Perception and modification of plant flavonoid signals by rhizosphere microorganisms

Flavonoids are a diverse class of polyphenolic compounds that are produced as a result of plant secondary metabolism. They are known to play a multifunctional role in rhizospheric plant-microbe and plant-plant communication. Most familiar is their function as a signal in initiation of the legume-rhizobia symbiosis, but, flavonoids may also be signals in the establishment of arbuscular mycorrhizal symbiosis and are known agents in plant defence and in allelopathic interactions. Flavonoid perception by, and impact on, their microbial targets (e.g. rhizobia, plant pathogens) is relatively well characterized. However, potential impacts on 'non-target' rhizosphere inhabitants ('non-target' is used to distinguish those microorganisms not conventionally known as targets) have not been thoroughly investigated. Thus, this review first summarizes the conventional roles of flavonoids as nod gene inducers, phytoalexins and allelochemicals before exploring questions concerning 'non-target' impacts. We hypothesize that flavonoids act to shape rhizosphere microbial community structure because they represent a potential source of carbon and toxicity and that they impact on rhizosphere function, for example, by accelerating the biodegradation of xenobiotics. We also examine the reverse question, 'how do rhizosphere microbial communities impact on flavonoid signals?' The presence of microorganisms undoubtedly influences the quality and quantity of flavonoids present in the rhizosphere, both through modification of root exudation patterns and microbial catabolism of exudates. Microbial alteration and attenuation of flavonoid signals may have ecological consequences for below-ground plant-microbe and plant-plant interaction. We have a lack of knowledge concerning the composition, concentration and bioavailability of flavonoids actually experienced by microbes in an intact rhizosphere, but this may be addressed through advances in microspectroscopic and biosensor techniques. Through the use of plant mutants defective in flavonoid biosynthesis, we may also start to address the question of the significance of flavonoids in shaping rhizosphere community structure and function.     

Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria

Plant health and fitness widely depend on interactions with soil microorganisms. Some bacteria such as pseudomonads can inhibit pathogens by producing antibiotics, and controlling these bacteria could help improve plant fitness. In the present study, we tested whether plants induce changes in the antifungal activity of root-associated bacteria as a response to root pathogens. We grew barley plants in a split-root system with one side of the root system challenged by the pathogen Pythium ultimum and the other side inoculated with the biocontrol strain Pseudomonas fluorescens CHA0. We used reporter genes to follow the expression of ribosomal RNA indicative of the metabolic state and of the gene phlA, required for production of 2,4-diacetylphloroglucinol, a key component of antifungal activity. Infection increased the expression of the antifungal gene phlA. No contact with the pathogen was required, indicating that barley influenced gene expression by the bacteria in a systemic way. This effect relied on increased exudation of diffusible molecules increasing phlA expression, suggesting that communication with rhizosphere bacteria is part of the pathogen response of plants. Tripartite interactions among plants, pathogens, and bacteria appear as a novel determinant of plant response to root pathogens.     

Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition

Plants release a multitude of organic compounds into the rhizosphere, some of which are flavonoids. These products of secondary metabolism are mainly studied for their antioxidant properties and for their role in the establishment of rhizobium-legume symbiosis; however, it has been recently demonstrated that flavonoids can also affect nutrient availability through soil chemical changes. This review will give an overview of the types and amounts of flavonoids released by roots of different plant species, as well as summarize the available knowledge on root exudation mechanisms. Subsequently, factors influencing their release will be reported, and the methodological approaches used in the literature will be critically described. Finally, the direct contribution of plant-borne flavonoids on the nitrogen, phosphorous and iron availability into the rhizosphere will be discussed.     

