Mycorrhizosphere interactions to improve plant fitness and soil quality

Arbuscular mycorrhizal fungi are key components of soil microbiota and obviously interact with other microorganisms in the rhizosphere, i.e. the zone of influence of plant roots on microbial populations and other soil constituents. Mycorrhiza formation changes several aspects of plant physiology and some nutritional and physical properties of the rhizospheric soil. These effects modify the colonization patterns of the root or mycorrhizas (mycorrhizosphere) by soil microorganisms. The rhizosphere of mycorrhizal plants, in practice a mycorrhizosphere, harbors a great array of microbial activities responsible for several key ecosystem processes. This paper summarizes the main conceptual principles and accepted statements on the microbial interactions between mycorrhizal fungi and other members of rhizosphere microbiota and discusses current developments and future trends concerning the following topics: (i) effect of soil microorganisms on mycorrhiza formation; (ii) mycorrhizosphere establishment; (iii) interactions involved in nutrient cycling and plant growth; (iv) interactions involved in the biological control of plant pathogens; and (v) interactions to improve soil quality. The main conclusion is that microbial interactions in the rhizosphere of mycorrhizal plants improve plant fitness and soil quality, critical issues for a sustainable agricultural development and ecosystem functioning. This revised version was published online in August 2006 with corrections to the Cover Date.     

植物根际微生物群落构建的研究进展

植物根际是指植物根系与土壤的交界面,是根系自身生命活动和代谢对土壤影响最直接、最强烈的区域,其物理、化学和生物性质不同于土体土壤。在这个区域里,与植物发生相互作用的大量微生物,被称为根际微生物。根际微生物在植物的生长发育和植物病虫害的生物防治等方面都具有十分重要的意义。本文总结了根际微生物群落构建的研究现状,介绍了根际微生物的经典和最新的研究方法,包括根箱法、同位素技术以及高通量测序、菌群定量分析、高通量分离培养等方法在根际微生物研究中的应用,讨论了植物根系分泌物(碳水化物、氨基酸、黄酮类、酚类、激素及其信号物质)和土壤物理化学性质对根际微生物群落的影响,概述了根际微生物-植物的互作机制,以及根际微生物群落对植物的促生作用、提高植物抗逆性和抑制作用,并对根际微生物群落研究中存在的问题和未来发展方向进行了展望。     

Interaction between Earthworms and Arbuscular Mycorrhizal Fungi in Plants: A Review

Different kinds of soil animals and microorganisms inhabit the plant rhizosphere, which function closely to plant roots. Of them, arbuscular mycorrhizal fungi (AMF) and earthworms play a critical role in sustaining the soil-plant health. Earthworms and AMF belong to the soil community and are soil beneficial organisms at different trophic levels. Both of them improve soil fertility and structural development, collectively promoting plant growth and nutrient acquisition capacity. Earthworm activities redistribute mycorrhizal fungi spores and give diversified effects on root mycorrhizal fungal colonization. Dual inoculation with both earthworms and AMF strongly magnifies the response on plant growth through increased soil enzyme activities and changes in soil nutrient availability, collectively mitigating the negative effects of heavy metal pollution in plants and soils. This thus enhances phytoremediation and plant disease resistance. This review simply outlines the effects of earthworms and AMF on the soil-plant relationship. The effects of earthworms on root AMF colonization and activities are also analyzed. This paper also summarizes the interaction between earthworms and AMF on plants along with suggested future research.     

The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms

The rhizosphere is a hot spot of microbial interactions as exudates released by plant roots are a main food source for microorganisms and a driving force of their population density and activities. The rhizosphere harbors many organisms that have a neutral effect on the plant, but also attracts organisms that exert deleterious or beneficial effects on the plant. Microorganisms that adversely affect plant growth and health are the pathogenic fungi, oomycetes, bacteria and nematodes. Most of the soilborne pathogens are adapted to grow and survive in the bulk soil, but the rhizosphere is the playground and infection court where the pathogen establishes a parasitic relationship with the plant. The rhizosphere is also a battlefield where the complex rhizosphere community, both microflora and microfauna, interact with pathogens and influence the outcome of pathogen infection. A wide range of microorganisms are beneficial to the plant and include nitrogen-fixing bacteria, endo- and ectomycorrhizal fungi, and plant growth-promoting bacteria and fungi. This review focuses on the population dynamics and activity of soilborne pathogens and beneficial microorganisms. Specific attention is given to mechanisms involved in the tripartite interactions between beneficial microorganisms, pathogens and the plant. We also discuss how agricultural practices affect pathogen and antagonist populations and how these practices can be adopted to promote plant growth and health.     

