Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.     

丛枝菌根真菌脂类代谢对共生信号调控的响应和反馈

丛枝菌根(AM)真菌是自然生态系统中分布最为广泛的真菌之一,在自然界物质循环和能量流动中发挥着重要作用。经过长期的协同进化,AM真菌和宿主植物之间形成了完美的互惠互利的共生关系,而真菌的脂类代谢可能是揭示共生秘密的关键所在。本文综述了AM真菌脂类代谢在共生关系建立和维持中关键作用的最新研究进展,重点探讨了AM真菌脂类代谢对共生信号调控的响应和反馈机制,主要包括:AM真菌脂类存储和释放对共生和非共生状态的响应,以及脂类代谢产物变化与共生营养传递之间的关系;脂类分解过程在共生建立初期对信号分子调控发生的响应,以及相应的物质转化和能量代谢;菌根共生互惠互利关系维持中,真菌脂类代谢与信号分子交流通道的相互渗透和影响。本文对于理解菌根共生机制,促进菌根在生产中的应用具有促进作用。     

丛枝菌根真菌-豆科植物-根瘤菌共生体系的研究进展

丛枝菌根真菌（Arbuscular Mycorrhizal Fungi,AMF）-豆科植物-根瘤菌（Rhizobia）三者形成的共生体。是植物与微生物共生中的一种特殊类型。本文对这种共生体中微生物与植物之间的营养关系;AMF和根瘤菌双接种豆科植物的效应以及影响双接种效应的因素;AMF和根瘤菌在与豆科植物形成共生过程中的分子互作机制等进行了综述。同时对这种共生体还需进一步研究的问题及其在基础研究和实践应用方面的前景进行了讨论。     

Biolistic transformation of arbuscular mycorrhizal fungi

Gene transfer systems have proved effective for the transformation of a range of organisms for both fundamental and applied studies. Biolistic transformation is a powerful method for the gene transfer into various organisms and tissues that have proved recalcitrant to more conventional means. For fungi, the biolistic approach is particularly effective where protoplasts are difficult to obtain and/or the organisms are difficult to culture. This is particularly applicable to arbuscular mycorrhizal (AM) fungi, being as they are obligate symbionts that can only be propagated in association with intact plants or root explants. Furthermore, these fungi are aseptate and protoplasts cannot be released. Recent advancements in gene transformation systems have enabled the use of biolistic technology to introduce foreign DNA linked to molecular markers into these fungi. In this review we discuss the development of transformation strategies for AM fungi by biolistics and highlight the areas of this technology which require further development for the stable transformation of these elusive organisms.     

On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: A root proteomic study

The arbuscular mycorrhizal (AM) symbiosis belongs to the strategies plants have developed to cope with adverse environmental conditions including contamination by heavy metals such as cadmium (Cd). In the present work, we report on the protective effect conferred by AM symbiosis to the model legume Medicago truncatula grown in presence of Cd, and on the 2‐D‐based proteomic approach further used to compare the proteomes of M. truncatula roots either colonised or not with the AM fungus Glomus intraradices in Cd‐free and Cd‐contaminated substrates. The results indicated that at the proteome level, 9 out of the 15 cadmium‐induced changes in nonmycorrhizal roots were absent or inverse in those Cd‐treated and colonized by G. intraradices, including the G. intraradices‐dependent down‐accumulation of Cd stress‐responsive proteins. Out of the twenty‐six mycorrhiza‐related proteins that were identified, only six displayed changes in abundance upon Cd exposure, suggesting that part of the symbiotic program, which displays low sensitivity to Cd, may be recruited to counteract Cd toxicity through the mycorrhiza‐dependent synthesis of proteins having functions putatively involved in alleviating oxidative damages, including a cyclophilin, a guanine nucleotide‐binding protein, an ubiquitin carboxyl‐terminal hydrolase, a thiazole biosynthetic enzyme, an annexin, a glutathione S‐transferase (GST)‐like protein, and a S‐adenosylmethionine (SAM) synthase.     

Molecular and cell biology of arbuscular mycorrhizal symbiosis

The roots of most extant plants are able to become engaged in an interaction with a small group of fungi of the fungal order Glomales (Glomeromycota). This interaction—arbuscular mycorrhizal (AM) symbiosis—is the evolutionary precursor of most other mutualistic root-microbe associations. The molecular analysis of this interaction can elucidate basic principles regarding such associations. This review summarizes our present knowledge about cellular and molecular aspects of AM. Emphasis is placed on morphological changes in colonized cells, transfer of nutrients between both interacting partners, and plant defence responses. Similarities to and differences from other associations of plant and microorganisms are highlighted regarding defence reactions and signal perception.     

