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.     

共生菌与昆虫的免疫

共生菌可通过产生抗菌物质、调控宿主免疫相关基因和微生物种间竞争作用等方式保护昆虫宿主免受病原体的侵染。为维持共生关系,昆虫进化出精细的调控机制避免对共生菌的过激免疫应答,共生菌通过免疫识别信号多态性或化学拟态来降低或躲避宿主免疫系统对自身的伤害。本文在分析共生菌对宿主免疫的功能及其机制的基础上,探讨宿主对免疫应答的精准调控以及共生体系的协同进化,以期为共生菌对宿主免疫影响的深入研究提供参考。     

Insect endosymbionts: manipulators of insect herbivore trophic interactions?

Throughout their evolutionary history, insects have formed multiple relationships with bacteria. Although many of these bacteria are pathogenic, with deleterious effects on the fitness of infected insects, there are also numerous examples of symbiotic bacteria that are harmless or even beneficial to their insect host. Symbiotic bacteria that form obligate or facultative associations with insects and that are located intracellularly in the host insect are known as endosymbionts. Endosymbiosis can be a strong driving force for evolution when the acquisition and maintenance of a microorganism by the insect host results in the formation of novel structures or changes in physiology and metabolism. The complex evolutionary dynamics of vertically transmitted symbiotic bacteria have led to distinctive symbiont genome characteristics that have profound effects on the phenotype of the host insect. Symbiotic bacteria are key players in insect–plant interactions influencing many aspects of insect ecology and playing a key role in shaping the diversification of many insect groups. In this review, we discuss the role of endosymbionts in manipulating insect herbivore trophic interactions focussing on their impact on plant utilisation patterns and parasitoid biology.     

Bacterial adaptation to life in association with plants - A proteomic perspective from culture to in situ conditions

Diverse bacterial taxa that live in association with plants affect plant health and development. This is most evident for those bacteria that undergo a symbiotic association with plants or infect the plants as pathogens. Proteome analyses have contributed significantly toward a deeper understanding of the molecular mechanisms underlying the development of these associations. They were applied to obtain a general overview of the protein composition of these bacteria, but more so to study effects of plant signaling molecules on the cytosolic proteome composition or metabolic adaptations upon plant colonization. Proteomic analyses are particularly useful for the identification of secreted proteins, which are indispensable to manipulate a host plant. Recent advances in the field of proteome analyses have initiated a new research area, the analysis of more complex microbial communities. Such studies are just at their beginning but hold great potential for the future to elucidate not only the interactions between bacteria and their host plants, but also of bacteria-bacteria interactions between different bacterial taxa when living in association with plants. These include not only the symbiotic and pathogenic bacteria, but also the commensal bacteria that are consistently found in association with plants and whose functions remain currently largely uncovered.     

Conservation and divergence of signalling pathways between roots and soil microbes – the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls

This review compares endophytic symbiotic and pathogenic root–microbe interactions and examines how the development of root structures elicited by various micro-organisms could have evolved by recruitment of existing plant developmental pathways. Plants are exposed to a multitude of soil micro-organisms which affect root development and performance. Their interactions can be of symbiotic and pathogenic nature, both of which can result in the formation of new root structures – how does the plant regulate the different outcomes of interactions with microbes? The idea that pathways activated in plant by micro-organisms could have been `hijacked' from plant developmental pathways is not new, it was essentially proposed by P. S. Nutman in 1948, but at that time, the molecular evidence to support that hypothesis was missing. Genetic evidence for overlaps between different plant–microbe interactions have previously been examined. This review compares the physiological and molecular plant responses to symbiotic rhizobia with those to arbuscular mycorrhizal fungi, pathogenic nematodes and the development of lateral roots and summarises evidence from both molecular and cellular studies for substantial overlaps in the signalling pathways underlying root–micro-organism interactions. A more difficult question has been why plant responses to micro-organisms are so similar, even though the outcomes are very different. Possible hypotheses for divergence of signalling pathways and future approaches to test these ideas are presented.     

The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice,citrus and crucifers

Background  

Lipopolysaccharide (LPS) is a pathogen associated molecular pattern (PAMP) of animal and plant pathogenic bacteria. Variation at the interstrain level is common in LPS biosynthetic gene clusters of animal pathogenic bacteria. This variation has been proposed to play a role in evading the host immune system. Even though LPS is a modulator of plant defense responses, reports of interstrain variation in LPS gene clusters of plant pathogenic bacteria are rare.     