Rhizosphere engineering and management for sustainable agriculture

This paper reviews strategies for manipulating plants and their root-associated microorganisms to improve plant health and productivity. Some strategies directly target plant processes that impact on growth, while others are based on our knowledge of interactions among the components of the rhizosphere (roots, microorganisms and soil). For instance, plants can be engineered to modify the rhizosphere pH or to release compounds that improve nutrient availability, protect against biotic and abiotic stresses, or encourage the proliferation of beneficial microorganisms. Rhizobacteria that promote plant growth have been engineered to interfere with the synthesis of stress-induced hormones such as ethylene, which retards root growth, and to produce antibiotics and lytic enzymes active against soilborne root pathogens. Rhizosphere engineering also can involve the selection by plants of beneficial microbial populations. For example, some crop species or cultivars select for and support populations of antibiotic-producing strains that play a major role in soils naturally suppressive to soil-borne fungal pathogens. The fitness of root-associated bacterial communities also can be enhanced by soil amendment, a process that has allowed the selection of bacterial consortia that can interfere with bacterial pathogens. Plants also can be engineered specifically to influence their associated bacteria, as exemplified by quorum quenching strategies that suppress the virulence of pathogens of the genus Pectobacterium. New molecular tools and powerful biotechnological advances will continue to provide a more complete knowledge of the complex chemical and biological interactions that occur in the rhizosphere, ensuring that strategies to engineer the rhizosphere are safe, beneficial to productivity, and substantially improve the sustainability of agricultural systems.     

The ecology of ectomycorrhiza formation and functioning

Factors in inoculum potential/infection levels/plant growth response are analysed and experimental approaches to propagule germination, growth through soil and rhizosphere growth are indicated. It is suggested that seedling rhizosphere germination of basidiospores occurs particularly with early stage fungi, while late stage fungi may be advantaged by germination/growth on exudates from older parts of roots or on litter (and its associated microorganisms) and their tolerance of antimicrobial substances in litter. Relative growth in the rhizosphere is likely to dominate the mycorrhizal species composition and this may be a good selection method for organisms tolerant of stress and pollution conditions. As mycorrhizal function in nutrient uptake is largely determined by fungus growth into soil, there is need for much more experimental study of factors affecting this, and of the potential photosynthate drain this could represent. The possibility of selection/breeding mycorrhizal fungi with both ‘early stage’ and ‘late stage’ attributes is raised.     

Harnessing rhizobacteria to fulfil inter-linked nutrient dependency on soil and alleviate stresses in plants

Plant rhizo-microbiome comprises complex microbial communities that colonize at the interphase of plant roots and soil. Plant growth-promoting rhizobacteria (PGPR) in the rhizosphere provide important ecosystem services ranging from the release of essential nutrients for enhancing soil quality and improving plant health to imparting protection to plants against rising biotic and abiotic stresses. Hence, PGPR serve as restoring agents to rejuvenate soil health and mediate plant fitness in the facet of changing climate. Though it is evident that nutrient availability in soil is managed through inter-linked mechanisms, how PGPR expedite these processes remain less recognized. Promising results of PGPR inoculation on plant growth are continually reported in controlled environmental conditions, however, their field application often fails due to competition with native microbiota and low colonization efficiency in roots. The development of highly efficient and smart bacterial synthetic communities by integrating bacterial ecological and genetic features provides better opportunities for successful inoculant formulations. This review provides an overview of the interplay between nutrient availability and disease suppression governed by rhizobacteria in soil followed by the role of synthetic bacterial communities in developing efficient microbial inoculants. Moreover, an outlook on the beneficial activities of rhizobacteria in modifying soil characteristics to sustainably boost agroecosystem functioning is also provided.     

