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.     

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.     

Exploiting New Systems-Based Strategies to Elucidate Plant-Bacterial Interactions in the Rhizosphere

The rhizosphere is the site of intense interactions between plant, bacterial, and fungal partners. In plant-bacterial interactions, signal molecules exuded by the plant affect both primary initiation and subsequent behavior of the bacteria in complex beneficial associations such as biocontrol. However, despite this general acceptance that plant-root exudates have an effect on the resident bacterial populations, very little is still known about the influence of these signals on bacterial gene expression and the roles of genes found to have altered expression in plant-microbial interactions. Analysis of the rhizospheric communities incorporating both established techniques, and recently developed “omic technologies” can now facilitate investigations into the molecular basis underpinning the establishment of beneficial plant-microbial interactomes in the rhizosphere. The understanding of these signaling processes, and the functions they regulate, is fundamental to understanding the basis of beneficial microbial–plant interactions, to overcoming existing limitations, and to designing improved strategies for the development of novel Pseudomonas biocontrol strains.     

Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth

Arbuscular mycorrhizal (AM) fungi and bacteria can interact synergistically to stimulate plant growth through a range of mechanisms that include improved nutrient acquisition and inhibition of fungal plant pathogens. These interactions may be of crucial importance within sustainable, low-input agricultural cropping systems that rely on biological processes rather than agrochemicals to maintain soil fertility and plant health. Although there are many studies concerning interactions between AM fungi and bacteria, the underlying mechanisms behind these associations are in general not very well understood, and their functional properties still require further experimental confirmation. Future mycorrhizal research should therefore strive towards an improved understanding of the functional mechanisms behind such microbial interactions, so that optimized combinations of microorganisms can be applied as effective inoculants within sustainable crop production systems. In this context, the present article seeks to review and discuss the current knowledge concerning interactions between AM fungi and plant growth-promoting rhizobacteria, the physical interactions between AM fungi and bacteria, enhancement of phosphorus and nitrogen bioavailability through such interactions, and finally the associations between AM fungi and their bacterial endosymbionts. Overall, this review summarizes what is known to date within the present field, and attempts to identify promising lines of future research.     

More than words: the chemistry behind the interactions in the plant holobiont

Plants and microbes have evolved sophisticated ways to communicate and coexist. The simplest interactions that occur in plant-associated habitats, i.e., those involved in disease detection, depend on the production of microbial pathogenic and virulence factors and the host's evolved immunological response. In contrast, microbes can also be beneficial for their host plants in a number of ways, including fighting pathogens and promoting plant growth. In order to clarify the mechanisms directly involved in these various plant–microbe interactions, we must still deepen our understanding of how these interkingdom communication systems, which are constantly modulated by resident microbial activity, are established and, most importantly, how their effects can span physically separated plant compartments. Efforts in this direction have revealed a complex and interconnected network of molecules and associated metabolic pathways that modulate plant–microbe and microbe–microbe communication pathways to regulate diverse ecological responses. Once sufficiently understood, these pathways will be biotechnologically exploitable, for example, in the use of beneficial microbes in sustainable agriculture. The aim of this review is to present the latest findings on the dazzlingly diverse arsenal of molecules that efficiently mediate specific microbe–microbe and microbe–plant communication pathways during plant development and on different plant organs.     

Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved

 Biological control of plant pathogens is currently accepted as a key practice in sustainable agriculture because it is based on the management of a natural resource, i.e. certain rhizosphere organisms, common components of ecosystems, known to develop antagonistic activities against harmful organisms (bacteria, fungi, nematodes etc.). Arbuscular mycorrhizal (AM) associations have been shown to reduce damage caused by soil-borne plant pathogens. Although few AM isolates have been tested in this regard, some appear to be more effective than others. Furthermore, the degree of protection varies with the pathogen involved and can be modified by soil and other environmental conditions. This prophylactic ability of AM fungi could be exploited in cooperation with other rhizospheric microbial angatonists to improve plant growth and health. Despite past achievements on the application of AM in plant protection, further research is needed for a better understanding of both the ecophysiological parameters contributing to effectiveness and of the mechanisms involved. Although the improvement of plant nutrition, compensation for pathogen damage, and competition for photosynthates or colonization/infection sites have been claimed to play a protective role in the AM symbiosis, information is scarce, fragmentary or even controversial, particularly concerning other mechanisms. Such mechanisms include (a) anatomical or morphological AM-induced changes in the root system, (b) microbial changes in rhizosphere populations of AM plants, and (c) local elicitation of plant defence mechanisms by AM fungi. Although compounds typically involved in plant defence reactions are elicited by AM only in low amounts, they could act locally or transiently by making the root more prone to react against pathogens. Current research based on molecular, immunological and histochemical techniques is providing new insights into these mechanisms. Accepted: 29 October 1996     

Biological costs and benefits to plant-microbe interactions in the rhizosphere

This review looks briefly at plants and their rhizosphere microbes, the chemical communications that exist, and the biological processes they sustain. Primarily it is the loss of carbon compounds from roots that drives the development of enhanced microbial populations in the rhizosphere when compared with the bulk soil, or that sustains specific mycorrhizal or legume associations. The benefits to the plant from this carbon loss are discussed. Overall the general rhizosphere effect could help the plant by maintaining the recycling of nutrients, through the production of hormones, helping to provide resistance to microbial diseases and to aid tolerance to toxic compounds. When plants lack essential mineral elements such as P or N, symbiotic relationships can be beneficial and promote plant growth. However, this benefit may be lost in well-fertilized (agricultural) soils where nutrients are readily available to plants and symbionts reduce growth. Since these rhizosphere associations are commonplace and offer key benefits to plants, these interactions would appear to be essential to their overall success.     

Wired to the roots: Impact of root-beneficial microbe interactions on aboveground plant physiology and protection

Often, plant-pathogenic microbe interactions are discussed in a host-microbe two-component system, however very little is known about how the diversity of rhizospheric microbes that associate with plants affect host performance against pathogens. There are various studies, which specially direct the importance of induced systemic defense (ISR) response in plants interacting with beneficial rhizobacteria, yet we don’t know how rhizobacterial associations modulate plant physiology. In here, we highlight the many dimensions within which plant roots associate with beneficial microbes by regulating aboveground physiology. We review approaches to study the causes and consequences of plant root association with beneficial microbes on aboveground plant-pathogen interactions. The review provides the foundations for future investigations into the impact of the root beneficial microbial associations on plant performance and innate defense responses.     

Soil microbial diversity and the sustainability of agricultural soils

Many world ecosystems are in various states of decline evidenced by erosion, low productivity, and poor water quality caused by forest clearing, intensive agricultural production, and continued use of land resources for purposes that are not sustainable. The biological diversity of these systems is being altered. Little research has been conducted to quantify the beneficial relationships between microbial diversity, soil and plant quality, and ecosystem sustainability. Ecosystem functioning is governed largely by soil microbial dynamics. Differences in microbial properties and activities of soils have been reported but are restricted to general ecological enumeration methods or activity levels, which are limited in their ability to describe a particular ecosystem. Microbial populations and their responses to stresses have been traditionally studied at the process level, in terms of total numbers of microorganisms, biomass, respiration rates, and enzyme activities, with little attention being paid to responses at the community or the organismal levels. These process level measurements, although critical to understanding the ecosystem, may be insensitive to community level changes due to the redundancy of these functions. As microbial communities comprise complex interactions between diverse organisms, they should be studied as such, and not as a black box into which inputs are entered and outputs are received at measured rates. Microbial communities and their processes need to be examined in relation to not only the individuals that comprise the community, but the effect of perturbations or environmental stresses on those communities.     

How do earthworms affect microfloral and faunal community diversity?

