Positive interactions between mycorrhizal fungi and bacteria are widespread and benefit plant growth

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Arbuscular mycorrhizal fungi, Collembola and plant growth

Arbuscular mycorrhizal fungi are ubiquitous in field soils, as are mycophagous animals such as Collembola. It has been suggested that these animals reduce the functioning of the mycorrhiza and are thus detrimental to plant growth. However, recent choice experiments suggest that Collembola preferentially feed on nonmycorrhizal fungi in the rhizosphere. If these preferences also occur in field soils, then Collembola might indirectly benefit plants through an enhancement of mycorrhizal functioning and indirect multitrophic links to foliar-feeding insect herbivores.     

Towards growth of arbuscular mycorrhizal fungi independent of a plant host

When surface-sterilized spores of the arbuscular mycorrhizal fungus (AMF) Glomus intraradices Sy167 were germinated on agar plates in the slightly modified minimum mineral medium described by G. Bécard and J. A. Fortin (New Phytol. 108:211-218, 1988), slime-forming bacteria, identified as Paenibacillus validus, frequently grew up. These bacteria were able to support growth of the fungus on the agar plates. In the presence of P. validus, hyphae branched profusely and formed coiled structures. These were much more densely packed than the so-called arbuscule-like structures which are formed by AMF grown in coculture with carrot roots transformed with T-DNA from Agrobacterium rhizogenes. The presence of P. validus alone also enabled G. intraradices to form new spores, mainly at the densely packed hyphal coils. The new spores were not as abundant as and were smaller than those formed by AMF in the monoxenic culture with carrot root tissues, but they also contained lipid droplets and a large number of nuclei. In these experiments P. validus could not be replaced by bacteria such as Escherichia coli K-12 or Azospirillum brasilense Sp7. Although no conditions under which the daughter spores regerminate and colonize plants have been found yet, and no factor(s) from P. validus which stimulates fungal growth has been identified, the present findings might be a significant step forward toward growth of AMF independent of any plant host.     

Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots

 The most widespread type of mycorrhiza is the so-called vesicular-arbuscular mycorrhiza. In this endomycorrhiza, fungal hyphae penetrate plant cell walls in the root cortex. There they form densely branched arbuscules. Fungus and plant plasma membrane are separated by a common interfacial apoplast. The pH of the compartment between the symbionts is of pivotal importance for nutrient transfer. Histochemical experiments were conducted to check for an acidic nature of the interface in the model system Glomus versiforme (Karst.) Berch-Allium porrum L. Two chemically different acidotropic dyes (neutral red and LysoSensor Green DND-189) stained the arbuscules intensely. The staining of arbuscules could be eliminated by addition of the protonophore carbonylcyanide m-chlorophenylhydrazone (CCCP) or treatments leading to membrane rupture. Therefore, the staining of the arbuscules was based on the ion-trap mechanism, which indicates acidic, membrane-bound compartments. Microscopic examination of stained arbuscules at high optical resolution revealed a peripheral accumulation of the dye. Since plasmolysis rapidly destained the arbuscules, it is concluded that the dyes accumulate in the arbuscular interface, indicating the highly acidic nature of this compartment. The findings are discussed with respect to their relevance for the nutrient transfer in mycorrhizas. In addition, evidence for a discontinuity in the arbuscular interface between the stem and the branches of the arbuscule is given. Received: 15 September 1999 / Accepted: 20 February 2000     

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.     

Uvitex2B: a rapid and efficient stain for detection of arbuscular mycorrhizal fungi within plant roots

The study of arbuscular mycorrhiza often requires the staining of fungal structures using specific dyes. Fluorescent dyes such as acid fuchsin and wheat germ agglutinin conjugates give excellent results, but these compounds are either hazardous or very expensive. Here, we show that a safer and inexpensive dye, Uvitex2B, can be efficiently used to stain intraradical fungal structures formed by the arbuscular mycorrhizal fungus Glomus intraradices in three plant species: carrot, Casuarina equisetifolia, and Medicago truncatula. The intensity and stability of Uvitex2B allow the acquisition of high-quality images using not only confocal laser scanning microscopy but also epifluorescence microscopy coupled with image deconvolution. Furthermore, we demonstrate that Uvitex2B and β-glucuronidase staining are compatible and can thus be used to reveal arbuscular mycorrhizal structures in the context of promoter activation analysis.     

