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.     

Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere

BACKGROUND: Roots growing in soil encounter physical, chemical and biological environments that influence their rhizospheres and affect plant growth. Exudates from roots can stimulate or inhibit soil organisms that may release nutrients, infect the root, or modify plant growth via signals. These rhizosphere processes are poorly understood in field conditions. SCOPE AND AIMS: We characterize roots and their rhizospheres and rates of growth in units of distance and time so that interactions with soil organisms can be better understood in field conditions. We review: (1) distances between components of the soil, including dead roots remnant from previous plants, and the distances between new roots, their rhizospheres and soil components; (2) characteristic times (distance(2)/diffusivity) for solutes to travel distances between roots and responsive soil organisms; (3) rates of movement and growth of soil organisms; (4) rates of extension of roots, and how these relate to the rates of anatomical and biochemical ageing of root tissues and the development of the rhizosphere within the soil profile; and (5) numbers of micro-organisms in the rhizosphere and the dependence on the site of attachment to the growing tip. We consider temporal and spatial variation within the rhizosphere to understand the distribution of bacteria and fungi on roots in hard, unploughed soil, and the activities of organisms in the overlapping rhizospheres of living and dead roots clustered in gaps in most field soils. CONCLUSIONS: Rhizosphere distances, characteristic times for solute diffusion, and rates of root and organism growth must be considered to understand rhizosphere development. Many values used in our analysis were estimates. The paucity of reliable data underlines the rudimentary state of our knowledge of root-organism interactions in the field.     

Dissecting the Rhizosphere complexity: The truffle-ground study case

The word Rhizosphere describes the part of the soil which is immediately adjacent to and affected by plant roots. This is a very dynamic environment where plants, soil and microorganisms interact. The plant releases, in addition to biologically active substances, nutritive substances (exudates), which create a privileged habitat for many microbial populations. The same microbes that live in the rhizosphere may be useful for the plant. Interest in this fascinating environment has increased over the years. However, our knowledge of the biology and diversity of microbial populations in the rhizosphere is still limited, because it has always been linked to traditional culture-based techniques. These methods, which only allow the study of cultured microorganisms, do not allow the majority of the organisms existing in nature to be characterized. Over the last few years, this limitation has been overcome through the introduction of methodologies that are independent of culture techniques. This different approach, which has revolutionized scientific research, is known as metagenomics. In this review, the rhizosphere environment is considered with particular attention to the fungal and symbiotic organisms, which populate it. The new environmental genomic techniques and how these have been applied to the study of the various environments and the rhizosphere are described. Finally, a specific rhizosphere, a truffle-ground, is described as our study case.      

Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata

Plant secondary metabolites play an important role in constitutive and inducible direct defense of plants against their natural enemies. While induction of defense by aboveground pathogens and herbivores is well-studied, induction by belowground organisms is less explored. Here, we examine whether soil microorganisms and nematodes can induce changes in levels of the secondary metabolites aucubin and catalpol (iridoid glycosides, IG) in roots and root exudates of two full-sib families of Plantago lanceolata originating from lines selected for low and high constitutive levels of IG in leaves. Addition of soil microorganisms enhanced the shoot and root biomass, and the concentration of aucubin in roots of both Plantago lines without affecting IG levels in the rhizosphere. By contrast, nematode addition tended to reduce the root biomass and enhanced the stalk biomass, and increased the levels of aucubin and catalpol in root exudates of both Plantago lines, without affecting root IG concentrations. The Plantago lines did not differ in constitutive levels of aucubin and total IG in roots, while the concentration of catalpol was slightly higher in roots of plants originally selected for low constitutive levels of IG in leaves. Root exudates of “high IG line” plants contained significantly higher levels of aucubin, which might be explained by their higher root biomass. We conclude that soil microorganisms can induce an increase of aucubin concentrations in the roots, whereas nematodes (probably plant feeders) lead to an enhancement of aucubin and catalpol levels in root exudates of P. lanceolata. A potential involvement of secondary metabolites in belowground interactions between plants and soil organisms is discussed.     

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.     