Micronutrient transport in mycorrhizal symbiosis; zinc steals the show

Mycorrhizas are mutually beneficial associations between soil-borne fungi and plant roots. Mycorrhizal fungi provide their host plant with essential nutrients in exchange for sugars and/or lipids. Traditionally, transport and translocation of macronutrients, including nitrogen and phosphorus, throughout the fungal mycelium and towards the host plant are well studied. However, the regulation of nutrient exchange and their contribution in the morphogenesis and development of mycorrhizas remains unclear. In this Opinion, we argue that adding micronutrients in the current models of symbiotic transport is essential to fully understand the establishment, maintenance, and functioning of mycorrhizal associations. Homeostatic mechanisms at the cellular level and the first transport proteins involved have been recently documented for zinc (Zn) in arbuscular mycorrhizal, ectomycorrhizal, and ericoid mycorrhizal fungi. Mycorrhizal plants benefit from an improved Zn status in control conditions and are better protected when environmental Zn availability fluctuates. These recent progresses are paving the way for a better understanding of micronutrient allocation in mycorrhizas. Revising our vision on the role of micronutrients, particularly of Zn, in these interactions will allow a better use of mycorrhizal fungi in sustainable agriculture and forestry, and will increase management practices in waste land, as well as in agricultural and natural ecosystems.     

Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis

Maize mutants affected in the symbiotic interaction with the arbuscular mycorrhizal fungus Glomus mosseae have been found by a visual, macroscopic screen in a Mutator-tagged population of maize. Seven mutants have been identified, falling into three phenotypic classes. For each class one mutant has been characterized in more detail. The nope1 (no perception 1) mutant does not support appressoria formation of G. mosseae, suggesting the absence of a plant-encoded function necessary for early recognition prior to contact. The phenotype segregated as a monogenic recessive trait, indicating that a mutation in a single locus abolished compatibility of maize to G. mosseae. On a second mutant termed taci1 (taciturn 1), appressoria form at reduced frequency but their morphology is normal and leads to penetration of the rhizodermis. However, intraradically, the majority of hyphae are septate, resulting in terminated fungal spreading. This phenotype suggests that the mutation of taci1 has an effect on recognition and on cortex invasion. Segregation analysis indicates taci1 to carry a recessive mutation. In contrast, wild-type fungal morphology has been recorded in the Pram1 (Precocious arbuscular mycorrhiza 1) mutant, which displays enhanced and earlier fungal invasion. This trait segregates in a dominant fashion indicative of a gain-of-function mutation affecting the plant's control over restricting fungal colonization.     

The arbuscular mycorrhizal symbiosis links N mineralization to plant demand

Arbuscular mycorrhizal (AM) fungi facilitate inorganic N (NH₄ ⁺ or NO₃ ⁻) uptake by plants, but their role in N mobilization from organic sources is unclear. We hypothesized that arbuscular mycorrhizae enhance the ability of a plant to use organic residues (ORs) as a source of N. This was tested under controlled glasshouse conditions by burying a patch of OR in soil separated by 20-μm nylon mesh so that only fungal hyphae can pass through it. The fate of the N contained in the OR patch, as influenced by Glomus claroideum, Glomus clarum, or Glomus intraradices over 24 weeks, was determined using ¹⁵N as a tracer. AM fungal species enhanced N mineralization from OR to different levels. N recovery and translocation to Russian wild rye by hyphae reached 25% of mineralized N in G. clarum, which was most effective despite its smaller extraradical development in soil. Mobilization of N by G. clarum relieved plant N deficiency and enhanced plant growth. We show that AM hyphae modify soil functioning by linking plant growth to N mineralization from OR. AM species enhance N mineralization differentially leading to species-specific changes in the quality of the soil environment (soil C-to-N ratio) and structure of the soil microbial community.     

