Modulation of host immunity by beneficial microbes

In nature, plants abundantly form beneficial associations with soilborne microbes that are important for plant survival and, as such, affect plant biodiversity and ecosystem functioning. Classical examples of symbiotic microbes are mycorrhizal fungi that aid in the uptake of water and minerals, and Rhizobium bacteria that fix atmospheric nitrogen for the plant. Several other types of beneficial soilborne microbes, such as plant-growth-promoting rhizobacteria and fungi with biological control activity, can stimulate plant growth by directly suppressing deleterious soilborne pathogens or by priming aboveground plant parts for enhanced defense against foliar pathogens or insect herbivores. The establishment of beneficial associations requires mutual recognition and substantial coordination of plant and microbial responses. A growing body of evidence suggests that beneficial microbes are initially recognized as potential invaders, after which an immune response is triggered, whereas, at later stages of the interaction, mutualists are able to short-circuit plant defense responses to enable successful colonization of host roots. Here, we review our current understanding of how symbiotic and nonsymbiotic beneficial soil microbes modulate the plant immune system and discuss the role of local and systemic defense responses in establishing the delicate balance between the two partners.     

Endophyte roles in nutrient acquisition,root system architecture development and oxidative stress tolerance

Plants associate with communities of microbes (bacteria and fungi) that play critical roles in plant development, nutrient acquisition and oxidative stress tolerance. The major share of plant microbiota is endophytes which inhabit plant tissues and help them in various capacities. In this article, we have reviewed what is presently known with regard to how endophytic microbes interact with plants to modulate root development, branching, root hair formation and their implications in overall plant development. Endophytic microbes link the interactions of plants, rhizospheric microbes and soil to promote nutrient solubilization and further vectoring these nutrients to the plant roots making the soil-plant-microbe continuum. Further, plant roots internalize microbes and oxidatively extract nutrients from microbes in the rhizophagy cycle. The oxidative interactions between endophytes and plants result in the acquisition of nutrients by plants and are also instrumental in oxidative stress tolerance of plants. It is evident that plants actively cultivate microbes internally, on surfaces and in soils to acquire nutrients, modulate development and improve health. Understanding this continuum could be of greater significance in connecting endophytes with the hidden half of the plant that can also be harnessed in applied terms to enhance nutrient acquisition through the development of favourable root system architecture for sustainable production under stress conditions.     

Plant interactions with microbes and insects: from molecular mechanisms to ecology

Plants are members of complex communities and interact both with antagonists and beneficial organisms. An important question in plant defense-signaling research is how plants integrate signals induced by pathogens, beneficial microbes and insects into the most appropriate adaptive response. Molecular and genomic tools are now being used to uncover the complexity of the induced defense signaling networks that have evolved during the arms races between plants and their attackers. Molecular biologists and ecologists are joining forces to place molecular mechanisms of plant defense into an ecological perspective. Here, we review our current understanding of the molecular mechanisms of induced plant defense and their potential ecological relevance in nature.     

Plants as green phones: Novel insights into plant-mediated communication between below- and above-ground insects

Plants can act as vertical communication channels or ‘green phones’ linking soil-dwelling insects and insects in the aboveground ecosystem. When root-feeding insects attack a plant, the direct defense system of the shoot is activated, leading to an accumulation of phytotoxins in the leaves. The protection of the plant shoot elicited by root damage can impair the survival, growth and development of aboveground insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and insects that develop in the aboveground ecosystem. The interactions between spatially separated insects below- and aboveground are not restricted to root and foliar plant-feeding insects, but can be extended to higher trophic levels such as insect parasitoids. Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked by root-feeding insects are significantly less attractive for the parasitoids of foliar-feeding insects.Key words: above-belowground interactions, green phones, multitrophic plant-insect interactions, plant defense, plant volatiles, parasitoids     

Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions.     