环境DNA技术在地下生态学中的应用

地下生态过程是生态系统结构、功能和过程研究中最不确定的因素。由于技术和方法的限制,作为"黑箱"的地下生态系统已经成为限制生态学发展的瓶颈,也是未来生态学发展的主要方向。环境DNA技术,是指从土壤等环境样品中直接提取DNA片段,然后通过DNA测序技术来定性或定量化目标生物,以确定目标生物在生态系统中的分布及功能特征。环境DNA技术已成功用于地下生态过程的研究。目前,环境DNA技术在土壤微生物多样性及其功能方面的研究相对成熟,克服了土壤微生物研究中不能培养的问题,可以有效地分析土壤微生物的群落组成、多样性及空间分布,尤其是宏基因组学技术的发展,使得微生物生态功能方面的研究成为可能;而且,环境DNA技术已经在土壤动物生态学的研究中得到了初步应用,可快速分析土壤动物的多样性及其分布特征,更有效地鉴定出未知的或稀少的物种,鉴定土壤动物类群的幅度较宽;部分研究者通过提取分析土壤中DNA片段信息对生态系统植物多样性及植物分类进行了研究,其结果比传统的植物分类及物种多样性测定更精确,改变了以往对植物群落物种多样性模式的理解。同时,环境DNA技术克服传统根系研究方法中需要洗根、分根、只能测定单物种根系的局限,降低根系研究中细根区分的误差,并探索性地用于细根生物量的研究。主要综述了基于环境DNA技术的分子生物学方法在土壤微生物多样性及功能、土壤动物多样性、地下植物多样性及根系生态等地下生态过程研究中的应用进展。环境DNA技术对于以土壤微生物、土壤动物及地下植物根系为主体的地下生态学过程的研究具有革命性意义,并展现出良好的应用前景。可以预期,分子生物学技术与传统的生态学研究相结合将成为未来地下生态学研究的一个发展趋势。     

土壤生物与土壤污染研究前沿与展望

随着社会经济发展,人类生产活动对自然环境产生越来越广泛深刻的影响,土壤污染已成为危及生态系统稳定、农产品质量安全和人体健康的突出环境问题之一。重金属、有机污染化合物、病原菌及抗性基因等各类污染物大量进入土壤后,对土壤生物系统造成毒害作用,影响到土壤生态功能;另一方面,土壤生物如细菌、真菌、土壤动物等在一定程度上能够适应土壤污染,深刻影响着污染物在土壤中的迁移转化过程,在土壤污染修复中具有潜在重要作用。从土壤污染的生态毒理效应、土壤生物对土壤污染的响应与适应机制、污染土壤修复原理与技术等三方面综述了土壤生物与土壤污染相关研究前沿,展望了重点研究方向。     

Manipulation of Auxin Transport in Plant Roots during Rhizobium Symbiosis and Nematode Parasitism

The plant rhizosphere harbors many different microorganisms, ranging from plant growth–promoting bacteria to devastating plant parasites. Some of these microbes are able to induce de novo organ formation in infected roots. Certain soil bacteria, collectively called rhizobia, form a symbiotic interaction with legumes, leading to the formation of nitrogen-fixing root nodules. Sedentary endoparasitic nematodes, on the other hand, induce highly specialized feeding sites in infected plant roots from which they withdraw nutrients. In order to establish these new root structures, it is thought that these organisms use and manipulate the endogenous molecular and physiological pathways of their hosts. Over the years, evidence has accumulated reliably demonstrating the involvement of the plant hormone auxin. Moreover, the auxin responses during microbe-induced de novo organ formation seem to be dynamic, suggesting that plant-associated microbes can actively modify their host''s auxin transport. In this review, we focus on recent findings in auxin transport mechanisms during plant development and on how plant symbionts and parasites have evolved to manipulate these mechanisms for their own purposes.     

