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.     

Plant–Microbe Symbiosis: What Has Proteomics Taught Us?

Beneficial microbes have a positive impact on the productivity and fitness of the host plant. A better understanding of the biological impacts and underlying mechanisms by which the host derives these benefits will help to address concerns around global food production and security. The recent development of omics‐based technologies has broadened our understanding of the molecular aspects of beneficial plant–microbe symbiosis. Specifically, proteomics has led to the identification and characterization of several novel symbiosis‐specific and symbiosis‐related proteins and post‐translational modifications that play a critical role in mediating symbiotic plant–microbe interactions and have helped assess the underlying molecular aspects of the symbiotic relationship. Integration of proteomic data with other “omics” data can provide valuable information to assess hypotheses regarding the underlying mechanism of symbiosis and help define the factors affecting the outcome of symbiosis. Herein, an update is provided on the current and potential applications of symbiosis‐based “omic” approaches to dissect different aspects of symbiotic plant interactions. The application of proteomics, metaproteomics, and secretomics as enabling approaches for the functional analysis of plant‐associated microbial communities is also discussed.     

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.     

Innate immunity effectors and virulence factors in symbiosis

Rhizobium-legume symbiosis has been considered as a mutually favorable relationship for both partners. However, in certain phylogenetic groups of legumes, the plant directs the bacterial symbiont into an irreversible terminal differentiation. This is mediated by the actions of hundreds of symbiosis-specific plant peptides resembling antimicrobial peptides, the effectors of innate immunity. The bacterial BacA protein, associated in animal pathogenic bacteria with the maintenance of chronic intracellular infections, is also required for terminal differentiation of rhizobia. Thus, a virulence factor of pathogenesis and effectors of the innate immunity were adapted in symbiosis for the benefit of the plant partner.     

Moving targets: rapid evolution of oomycete effectors

Plant pathogenic microbes secrete proteins known as effectors, which enter the cytoplasm of plant cells and suppress host defences. Known effectors in oomycete pathogens possess an RXLR-EER motif in their amino acid sequence that is necessary for transport of the effector into a host plant cell. A large number of putative effectors have now been identified in oomycete genomes, the sequences of which show evidence of diversifying selection at their C terminus. Here, we describe recent progress in characterizing RXLR-EER effectors and discuss why so many of these rapidly evolving proteins are encoded by the genomes of plant pathogenic oomycetes.     

Medicago truncatula proteomics

Legumes (Fabaceae) are unique in their ability to enter into an elaborate symbiosis with nitrogen-fixing rhizobial bacteria. Rhizobia-legume (RL) symbiosis represents one of the most productive nitrogen-fixing systems and effectively renders the host plants to be more or less independent of other nitrogen sources. Due to high protein content, legumes are among the most economically important crop families. Beyond that, legumes consist of over 16,000 species assigned to 650 genera. In most cases, the genomes of legumes are large and polyploid, which originally did not predestine these plants as genetic model systems. It was not until the early 1990th that Medicago truncatula was selected as the model plant for studying Fabaceae biology. M. truncatula is closely related to many economically important legumes and therefore its investigation is of high relevance for agriculture. Recently, quite a number of studies were published focussing on in depth characterizations of the M. truncatula proteome. The present review aims to summarize these studies, especially those which focus on the root system and its dynamic changes induced upon symbiotic or pathogenic interactions with microbes.     

Identification and structure of the Rhizobium galegae common nodulation genes: evidence for horizontal gene transfer

