxins, exopolysaccharides and phenazine antibiotics, has involved use of molecular and biochemical/physiological and fungal bioassay methodology. Target genes controlling activation of induced systemic resistance in the host plant following rhizosphere biofilm development have been identified using standard molecular methodology but, as pointed out by Chin-a-Woeng et al., global gene expression patterns need to be characterised using the powerful new molecular tools of transcriptomics and proteomics.

Interactions between mycorrhizal and saprotrophic fungi and bacteria in the rhizosphere, or, more strictly, the mycorrhizosphere, developed in mineral and forest soils are now being characterised (Garbaye, 1994; Cairney & Meharg, 2002; Read & Perez-Moreno). Preliminary studies of mycorrhizal root systems of forest trees developed on highly organic forest and petroleum contaminated mineral soils have highlighted catabolic bacterial biofilm development on soil colonizing mycorrhizal fungal hyphae (Sen, 2000). Most recently the presence of noncultivatable Archaea (Crenarchaeota) were also identified in the mycorrhizospheres in the same forest soil (Bomberg et al., 2003). Arbuscular mycorrhizal fungi, which form mycorrhizas with the roots of nearly all major crop and native grassland and many tree species, were found to host obligate nitrogen fixing endosymbiotic bacteria at intracellular locations in fungal spores and hyphae (Minerdi et al., 2002). Clearly, analyses of PGPR distribution and activities must now be extended to accommodate their common associations with other key root associated microbial groups. We do have a precedent from clinical and ruminant microbiology of the gut and rumen of higher mammals (Gibson & Roberfroid, 1999 and references therein; Dehority, 2002). There appear to be strong parallels with corresponding root associated bacterial, Archaeal and fungal biofilms that develop in native organic soils. Both systems have evolved under similar selective conditions that promote microbe association and biofilm development on nutrient rich living surfaces of their hosts. Respective biofilm exposure to complex high organic matter in the form of ligno-cellulose and proteins, the main constituents of consumed food and soil, drive the required degradative secondary metabolism that enables host-microbial uptake of released monosaccharides, amino acids and mineral nutrients.

Alleviating threats to soils through management of soil microbiota

Our present understanding of soil and root associated microbial communities and activities come at a time of growing concern at the extent of soil erosion and degradation (e.g. salinization) in intensively managed agroecosystems around the world. These concerns and proposed solutions (e.g. raising organic matter content of soils under cultivation) were identified in resolutions passed following much debate among soil scientists at the 17th World Congress of Soil Sciences (WCSS) held in Bangkok, Thailand in August 2002 (see http://www.iuss.org/Resolutions%2017th%20WCSS.htm). While maintaining crop yield in countries with highly developed agriculture, long-term NPK fertilizer application is now seen as the prime cause for the elevated nutrient status of ground water supplies and eutrophication of water bodies. In developing countries, exhaustion of agricultural land is often compensated for through expansion into native grassland or forest ecosystems. Nonsustainable slash-and-burn cropping regimes further exacerbate the problems of soil degradation and habitat loss.

These crop production regimes adversely affect diversity and functioning of beneficial soil- and root-associated microbiota. The resulting loss of soil structure leads to reduced water and nutrient carrying capacity that has obvious negative ramifications for soil fertility and maintenance of plant production. A greater appreciation of the importance of root associated microbes in maintaining soil structure (i.e. aggregate stability) has come from studies identifying significant quantities of a glycoprotein, glomalin, produced by root symbiotic arbuscular mycorrhizal fungi in stable well structured field and native forest soils (Wright & Anderson, 2000; Rillig et al., 2001). It is no coincidence that arbuscular mycorrhizal fungal diversity and functioning are known to be negatively correlated with high available P status typically found in NPK fertilized agricultural soils (Smith & Read, 1997; Helgason et al., 1998). Smith (2002) stressed the need to better integrate information on root and soil microbe distribution dynamics and activities with known spatial and physicochemical properties of soils. This should be achieved through greater collaborative effort between biologists, soil chemists and physicists.

Perspectives

News from the root–microbe–soil interface has already, and will continue, to provide us with new tools to promote sustainable agricultural and forestry practices. Traditional management techniques have to be used but, in the future, will incorporate the new products of plant and microbial biotechnology research and development. However, much can also still be learnt from our increasingly threatened, but productive, seminatural or natural vegetated ecosystems that so desperately need to be protected.

Acknowledgements

Reviews in this special issue were developed by some of the key speakers at the 8th New Phytologist Symposium ‘Impacts of Soil Microbes on Plant Population Dynamics and Productivity’ held at the University of Helsinki, Finland in June 2002 (see http://www.biocenter.helsinki.fi/nps2002/). I would particularly like to thank my co-organisers, Andrew Watkinson, Francis Martin and Jonathan Ingram, for invaluable support and encouragement. We are grateful to our Symposium sponsors: the New Phytologist Trust, University of Helsinki, Academy of Finland, City of Helsinki, Viikki Graduate School of Biosciences, FIBRE and Forelia OY.

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