Effects of mycorrhizal fungi on plant populations

We discuss four potentially important interactions between mycorrhizal fungi and populations of plants. First, vesicular-arbuscular mycorrhizal colonization has been shown to increase reproduction (via both male and female functions) and offspring survival, and thus it can increase population size, at least in the short term. This is undoubtedly important to wild plant species and especially to those whose success depends on high rates of reproduction such as early successional annuals. Second, the positive response in growth and reproduction to vesicular-arbuscular mycorrhizal colonization may be inversely related to plant population density. All else being equal, this would tend to stabilize the density of natural plant populations over time. It may also explain why positive responses to mycorrhizal inoculation of dense crops are rare. Third, vesicular-arbuscular mycorrhizal fungi can increase inequality in size and reproduction among plants within a population. Mycorrhizal fungi may thus exaggerate the genetic overrepresentation in the next generation of the most robust individuals in the current generation. Fourth, established mycorrhizal plants may serve as important sources of inoculum for initially nonmycorrhizal, conspecific seedlings. This may affect regeneration, and could contribute to patchy distributions of species within the community.     

Relatedness among arbuscular mycorrhizal fungi drives plant growth and intraspecific fungal coexistence

Arbuscular mycorrhizal fungi (AMF) form symbioses with most plant species. They are ecologically important determinants of plant growth and diversity. Considerable genetic variation occurs in AMF populations. Thus, plants are exposed to AMF of varying relatedness to each other. Very little is known about either the effects of coexisting AMF on plant growth or which factors influence intraspecific AMF coexistence within roots. No studies have addressed whether the genetics of coexisting AMF, and more specifically their relatedness, influences plant growth and AMF coexistence. Relatedness is expected to influence coexistence between individuals, and it has been suggested that decreasing ability of symbionts to coexist can have negative effects on the growth of the host. We tested the effect of a gradient of AMF genetic relatedness on the growth of two plant species. Increasing relatedness between AMFs lead to markedly greater plant growth (27% biomass increase with closely related compared to distantly related AMF). In one plant species, closely related AMF coexisted in fairly equal proportions but decreasing relatedness lead to a very strong disequilibrium between AMF in roots, indicating much stronger competition. Given the strength of the effects with such a shallow relatedness gradient and the fact that in the field plants are exposed to a steeper gradient, we consider that AMF relatedness can have a strong role in plant growth and the ability of AMF to coexist. We conclude that AMF relatedness is a driver of plant growth and that relatedness is also a strong driver of intraspecific coexistence of these ecologically important symbionts.     

Combined application of arbuscular mycorrhizal fungi and steel slag improves plant growth and reduces Cd,Pb accumulation in Zea mays

Abstract

Little attention has been paid to the combined use of arbuscular mycorrhizal fungus (AMF) and steel slag (SS) for ameliorating heavy metal polluted soils. A greenhouse pot experiment was conducted to study the effects of SS and AMF?Funneliformis mosseae (Fm), Glomus versiforme (Gv) and Rhizophagus intraradices (Ri) on plant growth and Cd, Pb uptake by maize grown in soils added with 5?mg Cd kg^?1 and 300?mg Pb kg^?1 soil. The combined usage of AMF and SS (AMF?+?SS) promoted maize growth, and Gv?+?SS had the most obvious effect. Meanwhile, single SS addition and AMF?+?SS decreased Cd, Pb concentrations in maize, and the greater reductions were found in combined utilization, and the lowest Cd, Pb concentrations of maize appeared in Gv?+?SS. Single SS amendment and AMF?+?SS enhanced soil pH and decreased soil diethylenetriaminepentaacetic acid (DTPA)-extractable Cd, Pb concentrations. Furthermore, alone and combined usage of AMF and SS increased contents of soil total glomalin. Our research indicated a synergistic effect between AMF and SS on enhancing plant growth and reducing Cd, Pb accumulation in maize, and Gv?+?SS exerted the most pronounced effect. This work suggests that AMF inoculation in combination with SS addition may be a potential method for not only phytostabilization of Pb-Cd-contaminated soil but maize safety production.     

Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil

The seasonality of arbuscular mycorrhizal (AM) fungi–plant symbiosis in Lotus glaber Mill. and Stenotaphrum secundatum (Walt.) O.K. and the association with phosphorus (P) plant nutrition were studied in a saline-sodic soil at the four seasons during a year. Plant roots of both species were densely colonized by AM fungi (90 and 73%, respectively in L. glaber and S. secundatum) at high values of soil pH (9.2) and exchangeable sodium percentage (65%). The percentage of colonized root length differed between species and showed seasonality. The morphology of root colonization had a similar pattern in both species. The arbuscular colonization fraction increased at the beginning of the growing season and was positively associated with increased P concentration in both shoot and root tissue. The vesicular colonization fraction was high in summer when plants suffer from stress imposed by high temperatures and drought periods, and negatively associated with P in plant tissue. Spore and hyphal densities in soil were not associated with AM root colonization and did not show seasonality. Our results suggest that AM fungi can survive and colonize L. glaber and S. secundatum roots adapted to extreme saline-sodic soil condition. The symbiosis responds to seasonality and P uptake by the host altering the morphology of root colonization.     