Rhizobia are soil bacteria able to fix atmospheric nitrogen in symbiosis with leguminous plants. In response to a signal cascade coded by genes of both symbiotic partners, a specific plant organ, the nodule, is formed. Rhizobial nodulation (nod) genes trigger nodule formation through the synthesis of Nod factors, a family of chitolipooligosaccharides that are specifically recognized by the host plant at the first stages of the nodulation process. Here, we present the organization and sequence of the common nod genes from Rhizobium galegae, a symbiotic member of the RHIZOBIACEAE: This species has an intriguing phylogenetic position, being symbiotic among pathogenic agrobacteria, which induce tumors instead of nodules in plant shoots or roots. This apparent incongruence raises special interest in the origin of the symbiotic apparatus of R. galegae. Our analysis of DNA sequence data indicated that the organization of the common nod gene region of R. galegae was similar to that of Sinorhizobium meliloti and Rhizobium leguminosarum, with nodIJ downstream of nodABC and the regulatory nodD gene closely linked to the common nod operon. Moreover, phylogenetic analyses of the nod gene sequences showed a close relationship especially between the common nodA sequences of R. galegae, S. meliloti, and R. leguminosarum biovars viciae and trifolii. This relationship in structure and sequence contrasts with the phylogeny based on 16S rRNA, which groups R. galegae close to agrobacteria and separate from most other rhizobia. The topology of the nodA tree was similar to that of the corresponding host plant tree. Taken together, these observations indicate that lateral nod gene transfer occurred from fast-growing rhizobia toward agrobacteria, after which the symbiotic apparatus evolved under host plant constraint.     

从细胞内共生到多尺度共生：回顾与展望

基于共生概念的历史变化,目前人们普遍接受了广义共生概念。即共生是包含互利共生（mutualism）、偏利共生（commensalism）和拮抗/寄生（antagonism/parasitism）的共生连续体。本文简述了近20年间,全球9次国际共生学术大会取得的重要成果,对细胞内共生、时间、空间以及多种互作尺度共生关系的研究利用进展进行了评述。同时展望了一些活跃共生领域的研究概况,如共生失调 （dysbiosis）、植物-微生物-昆虫三角共生关系（plant-microbe-insect triangle）、细菌-真菌互作（bacterial- fungal interaction,BFI）、菌根菌-真菌内生细菌-植物多方共生联盟（multipartite symbiosis consortium）以及与共生相关微生物组的集合群落（metacommunity）研究及应用等。共生（symbiosis）正成为当代生物学的核心原则,正以一种与更宏大系统方法相一致的概念,从根本上改变了传统上的一些生物学概念,如孤立性的个体（individuality）概念。基因组测序和高通量RNA技术分析揭示,动、植物与共生微生物的重要互作,打破了迄今为止生物个体的特征边界,挑战了这些学科的定义;共生不仅是一对一的互利共生关系,共生实际是多种共生模式的连续共生体。此外,植物-昆虫-微生物互作的三角关系;菌根-真菌-真菌内生细菌-植物的多方联盟等新关系的发现,更把生命科学推向了快速发展的方向。这些科学进展不仅对生物科学的遗传学、免疫学、进化、发育、解剖学和生理学的研究至关重要,拓宽了新的视野,而且对农业中生物制剂研发,人类微生物组的管理及调控,以及对发酵食品及工业微生物生产的设计和管理将产生积极影响。     

Database mining of plant peptide homologues

In plant-pathogen interactions, pathogens employ secreted molecules, known as effectors to overcome physical barriers, modulate plant immunity, and facilitate colonization. Among these diverse effectors, some are found to mimic the plant peptides, to target host’s peptide receptors, and intervene in the peptide-regulated defense pathways and/or plant development. To better understand how pathogens have co-evolved with their plant hosts in order to improve disease management, we explored the presence of plant peptide mimics in microbes by bioinformatic analysis. In total, 36 novel peptide mimics belong to five plant peptide families were detected in bacterial and fungal kingdoms. Among them, phytosulfokine homologues were widely distributed in 22 phytopathogens and one bacterium, thereby constituted the largest proportion of the identified mimics. The putative functional peptide region is well conserved between plant and microbes, while the existence of a putative signal peptide varies between species. Our findings will increase understanding of plant-pathogen interactions, and provide new ideas for future studies of pathogenic mechanisms and disease management.     