The role of root exudates and allelochemicals in the rhizosphere

Plant roots serve a multitude of functions in the plant including anchorage, provision of nutrients and water, and production of exudates with growth regulatory properties. The root–soil interface, or rhizosphere, is the site of greatest activity within the soil matrix. Within this matrix, roots affect soil structure, aeration and biological activity as they are the major source of organic inputs into the rhizosphere, and are also responsible for depletion of large supplies of inorganic compounds. Roots are very complicated morphologically and physiologically, and their metabolites are often released in large quantities into the soil rhizosphere from living root hairs or fibrous root systems. Root exudates containing root-specific metabolites have critical ecological impacts on soil macro and microbiota as well as on the whole plant itself. Through the exudation of a wide variety of compounds, roots impact the soil microbial community in their immediate vicinity, influence resistance to pests, support beneficial symbioses, alter the chemical and physical properties of the soil, and inhibit the growth of competing plant species. In this review, we outline recent research on root exudation and the role of allelochemicals in the rhizosphere by studying the case of three plants that have been shown to produce allelopathic root exudates: black walnut, wheat and sorghum     

Rhizosphere engineering and management for sustainable agriculture

This paper reviews strategies for manipulating plants and their root-associated microorganisms to improve plant health and productivity. Some strategies directly target plant processes that impact on growth, while others are based on our knowledge of interactions among the components of the rhizosphere (roots, microorganisms and soil). For instance, plants can be engineered to modify the rhizosphere pH or to release compounds that improve nutrient availability, protect against biotic and abiotic stresses, or encourage the proliferation of beneficial microorganisms. Rhizobacteria that promote plant growth have been engineered to interfere with the synthesis of stress-induced hormones such as ethylene, which retards root growth, and to produce antibiotics and lytic enzymes active against soilborne root pathogens. Rhizosphere engineering also can involve the selection by plants of beneficial microbial populations. For example, some crop species or cultivars select for and support populations of antibiotic-producing strains that play a major role in soils naturally suppressive to soil-borne fungal pathogens. The fitness of root-associated bacterial communities also can be enhanced by soil amendment, a process that has allowed the selection of bacterial consortia that can interfere with bacterial pathogens. Plants also can be engineered specifically to influence their associated bacteria, as exemplified by quorum quenching strategies that suppress the virulence of pathogens of the genus Pectobacterium. New molecular tools and powerful biotechnological advances will continue to provide a more complete knowledge of the complex chemical and biological interactions that occur in the rhizosphere, ensuring that strategies to engineer the rhizosphere are safe, beneficial to productivity, and substantially improve the sustainability of agricultural systems.     

Vesicular-arbuscular mycorrhizae in relation to plant disease

Vesicular-arbuscular mycorrhizae (VAM) enhance plant growth through increased nutrient uptake, stress tolerance and disease resistance. As an integral part of the root system, they interact with other microorganisms in soil and result in increased root exudation approaching about 25% of the plant dry matter production. Roots support a multitude of microorganisms that, in concert, can have profound influence on growth and survival of the plant. VAM fungi can alter the root exudation pattern, enhance chitinolytic activity and alter photosynthetic/respiratory deficiencies. VAM-positive plants are known to exhibit varied resistance towards soil-borne and foliar pathogens. The known interactions include a number of mechanisms, such as exclusion of the pathogen, lignification of plant cell walls, changed phosphate nutrition resulting in altered exudation by roots, and formation of inhibitory low molecular weight compounds. The purpose of this review is to discuss VAM-plant-pathogen interactions and the possible mechanisms involved in altered resistance. Based on these observations, a working model is proposed to explain the VAM-disease interaction under varied environmental conditions.     

Effect of transporters on the secretion of phytochemicals by the roots of <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis>

Root exudation, the process by which plants secrete compounds into the soil, is becoming accepted as a communicative process that determines organismal interactions in the rhizosphere. However, the mechanistic processes involved in the root exudation of phytochemicals have not been elucidated; traditionally, exudation has been regarded as a passive process. There is evidence that transporters in plants (and other organisms) have been involved in the movement of chemicals across different membranes. Here, we describe the involvement of different transporters in root exudation of phytochemicals by employing a pharmacological approach. We used a range of concentrations of several compounds known to inhibit different transporters, including potassium cyanide, orthovanadate, quinidine, glibenclamide, nifedipine and verapamil, to examine the effects of transporter inhibition on root exudation profiles in Arabidopsis. Generally, the exudation profile of phenolic compounds in 18-day-old plants shows more than 15 major phytochemicals. In contrast, the inhibitors listed above caused differences in the secretion of specific compounds. For instance, nifedipine and verapamil completely inhibited the exudation of the phytochemicals with molecular masses of 142 and 294, respectively. These results highlight that root exudation of phytochemicals is an active process controlled at the biochemical level and that different transporters may be involved in this root-specific mechanism. Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .     