植物与土壤微生物在调控生态系统养分循环中的作用

陆地生态系统的地上、地下是相互联系的。植物与土壤微生物作为陆地生态系统中的重要组成部分, 它们之间的相互作用是生态系统地上、地下结合的重要纽带。该文首先介绍了植物在养分循环中对营养元素的吸收、积累和归还等作用, 阐述了土壤微生物对养分有效性及土壤质量具有重要的作用。其次, 重点综述了植物与土壤微生物之间相互依存、相互竞争的关系。植物通过其凋落物与分泌物为土壤微生物提供营养, 土壤微生物作为分解者提供植物可吸收的营养元素, 比如共生体菌根真菌即可使植物根与土壤真菌达到互惠。然而, 植物的养分吸收与微生物的养分固持同时存在, 因而两者之间存在对养分的竞争。通过植物多样性对土壤微生物多样性的影响分析, 以及土壤微生物直接或间接作用于植物多样性和生产力的分析, 探讨了植物物种多样性与土壤微生物多样性之间的内在联系。针对当前植物与土壤微生物对养分循环的调控机制的争论, 提出植物凋落物是调节植物与土壤微生物养分循环的良好媒介, 植物与土壤微生物的共同作用对维持整个生态系统的稳定性具有重要意义。也指出了目前在陆地生态系统地上、地下研究中存在的不足和亟待解决的问题。     

The rhizosphere microbiome: Plant–microbial interactions for resource acquisition

While horticulture tools and methods have been extensively developed to improve the management of crops, systems to harness the rhizosphere microbiome to benefit plant crops are still in development. Plants and microbes have been coevolving for several millennia, conferring fitness advantages that expand the plant’s own genetic potential. These beneficial associations allow the plants to cope with abiotic stresses such as nutrient deficiency across a wide range of soils and growing conditions. Plants achieve these benefits by selectively recruiting microbes using root exudates, positively impacting their nutrition, health and overall productivity. Advanced knowledge of the interplay between root exudates and microbiome alteration in response to plant nutrient status, and the underlying mechanisms there of, will allow the development of technologies to increase crop yield. This review summarizes current knowledge and perspectives on plant–microbial interactions for resource acquisition and discusses promising advances for manipulating rhizosphere microbiomes and root exudation.     

A soil-free root observation system for the study of root-microorganism interactions in maize

Background and aims

The root surface of a plant usually exceeds the leaf area and is constantly exposed to a variety of soil-borne microorganisms. Root pathogens and pests, as well as belowground interactions with beneficial microbes, can significantly influence a plants' performance. Unfortunately, the analysis of these interactions is often limited because of the arduous task of accessing roots growing in soil. Here, we present a soil-free root observation system (SF-ROBS) designed to grow maize (Zea mays) plants and to study root interactions with either beneficial or pathogenic microbes.

Methods

The SF-ROBS consists of pouches lined with wet filter paper supplying nutrient solution.

Results

The aspect of maize grown in the SF-ROBS was similar to soil-grown maize; the plant growth was similar for the shoot but different for the roots (biomass and length increased in the SF-ROBS). SF-ROBS-grown roots were successfully inoculated with the hemi-biotrophic maize fungal pathogen Colletotrichum graminicola and the beneficial rhizobacteria Pseudomonas putida KT2440. Thus, the SF-ROBS is a system suitable to study two major belowground phenomena, namely root fungal defense reactions and interactions of roots with beneficial soil-borne bacteria.

Conclusions

This system contributes to a better understanding of belowground plant microbe interactions in maize and most likely also in other crops.     

Colorado potato beetle manipulates plant defenses in local and systemic leaves

Herbivore microbial associates can affect diverse interactions between plants and insect herbivores. Some insect symbionts enable herbivores to expand host plant range or to facilitate host plant use by modifying plant physiology. However, little attention has been paid to the role of herbivore-associated microbes in manipulating plant defenses. We have recently shown that Colorado potato beetle secrete the symbiotic bacteria to suppress plant defenses. The bacteria in oral secretions from the beetle hijack defense signaling pathways of host plants and the suppression of induced plant defenses benefits the beetle’s performance. While the defense suppression by the beetle-associated bacteria has been investigated in local damaged leaves, little is known about the effects of the symbiotic bacteria on the manipulation of plant defenses in systemic undamaged leaves. Here, we demonstrate that the symbiotic bacteria suppress plant defenses in both local and systemic tissues when plants are attacked by antibiotic-untreated larvae.     

