Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth

Recent research on arbuscular mycorrhizas has demonstrated that AM fungi play a significant role in plant phosphorus (P) uptake, regardless of whether the plant responds positively to colonization in terms of growth or P content. Here we focus particularly on implications of this finding for consideration of the balance between organic carbon (C) use by the fungi and P delivery (i.e. the C-P trade between the symbionts). Positive growth responses to arbuscular mycorrhizal (AM) colonization are attributed frequently to increased P uptake via the fungus, which results in relief of P deficiency and increased growth. Zero AM responses, compared with non-mycorrhizal (NM) plants, have conventionally been attributed to failure of the fungi to deliver P to the plants. Negative responses, combined with excessive C use, have been attributed to this failure. The fungi were viewed as parasites. Demonstration that the AM pathway of P uptake operates in such plants indicates that direct P uptake by the roots is reduced and that the fungi are not parasites but mutualists because they deliver P as well as using C. We suggest that poor plant growth is the result of P deficiency because AM fungi lower the amount of P taken up directly by roots but the AM uptake of P does compensate for the reduction. The implications of interplay between direct root uptake and AM fungal uptake of P also include increased tolerance of AM plants to toxins such as arsenate and increased success when competing with NM plants. Finally we discuss the new information on C-P trade in the context of control of the symbiosis by the fungus or the plant, including new information (from NM plants) on sugar transport and on the role of sucrose in the signaling network involved in responses of plants to P deprivation.     

内蒙古中西部草原主要植物的丛枝菌根及其结构类型研究

2002年6-9月,对内蒙古中西部草原建群植物及优势植物的丛枝菌根共生状况进行了调查。在观察的28科125种植物中,被丛枝菌根真菌侵染的植物有104种(占83．2％);在过去认为不能侵染的莎草科植物中发现卯穗苔草(Carex duriuscula)和黄囊苔草( C. korshinskyi)有侵染现象。在所调查的植物中,多年生草本和灌木类植物被丛枝菌根真菌侵染的比例较高,占被调查该类植物总数的90．4％;而一年生和二年生草本植物被侵染的比例仅为47．6％。本地区野生植物的丛枝菌根结构类型多数为Arum类型,占65．38％,尤其在百合科(Liliaceae)、菊科(Compositae)、豆科(Leguminosae)和蔷薇科(Rosaceae)植物中比例较高;而Paris类型仅有19．23％,多见于禾本科(Gramineae!)、唇形科(Labiatae)、桔梗科(Campanulaceae)和百合科。丛枝菌根的结构类型与植物的根系类型、生活型和菌根侵染率无关,而与植物所属的科属关系比较密切。     

Phosphorus,arbuscular mycorrhizal fungi and performance of the wetland plant Lythrum salicaria L. under inundated conditions

The role of arbuscular mycorrhizal (AM) fungi in aquatic and semi-aquatic environments is poorly understood, although they may play a significant role in the establishment and maintenance of wetland plant communities. We tested the hypothesis that AM fungi have little effect on plant response to phosphorus (P) supply in inundated soils as evidenced by an absence of increased plant performance in inoculated (AM+) versus non-inoculated (AM-) Lythrum salicaria plants grown under a range of P availabilities (0-40 mg/l P). We also assessed the relationship between P supply and levels of AM colonization under inundated conditions. The presence of AM fungi had no detectable benefit for any measures of plant performance (total shoot height, shoot dry weight, shoot fresh weight, root fresh weight, total root length or total root surface area). AM+ plants displayed reduced shoot height at 10 mg/l P. Overall, shoot fresh to dry weight ratios were higher in AM+ plants although the biological significance of this was not determined. AM colonization levels were significantly reduced at P concentrations of 5 mg/l and higher. The results support the hypothesis that AM fungi have little effect on plant response to P supply in inundated conditions and suggest that the AM association can become uncoupled at relatively high levels of P supply.     