真菌与植物共生机制研究进展

真菌与植物共生是一种非常普遍、复杂和重要的生物学现象。真菌与植物共生部位、共生类型和共生结构的多样性,以及参入共生的真菌和植物多样性奠定真菌与植物共生的生物学基础。真菌与植物首先通过分子"对话"的生化机制相互识别构建共生体,进而由真菌和植物双方生理机制调控共生体发育及其生理功能,以构建稳定有效的共生体。真菌与植物的空间、营养和功能生态位很多是相近的,双方均面临相同的生态选择压力,需要共同抵抗不良生境,以适应更多环境。因此,真菌和植物通过两者共生的生态学机制增强植物抗逆性,减轻有害生物危害,提高其竞争力和生境的适应能力。真菌和植物长期的协同演化过程中,种群间的基因交流及其差异导致不同的基因组合,奠定了共生体多样化的基础与资源。此遗传学机制形成的多种遗传组合的共生体不仅使真菌和植物在各环境压力下共存,还可以不断进化发展。真菌和植物共生研究方面已形成较为完善的体系,加强真菌与植物共生理论的研究,特别是该类共生体遗传背景、基因与环境互作效应及其机制的阐明,将有助于诠释真菌与植物共生的生物学机制。     

Molecular genetic mechanisms used by legumes to control early stages of mutually beneficial (mutualistic) symbiosis

Recent data on the plant control of early stages of mutually beneficial (mutualistic) symbioses of legumes, the mechanisms of perception and transmission of the microsymbiont’s molecular signals in the macrosymbiont’s cells, and induction of the genetic programs of the development of symbiotic compartments and organs of the plant are summarized. It is demonstrated that the genetic system of the plant controlling the development of nitrogen-fixing symbiosis of legumes (symbiotic root nodules), which emerged 70–80 Ma ago, has undoubtedly evolved on the basis of the genetic system controlling the development of the symbiosis with arbuscular mycorrhizal fungi (which emerged 400–500 Ma ago). Interactions between genes and between gene products, as well as exchange of molecular signals, form the basis of mutually beneficial (mutualistic) plant-bacterium interactions. Even in the case of a highly specific nitrogen-fixing symbiosis of legumes (symbiotic nodules), the receptors perceiving the signal from root-nodule bacteria may function in different ways. The development of arbuscular mycorrhiza and nitrogen-fixing symbiosis in legumes is a multistep process involving hundreds of genes of both the macro- and microsymbionts. For the symbioses to develop successfully, these genes should act in a coordinated way in the newly formed superorganismal system. Further studies are necessary to shed light onto the complexity of the plant genetic control of the development of mutualistic symbioses in legumes and provide information required for improving their functions in adaptive plant-breeding systems.     

The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling

Arbuscular mycorrhiza and the rhizobia-legume symbiosis are two major root endosymbioses that facilitate plant nutrition. In Lotus japonicus, two symbiotic cation channels, CASTOR and POLLUX, are indispensable for the induction of nuclear calcium spiking, one of the earliest plant responses to symbiotic partner recognition. During recent evolution, a single amino acid substitution in DOES NOT MAKE INFECTIONS1 (DMI1), the POLLUX putative ortholog in the closely related Medicago truncatula, rendered the channel solo sufficient for symbiosis; castor, pollux, and castor pollux double mutants of L. japonicus were rescued by DMI1 alone, while both Lj-CASTOR and Lj-POLLUX were required for rescuing a dmi1 mutant of M. truncatula. Experimental replacement of the critical serine by an alanine in the selectivity filter of Lj-POLLUX conferred a symbiotic performance indistinguishable from DMI1. Electrophysiological characterization of DMI1 and Lj-CASTOR (wild-type and mutants) by planar lipid bilayer experiments combined with calcium imaging in Human Embryonic Kidney-293 cells expressing DMI1 (the wild type and mutants) suggest that the serine-to-alanine substitution conferred reduced conductance with a long open state to DMI1 and improved its efficiency in mediating calcium oscillations. We propose that this single amino acid replacement in the selectivity filter made DMI1 solo sufficient for symbiosis, thus explaining the selective advantage of this allele at the mechanistic level.     

Plant lectins: the ties that bind in root symbiosis and plant defense

Lectins are a diverse group of carbohydrate-binding proteins that are found within and associated with organisms from all kingdoms of life. Several different classes of plant lectins serve a diverse array of functions. The most prominent of these include participation in plant defense against predators and pathogens and involvement in symbiotic interactions between host plants and symbiotic microbes, including mycorrhizal fungi and nitrogen-fixing rhizobia. Extensive biological, biochemical, and molecular studies have shed light on the functions of plant lectins, and a plethora of uncharacterized lectin genes are being revealed at the genomic scale, suggesting unexplored and novel diversity in plant lectin structure and function. Integration of the results from these different types of research is beginning to yield a more detailed understanding of the function of lectins in symbiosis, defense, and plant biology in general.     