Allocation,stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology?

Despite the crucial role of carbon transport in whole plant physiology and its impact on plant–environment interactions and ecosystem function, relatively little research has tried to examine how phloem physiology impacts plant ecology. In this review, we highlight several areas of active research where inquiry into phloem physiology has increased our understanding of whole plant function and ecological processes. We consider how xylem–phloem interactions impact plant drought tolerance and reproduction, how phloem transport influences carbon allocation in trees and carbon cycling in ecosystems and how phloem function mediates plant relations with insects, pests, microbes and symbiotes. We argue that in spite of challenges that exist in studying phloem physiology, it is critical that we consider the role of this dynamic vascular system when examining the relationship between plants and their biotic and abiotic environment.     

Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis

Aims

Arbuscular mycorrhizal (AM) fungi associate with the majority of terrestrial plants, influencing their growth, nutrient uptake and defence chemistry. Consequently, AM fungi can significantly impact plant-herbivore interactions, yet surprisingly few studies have investigated how AM fungi affect plant responses to root herbivores. This study aimed to investigate how AM fungi affect plant tolerance mechanisms to belowground herbivory.

Methods

We examined how AM fungi affect plant (Saccharum spp. hybrid) growth, nutrient dynamics and secondary chemistry (phenolics) in response to attack from a root-feeding insect (Dermolepida albohirtum).

Results

Root herbivory reduced root mass by almost 27%. In response, plants augmented investment in aboveground biomass by 25%, as well as increasing carbon concentrations. The AM fungi increased aboveground biomass, phosphorus and carbon. Meanwhile, root herbivory increased foliar phenolics by 31% in mycorrhizal plants, and increased arbuscular colonisation of roots by 75% overall. AM fungi also decreased herbivore performance, potentially via increasing root silicon concentrations.

Conclusions

Our results suggest that AM fungi may be able to augment plant tolerance to root herbivory via resource allocation aboveground and, at the same time, enhance plant root resistance by increasing root silicon. The ability of AM fungi to facilitate resource allocation aboveground in this way may be a more widespread strategy for plants to cope with belowground herbivory.

     

Bidirectional plant‐mediated interactions between rhizobacteria and shoot‐feeding herbivorous insects: a community ecology perspective

1. Plants interact with various organisms, aboveground as well as belowground. Such interactions result in changes in plant traits with consequences for members of the plant‐associated community at different trophic levels. Research thus far focussed on interactions of plants with individual species. However, studying such interactions in a community context is needed to gain a better understanding.
2. Members of the aboveground insect community induce defences that systemically influence plant interactions with herbivorous as well as carnivorous insects. Plant roots are associated with a community of plant‐growth promoting rhizobacteria (PGPR). This PGPR community modulates insect‐induced defences of plants. Thus, PGPR and insects interact indirectly via plant‐mediated interactions.
3. Such plant‐mediated interactions between belowground PGPR and aboveground insects have usually been addressed unidirectionally from belowground to aboveground. Here, we take a bidirectional approach to these cross‐compartment plant‐mediated interactions.
4. Recent studies show that upon aboveground attack by insect herbivores, plants may recruit rhizobacteria that enhance plant defence against the attackers. This rearranging of the PGPR community in the rhizosphere has consequences for members of the aboveground insect community. This review focusses on the bidirectional nature of plant‐mediated interactions between the PGPR and insect communities associated with plants, including (a) effects of beneficial rhizobacteria via modification of plant defence traits on insects and (b) effects of plant defence against insects on the PGPR community in the rhizosphere. We discuss how such knowledge can be used in the development of sustainable crop‐protection strategies.