Root exudates as mediators of mineral acquisition in low-nutrient environments

Plant developmental processes are controlled by internal signals that depend on the adequate supply of mineral nutrients by soil to roots. Thus, the availability of nutrient elements can be a major constraint to plant growth in many environments of the world, especially the tropics where soils are extremely low in nutrients. Plants take up most mineral nutrients through the rhizosphere where micro-organisms interact with plant products in root exudates. Plant root exudates consist of a complex mixture of organic acid anions, phytosiderophores, sugars, vitamins, amino acids, purines, nucleosides, inorganic ions (e.g. HCO₃ ^–, OH^–, H⁺), gaseous molecules (CO₂, H₂), enzymes and root border cells which have major direct or indirect effects on the acquisition of mineral nutrients required for plant growth. Phenolics and aldonic acids exuded directly by roots of N₂-fixing legumes serve as major signals to Rhizobiaceae bacteria which form root nodules where N₂ is reduced to ammonia. Some of the same compounds affect development of mycorrhizal fungi that are crucial for phosphate uptake. Plants growing in low-nutrient environments also employ root exudates in ways other than as symbiotic signals to soil microbes involved in nutrient procurement. Extracellular enzymes release P from organic compounds, and several types of molecules increase iron availability through chelation. Organic acids from root exudates can solubilize unavailable soil Ca, Fe and Al phosphates. Plants growing on nitrate generally maintain electronic neutrality by releasing an excess of anions, including hydroxyl ions. Legumes, which can grow well without nitrate through the benefits of N₂ reduction in the root nodules, must release a net excess of protons. These protons can markedly lower rhizosphere pH and decrease the availability of some mineral nutrients as well as the effective functioning of some soil bacteria, such as the rhizobial bacteria themselves. Thus, environments which are naturally very acidic can pose a challenge to nutrient acquisition by plant roots, and threaten the survival of many beneficial microbes including the roots themselves. A few plants such as Rooibos tea (Aspalathus linearis L.) actively modify their rhizosphere pH by extruding OH^– and HCO₃ ^– to facilitate growth in low pH soils (pH 3 – 5). Our current understanding of how plants use root exudates to modify rhizosphere pH and the potential benefits associated with such processes are assessed in this review.     

Plant growth-promoting bacteria as inoculants in agricultural soils

Plant-microbe interactions in the rhizosphere are the determinants of plant health, productivity and soil fertility. Plant growth-promoting bacteria (PGPB) are bacteria that can enhance plant growth and protect plants from disease and abiotic stresses through a wide variety of mechanisms; those that establish close associations with plants, such as the endophytes, could be more successful in plant growth promotion. Several important bacterial characteristics, such as biological nitrogen fixation, phosphate solubilization, ACC deaminase activity, and production of siderophores and phytohormones, can be assessed as plant growth promotion (PGP) traits. Bacterial inoculants can contribute to increase agronomic efficiency by reducing production costs and environmental pollution, once the use of chemical fertilizers can be reduced or eliminated if the inoculants are efficient. For bacterial inoculants to obtain success in improving plant growth and productivity, several processes involved can influence the efficiency of inoculation, as for example the exudation by plant roots, the bacterial colonization in the roots, and soil health. This review presents an overview of the importance of soil-plant-microbe interactions to the development of efficient inoculants, once PGPB are extensively studied microorganisms, representing a very diverse group of easily accessible beneficial bacteria.     

Rhizospheric Processes Influencing the Biogeochemistry of Forest Ecosystems

In the rhizosphere, biotic and abiotic processes interact to create a zone distinct from the bulk soil that may strongly influence the biogeochemistry of forest ecosystems. This paper presents a conceptual model based upon three operationally defined soil-root compartments (bulk soil, rhizosphere and soil-root interface) to assess nutrient availability in the mineral soil-root system. The model is supported by chemical and mineralogical analyses from bulk and rhizosphere soils collected from a Norway spruce forest. The rhizosphere was more intensively weathered and had accumulated more acidity, base cations and phosphorus than the bulk soil. The quantity and quality of organic matter regulate the reciprocal relationships between soil and roots with their associated biota. However, the biogeochemical role of organic matter in the rhizosphere still remains as an area in which more future research is needed. The mechanisms that may regulate nutrient availability in the rhizosphere are also discussed and related to nutrient cycling and adaptation of forests growing under nutrient poor or perturbed conditions. We suggest that the rhizosphere is not an ephemeral environment in the soil, but persists over time and is resilient against perturbation as evinced by consistent differences between rhizosphere and bulk chemistry and mineralogy over wide range of field treatments.     

Nutrient availability and management in the rhizosphere: exploiting genotypic differences

Crop nutrition is frequently inadequate as a result of the expansion of cropping into marginal lands, elevated crop yields placing increasing demands on soil nutrient reserves, and environmental and economic concerns about applying fertilizers. Plants exposed to nutrient deficiency activate a range of mechanisms that result in increased nutrient availability in the rhizosphere compared with the bulk soil. Plants may change their root morphology, increase the affinity of nutrient transporters in the plasma membrane and exude organic compounds (carboxylates, phenolics, carbohydrates, enzymes, etc.) and protons. Chemical changes in the rhizosphere result in altered abundance and composition of microbial communities. Nutrient-efficient genotypes are adapted to environments with low nutrient availability. Nutrient efficiency can be enhanced by targeted breeding through pyramiding efficiency mechanisms in a desirable genotype as well as by gene transfer and manipulation. Rhizosphere microorganisms influence nutrient availability; adding beneficial microorganisms may result in enhanced availability of nutrients to crops. Understanding the role of plant-microbe-soil interactions in governing nutrient availability in the rhizosphere will enhance the economic and environmental sustainability of crop production.     