AM fungi root colonization increases the production of essential isoprenoids vs. nonessential isoprenoids especially under drought stress conditions or after jasmonic acid application

Previous studies have shown that root colonization by arbuscular mycorrhiza (AM) fungi enhances plant resistance to abiotic and biotic stressors and finally plant growth. However, little is known about the effect of AM on isoprenoid foliar and root content. In this study we tested whether the AM symbiosis affects carbon resource allocation to different classes of isoprenoids such as the volatile nonessential isoprenoids (monoterpenes and sesquiterpenes) and the non-volatile essential isoprenoids (abscisic acid, chlorophylls and carotenoids). By subjecting the plants to stressors such as drought and to exogenous application of JA, we wanted to test their interaction with AM symbiosis in conditions where isoprenoids usually play a role in resistance to stress and in plant defence. Root colonization by AM fungi favoured the leaf production of essential isoprenoids rather than nonessential ones, especially under drought stress conditions or after JA application. The increased carbon demand brought on by AM fungi might thus influence not only the amount of carbon allocated to isoprenoids, but also the carbon partitioning between the different classes of isoprenoids, thus explaining the not previously shown decrease of root volatile isoprenoids in AM plants. We propose that since AM fungi are a nutrient source for the plant, other carbon sinks normally necessary to increase nutrient uptake can be avoided and therefore the plant can devote more resources to synthesize essential isoprenoids for plant growth.     

Arbuscular mycorrhizal adaptation,spore germination,root colonization,and host plant growth and mineral acquisition at low pH

Arbuscular mycorrhizal (AM) fungi colonize plant roots and often enhance host plant growth and mineral acquisition, particularly for plants grown under low nutrient and mineral stress conditions. Information about AM fungi and mycorrhizal ( +AM) host plant responses at low pH ( < 5) is limited. Acaulospora are widely reported in acid soil, and Gigaspora sp. appear to be more common in acid soils than Glomus sp. Spores of some AM fungi are more tolerant to acid conditions and high Al than others; t Acaulospora sp., Gigaspora sp., and Glomus manihotis are particularly tolerant. Root colonization is generally less in low than in high pH soils. Percentage root colonization is generally not related to dry matter (DM) produced. Maximum enhancement of plant growth in acid soil varies with AM fungal isolate and soil pH, indicating adaptation of AM isolates to edaphic conditions. Acquisition of many mineral nutrients other than P and Zn is enhanced by +AM plants in acid soil, and the minerals whose concentration is enhanced are those commonly deficient in acid soils (Ca, Mg, and K). Some AM fungal isolates are effective in overcoming soil acidity factors, especially Al toxicity, that restrict plant growth at low pH.     

毛乌素沙地克隆植物生长对AM真菌多样性和菌根形成的影响

克隆植物的生态功能在沙地植被恢复过程中占据着重要位置。在毛乌素沙地由北向南选择两个典型样地,以根茎克隆植物沙鞭和羊柴为试验材料,连续2a系统地研究了克隆植物生长对AM真菌物种多样性和菌根形成的影响。结果表明:克隆植物生长对AM真菌物种多样性和丛枝菌根形成的影响因植物种类和样地不同而异。沙鞭通过克隆生长侵入灌丛空地后,AM真菌多样性指数在中国科学院植物研究所鄂尔多斯沙地草地生态研究站(简称OSES)和陕西榆林珍稀沙生植物保护基地(简称RSCF)样地均上升;孢子密度、菌丝、丛枝和总定殖率均显著提高;泡囊定殖率也有所增加,在OSES样地达显著水平,在RSCF样地未达显著水平。羊柴通过克隆生长侵入灌丛空地后,AM(Arbuscular mycorrhizal)真菌多样性指数在OSES样地上升,而在RSCF样地下降;孢子密度和丛枝定殖率在OSES和RSCF样地均显著增加,而泡囊定殖率均显著降低;菌丝和总定殖率也降低,在OSES样地未达显著水平,在RSCF样地达显著水平。     

Arbuscular mycorrhizal fungi might alleviate aluminium toxicity in banana plants

Under defined laboratory conditions it was shown that two glucosinolate-containing plant species, Tropaeolum majus and Carica papaya , were colonized by arbuscular mycorrhizal (AM) fungi, whereas it was not possible to detect AM fungal structures in other glucosinolate-containing plants (including several Brassicaceae). Benzylglucosinolate was present in all of the T. majus cultivars and in C. papaya it was the major glucosinolate. 2-Phenylethylglucosinolate was found in most of the non-host plants tested. Its absence in the AM host plants indicates a possible role for the isothiocyanate produced from its myrosinase-catalysed hydrolysis as a general AM inhibitory factor in non-host plants. The results suggest that some of the indole glucosinolates might also be involved in preventing AM formation in some of the species. In all plants tested, both AM hosts and non-hosts, the glucosinolate pattern was altered after inoculation with one of three different AM fungi ( Glomus mosseae , Glomus intraradices and Gigaspora rosea ), indicating signals between AM fungi and plants even before root colonization. The glucosinolate induction was not specifically dependent on the AM fungus. A time-course study in T. majus showed that glucosinolate induction was present during all stages of mycorrhizal colonization.     