     

Plant symbionts: keys to the phytosphere

The exterior and interior of plants, aboveground and belowground, comprise a complex plant micro-ecosystem, known in recent years as the phytosphere. There are three components: the phyllosphere, endosphere, and rhizosphere. Although in comparison with other ecosystems the phytosphere is small, it similarly includes a great variety of functional microbes. Among these are certain microbes that live in symbiotic relationships with plants; these microbes are known as plant symbionts. Recent research has shown that these symbionts have tremendous effects on plant growth, confer resistance to abiotic stresses and pathogens, aid in the accumulation of metabolites, and have crucial relationships with other plant-associated microbes in the phytosphere. We review the ecological effects of plant symbionts on other microbes, and interactions between plant symbionts in the phytosphere. In addition, we discuss internal mechanisms and suggest future hot spots for research.     

A Novel Interaction between Plant-Beneficial Rhizobacteria and Roots: Colonization Induces Corn Resistance against the Root Herbivore Diabrotica speciosa

A number of soil-borne microorganisms, such as mycorrhizal fungi and rhizobacteria, establish mutualistic interactions with plants, which can indirectly affect other organisms. Knowledge of the plant-mediated effects of mutualistic microorganisms is limited to aboveground insects, whereas there is little understanding of what role beneficial soil bacteria may play in plant defense against root herbivory. Here, we establish that colonization by the beneficial rhizobacterium Azospirillum brasilense affects the host selection and performance of the insect Diabrotica speciosa. Root larvae preferentially orient toward the roots of non-inoculated plants versus inoculated roots and gain less weight when feeding on inoculated plants. As inoculation by A. brasilense induces higher emissions of (E)-β-caryophyllene compared with non-inoculated plants, it is plausible that the non-preference of D. speciosa for inoculated plants is related to this sesquiterpene, which is well known to mediate belowground insect-plant interactions. To the best of our knowledge, this is the first study showing that a beneficial rhizobacterium inoculant indirectly alters belowground plant-insect interactions. The role of A. brasilense as part of an integrative pest management (IPM) program for the protection of corn against the South American corn rootworm, D. speciosa, is considered.     

Effect of long-term organic and mineral fertilization strategies on rhizosphere microbiota assemblage and performance of lettuce

Long-term agricultural fertilization strategies gradually change soil properties including the associated microbial communities. Cultivated crops recruit beneficial microbes from the surrounding soil environment via root exudates. In this study, we aimed to investigate the effects of long-term fertilization strategies across field sites on the rhizosphere prokaryotic (Bacteria and Archaea) community composition and plant performance. We conducted growth chamber experiments with lettuce (Lactuca sativa L.) cultivated in soils from two long-term field experiments, each of which compared organic versus mineral fertilization strategies. 16S rRNA gene amplicon sequencing revealed the assemblage of a rhizosphere core microbiota shared in all lettuce plants across soils, going beyond differences in community composition depending on field site and fertilization strategies. The enhanced expression of several plant genes with roles in oxidative and biotic stress signalling pathways in lettuce grown in soils with organic indicates an induced physiological status in plants. Lettuce plants grown in soils with different fertilization histories were visibly free of stress symptoms and achieved comparable biomass. This suggests a positive aboveground plant response to belowground plant–microbe interactions in the rhizosphere. Besides effects of fertilization strategy and field site, our results demonstrate the crucial role of the plant in driving rhizosphere microbiota assemblage.     