Distribution of cutin and suberin biomarkers under forest trees with different root systems

Background and aims

The rhizosphere, the soil immediately surrounding roots, provides a critical bridge for water and nutrient uptake. The rhizosphere is influenced by various forms of root–soil interactions of which mechanical deformation due to root growth and its effects on the hydraulics of the rhizosphere are the least studied. In this work, we focus on developing new experimental and numerical tools to assess these changes.

Methods

This study combines X-ray micro-tomography (XMT) with coupled numerical simulation of fluid and soil deformation in the rhizosphere. The study provides a new set of tools to mechanistically investigate root-induced rhizosphere compaction and its effect on root water uptake. The numerical simulator was tested on highly deformable soil to document its ability to handle a large degree of strain.

Results

Our experimental results indicate that measured rhizosphere compaction by roots via localized soil compaction increased the simulated water flow to the roots by 27 % as compared to an uncompacted fine-textured soil of low bulk density characteristic of seed beds or forest topsoils. This increased water flow primarily occurred due to local deformation of the soil aggregates as seen in the XMT images, which increased hydraulic conductivity of the soil. Further simulated root growth and deformation beyond that observed in the XMT images led to water uptake enhancement of ~50 % beyond that due to root diameter increase alone and demonstrated the positive benefits of root compaction in low density soils.

Conclusions

The development of numerical models to quantify the coupling of root driven compaction and fluid flow provides new tools to improve the understanding of plant water uptake, nutrient availability and agricultural efficiency. This study demonstrated that plants, particularly during early growth in highly deformable low density soils, are involved in active mechanical management of their surroundings. These modeling approaches may now be used to quantify compaction and root growth impacts in a wide range of soils.     

Vesicular-arbuscular mycorrhizae in relation to plant disease

Vesicular-arbuscular mycorrhizae (VAM) enhance plant growth through increased nutrient uptake, stress tolerance and disease resistance. As an integral part of the root system, they interact with other microorganisms in soil and result in increased root exudation approaching about 25% of the plant dry matter production. Roots support a multitude of microorganisms that, in concert, can have profound influence on growth and survival of the plant. VAM fungi can alter the root exudation pattern, enhance chitinolytic activity and alter photosynthetic/respiratory deficiencies. VAM-positive plants are known to exhibit varied resistance towards soil-borne and foliar pathogens. The known interactions include a number of mechanisms, such as exclusion of the pathogen, lignification of plant cell walls, changed phosphate nutrition resulting in altered exudation by roots, and formation of inhibitory low molecular weight compounds. The purpose of this review is to discuss VAM-plant-pathogen interactions and the possible mechanisms involved in altered resistance. Based on these observations, a working model is proposed to explain the VAM-disease interaction under varied environmental conditions.     

Soil acidification and adaptations of plants and microorganisms in Bornean tropical forests

In tropical forest ecosystems, a paradoxical relationship is commonly observed between massive biomass production and low soil fertility (low pH). The loss and deficiency of soil phosphorus (P) and bases generally constrain biomass production; however, high productivity on nutrient-deficient soils of Bornean tropical forests is hypothesized to be maintained by plant and microorganism adaptation to an acidic soil environment. Proton budgets in the plant–soil system indicated that plants and microorganisms promote acidification to acquire bases, even in highly acidic tropical soils. The nitric and organic acids they produce contribute to the mobilization of basic cations and their uptake by plants. In response to soil P deficiency and the recalcitrance of lignin-rich organic matter, specific trees and fungi can release organic acids and enzymes for nutrient acquisition. Organic acids exuded by roots and rhizosphere microorganisms can promote the solubilization of P bonded to aluminum and iron oxides and its uptake by plants from P-poor soils. Lignin degradation, a rate-limiting step in organic matter decomposition, is specifically enhanced in acidic organic layers by lignin peroxidase, produced by white-rot fungi, which may solubilize recalcitrant lignin and release soluble aromatic substances into the soil solution. This dissolved organic matter functions in the transport of nitrogen, P, and basic cations in acidic soils without increasing leaching loss. In Bornean tropical forests, soil acidification is promoted by plants and microorganisms as a nutrient acquisition strategy, while plant roots and fungi can develop rhizosphere and enzymatic processes that promote tolerance of low pH.     