The mycorrhizal dependence of subordinates determines the effect of arbuscular mycorrhizal fungi on plant diversity

It is widely recognized that arbuscular mycorrhizal fungi (AMF) influence plant community structure. Several studies in the past few years have focused on the effect of AMF on plant diversity, showing contradictory results. On the basis of studies carried out in grasslands, it has been proposed that these results may not be in conflict but rather depend on mycorrhizal dependence of dominant and subordinate species in the plant community. Here, we propose a simple conceptual model to explain the effect of AMF on plant diversity and dominance hierarchy. Our model suggests that the effect of AMF on plant diversity can be explained mainly by mycorrhizal dependence of subordinates. It also gives predictions for a wider range of community types, and helps in identifying the systems in which empirical data are most critically needed.     

丛枝菌根真菌繁殖体的高效扩繁

【背景】丛枝菌根(arbuscular mycorrhiza, AM)真菌能够和大多数植物形成互利共生体系,以促进植物生长、提高抗逆能力,在生产中具有重要作用,但AM真菌的繁殖技术限制了其应用。【目的】构建AM真菌的高效繁殖体系。【方法】于温室盆栽条件下,将根内根孢囊霉(Rhizophagus intraradice)接种于由3种寄主植物高粱(Sorghum bicolor)、玉米(Zea mays)、红三叶草(Trifolium repens)与5种培养基质(沸石、河砂、草炭、珍珠岩和蛭石)构建的4种繁殖体系中进行培养。研究不同繁殖体系对根内根孢囊霉侵染程度、产孢量的影响;然后利用高粱接种扩繁的菌剂进行AM真菌侵染能力的测定以验证其扩繁效果;最后基于筛选出的最优扩繁条件探讨对其他种类AM真菌摩西斗管囊霉(Funneliformis mosseae)、幼套近明球囊霉(Clariodeoglous etunicatum)、地表多样孢囊霉(Diversispora versiformis)和脆无梗囊霉(Acaulospora delicate)的扩繁效果。【结果】基质为河砂+蛭石+草炭(体...     

Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China

Arbuscular mycorrhizal and dark septate endophytic fungal colonization in a grassland in Kunming, southwest China, was investigated monthly over one year. All plant roots surveyed were co-colonized by arbuscular mycorrhizal and dark septate endophytic fungi in this grassland. Both arbuscular mycorrhizal and dark septate endophytic fungal colonization fluctuated significantly throughout the year, and their seasonal patterns were different in each plant species. The relationships between environmental (climatic and edaphic) factors and fungal colonization were also studied. Correlation analysis demonstrated that arbuscular mycorrhizal colonization was significantly correlative with environmental factors (rainfall, sunlight hours, soil P, etc.), but dark septate endophytic fungal colonization was only correlative with relative humidity and sunlight hours.     

Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment

Prunella vulgaris was inoculated with different arbuscular mycorrhizal fungi (AMF) and grown at two concentrations of CO₂ (ambient, 350 μl l⁻¹, and elevated, 600 μl l⁻¹) to test whether a plants response to elevated CO₂ is dependent on the species of AMF colonizing the roots. Using compartments accessible only to AMF hyphae but not to roots, we also tested whether elevated CO₂ affects the growth of external AMF hyphae. Plant biomass was significantly greater at elevated than at ambient CO₂; the biomass of the root system, for example, increased by a factor of 2. The colonization of AMF inside the root remained constant, indicating that the total AMF inside the root system also increased by a factor of 2. The length of external AMF hyphae at elevated CO₂ was up to 5 times that at ambient CO₂, indicating that elevated CO₂ promoted allocation of AMF biomass to the external hyphae. The concentration and content of phosphorus in the stolons differed significantly between ambient and elevated CO₂ but this resulted in either an increase or a decrease, according to which AMF isolate occupied the roots. We hypothesized that an increase in external hyphal growth at elevated CO₂ would result in increased P acquistion by the plant. To test this we supplied phosphorus, in a compartment only accessible to AMF hyphae. Plants did not acquire more phosphorus at elevated CO₂ when phosphorus was added to this compartment. Large increases in AMF hyphal growth could, however, play a significant role in the movement of fixed carbon to the soil and increase soil aggregation. Received: 28 March 1998 / Accepted: 27 August 1998     

A purple acid phosphatase,GmPAP33, participates in arbuscule degeneration during arbuscular mycorrhizal symbiosis in soybean

