At the Root of the Wood Wide Web: Self Recognition and Non-Self Incompatibility in Mycorrhizal Networks

Arbuscular mycorrhizal (AM) fungi are mutualistic symbionts living in the roots of 80% of land plant species, and developing extensive, below-ground extraradical hyphae fundamental for the uptake of soil nutrients and their transfer to host plants. Since AM fungi have a wide host range, they are able to colonize and interconnect contiguous plants by means of hyphae extending from one root system to another. Such hyphae may fuse due to the widespread occurrence of anastomoses, whose formation depends on a highly regulated mechanism of self recognition. Here, we examine evidences of self recognition and non-self incompatibility in hyphal networks formed by AM fungi and discuss recent results showing that the root systems of plants belonging to different species, genera and families may be connected by means of anastomosis formation between extraradical mycorrhizal networks, which can create indefinitely large numbers of belowground fungal linkages within plant communities.Key Words: arbuscular mycorrhizal symbiosis, extraradical mycelium, anastomosis, plant interconnectedness, self recognition, non-self incompatibility, mycorrhizal networks     

Gibberellin regulates infection and colonization of host roots by arbuscular mycorrhizal fungi

Arbuscular mycorrhiza (AM) is established by the entry of AM fungi into the host plant roots and the formation of symbiotic structures called arbuscules. The host plant supplies photosynthetic products to the AM fungi, which in return provide phosphate and other minerals to the host through the arbuscules. Both partners gain great advantages from this symbiotic interaction, and both regulate AM development. Our recent work revealed that gibberellic acids (GAs) are required for AM development in the legume Lotus japonicus. GA signaling interact with symbiosis signaling pathways, directing AM fungal colonization in host roots. Expression analysis showed that genes for GA biosynthesis and metabolism were induced in host roots around AM fungal hyphae, suggesting that the GA signaling changes with both location and time during AM development. The fluctuating GA concentrations sometimes positively and sometimes negatively affect the expression of AM-induced genes that regulate AM fungal infection and colonization.     

Reflections on the role of environmentally-governed reproductive versatility in the adaptation of plant populations

Summary

Mycorrhizal associations vary widely in structure and function, but the commonest interaction is the Arbuscular Mycorrhizal (AM) symbiosis which forms between the roots of over 80% of all terrestrial plant species and Zygomycete fungi of the Order Glomales. These are obligate symbionts which colonise plant root cells. This symbiosis confers benefits directly to the host plants through the acquisition of phosphate and other mineral nutrients from the soil by the fungus while the fungus receives a carbon source from the host. In addition, the symbiosis may also enhance the plants resistance to biotic and abiotic stresses. The beneficial effects of AM symbioses occur as a result of a complex molecular dialogue between the two symbiotic partners. Identifying the molecules and genes involved in the dialogue is necessary for a greater understanding of the symbiosis. This paper reviews the process of AM fungal colonisation of plant roots and the underlying molecular mechanisms associated with the formation and functioning of an AM symbiosis.     

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.     

Induction of glycyrrhizin and total phenolic compound production in licorice by using arbuscular mycorrhizal fungi

Arbuscular mycorrhizal fungi have mutualistic symbiosis with higher plants, increasing plant resistance to environmental stresses and nutrient uptake and improving soil. During arbuscular mycorrhizal symbiosis, a range of chemical and biological factors are affected. In this study, two species of arbuscular mycorrhiza (Glomus mosseae and G. intraradices) were used to assess the effects of inoculation on licorice growth and secondary metabolite production. After successful inoculation, the increase in the growth rate, P and Zn uptake, and the accumulation of secondary metabolites in licorice (Glycyrrhiza glabra L.) roots were observed in two periods of 3 and 6 months compared to control. After 6 months, more increments in growth, secondary metabolites, and P and Zn uptake were observed compared with the first 3-months period. Two groups of secondary metabolites arising from phenolic and terpenoid metabolism obviously responded to mycorrhizal fungi colonization in licorice roots.     