Much of the work regarding earthworm effects on other organisms has focused on the functional significance of microbial-earthworm interactions, and little is known on the effects of earthworms on microfloral and faunal diversity. Earthworms can affect soil microflora and fauna populations directly and indirectly by three main mechanisms: (1) comminution, burrowing and casting; (2) grazing; (3) dispersal. These activities change the soil's physico-chemical and biological status and may cause drastic shifts in the density, diversity, structure and activity of microbial and faunal communities within the drilosphere. Certain organisms and species may be enhanced, reduced or not be affected at all depending on their ability to adapt to the particular conditions of different earthworm drilospheres. A large host of factors (including CaCO₃, enzymes, mucus and antimicrobial substances) influence the ability of preferentially or randomly ingested organisms to survive (or not) passage through the earthworm gut, and their resultant capacity to recover and proliferate (or not) in earthworm casts. Small organisms, particularly microflora and microfauna, with limited ability to move within the soil, may benefit from the (comparatively) long ranging movements of earthworms. Microflora and smaller fauna appear to be particularly sensitive to earthworm activities, and priming effects enhancing nutrient release, particularly in casts, are common. Larger fauna such as microarthropods, enchytraeids and Isopods may be enhanced under some conditions (e.g., in earthworm middens), but in other cases earthworm activity may lead to a decrease in their populations due to competition for food (microbes and organic materials), and spatial and temporal changes in food abundance. Nevertheless, considering the presently available data, the beneficial interactions of earthworms and microflora and fauna appear to far outweigh the potential negative effects. However, much is still unknown regarding the interactions of earthworms of different ecological categories on the diversity and function of microfloral and faunal communities, and much more interdisciplinary research is needed to assess the potential role of earthworms in regulating the diversity of microflora and fauna in soil systems and the potentially beneficial or harmful effects this regulation may have on ecosystem function and plant growth in different ecosystems.     

New frontiers in agriculture productivity: Optimised microbial inoculants and in situ microbiome engineering

Increasing agricultural productivity is critical to feed the ever-growing human population. Being linked intimately to plant health, growth and productivity, harnessing the plant microbiome is considered a potentially viable approach for the next green revolution, in an environmentally sustainable way. In recent years, our understanding of drivers, roles, mechanisms, along with knowledge to manipulate the plant microbiome, have significantly advanced. Yet, translating this knowledge to expand farm productivity and sustainability requires the development of solutions for a number of technological and logistic challenges. In this article, we propose new and emerging strategies to improve the survival and activity of microbial inoculants, including using selected indigenous microbes and optimising microbial delivery methods, as well as modern gene editing tools to engineer microbial inoculants. In addition, we identify multiple biochemical and molecular mechanisms and/approaches which can be exploited for microbiome engineering in situ to optimise plant-microbiome interactions for improved farm yields. These novel biotechnological approaches can provide effective tools to attract and maintain activities of crop beneficial microbiota that increase crop performance in terms of nutrient acquisition, and resistance to biotic and abiotic stresses, resulting in an increased agricultural productivity and sustainability.     

Inbreeding Alters Activities of the Stress-Related Enzymes Chitinases and β-1,3-Glucanases

Pathogenesis-related proteins, chitinases (CHT) and β-1,3-glucanases (GLU), are stress proteins up-regulated as response to extrinsic environmental stress in plants. It is unknown whether these PR proteins are also influenced by inbreeding, which has been suggested to constitute intrinsic genetic stress, and which is also known to affect the ability of plants to cope with environmental stress. We investigated activities of CHT and GLU in response to inbreeding in plants from 13 Ragged Robin (Lychnis flos-cuculi) populations. We also studied whether activities of these enzymes were associated with levels of herbivore damage and pathogen infection in the populations from which the plants originated. We found an increase in pathogenesis-related protein activity in inbred plants from five out of the 13 investigated populations, which suggests that these proteins may play a role in how plants respond to intrinsic genetic stress brought about by inbreeding in some populations depending on the allele frequencies of loci affecting the expression of CHT and the past levels of inbreeding. More importantly, we found that CHT activities were higher in plants from populations with higher levels of herbivore or pathogen damage, but inbreeding reduced CHT activity in these populations disrupting the increased activities of this resistance-related enzyme in populations where high resistance is beneficial. These results provide novel information on the effects of plant inbreeding on plant-enemy interactions on a biochemical level.     

Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads

Here we characterized the effect of the ectomycorrhizal symbiosis on the genotypic and functional diversity of soil Pseudomonas fluorescens populations and analysed its possible consequences in terms of plant nutrition, development and health. Sixty strains of P. fluorescens were isolated from the bulk soil of a forest nursery, the ectomycorrhizosphere and the ectomycorrhizas of the Douglas fir (Pseudostuga menziesii) seedlings-Laccaria bicolor S238N. They were characterized in vitro with the following criteria: ARDRA, phosphate solubilization, siderophore, HCN and AIA production, genes of N2-fixation and antibiotic synthesis, in vitro confrontation with a range of phytopathogenic and ectomycorrhizal fungi, effect on the Douglas fir-L. bicolor symbiosis. For most of these criteria, we demonstrated that the ectomycorrhizosphere significantly structures the P. fluorescens populations and selects strains potentially beneficial to the symbiosis and to the plant. This prompts us to propose the ectomycorrhizal symbiosis as a true microbial complex where multitrophic interactions take place. Moreover it underlines the fact that this symbiosis has an indirect positive effect on plant growth, via its selective pressure on bacterial communities, in addition to its known direct positive effect.     

Seed mucilage interacts with soil microbial community and physiochemical processes to affect seedling emergence on desert sand dunes

Seedling emergence is a critical stage in the establishment of desert plants. Soil microbes participate in plant growth and development, but information is lacking with regard to the role of microbes on seedling emergence. We applied the biocides (captan and streptomycin) to assess how seed mucilage interacts with soil microbial community and physiochemical processes to affect seedling emergence of Artemisia sphaerocephala on the desert sand dune. Fungal and bacterial community composition and diversity and fungal–bacterial interactions were changed by both captan and streptomycin. Mucilage increased soil enzyme activities and fungal–bacterial interactions. Highest seedling emergence occurred under streptomycin and mucilage treatment. Members of the phyla Firmicutes and Glomeromycota were the keystone species that improved A. sphaerocephala seedling emergence, by increasing resistance of young seedlings to drought and pathogen. Seed mucilage directly improved seedling emergence and indirectly interacted with the soil microbial community through strengthening fungal–bacterial interactions and providing favourable environment for soil enzymes to affect seedling emergence. Our study provides a comprehensive understanding of the regulatory mechanisms by which soil microbial community and seed mucilage interactively promote successful establishment of populations of desert plants on the barren and stressful sand dune.     

Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions

A wide variety of microorganisms known to produce auxin and auxin precursors form beneficial relationships with plants and alter host root development. Moreover, other signals produced by microorganisms affect auxin pathways in host plants. However, the precise role of auxin and auxin‐signalling pathways in modulating plant–microbe interactions is unknown. Dissecting out the auxin synthesis, transport and signalling pathways resulting in the characteristic molecular, physiological and developmental response in plants will further illuminate upon how these intriguing inter‐species interactions of environmental, ecological and economic significance occur. The present review seeks to survey and summarize the scattered evidence in support of known host root modifications brought about by beneficial microorganisms and implicate the role of auxin synthesis, transport and signal transduction in modulating beneficial effects in plants. Finally, through a synthesis of the current body of work, we present outstanding challenges and potential future research directions on studies related to auxin signalling in plant–microbe interactions.     