Arbuscules are the central structures of the symbiotic association between terrestrial plants and arbuscular mycorrhizal (AM) fungi. However, arbuscules are also ephemeral structures, and following development, these structures are soon digested and ultimately disappear. Currently, little is known regarding the mechanism underlying the digestion of senescent arbuscules. Here, biochemical and functional analyses were integrated to test the hypothesis that a purple acid phosphatase, GmPAP33, controls the hydrolysis of phospholipids during arbuscule degeneration. The expression of GmPAP33 was enhanced by AM fungal inoculation independent of the P conditions in soybean roots. Promoter‐β‐glucuronidase (GUS) reporter assays revealed that the expression of GmPAP33 was mainly localized to arbuscule‐containing cells during symbiosis. The recombinant GmPAP33 exhibited high hydrolytic activity towards phospholipids, phosphatidylcholine, and phosphatidic acid. Furthermore, soybean plants overexpressing GmPAP33 exhibited increased percentages of large arbuscules and improved yield and P content compared with wild‐type plants when inoculated with AM fungi. Mycorrhizal RNAi plants had high phospholipid levels and a large percentage of small arbuscules. These results in combination with the subcellular localization of GmPAP33 at the plasma membrane indicate that GmPAP33 participates in arbuscule degeneration during AM symbiosis via involvement in phospholipid hydrolysis.     

Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth

Different species of arbuscular mycorrhizal fungi (AMF) alter plant growth and affect plant coexistence and diversity. Effects of within-AMF species or within-population variation on plant growth have received less attention. High genetic variation exists within AMF populations. However, it is unknown whether genetic variation contributes to differences in plant growth. In our study, a population of AMF was cultivated under identical conditions for several generations prior to the experiments thus avoiding environmental maternal effects. We show that genetically different Glomus intraradices isolates from one AMF population significantly alter plant growth in an axenic system and in greenhouse experiments. Isolates increased or reduced plant growth meaning that plants potentially receive benefits or are subject to costs by forming associations with different individuals in the AMF population. This shows that genetic variability in AMF populations could affect host-plant fitness and should be considered in future research to understand these important soil organisms.     

Breakdown and delayed cospeciation in the arbuscular mycorrhizal mutualism

The ancient arbuscular mycorrhizal association between the vast majority of plants and the fungal phylum Glomeromycota is a dominant nutritional mutualism worldwide. In the mycorrhizal mutualism, plants exchange photosynthesized carbohydrates for mineral nutrients acquired by fungi from the soil. This widespread cooperative arrangement is broken by 'cheater' plant species that lack the ability to photosynthesize and thus become dependent upon three-partite linkages (cheater-fungus-photosynthetic plant). Using the first fine-level coevolutionary analysis of mycorrhizas, we show that extreme fidelity towards fungi has led cheater plants to lengthy evolutionary codiversification. Remarkably, the plants' evolutionary history closely mirrors that of their considerably older mycorrhizal fungi. This demonstrates that one of the most diffuse mutualistic networks is vulnerable to the emergence, persistence and speciation of highly specific cheaters.     

丛枝菌根真菌与植物共生对植物水分关系的影响及机理

自1885年Frank首次提到菌根(mykorhiza)概念以来,大量的试验证实了丛枝菌根真菌(AMF)与植物根系之间形成具有一定结构和功能的共生体,促进植物生长并提高干旱耐受能力,在干旱生态系统中发挥重要的作用。该研究多集中在对宿主植物生理生态的影响及其机制方面,然而菌根共生对宿主植物水分吸收和信号产生、传递的影响研究少而分散,缺少系统总结。综述了最近四十多年丛枝菌根真菌与植物共生体对宿主植物干旱适应性影响研究进展,讨论了菌根共生对植物根冠通讯的影响及机理。干旱胁迫下AMF与植物共生,通过影响宿主植物一系列生理生态过程,提高宿主植物横向根压和纵向蒸腾拉力。经典的Ohm吸水模型是该方向最有代表性的研究成果,该模型揭示了菌根共生的根外菌丝具有不同于根细胞的细胞结构和水分运输性能,这为宿主植物提供一种特殊的快速吸水方式,可提高植物对土壤水分的吸收和运输能力。研究表明,AMF会影响宿主植物根冠通讯过程,如诱发信号级联反应,诱导根系尽早感知水分胁迫并产生非水力根源信号,提高宿主对干旱的耐受性。讨论了AMF在根冠通讯分子机制研究方面存在的问题及可能的解决途径,展望了AMF在干旱农业生产中的应用潜力。