根分泌物对根际矿物营养及根际微生物的效应

综述了根系分泌物对植物生长的生理生态学效应,并就根系分泌物的定义、产生机制、组成成分和影响因素等方面进行了讨论。指出根系分泌物在缓解低矿物营养胁迫对植株造成的伤害及决定根际微生物的种群密度和数量方面起着重要的作用;根系分泌物的产生机制多样,组成成分复杂,影响因素繁多。对根分泌物的深入研究有助于进一步了解植物体与土壤间进行的生理生化过程及其调控机制。     

Root exudates and their ecological consequences in forest ecosystems: Problems and perspective

植物根际过程与调控机理研究已成为当前土壤学最活跃、最敏感的研究领域, 而根系分泌物作为根系-土壤-微生物界面物质能量交换和信息传递的重要媒介物质, 是构成根际微生态系统活力与功能特征的内在驱动因素, 是根际概念与根际过程存在的重要前提和基础。然而, 由于传统的根际过程研究更强调以实际生产问题为导向, 加之农作物生长周期较短、操作便利等诸多因素, 以往对植物根系分泌物研究主要聚焦在农业生态系统, 而有关根系分泌物在森林生态系统中的重要作用与调控机理研究甚少, 认识相对零散和片段化。基于此, 该文结合作者实际研究工作中的主要成果和该领域国际前沿动态, 综述了森林根系分泌物的生态重要性, 重点论述了目前森林根系分泌物生态学研究中存在的主要问题与不足, 在此基础上展望了未来森林根系分泌物生态学研究中值得关注的重点方向和研究内容。     

植物根际微生物群落构建的研究进展

植物根际是指植物根系与土壤的交界面,是根系自身生命活动和代谢对土壤影响最直接、最强烈的区域,其物理、化学和生物性质不同于土体土壤。在这个区域里,与植物发生相互作用的大量微生物,被称为根际微生物。根际微生物在植物的生长发育和植物病虫害的生物防治等方面都具有十分重要的意义。本文总结了根际微生物群落构建的研究现状,介绍了根际微生物的经典和最新的研究方法,包括根箱法、同位素技术以及高通量测序、菌群定量分析、高通量分离培养等方法在根际微生物研究中的应用,讨论了植物根系分泌物(碳水化物、氨基酸、黄酮类、酚类、激素及其信号物质)和土壤物理化学性质对根际微生物群落的影响,概述了根际微生物-植物的互作机制,以及根际微生物群落对植物的促生作用、提高植物抗逆性和抑制作用,并对根际微生物群落研究中存在的问题和未来发展方向进行了展望。     

Beneficial bacteria of agricultural importance

The rhizosphere is the soil–plant root interphase and in practice consists of the soil adhering to the root besides the loose soil surrounding it. Plant growth-promoting rhizobacteria (PGPR) are potential agents for the biological control of plant pathogens. A biocontrol strain should be able to protect the host plant from pathogens and fulfill the requirement for strong colonization. Numerous compounds that are toxic to pathogens, such as HCN, phenazines, pyrrolnitrin, and pyoluteorin as well as, other enzymes, antibiotics, metabolites and phytohormones are the means by which PGPR act, just as quorum sensing and chemotaxis which are vital for rhizosphere competence and colonization. The presence of root exudates has a pronounced effect on the rhizosphere where they serve as an energy source, promoting growth and influencing the root system for the rhizobacteria. In certain instances they have products that inhibit the growth of soil-borne pathogens to the advantage of the plant root. A major source of concern is reproducibility in the field due to the complex interaction between the plant (plant species), microbe and the environment (soil fertility and moisture, day length, light intensity, length of growing season, and temperature). This review listed most of the documented PGPR genera and discussed their exploitation.     