丛枝菌根共生关系的信号机制研究进展

在植物与微生物的共生体中,最广泛的互惠共生体就是丛枝菌根.真菌在植物根系形成菌根后,菌丝通过根的皮层细胞获取植物提供的碳源,同时将矿物营养和水从土壤转运到皮层细胞,这种共生过程的研究在生物多样性的保护、陆生植物的起源与演化、退化生态系统的修复与重建以及农业、林业和园艺业的应用具有重要的意义.近年来丛枝菌根真菌与植物根系建立共生关系的信号传导途径和作用机制备受关注,也取得了突破性的进展.本文对丛枝菌根真菌与植物根系在共生关系形成、营养交换以及防御方面的分子信号和细胞方面的研究进展进行综述,并对发展前景作以展望.     

Roots and Their Symbiotic Microbes: Strategies to Obtain Nitrogen and Phosphorus in a Nutrient-Limiting Environment

The association between Rhizobium and legumes and that between arbuscular mycorrhizal (AM) fungi and most land plants display a remarkable degree of similarity. Both events involve the recognition of, entrance into, and coexistence within the plant root, with the development of a specialized interface that always separates the two partners and at which nutrient exchange occurs. Molecules produced by rhizobia during the early stages of the symbiosis are related to fungal chitin, and the plant responds to both microbes with an increase in the production of flavonoids, which may assist in recognition and development of the symbioses. Many of the same plant genes are up-regulated in the two symbiotic pathways, and notably plants that are Nod^? are often defective in the AM association as well. However, there are a number of differences between the associations, and these are important for understanding the relationship between the two symbioses. The Rhizobium and AM symbioses will be compared and the question of whether the nitrogen-fixing association evolved from the much more ancient AM symbiosis will be discussed.     

Common molecular mechanisms of symbiosis and pathogenesis

Traditionally, symbiotic and pathogenic interactions were considered different manifestations of the bacteria-host interaction. However, the molecular mechanisms that mediate communication between and cellular modulation of the involved partners are quite similar. With this review we aim to contribute to a reduction of the traditional gap between symbiosis and pathogenesis research.     

Nitric oxide in legume-rhizobium symbiosis

Nitric oxide (NO) is a gaseous signaling molecule with a broad spectrum of regulatory functions in plant growth and development. NO has been found to be involved in various pathogenic or symbiotic plant-microbe interactions. During the last decade, increasing evidence of the occurrence of NO during legume-rhizobium symbioses has been reported, from early steps of plant-bacteria interaction, to the nitrogen-fixing step in mature nodules. This review focuses on recent advances on NO production and function in nitrogen-fixing symbiosis. First, the potential plant and bacterial sources of NO, including NO synthase-like, nitrate reductase or electron transfer chains of both partners, are presented. Then responses of plant and bacterial cells to the presence of NO are presented in the context of the N₂-fixing symbiosis. Finally, the roles of NO as either a regulatory signal of development, or a toxic compound with inhibitory effects on nitrogen fixation, or an intermediate involved in energy metabolism, during symbiosis establishment and nodule functioning are discussed.     

Developing symbiotic consortia for lignocellulosic biofuel production

The search for petroleum alternatives has motivated intense research into biological breakdown of lignocellulose to produce liquid fuels such as ethanol. Degradation of lignocellulose for biofuel production is a difficult process which is limited by, among other factors, the recalcitrance of lignocellulose and biological toxicity of the products. Consolidated bioprocessing has been suggested as an efficient and economical method of producing low value products from lignocellulose; however, it is not clear whether this would be accomplished more efficiently with a single organism or community of organisms. This review highlights examples of mixtures of microbes in the context of conceptual models for developing symbiotic consortia for biofuel production from lignocellulose. Engineering a symbiosis within consortia is a putative means of improving both process efficiency and stability relative to monoculture. Because microbes often interact and exist attached to surfaces, quorum sensing and biofilm formation are also discussed in terms of consortia development and stability. An engineered, symbiotic culture of multiple organisms may be a means of assembling a novel combination of metabolic capabilities that can efficiently produce biofuel from lignocellulose.