Plant-Associated Symbiotic Burkholderia Species Lack Hallmark Strategies Required in Mammalian Pathogenesis

Burkholderia is a diverse and dynamic genus, containing pathogenic species as well as species that form complex interactions with plants. Pathogenic strains, such as B. pseudomallei and B. mallei, can cause serious disease in mammals, while other Burkholderia strains are opportunistic pathogens, infecting humans or animals with a compromised immune system. Although some of the opportunistic Burkholderia pathogens are known to promote plant growth and even fix nitrogen, the risk of infection to infants, the elderly, and people who are immunocompromised has not only resulted in a restriction on their use, but has also limited the application of non-pathogenic, symbiotic species, several of which nodulate legume roots or have positive effects on plant growth. However, recent phylogenetic analyses have demonstrated that Burkholderia species separate into distinct lineages, suggesting the possibility for safe use of certain symbiotic species in agricultural contexts. A number of environmental strains that promote plant growth or degrade xenobiotics are also included in the symbiotic lineage. Many of these species have the potential to enhance agriculture in areas where fertilizers are not readily available and may serve in the future as inocula for crops growing in soils impacted by climate change. Here we address the pathogenic potential of several of the symbiotic Burkholderia strains using bioinformatics and functional tests. A series of infection experiments using Caenorhabditis elegans and HeLa cells, as well as genomic characterization of pathogenic loci, show that the risk of opportunistic infection by symbiotic strains such as B. tuberum is extremely low.     

Friends and foes: streptomycetes as modulators of plant disease and symbiosis

The ecological role of soil streptomycetes within the plant root environment is currently gaining increased attention. This review describes our recent advances in elucidating the complex interactions between streptomycetes, plants, pathogenic and symbiotic microorganisms. Streptomycetes play diverse roles in plant-associated microbial communities. Some act as biocontrol agents, inhibiting plant interactions with pathogenic organisms. Owing to the antagonistic properties of streptomycetes, they exert a selective pressure on soil microbes, which may not always be for plant benefit. Others promote the formation of symbioses between plant roots and microbes, and this is in part due to their direct positive influence on the symbiotic partner, expressed as, e.g., promotion of hyphal elongation of symbiotic fungi. Recently, streptomycetes have been identified as modulators of plant defence. By repressing plant responses to pathogens they facilitate root colonisation with pathogenic fungi. In contrast, other strains induce local and systemic resistance against pathogens or enhance plant growth. In conclusion, while streptomycetes have a clear potential of acting as biocontrol agents, care has to be taken to avoid strains that select for virulent pathogens or enhance disease development. We argue towards the use of an integrated screening approach in the search for efficient biocontrol agents, including assays on in vitro antagonism, plant growth, and disease suppression.     

The intestinal flora: the scales without the sword

The intestine is colonised by a vast population of resident bacteria which have established mutualistic relationships with their host throughout evolution, progressing from commensalism to symbiotic interactions. Intestinal bacteria benefit from resources available in their host, but reciprocally provide advantages to their host, by supplying enzymatic activities not encoded in the host genome, by promoting maturation of the intestine and of the gut associated immune system as well as by modifying the host metabolism. The commensal bacteria, although deprived of pathogenic attributes, might however become a danger for the host in case of translocation, acquisition of pathogenic features or via the inappropriate activation of intestinal inflammation. Remarkably, the commensal flora promotes the onset of innate and adaptive immune defences which, in turn, allow to set up a subtle balance between the host and the flora that promotes the symbiosis.     

Bacteria in the plant tissue culture environment

Bacteria and plants are joined in various symbiotic relationships that have developed over millennia and have influenced the evolution of both groups. Bacteria inhabit the surfaces of most plants and are also present inside many plant organs. These bacteria may have positive, neutral or negative impacts on their plant hosts. Probiotic effects may improve plant nutrition or increase resistance to biotic and abiotic stresses. Conversely pathogenic bacteria may kill or reduce the vigor of plant hosts. In addition some bacteria inhabit plants and profit from excess metabolites or shelter while not injuring the plant. Micropropagation of plants is based on the stimulation of organogenesis or embryogenesis from explants that are superficially decontaminated and placed into a sterile environment. If successful, this process removes bacteria from surfaces, but those inhabiting inner tissues and organs are usually not affected by these steriliants. In vitro conditions are designed for optimal plant growth and development, however these conditions are also often ideal for bacterial multiplication. The presence of bacteria in the in vitro environment was almost universally considered negative for plant culture, but more recently this view has been questioned. Certain bacteria appear to have a beneficial effect on the explants in culture; increasing multiplication and rooting, increasing explant quality, and organo- and embryogenesis of recalcitrant genotypes. The most important role of beneficial bacteria for micropropagated plants is likely to be during acclimatization, when growth is resumed under natural conditions. This review includes the role of bacterial interactions in plants, especially those grown in vitro.     

Role of plant defence in alfalfa during symbiosis

During effective symbiosis, rhizobia colonize their hosts, and avoid plant defence mechanisms. To determine whether the host defence responses can be elicited by the symbiotic bacteria, specific markers involved in incompatible pathogenic interactions are required. The available markers of alfalfa defence mechanisms are described and their use in the study of the symbiotic interaction discussed. As defence-related gene expression in roots is not always related to defence mechanisms, other model systems have been established allowing confirmation of an important role of bacterial surface components in alfalfa-Rhizobium meliloti interactions. Nod factors at high concentrations have been shown to elicit defence-like responses in Medicago cell suspensions and roots. Elicitation of defence mechanisms by high levels of Nod factors in Rhizobium-infected roots may be a part of the mechanism by which nodulation is feed-back regulated.The authors are with the Institut des Sciences Végétales, CNRS, F-91198 Gif-sur-Yvette cédex, France.     