Root exudates and their ecological consequences in forest ecosystems: Problems and perspective北大核心CSCD

Researches on rhizosphere ecological processes and the underlying mechanisms have become one of the most active and sensitive hotspots in soil science. Root exudates have specialized roles in mediating the nutrient cycling and signal transduction within root-soil-microbe interactions. They are the key driving factors in regulating the functions of rhizosphere micro-ecosystem, and serve as a major premise for the concept and ecological processes in rhizosphere. However, due to the instinctive advantages of crops, such as short life cycles and convenient operation, most previous studies on root exudation mainly focused on agricultural ecosystems and were primarily targeted at providing practical guidelines. In contrast, there have been relatively few investigations on root exudates of trees, which highly limited the comprehensive knowledge of the potential mechanisms of root exudates in mediating soil biogeochemical processes in forest ecosystems. Hence, in this review, based on the main findings in our previous studies and the emerging frontiers in rhizosphere ecology, we specifically reviewed the ecological consequences and key remaining challenges in researches on root exudation in forests. Finally, we identify several topics and research outlooks for guiding future work to facilitate studies on root exudation and its ecological consequences in forest ecosystems. © Chinese Journal of Plant Ecology     

Involvement of a soybean ATP-binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-Rhizobium symbiosis

Legume plants have an ability to fix atmospheric nitrogen into nutrients via symbiosis with soil microbes. As the initial event of the symbiosis, legume plants secrete flavonoids into the rhizosphere to attract rhizobia. Secretion of flavonoids is indispensable for the establishment of symbiotic nitrogen fixation, but almost nothing is known about the membrane transport mechanism of flavonoid secretion from legume root cells. In this study, we performed biochemical analyses to characterize the transport mechanism of flavonoid secretion using soybean (Glycine max) in which genistein is a signal flavonoid. Plasma membrane vesicles prepared from soybean roots showed clear transport activity of genistein in an ATP-dependent manner. This transport activity was inhibited by sodium orthovanadate, a typical inhibitor of ATP-binding cassette (ABC) transporters, but was hardly affected by various ionophores, such as gramicidin D, nigericin, or valinomycin, suggesting involvement of an ABC transporter in the secretion of flavonoids from soybean roots. The K(m) and V(max) values of this transport were calculated to be 158 mum and 322 pmol mg protein(-1) min(-1), respectively. Competition experiments using various flavonoids of both aglycone and glucoside varieties suggested that this ABC-type transporter recognizes genistein and daidzein, another signaling compound in soybean root exudates, as well as other isoflavonoid aglycones as its substrates. Transport activity was constitutive regardless of the availability of nitrogen nutrition. This is, to our knowledge, the first biochemical characterization of the membrane transport of flavonoid secretion from roots.     

Evaluation of a novel tool for sampling root exudates from soil-grown plants compared to conventional techniques

The release of low molecular weight (LMW) organic compounds (e.g. organic acids, amino acids, sugars, etc.) by living plant roots significantly contributes to the development of chemical, physical as well as microbial rhizosphere gradients. Suitable and accurate sampling procedures are crucial for enhancing our understanding of the dynamics of related rhizosphere processes. Here we compare common sampling techniques with a novel tool for root exudate collection that allows non-destructive and repetitive sampling from soil-grown roots. Root exudates from Zea mays L. were collected using the following techniques: (i) hydroponic growth and sampling, (ii) soil growth and hydroponic sampling and (iii) rhizoboxes fitted with a novel in situ root exudate collecting tool. Furthermore, rhizosphere soil solution for the analysis of exudates and microbial metabolites was sampled using micro-suction cups (iv). The effect of different sampling solutions (deionised water and 0.5 mM CaCl₂) on organic acid and amino acid exudation patterns was also investigated. The novel exudate collecting tool was successfully tested for root exudate sampling. Results showed that particularly amino acid exudation rates were significantly affected by growth conditions and sampling procedures, while organic acid exudation patterns varied less across the different sampling setups. Despite qualitative and quantitative differences, exudation rates were in the same order of magnitude across the different sampling procedures. Soil solution concentrations obtained from micro-suction-cup sampling at defined distance to the root surface showed no distinct gradient, highlighting the importance of soil microorganisms in regulating the soil solution concentration of LMW C compounds either via microbial degradation or the release of microbial metabolites. The exudate collector offers new opportunities to assess root exudation rates and composition from soil-grown plants and thus enhances our knowledge of fundamental rhizosphere processes.     