More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses

Symbiosis is well recognized as a major force in plant ecology and evolution. However, there is considerable uncertainty about the functional, ecological and evolutionary benefits of the very widespread facultative arbuscular mycorrhizal (AM) associations, in which the plants can grow and reproduce whether or not they are colonized by AM fungi. Here we address the significance of new research findings that are overturning conventional views that facultative AM associations can be likened to parasitic fungus–plant associations. Specifically, we address the occurrence and importance of phosphate uptake via AM fungi that does not result in increases in total phosphorus (P) uptake or in plant growth, and possible signalling between AM fungi and plants that can result in plant growth depressions even when fungal colonization remains very low. We conclude that, depending on the individual AM fungi that are present, the role of facultative AM associations in the field, especially in relation to plant competition, may be much more subtle than has been previously envisaged.     

Meeting a non-host: the behaviour of AM fungi

 Arbuscular mycorrhizal (AM) fungi are obligately biotrophic organisms that live symbiotically with the roots of most plants. The establishment of a functional symbiosis between AM fungi and host plants involves a sequence of recognition events leading to the morphological and physiological integration of the two symbionts. The developmental switches in the fungi are triggered by host signals which induce changes in gene expression and a process leading to unequivocal recognition between the two partners of the symbiosis. It has been calculated that about 80% of plant families from all phyla of land plants are hosts of AM fungi. The remaining plant species are either non-mycorrhizal or hosts of mycorrhizas other than the arbuscular type. Non-host plants have been used to obtain information on the factors regulating the development of a functional symbiosis. The aim of this present review is to highlight present-day knowledge of the fungal developmental switches involved in the process of host/non-host discrimination. The following stages of the life cycle of AM fungi are analysed in detail: spore germination, presymbiotic mycelial growth, differential branching pattern and chemotropism, appressorium formation, root colonization. Accepted: 17 June 1998     

Investment in Fine Roots and Arbuscular Mycorrhizal Fungi Decrease During Succession in Three Brazilian Ecosystems

The functional groups of plants that characterize different phases of succession are expected to show differences in root distribution, fine‐root traits and degrees of association with arbuscular mycorrhizal (AM) fungi. The relationship involving fine‐root traits and AM fungi that regulate the nutrient acquisition potential among different plant functional groups are still not well understood. We assessed fine‐root morphology, AM fungal variables and soil fertility in grassland, secondary forest and mature forest in Atlantic, Araucaria and Pantanal ecosystems in Brazil. Soil cores were collected at 0–10 and 10–20 cm depths. Fine roots were extracted from soil by sieving and root morphological traits and AM colonization were determined. The AM spores were extracted from soil and counted. In all ecosystems, soil fertility, fine‐root mass and root diameter increased with the succession, while root length, specific root length, root‐hair length, root‐hair incidence, AM colonization and AM spore density decreased. These results suggest that plant species from early stages of tropical succession with inherent rapid growth invest in fine roots and maintain a high degree of AM colonization in order to increase the capacity for nutrient acquisition. Conversely, fine root morphological characteristics and low degree of AM colonization exhibited by plants of the later stages of succession lead toward a low nutrient uptake capacity that combine with their typical low growth rates. Abstract in Portuguese is available at http://www.blackwell‐synergy.com/loi/btp .     

Fungal root colonization responses in natural grasslands after long-term exposure to elevated atmospheric CO2

Arbuscular mycorrhizae, ubiquitous mutualistic symbioses between plant roots and fungi in the order Glomales, are believed to be important controllers of plant responses to global change, in particular to elevated atmospheric CO₂. In order to test if any effects on the symbiosis can persist after long-term treatment, we examined root colonization by arbuscular mycorrhizal (AM) and other fungi of several plant species from two grassland communities after continuous exposure to elevated atmospheric CO₂ for six growing seasons in the field. For plant species from both a sandstone and a serpentine annual grassland there was evidence for changes in fungal root colonization, with changes occurring as a function of plant host species. We documented decreases in percentage nonmycorrhizal fungal root colonization in elevated CO₂ for several plant species. Total AM root colonization (%) only increased significantly for one out of the five plant species in each grassland. However, when dividing AM fungal hyphae into two groups of hyphae (fine endophyte and coarse endophyte), we could document significant responses of AM fungi that were hidden when only total percentage colonization was measured. We also documented changes in elevated CO₂ in the percentage of root colonized by both AM hyphal types simultaneously. Our results demonstrate that changes in fungal root colonization can occur after long-term CO₂ enrichment, and that the level of resolution of the study of AM fungal responses may have to be increased to uncover significant changes to the CO₂ treatment. This study is also one of the first to document compositional changes in the AM fungi colonizing roots of plants grown in elevated CO₂. Although it is difficult to relate the structural data directly to functional changes, possible implications of the observed changes for plant communities are discussed.     