Soil solarization reduces arbuscular mycorrhizal fungi as a consequence of weed suppression

Soil solarization, the process of heating soil by covering fields with clear plastic, is a promising method to reduce populations of soilborne pests and weeds without the use of pesticides. However, the destruction of beneficial organisms such as arbuscular mycorrhizal (AM) fungi also may occur, thereby reducing positive effects of solarization. We compared the effects of solarization and chemical fumigants on the survival of indigenous AM fungi in 1995 and 1996. The infectivity of AM fungi was monitored before and after solarization using a greenhouse bioassay with Sorghum bicolor L. for both years. AM colonization of roots was also monitored in the field 8 months after solarization in 1995. Weed densities were measured 8 months after treatment in 1996. Solarization increased the average daily soil temperature 6-10°C and the maximum soil temperature reached by 10-16°C (5-20 cm depth). Solarization did not reduce the infectivity of AM fungi immediately after the solarization period in either year, as determined by the greenhouse bioassay. Infectivity was greatly reduced in solarized plots 8 months after solarization (over winter) in both years as assessed in the field (1995) or with the greenhouse bioassay (1996). Fumigation with metam sodium at 930 l ha^-1 (350 kg active ingredient ha^-1) reduced the infectivity of AM fungi in both years, and fumigation with methyl bromide at 800 kg ha^-1 eliminated infection by AM fungi. Solarization was as effective as methyl bromide and metam sodium at 930 l ha^-1 in controlling winter annual weeds measured 8 months after treatment. Solarization apparently reduced AM fungi in soil indirectly by reducing weed populations that maintained infective propagules over the winter. Fumigation with metam sodium or methyl bromide directly reduced AM fungi in soil.     

The impact of arbuscular mycorrhizal fungi on plant growth following herbivory: A search for pattern

Arbuscular mycorrhizal (AM) fungi can facilitate nutrient uptake and increase host plant growth but also place constraints on the host's carbon budget. When plants are stressed by herbivory the net effect of the symbiosis may be altered tolerance. Individual experiments manipulating AM fungi and herbivory have demonstrated increased, decreased, and no effect on tolerance but patterns with respect to plant, herbivore, or fungus characteristics have not emerged. Meta-analysis of published results from factorial experiments was used to describe the size of the effects of herbivory and of AM fungi on host growth when factors such as cause of damage, inoculum, and host characteristics are considered, and to determine whether AM fungi alter the effects of herbivory. Also, the correlation between the effect of AM fungi on tolerance and resistance was tested with data from studies that examined insect performance. Herbivory strongly and consistently reduced shoot and root growth, especially in perennial plants and crops. AM fungi increased shoot growth of perennials but not annuals, and when insects caused damage but not when artificial defoliation was applied. Root growth was consistently greater with AM fungi. The interaction of AM fungi and herbivory, which indicates whether AM fungi alter the effects of herbivory, was variable and never significant overall but homogeneity tests indicated underlying structure. In experiments that used single species inoculum, Glomus intraradices increased, whereas Glomus mosseae reduced, effects of herbivory on shoot growth. Multispecies inocula magnified effects of herbivory on root growth whereas single species inocula ameliorated effects. The impact of AM fungi on resistance to herbivory was positively correlated with the impact on tolerance; however AM fungi reduced both tolerance and resistance in many cases. Review of these results with respect to the types of systems studied suggests directions for future investigation.     