The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments

Both biotic and abiotic stresses are major constrains to agricultural production. Under stress conditions, plant growth is affected by a number of factors such as hormonal and nutritional imbalance, ion toxicity, physiological disorders, susceptibility to diseases, etc. Plant growth under stress conditions may be enhanced by the application of microbial inoculation including plant growth promoting rhizobacteria (PGPR) and mycorrhizal fungi. These microbes can promote plant growth by regulating nutritional and hormonal balance, producing plant growth regulators, solubilizing nutrients and inducing resistance against plant pathogens. In addition to their interactions with plants, these microbes also show synergistic as well as antagonistic interactions with other microbes in the soil environment. These interactions may be vital for sustainable agriculture because they mainly depend on biological processes rather than on agrochemicals to maintain plant growth and development as well as proper soil health under stress conditions. A number of research articles can be deciphered from the literature, which shows the role of rhizobacteria and mycorrhizae alone and/or in combination in enhancing plant growth under stress conditions. However, in contrast, a few review papers are available which discuss the synergistic interactions between rhizobacteria and mycorrhizae for enhancing plant growth under normal (non-stress) or stressful environments. Biological interactions between PGPR and mycorrhizal fungi are believed to cause a cumulative effect on all rhizosphere components, and these interactions are also affected by environmental factors such as soil type, nutrition, moisture and temperature. The present review comprehensively discusses recent developments on the effectiveness of PGPR and mycorrhizal fungi for enhancing plant growth under stressful environments. The key mechanisms involved in plant stress tolerance and the effectiveness of microbial inoculation for enhancing plant growth under stress conditions have been discussed at length in this review. Growth promotion by single and dual inoculation of PGPR and mycorrhizal fungi under stress conditions have also been discussed and reviewed comprehensively.     

The importance of reproductive interference in ecology and evolution: from organisms to communities

Knowledge of species interactions is vital to understand ecological and evolutionary patterns in nature. Traditional species interactions (e.g., competition, predation, symbiosis) have received a great deal of deserved attention and their general importance in shaping the evolution of populations and structure of communities is unquestioned. Recently, reproductive interference has been receiving attention as an important species interaction. Reproductive interference is defined as interspecific reproductive activities that decrease the fitness of at least one of the species involved in the interaction. Reproductive interference has the potential to affect the evolutionary trajectories of populations and structure of communities. Here, I comment on seven papers that make up this special feature on reproductive interference. Along the way I highlight key discoveries of these studies and areas of research that may contribute to our understanding of the causes and consequences of reproductive interference.     

植物内生菌的研究进展

植物内生菌是存在于植物内部与植物密不可分的一类微生物,包括内生真菌和内生细菌两大类。随着研究的不断深入,发现内生菌不仅产生多种有益的生物学作用,如防病、促生、固氮等,还能对寄主植物的生长发育产生不利影响。近年来,植物内生菌已成为我国微生物学领域研究的热点问题之一。本文综述了植物内生真菌和内生细菌的研究概况,以期更好地研究和了解植物内生菌。     

The role of plant-associated rhizobacteria in plant growth,biocontrol and abiotic stress management

The rhizosphere is the region around the plant roots where maximum microbial activities occur. In the rhizosphere, microorganisms' beneficial and harmful activities affect plant growth and development. The mutualistic rhizospheric bacteria which improve plant growth and health are known as plant growth-promoting rhizobacteria (PGPR). They are very important due to their ability to help the plant in diverse ways. PGPR such as Pseudomonas, Bacillus, Azospirillum, Azotobacter, Arthrobacter, Achromobacter, Micrococcus, Enterobacter, Rhizobium, Agrobacterium, Pantoea and Serratia are now very well known. Rhizomicrobiome plays critical roles in nutrient acquisition and assimilation, improved soil texture, secreting and modulating extracellular molecules such as hormones, secondary metabolites, antibiotics and various signal compounds, all leading to the enhancement of plant growth and development. The microbes and compounds they secrete constitute valuable biostimulants and play pivotal roles in modulating plant stress responses. In this review, we highlight the rhizobacteria diversity and cutting-edge findings focusing on the role of a PGPR in plant growth and development. We also discussed the role of PGPR in resisting the adverse effects arising from various abiotic (drought, salinity, heat, heavy metals) stresses.