Mechanism of plant growth promotion by rhizobacteria

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

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.     

Quantitative evaluation of the role of organic acid exudation in the mobilization of rock phosphate by rape

Phosphorus-deficient rape plants appear to acidify part of their rhizosphere by exuding malic and citric acid. A simulation model was used to evaluate the effect of measured exudation rates on phosphate uptake from Mali rock phosphate. The model used was one on nutrient uptake, extended to include both the effect of ion uptake and exudation on rhizosphere pH and the effect of rhizosphere pH on the solubilization of rock phosphate. Only the youngest zones of the root system were assumed to exude organic acids. The transport of protons released by organic acids was described by mass flow and diffusion. An experimentally determined relation was used describing pH and phosphate concentration in the soil solution as a function of total soil acid concentration. Model parameters were determined in experiments on organic acid exudation and on the uptake of phosphate by rape from a mixture of quartz sand and rock phosphate. Results based on simulation calculations indicated that the exudation rates measured in rape plants deficient in phosphorus can provide the roots with more phosphate than is actually taken up. Presence of root hairs enhanced the effect of organic acid exudation on calculated phosphate uptake. However, increase of root hair length without exudation as an alternative strategy to increase phosphate uptake from rock phosphate appeared to be less effective than exudation of organic acids. It was concluded that organic acid exudation is a highly effective strategy to increase phosphate uptake from rock phosphate, and that it unlikely that other rhizosphere processes play an important role in rock phosphate mobilization by rape.     

微生物合成黄酮糖苷类天然产物研究进展

黄酮糖苷类天然产物是植物中黄酮类化合物的主要存在形式,通过糖基化修饰,可以改变其水溶性、稳定性等,赋予其新的生物活性和功能。黄酮类化合物的糖基化修饰通常由植物源或微生物源的糖基转移酶催化,根据糖基的位置、类型和数量的不同,可形成多种类型的黄酮糖苷类产物。随着合成生物学和代谢工程的快速发展,在微生物中合成植物源黄酮糖苷类天然产物取得了重要进展。综述了糖基转移酶的聚类分析及糖基供体的途径改造,并对代谢工程优化黄酮糖苷类天然产物的微生物合成进行了分析讨论,并对其发展前景进行了展望。     

Metabolic engineering of flavonoids in plants and microorganisms

Over 9,000 flavonoid compounds have been found in various plants, comprising one of the largest families of natural products. Flavonoids are an essential factor in plant interactions with the environment, often serving as the first line of defense against UV irradiation and pathogen attacks. Flavonoids are also major nutritional compounds in foods and beverages, with demonstrated health benefits. Some flavonoids are potent antioxidants, and specific flavonoid compounds are beneficial in many physiological and pharmacological processes. Therefore, engineering of flavonoid biosynthesis in plants or in microorganisms has significant scientific and economical importance. Construction of biosynthetic pathways in heterologous systems offers promising results for large-scale flavonoid production by fermentation or bioconversion. Genomics and metabolomics now offer unprecedented tools for detailed understanding of the engineered transgenic organism and for developing novel technologies to further increase flavonoid production yields. We summarize some of the recent metabolic engineering strategies in plants and microorganisms, with a focus on applications of metabolic flux analysis. We are confident that these engineering approaches will lead to successful industrial flavonoid production in the near future.