Signaling in plant disease resistance and symbiosis

Interactions between plants and microbes result in plant disease and symbiosis. The former causes considerable economic damage in modern agriculture, while the latter has produced great beneficial effects to our agriculture system. Comparison of the two interactions has revealed that a common panel of signaling pathways might participate in the establishment of the equilibrium between plant and microbes or its break-up. Plants appear to detect both pathogenic and symbiotic microbes by a similar set of genes. All symbiotic microbes seem to produce effectors to overcome plant basal defenses and it is speculated that symbiotic effectors have functions similar to pathogenic ones. Signaling molecules, salicylic acid (SA),jasmonic acid (JA) and ethylene (ET), are involved in both plant defense and symbiosis. Switching off signals contributing to deterioration of disease symptom would establish a new equilibrium between plant and pathogenic microbes. This would facilitate the development of strategies for durable disease resistance.     

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.     

Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction

Reactive oxygen species are produced as an early event in plant defense response against avirulent pathogens. We show here that alfalfa responds to infection with Sinorhizobium meliloti by production of superoxide and hydrogen peroxide. This similarity in the early response to infection by pathogenic and symbiotic bacteria addresses the question of which mechanism rhizobia use to counteract the plant defense response.     

Battling enteroinvasive bacteria: Nod1 comes to the rescue

Recognition of pathogenic bacteria by mammalian hosts is largely mediated by membrane-bound Toll-like receptors (TLRs). Recently, a family of cytosolic proteins, termed NODs, with homology to plant disease-resistance gene products has been implicated in sensing microbes within the cytosol. The role of NOD family members in host defense is largely unknown. However, a recent report revealed that Nod1 is a crucial sensor for certain enteroinvasive bacteria that avoid TLR signaling. This finding suggests that Nod1 plays an important role in the initial recognition of pathogenic bacteria at epithelial surfaces, such as the gut, where innate immune responses to commensal bacteria must be avoided.     

Plant-microbe interactions and the new biotechnological methods of plant disease control

Plants constitute an excellent ecosystem for microorganisms. The environmental conditions offered differ considerably between the highly variable aerial plant part and the more stable root system. Microbes interact with plant tissues and cells with different degrees of dependence. The most interesting from the microbial ecology point of view, however, are specific interactions developed by plant-beneficial (either non-symbiotic or symbiotic) and pathogenic microorganisms. Plants, like humans and other animals, also become sick, but they have evolved a sophisticated defense response against microbes, based on a combination of constitutive and inducible responses which can be localized or spread throughout plant organs and tissues. The response is mediated by several messenger molecules that activate pathogen-responsive genes coding for enzymes or antimicrobial compounds, and produces less sophisticated and specific compounds than immunoglobulins in animals. However, the response specifically detects intracellularly a type of protein of the pathogen based on a gene-for-gene interaction recognition system, triggering a biochemical attack and programmed cell death. Several implications for the management of plant diseases are derived from knowledge of the basis of the specificity of plant-bacteria interactions. New biotechnological products are currently being developed based on stimulation of the plant defense response, and on the use of plant-beneficial bacteria for biological control of plant diseases (biopesticides) and for plant growth promotion (biofertilizers). Electronic Publication     

Independent Origins of Vectored Plant Pathogenic Bacteria from Arthropod-Associated <Emphasis Type="Italic">Arsenophonus</Emphasis> Endosymbionts

The genus Arsenophonus (Gammaproteobacteria) is comprised of intracellular symbiotic bacteria that are widespread across the arthropods. These bacteria can significantly influence the ecology and life history of their hosts. For instance, Arsenophonus nasoniae causes an excess of females in the progeny of parasitoid wasps by selectively killing the male embryos. Other Arsenophonus bacteria have been suspected to protect insect hosts from parasitoid wasps or to expand the host plant range of phytophagous sap-sucking insects. In addition, a few reports have also documented some Arsenophonus bacteria as plant pathogens. The adaptation to a plant pathogenic lifestyle seems to be promoted by the infection of sap-sucking insects in the family Cixiidae, which then transmit these bacteria to plants during the feeding process. In this study, we define the specific localization of an Arsenophonus bacterium pathogenic to sugar beet and strawberry plants within the plant hosts and the insect vector, Pentastiridius leporinus (Hemiptera: Cixiidae), using fluorescence in situ hybridization assays. Phylogenetic analysis on 16S rRNA and nucleotide coding sequences, using both maximum likelihood and Bayesian criteria, revealed that this bacterium is not a sister taxon to “Candidatus Phlomobacter fragariae,” a previously characterized Arsenophonus bacterium pathogenic to strawberry plants in France and Japan. Ancestral state reconstruction analysis indicated that the adaptation to a plant pathogenic lifestyle likely evolved from an arthropod-associated lifestyle and showed that within the genus Arsenophonus, the plant pathogenic lifestyle arose independently at least twice. We also propose a novel Candidatus status, “Candidatus Arsenophonus phytopathogenicus” novel species, for the bacterium associated with sugar beet and strawberry diseases and transmitted by the planthopper P. leporinus.