AM真菌与非菌根植物的相互作用关系

丛枝菌根(AM)真菌作为一类在全球分布广泛的土壤微生物,能够与陆地上大多数的维管植物形成专性共生关系,对于植物营养吸收和生态系统功能具有重要作用.而较少量的维管植物如苋科、黎科、石竹科、十字花科等植物被认为是非菌根植物.目前,对于这些非菌根植物与AM真菌之间的相互作用关系研究少且分散,缺乏系统总结.本文综述了非菌根植物的类型以及低侵染的原因,邻体植物形成的菌丝网络对AM真菌侵染非菌根植物的影响,并探讨AM真菌和非菌根植物之间可能存在的相互作用,以及植物-AM真菌之间的物质交换及可能存在的生态功能,旨在为进一步发挥非菌根植物在脆弱生态系统的功能潜力提供新思路.     

拉杰沙希大学校园药用植物菌根研究

Forty different medicinal plants were investigated for arbuscular mycorrhizal association in the Rajshahi University Campus in Bangladesh. The results indicated that 35 different plants were infected by AM (arbuscular mycorrhizal) fungi as found by trypan blue staining procedure. The percentage of root colonization by AM fungi varied from 13.3% to 100%. Mangifera indica and Morus indica have maximum percentage of colonization (100%). The intensity of root colonization were abundant in the plants belonging to the families Anacardiaceae, Asclepiadaceae, Moraceae, Leguminosae and Apocynaceae whereas the intensity of colonization of crop roots were moderate and poor belonging to Gramineae and Leguminosae. The presence of greater number of spore in soil was always associated with the incidence of abundant mycelia. In plant roots the formation of spore and mycelia was restricted by low pH. Number of mycorrhizal fungus spores ranged between 35 to100 per 100g air dried soil in different family respective soils. The frequency of mycorrhizal fungus infection showed positive correlation with soil pH, moisture, water holding capacity, texture, total nitrogen, organic carbon, phosphorus, calcium, potassium, and magnesium. Especially phosphorus and nitrogen in the soil greatly influenced the plant root infection by AM fungi.     

Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant

Many invasive plants have enhanced mutualistic arbuscular mycorrhizal (AM) fungal associations, however, mechanisms underlying differences in AM fungal associations between introduced and native populations of invasive plants have not been explored. Here we test the hypothesis that variation in root exudate chemicals in invasive populations affects AM fungal colonization and then impacts plant performance. We examined flavonoids (quercetin and quercitrin) in root exudates of native and introduced populations of the invasive plant Triadica sebifera and tested their effects on AM fungi and plant performance. We found that plants from introduced populations had higher concentrations of quercetin in root exudates, greater AM fungal colonization and higher biomass. Applying root exudates more strongly increased AM fungal colonization of target plants and AM fungal spore germination when exudate donors were from introduced populations. The role of root exudate chemicals was further confirmed by decreased AM fungal colonization when activated charcoal was added into soil. Moreover, addition of quercetin into soil increased AM fungal colonization, indicating quercetin might be a key chemical signal stimulating AM fungal associations. Together these results suggest genetic differences in root exudate flavonoids play an important role in enhancing AM fungal associations and invasive plants’ performance, thus considering root exudate chemicals is critical to unveiling mechanisms governing shifting plant-soil microbe interactions during plant invasions.Subject terms: Population dynamics, Community ecology, Plant ecology     

Competitive interactions are mediated in a sex‐specific manner by arbuscular mycorrhiza in Antennaria dioica