Causes and consequences of biological diversity in soil

There is a vast diversity of organisms that live in the soil, and the activities of the total soil biota, together with the diverse forms and functions of plant roots, have critical roles in soil functioning. In this paper I discuss the likely determinants of soil diversity and also comment on recent studies that have explored whether or not there is a relationship between soil organism diversity and ecosystem function. There is little evidence to suggest that soil diversity is regulated in a predicable fashion by competition or disturbance; rather it is attributed to the nature of the soil environment, in that soil offers an extremely heterogeneous habitat, both spatially and temporally, proving unrivalled potential for niche partitioning, or resource or habitat specialisation, thereby enabling co-existence of species. Most evidence that is available suggests that there is no predictable relationship between diversity and function in soils, and that ecosystem properties are governed more by individual traits of dominant species, and by the extraordinary complexity of biotic interactions that occur between components of soil food webs. There is evidence of redundancy in soil communities with respect to soil functions, but the scale of effect of changes in soil diversity on process rates depends on which species are removed from the community and the degree to which remaining species can compensate. As in aboveground communities, therefore, it would appear that species traits and changes in species composition, and alterations in the nature of the many important species interactions that occur in soil, are likely to be the main biotic control of ecosystem function. In view of this, consideration of these important biotic interactions and their sensitivity to environmental change must be a key priority for future research.     

Interspecific diversity in root antioxidative enzyme activities reflect root turnover strategies and preferred habitats in wetland graminoids

Antioxidant enzymes protect cells against oxidative stress and are associated with stress tolerance and longevity. In animals, variation in their activities has been shown to relate to species ecology, but in plants, comparative studies with wild species are rare. We investigated activities of five antioxidant enzymes – ascorbate peroxidase (APX), catalase (CAT), glutathione reductase (GR), peroxidase (POX), and superoxide dismutase (SOD) – in roots of four perennial graminoid wetland species over a growing season to find out whether differences in root turnover or habitat preferences would be associated with variation in seasonal patterns of antioxidant enzyme activities. The investigated species differ in their root turnover strategies (fine roots senesce in the fall or fine roots survive the winter) and habitat preferences (nutrient‐poor vs. productive wetlands). Roots were collected both in the field and from garden‐grown plants. Antioxidant enzyme activities were higher and lipid peroxidation rates lower in species with annual root systems, and for species of the nutrient‐poor wetland, compared with perennial roots and species of productive wetlands, respectively. There was variation in the activities of individual antioxidant enzymes, but discriminant analyses with all enzymes revealed a clear picture, indicating consistent associations of antioxidant enzyme activities with the type of root turnover strategy and with the preferred habitat. We conclude that antioxidant enzyme activities in plant roots are associated with the species' ecological strategies and can be used as traits for the characterization of the species' position along plant economics spectrum.     

Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms

Intraspecific variation in plants can affect soil organisms. However, little is known about whether the magnitude of the effect depends on the degree of interaction with the roots. We analyzed effects of plant intraspecific variation on root herbivores and other soil organisms that interact directly with living plant roots, as well as on decomposer organisms that interact more indirectly with roots. We used four different white cabbage (Brassica oleracea var. capitata) cultivars exhibiting a high degree of intraspecific variation in root glucosinolate profiles. Intraspecific variation affected root-feeding nematodes, whereas decomposer organisms such as earthworms and Collembola were not affected. Root-feeding nematodes were most abundant in one of the cultivars, Badger Shipper, which lacked the glucosinolate gluconasturtiin. The effect of the intraspecific variation in glucosinolate composition may have been restricted to root-feeding nematodes due to the rapid degradation of glucosinolates and their breakdown products in the soil. Additionally, the low biomass of root-feeding nematodes, relative to other soil organisms, limits the possibility to affect higher trophic level organisms. Our results show that variation in root chemistry predominantly affects belowground herbivores and that these effects do not extend into the soil food web.     

Differential foraging for resources, and structural plasticity in plants

Although ecologists have spent much effort in analysing the foraging behaviour of animals, the study of plants as foraging organisms is a relatively unexplored subject. There is often, however, much greater potential for analysis of foraging behaviour in plants than in animals. Unlike most animals, many plant species leave permanent or semi-permanent records of their foraging activities because their resource-acquiring structures (primarily leaves and roots), persist for a considerable time, as also do the structures (trunks, branches, stolons, runners or rhizomes) which enable leaves or roots to be projected into particular positions in the habitat. In addition, plant ecologists are not burdened with the difficulties associated with determining how changes in foraging behaviour affect fitness in animals(1), because plant mass (or, in the case of clonal species, number of ramets produced), is usually closely correlated with fitness.     