亚精胺和丛枝菌根真菌对黄瓜生长的影响

以黄瓜品种‘津春2号’为材料,在育苗基质中添加亚精胺(Spd)和丛枝菌根真菌(AMF),研究外源Spd和AMF对黄瓜幼苗生长、光合作用、果实产量和品质以及根际微生物和酶活性的影响.结果表明:育苗基质中同时添加Spd和AMF,可促进黄瓜幼苗生长,提高根系活力和果实产量,改善品质,并促进养分吸收;Spd和AMF提高黄瓜幼苗净光合速率、实际光化学效率、表观量子效率、羧化效率和光呼吸速率,增加基质中细菌和放线菌数量,而降低真菌数量,并提高蔗糖酶、中性磷酸酶、过氧化氢酶和脲酶的活性.说明育苗基质中同时添加Spd和AMF,可提高黄瓜植株光能利用效率,促使黄瓜幼苗根际微生物区系从低肥力的"真菌型"向高肥力的"细菌型"转化,加速有机磷和有机态氮的分解与转化,为黄瓜生长发育提供比较充足的N、P等养分,从而促进黄瓜植株生长,提高产量并改善品质.Spd可提高AMF侵染率,两者对黄瓜幼苗生长具有明显的叠加效应,说明在接种AMF的基质中添加Spd,是一种可增强AMF侵染率的有效方法.     

Arbuscular mycorrhizal fungi from three genera induce two-phase plant growth responses on a high P-fixing soil

Plant growth enhancing effects of arbuscular mycorrhizal (AM) fungi are suitably quantified by comparisons of mycorrhizal and non-mycorrhizal plant growth responses to added phosphorus (P). The ratio between the amounts of added P required for the same yield of mycorrhizal and non-mycorrhizal plants is termed the relative effectiveness of the mycorrhiza. Variation in this relative effectiveness was examined for subterranean clover grown on a high P-fixing soil. Plants were either left non-mycorrhizal or inoculated with one of three AM fungal species with well-characterised differences in external hyphal spread. With no P added, plants from all treatments produced <10% of their maximum growth achieved at non-limiting P supply. The growth response of non-mycorrhizal plants was markedly sigmoid. Mycorrhizal growth responses were not sigmoid but their shape was two-phased. The first phase was an asymptotic approach to 25–30% of maximum growth, followed by a second asymptotic rise to maximum growth. Growth effects of Glomus invermaium and Acaulospora laevis were quite similar. Plants in these treatments produced up to four times greater shoot dry biomass than non-mycorrhizal plants. Scutellospora calospora was less effective. The relative effectiveness of AM fungi varied with the level of P application. This is expected to apply to all soils on which a sigmoid response is obtained for growth of non-mycorrhizal plants. In a simple approximation the relative effectiveness was calculated to range from 1.46 to 15.57. Shoot P contents were increased by up to 25 times by A. laevis, significantly more than by the other two fungi. The further mycelial spread of this fungus is thought to have contributed to its relatively greater effect on plant P content.     

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.     

The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression

Plant and Soil - Colonisation of roots by arbuscular mycorrhizal fungi (AMF) can increase plant biomass and nutrition under soil zinc (Zn) deficiency and toxicity conditions, but the genes and...     

Evolutionary maintenance of genomic diversity within arbuscular mycorrhizal fungi

Most organisms are built from a single genome. In striking contrast, arbuscular mycorrhizal fungi appear to maintain genomic variation within an individual fungal network. Arbuscular mycorrhizal fungi dwell in the soil, form mutualistic networks with plants, and bear multiple, potentially genetically diverse nuclei within a network. We explore, from a theoretical perspective, why such genetic diversity might be maintained within individuals. We consider selection acting within and between individual fungal networks. We show that genetic diversity could provide a benefit at the level of the individual, by improving growth in variable environments, and that this can stabilize genetic diversity even in the presence of nuclear conflict. Arbuscular mycorrhizal fungi complicate our understanding of organismality, but our findings offer a way of understanding such biological anomalies.     

Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth

Arbuscular mycorrhizal (AM) fungi and bacteria can interact synergistically to stimulate plant growth through a range of mechanisms that include improved nutrient acquisition and inhibition of fungal plant pathogens. These interactions may be of crucial importance within sustainable, low-input agricultural cropping systems that rely on biological processes rather than agrochemicals to maintain soil fertility and plant health. Although there are many studies concerning interactions between AM fungi and bacteria, the underlying mechanisms behind these associations are in general not very well understood, and their functional properties still require further experimental confirmation. Future mycorrhizal research should therefore strive towards an improved understanding of the functional mechanisms behind such microbial interactions, so that optimized combinations of microorganisms can be applied as effective inoculants within sustainable crop production systems. In this context, the present article seeks to review and discuss the current knowledge concerning interactions between AM fungi and plant growth-promoting rhizobacteria, the physical interactions between AM fungi and bacteria, enhancement of phosphorus and nitrogen bioavailability through such interactions, and finally the associations between AM fungi and their bacterial endosymbionts. Overall, this review summarizes what is known to date within the present field, and attempts to identify promising lines of future research.