• Plants usually interact with other plants, and the outcome of such interaction ranges from facilitation to competition depending on the identity of the plants, including their sexual expression. Arbuscular mycorrhizal (AM) fungi have been shown to modify competitive interactions in plants. However, few studies have evaluated how AM fungi influence plant intraspecific and interspecific interactions in dioecious species.
• The competitive abilities of female and male plants of Antennaria dioica were examined in a greenhouse experiment. Females and males were grown in the following competitive settings: (i) without competition, (ii) with intrasexual competition, (iii) with intersexual competition, and (iv) with interspecific competition by Hieracium pilosella – a plant with similar characteristics to A. dioica. Half of the pots were grown with Claroideoglomus claroideum, an AM fungus isolated from the same habitat as the plant material. We evaluated plant survival, growth, flowering phenology, and production of AM fungal structures.
• Plant survival was unaffected by competition or AM fungi. Competition and the presence of AM fungi reduced plant biomass. However, the sexes responded differently to the interaction between fungal and competition treatments. Both intra‐ and interspecific competition results were sex‐specific, and in general, female performance was reduced by AM colonization. Plant competition or sex did not affect the intraradical structures, extraradical hyphae, or spore production of the AM fungus.
• These findings suggest that plant sexual differences affect fundamental processes such as competitive ability and symbiotic relationships with AM fungi.

     

Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi

The diversity of functional and life-history traits of organisms depends on adaptation as well as the legacy of shared ancestry. Although the evolution of traits in macro-organisms is well studied, relatively little is known about character evolution in micro-organisms. Here, we surveyed an ancient and ecologically important group of microbial plant symbionts, the arbuscular mycorrhizal (AM) fungi, and tested hypotheses about the evolution of functional and life-history traits. Variation in the extent of root and soil colonization by AM fungi is constrained to a few nodes basal to the most diverse groups within the phylum, with relatively little variation associated with recent divergences. We found no evidence for a trade-off in biomass allocated to root versus soil colonization in three published glasshouse experiments; rather these traits were positively correlated. Partial support was observed for correlated evolution between fungal colonization strategies and functional benefits of the symbiosis to host plants. The evolution of increased soil colonization was positively correlated with total plant biomass and shoot phosphorus content. Although the effect of AM fungi on infection by root pathogens was phylogenetically conserved, there was no evidence for correlated evolution between the extent of AM fungal root colonization and pathogen infection. Variability in colonization strategies evolved early in the diversification of AM fungi, and we propose that these strategies were influenced by functional interactions with host plants, resulting in an evolutionary stasis resembling trait conservatism.     

龙脑香科植物对丛枝菌根真菌的影响

在天然林地和温室盆栽条件下,比较研究了龙脑香科植物对丛枝菌根(Arbuscular mycorrhizas,AM)真菌孢子密度、相对多度、频度、属的组成、丰度和侵染状况等方面的影响.结果表明,用坡垒作盆栽寄主加富培养后,菌根侵染率、泡囊、丛枝和侵入点都低于原采样植物,以原坡垒土壤中栽植苗木的侵染率为最高,可达20.3%;而以望天树根围土壤栽植的苗木为最低,仅为10.6%;坡垒还不同程度地改变了原采样植物根围土壤中AM真菌孢子的密度、相对多度、频度、属的组成、丰度等.在4种土壤中,栽植坡垒苗木后,AM真菌的孢子密度都有不同程度的增长.采用与原采样相同种类的植物作为AM真菌加富培养的寄主更有利于促进AM真菌的生长发育、保持AM的多样性.     

Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa

Individual plants typically interact with multiple mutualists and enemies simultaneously. Plant roots encounter both arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi, while the leaves are exposed to herbivores. AMF are usually beneficial symbionts, while the functional role of DSE is largely unknown. Leaf herbivory may have a negative effect on root symbiotic fungi due to decreased carbon availability. However, evidence for this is ambiguous and no inoculation-based experiment on joint effects of herbivory on AM and DSE has been done to date. We investigated how artificial defoliation impacts root colonization by AM (Glomus intraradices) and DSE (Phialocephala fortinii) fungi and growth of Medicago sativa host in a factorial laboratory experiment. Defoliation affected fungi differentially, causing a decrease in arbuscular colonization and a slight increase in DSE-type colonization. However, the presence of one fungal species had no effect on colonization by the other or on plant growth. Defoliation reduced plant biomass, with this effect independent of the fungal treatments. Inoculation by either fungal species reduced root/shoot ratios, with this effect independent of the defoliation treatments. These results suggest AM colonization is limited by host carbon availability, while DSE may benefit from root dieback or exudation associated with defoliation. Reductions in root allocation associated with fungal inoculation combined with a lack of effect of fungi on plant biomass suggest DSE and AMF may be functional equivalent to the plant within this study. Combined, our results indicate different controls of colonization, but no apparent functional consequences between AM and DSE association in plant roots in this experimental setup.