Plant metabolomics for plant chemical responses to belowground community change by climate change

General circulation models on global climate change predict increase in surface air temperature and changes in precipitation. Increases in air temperature (thus soil temperature) and altered precipitation are known to affect the species composition and function of soil microbial communities. Plant roots interact with diverse soil organisms such as bacteria, protozoa, fungi, nematodes, annelids and insects. Soil organisms show diverse interactions with plants (eg. competition, mutualism and parasitism) that may alter plant metabolism. Besides plant roots, various soil microbes such as bacteria and fungi can produce volatile organic compounds (VOCs), which can serve as infochemicals among soil organisms and plant roots. While the effects of climate change are likely to alter both soil communities and plant metabolism, it is equally probable that these changes will have cascading consequnces for grazers and subsequent food web components aboveground. Advances in plant metabolomics have made it possibile to track changes in plant metabolomes as they respond to biotic and abiotic environmental changes. Recent developments in analytical instrumentation and bioinformatics software have established metabolomics as an important research tool for studying ecological interactions between plants and other organisms. In this review, we will first summarize recent progress in plant metabolomics methodology and subsequently review recent studies of interactions between plants and soil organisms in relation to climate change issues.     

Indigenous arbuscular mycorrhizal fungal assemblages protect grassland host plants from pathogens

Plant roots can establish associations with neutral, beneficial and pathogenic groups of soil organisms. Although it has been recognized from the study of individual isolates that these associations are individually important for plant growth, little is known about interactions of whole assemblages of beneficial and pathogenic microorganisms associating with plants.We investigated the influence of an interaction between local arbuscular mycorrhizal (AM) fungal and pathogenic/saprobic microbial assemblages on the growth of two different plant species from semi-arid grasslands in NE Germany (Mallnow near Berlin). In a greenhouse experiment each plant species was grown for six months in either sterile soil or in sterile soil with one of three different treatments: 1) an AM fungal spore fraction isolated from field soil from Mallnow; 2) a soil pathogen/saprobe fraction consisting of a microbial community prepared with field soil from Mallnow and; 3) the combined AM fungal and pathogen/saprobe fractions. While both plant species grew significantly larger in the presence of AM fungi, they responded negatively to the pathogen/saprobe treatment. For both plant species, we found evidence of pathogen protection effects provided by the AM fungal assemblages. These results indicate that interactions between assemblages of beneficial and pathogenic microorganisms can influence the growth of host plants, but that the magnitude of these effects is plant species-specific.     

Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms

The rhizosphere is a complex environment where roots interact with physical, chemical and biological properties of soil. Structural and functional characteristics of roots contribute to rhizosphere processes and both have significant influence on the capacity of roots to acquire nutrients. Roots also interact extensively with soil microorganisms which further impact on plant nutrition either directly, by influencing nutrient availability and uptake, or indirectly through plant (root) growth promotion. In this paper, features of the rhizosphere that are important for nutrient acquisition from soil are reviewed, with specific emphasis on the characteristics of roots that influence the availability and uptake of phosphorus and nitrogen. The interaction of roots with soil microorganisms, in particular with mycorrhizal fungi and non-symbiotic plant growth promoting rhizobacteria, is also considered in relation to nutrient availability and through the mechanisms that are associated with plant growth promotion.     

Mechanism of plant growth promotion by rhizobacteria

Plant growth results from interaction of roots and shoots with the environment. The environment for roots is the soil or planting medium which provide structural support as well as water and nutrients to the plant. Roots also support the growth and functions of a complex of microorganisms that can have a profound effect on the growth anti survival of plants. These microorganisms constitute rhizosphere microflora and can be categorized as deleterious, beneficial, or neutral with respect to root/plant health. Beneficial interactions between roots and microbes do occur in rhizosphere and can be enhanced. Increased plant growth and crop yield can be obtained upon inoculating seeds or roots with certain specific root-colonizing bacteria- 'plant growth promoting rhizobacteria'. In this review, we discuss the mechanisms by which plant growth promoting rhizobacteria may stimulate plant growth.     

Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review

The aim of the present review is to define the various origins of root-mediated changes of pH in the rhizosphere, i.e., the volume of soil around roots that is influenced by root activities. Root-mediated pH changes are of major relevance in an ecological perspective as soil pH is a critical parameter that influences the bioavailability of many nutrients and toxic elements and the physiology of the roots and rhizosphere microorganisms. A major process that contributes root-induced pH changes in the rhizosphere is the release of charges carried by H⁺ or OH^– to compensate for an unbalanced cation–anion uptake at the soil–root interface. In addition to the ions taken up by the plant, all the ions crossing the plasma membrane of root cells (e.g., organic anions exuded by plant roots) should be taken into account, since they all need to be balanced by an exchange of charges, i.e., by a release of either H⁺ or OH^–. Although poorly documented, root exudation and respiration can contribute some proportion of rhizosphere pH decrease as a result of a build-up of the CO₂ concentration. This will form carbonic acid in the rhizosphere that may dissociate in neutral to alkaline soils, and result in some pH decrease. Ultimately, plant roots and associated microorganisms can also alter rhizosphere pH via redox-coupled reactions. These various processes involved in root-mediated pH changes in the rhizosphere also depend on environmental constraints, especially nutritional constraints to which plants can respond. This is briefly addressed, with a special emphasis on the response of plant roots to deficiencies of P and Fe and to Al toxicity. Finally, soil pH itself and pH buffering capacity also have a dramatic influence on root-mediated pH changes.     

Time and litter species composition affect litter-mixing effects on decomposition rates

Aims

To assess whether the yew roots, which are able to provide a very constant environment due to their long life-span, can maintain the original arbuscular mycorrhizal (AM) fungal community during yew population decline.

Methods

The diversity of AM fungi (AMF) colonizing the roots of yew was analyzed by selecting the small subunit ribosomal RNA genes to construct a database of the overall community of AMF in the experimental area. A terminal restriction fragment length polymorphism (TRFLP) approach was used to identify the AMF communities present in yew roots. Physiological and environmental variables related to topology and soil and plant characteristics were determined as markers of habitat degradation.

Results

The AMF communities within yew roots were found to be dependent on soil, plant and topological variables indicative of habitat degradation surrounding the yew. The phylogenetic diversity of AMF associated to the yews was lower in habitats more exposed to degradation than in those better conserved.

Conclusions

The target yews can be grouped into two degradation levels. AMF communities were also affected by the degradation processes affecting their hosts. This finding rules out the role of these trees as refugia for their original AMF community, a fact that should be considered in plant reintroduction programs using AMF as bioenhancers.     

释放后的转抗病虫基因作物对土壤生物群落的影响

土壤生物,尤其是土壤微生物多样性与活性的保持是农业生态系统健康稳定的基础,农业活动尤其是农作物植被类型的改变对土壤生物的群落结构和活性具有显著的影响。释放后的转基因作物作为生态系统的一种新的生物组分,被引入农田生态系统之间后所引发的农田生物群落（包括土壤微生物群落）的变化及其对农业生态系统的健康与稳定产生的影响,已成为研究热点,本文对转抗虫Bt基因作物、转T4-溶菌酶基因作物,转蛋白酶抑制剂I基因作物的基因产物、作物残体在土壤中的行为（如降解产物的存留形态与生物活性）及其对根际或残体周围土壤中各类生物,尤其是微生物群落结构与功能的影响进行了简要综合评述,指出基因表达产物的后效肯定是存在的且长远的,由其引发的土壤生物群落结构的变化是复杂的,因而有必要对不同类型的转基因作物释放后的生态效应做长期的跟踪研究,建议未来的研究工作应集中在以下3个方面：（1）不同的转基因表达产物在环境中的迁移、结构变化、消长动态及其对生物保持毒杀性的时间;（2）不同类型转基因的植物对土壤生物群落结构的影响趋势;（3）在实验条件下,研究分离纯化的各种转基因表达产物对土壤各生物功能类群的影响。     

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.