How genetic modification of roots affects rhizosphere processes and plant performance

Genetic modification of plants has become common practice. However, root-specific genetic modifications have only recently been advocated. Here, a review is presented regarding how root-specific modifications can have both plant internal and rhizosphere-mediated effects on aboveground plant properties and plant performance. Plant internal effects refer to pleiotropic processes such as transportation of the modified gene product. Rhizosphere-mediated effects refer to altered plant-rhizosphere interactions, which subsequently feed back to the plant. Such plant-soil feedback mechanisms have been demonstrated both in natural systems and in crops. Here how plant internal and rhizosphere-mediated effects could enhance or counteract improvements in plant properties for which the genetic modification was intended is discussed. A literature survey revealed that rice is the most commonly studied crop species in the context of root-specific transgenesis, predominantly in relation to stress tolerance. Phytoremediation, a process in which plants are used to clean up pollutants, is also often an objective when transforming roots. These two examples are used to review potential effects of root genetic modifications on shoots. There are several examples in which root-specific genetic modifications only lead to better plant performance if the genes are specifically expressed in roots. Constitutive expression can even result in modified plants that perform worse than non-modified plants. Rhizosphere effects have rarely been examined, but clearly genetic modification of roots can influence rhizosphere interactions, which in turn can affect shoot properties. Indeed, field studies with root-transformed plants frequently show negative effects on shoots that are not seen in laboratory studies. This might be due to the simplified environments that are used in laboratories which lack the full range of plant-rhizosphere interactions that are present in the field.     

Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

Plants engage in complex multipartite interactions with mutualists and antagonists, but these interactions are rarely included in studies that explore plant invasiveness. When considered in isolation, we know that beneficial microbes can enhance an exotic plant’s invasive ability and that herbivorous insects often decrease an exotic plant’s likeliness of success. However, the effect of these partners on plant fitness has not been well characterized when all three species coevolve. We use computational evolutionary modeling of a trait-based system to test how microbes and herbivores simultaneously coevolving with an invading plant affect the invaders’ probability of becoming established. Specifically, we designed a model that explores how a beneficial microbe would influence the outcome of an interaction between a plant and herbivore. To model novel interactions, we included a phenotypic trait shared by each species. Making this trait continuous and selectable allows us to explore how trait similarities between coevolving plants, herbivores and microbes affect fitness. Using this model, we answer the following questions: (1) Can a beneficial plant-microbe interaction influence the evolutionary outcome of antagonistic interactions between plants and herbivores? (2) How does the initial trait similarity between interacting organisms affect the likelihood of plant survival in novel locations? (3) Does the effect of tripartite interactions on the invasion success of a plant depend on whether organisms interact through trait similarity [Enemy Release Hypothesis (ERH)] or dissimilarity (Biotic Resistance Hypothesis)? We found that it was much more difficult for plants to invade under the ERH but that beneficial microbes increase the probability of plant survival in a novel range under both hypotheses. To our knowledge, this model is the first to use tripartite interactions to explore novel species introductions. It represents a step towards gaining a better understanding of the factors influencing establishment of exotic species to prevent future invasions.     

Non‐pathogenic rhizobacteria interfere with the attraction of parasitoids to aphid‐induced plant volatiles via jasmonic acid signalling

Beneficial soil‐borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col‐0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant‐mediated interaction between the non‐pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore‐induced plant volatiles. The volatile blend from rhizobacteria‐treated aphid‐infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid‐infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore‐induced volatiles and parasitoid response to aphid‐infested plants is lost in an Arabidopsis mutant (aos/dde2‐2) that is impaired in jasmonic acid production. By modifying the blend of herbivore‐induced plant volatiles that depend on the jasmonic acid‐signalling pathway, root‐colonizing microbes interfere with the attraction of parasitoids of leaf herbivores.     

生长素在微生物调控根发育过程中的作用

很多微生物通过分泌生长素和生长素前体与植物建立了有益的关系并改变植物根系的形态结构,此外,微生物分泌的其他代谢产物也能改变植物生长素信号通路。因此,生长素和生长素信号通路在微生物调控植物根系发育的过程中起着至关重要的作用。该文从生长素合成、生长素信号和生长素极性运输3个方面总结了生长素在微生物调控植物根系发育过程中的作用,主要包括微生物增加了植物内源生长素的含量、增强了生长素的信号和调控PIN蛋白的表达水平,进而如何调控植物生理和分子水平来适应微生物对其根系的改变,为进一步开展该方面的研究奠定了基础。