Rhizosphere Properties of Poaceae Genotypes Under P-limiting Conditions

Plant genotypes differ in P efficiency, i.e. their capacity to grow in soil with low P availability. Plant properties such as root and root hair length, release of P mineralising and mobilising compounds by the roots and P requirement for optimal growth are known to influence P efficiency. In order to improve the understanding of the role of rhizosphere properties in plant P uptake, we grew three Poaceae genotypes [two wheat (Triticum aestivum L.) genotypes (the P-efficient Goldmark and the P-inefficient Janz), and the Australian native grass Austrostipa densiflora L.] to maturity in an acidic loamy sand with low P availability. Addition of 120 mg P as FePO₄ kg⁻¹ (P120) improved the growth of all three genotypes. In both P0 and P120, growth and P uptake were smaller in Janz than in Goldmark. During the vegetative phase, growth and P uptake of Austrostipa were smaller than in Goldmark in P0 but greater in P120. These differences can be explained by plant properties such as root growth, specific P uptake, mobilisation of inorganic and organic P by root exudates and P utilisation efficiency. In P120, P availability in the rhizosphere was least in Janz and greatest in Austrostipa. Microbial biomass P in the rhizosphere was least in Janz. Acid phosphatase activity was greatest in the rhizosphere of Austrostipa and least in Janz. Plant growth and P uptake were positively correlated with microbial P, acid phosphatase activity and resin P in the rhizosphere, suggesting that microorganisms contribute to uptake of P by plants in this soil. Microbial community composition in the rhizosphere [analysed by fatty acid methylester (FAME) analysis and denaturing gradient gel electrophoresis (DGGE)] differed among genotypes, changed during plant development and was affected by P addition to the soil. Genotype-specific microbial community composition in the rhizosphere may have contributed to the observed differential capacity of plants to grow at low P availability.     

Extracellular release of a heterologous phytase from roots of transgenic plants: does manipulation of rhizosphere biochemistry impact microbial community structure?

To maintain the sustainability of agriculture, it is imperative that the reliance of crops on inorganic phosphorus (P) fertilizers is reduced. One approach is to improve the ability of crop plants to acquire P from organic sources. Transgenic plants that produce microbial phytases have been suggested as a possible means to achieve this goal. However, neither the impact of heterologous expression of phytase on the ecology of microorganisms in the rhizosphere nor the impact of rhizosphere microorganisms on the efficacy of phytases in the rhizosphere of transgenic plants has been tested. In this paper, we demonstrate that the presence of rhizosphere microorganisms reduced the dependence of plants on extracellular secretion of phytase from roots when grown in a P-deficient soil. Despite this, the expression of phytase in transgenic plants had little or no impact on the microbial community structure as compared with control plant lines, whereas soil treatments, such as the addition of inorganic P, had large effects. The results demonstrate that soil microorganisms are explicitly involved in the availability of P to plants and that the microbial community in the rhizosphere appears to be resistant to the impacts of single-gene changes in plants designed to alter rhizosphere biochemistry and nutrient cycling.     

根际微型土壤动物——原生动物和线虫的生态功能

从养分释放、土壤有机碳积累和稳定、根系激素效应、微生物多样性和功能稳定性、地上部多营养级关系及污染土壤生物修复概述了根际微型土壤动物(原生动物和线虫)对根际生态功能的影响,特别针对微型土壤动物与微生物和根系的相互作用探讨了可能的机制。微型土壤动物的选择取食、主动迁移和代谢分泌行为,不仅贡献根际生态功能,而且对土壤整体及地上部群落有强烈的影响。总之,不考虑根际微型土壤动物与微生物和根系的相互作用,就不可能对根际生态功能和调控机制有全面的认识。     

Actinomycetales bacteria from a spruce stand: Characterization and effects on growth of root symbiotic and plant parasitic soil fungi in dual culture

The rhizosphere, the narrow zone of soil around living roots, is characterized by root exudates which attract soil microorganisms. Most importantly, certain soil fungi establish symbiotic interactions with fine roots which enhance nutrient availability for the plant partner (mycorrhiza). The establishment of such a symbiosis can be affected by soil bacteria. In this study we isolated Gram-positive soil bacteria from the rhizosphere of a spruce stand rich with fly agaric (Amanita muscaria) fruiting bodies. Using a coculture technique in Petri dishes, bacterial isolates were characterized by their effect on the growth of fungal hyphae. A group of bacterial strains were identified which significantly promoted growth of fly agaric hyphae. One of these strains was shown to additionally inhibit growth of pathogenic fungi such as Armillaria obscura (wide host range) and Heterobasidion annosum (causes wood decay in conifers). Taxonomic characterization of the effective bacterial isolates by their morphological appearance, by the analysis of diaminopimelic acid, cell wall sugars, and DNA sequencing (16S rDNA) identified them as actinomycetes, some of which are not yet contained in data banks.