Reduced Germination of Orobanche cumana Seeds in the Presence of Arbuscular Mycorrhizal Fungi or Their Exudates

Broomrapes (Orobanche and Phelipanche spp) are parasitic plants responsible for important crop losses, and efficient procedures to control these pests are scarce. Biological control is one of the possible strategies to tackle these pests. Arbuscular Mycorrhizal (AM) fungi are widespread soil microorganisms that live symbiotically with the roots of most plant species, and they have already been tested on sorghum for their ability to reduce infestation by witchweeds, another kind of parasitic plants. In this work AM fungi were evaluated as potential biocontrol agents against Orobanche cumana, a broomrape species that specifically attacks sunflower. When inoculated simultaneously with O. cumana seeds, AM fungi could offer a moderate level of protection against the broomrape. Interestingly, this protection did not only rely on a reduced production of parasitic seed germination stimulants, as was proposed in previous studies. Rather, mycorrhizal root exudates had a negative impact on the germination of O. cumana induced by germination stimulants. A similar effect could be obtained with AM spore exudates, establishing the fungal origin of at least part of the active compounds. Together, our results demonstrate that AM fungi themselves can lead to a reduced rate of parasitic seed germination, in addition to possible effects mediated by the mycorrhizal plant. Combined with the other benefits of AM symbiosis, these effects make AM fungi an attractive option for biological control of O. cumana.     

Mycorrhiza modulates aboveground tri‐trophic interactions to the fitness benefit of its host plant

1. Arbuscular mycorrhiza (AM), the association of AM fungi and plant roots, may alter morphological and physiological attributes of aboveground plant parts and thereby influence plant‐associated organisms such as herbivores and their natural enemies, predators and parasitoids. 2. The interactions between AM and the players of aboveground tri‐trophic systems have mainly been considered in isolation from each other. The effects of AM on aboveground herbivore–carnivore population dynamics and the consequences to plant fitness are unknown. 3. We explored AM‐induced compensatory mechanisms for AM‐promoted proliferation of the herbivorous spider mite, Tetranychus urticae Koch, on whole bean plants, Phaseolus vulgaris L. Vegetative and reproductive plant growth, AM fungal colonisation levels, and mite densities were assessed on spider mite‐infested plants colonised or not by the AM fungus Glomus mosseae Nicol. & Gerd, and harbouring the natural enemy of the spider mites, the predatory mite Phytoseiulus persimilis Anthias‐Henriot or not. 4. AM symbiosis modulated the aboveground tri‐trophic system to the fitness benefit of the plant. AM‐increased plant productivity outweighed the fitness decrease due to AM‐promoted herbivory: at similar vegetative growth, mycorrhizal plants produced more seeds than non‐mycorrhizal plants. 5. AM‐increased spider mite population levels were compensated for by enhanced population growth of the predators and increased plant tolerance to herbivory. 6. AM‐enhanced predator performance looped back to the AM fungus and stabilised its root colonisation levels, providing the first experimental evidence of a mutually beneficial interaction between AM and an aboveground third trophic level natural enemy.     

Arbuscular mycorrhiza: the mother of plant root endosymbioses

Arbuscular mycorrhiza (AM), a symbiosis between plants and members of an ancient phylum of fungi, the Glomeromycota, improves the supply of water and nutrients, such as phosphate and nitrogen, to the host plant. In return, up to 20% of plant-fixed carbon is transferred to the fungus. Nutrient transport occurs through symbiotic structures inside plant root cells known as arbuscules. AM development is accompanied by an exchange of signalling molecules between the symbionts. A novel class of plant hormones known as strigolactones are exuded by the plant roots. On the one hand, strigolactones stimulate fungal metabolism and branching. On the other hand, they also trigger seed germination of parasitic plants. Fungi release signalling molecules, in the form of 'Myc factors' that trigger symbiotic root responses. Plant genes required for AM development have been characterized. During evolution, the genetic programme for AM has been recruited for other plant root symbioses: functional adaptation of a plant receptor kinase that is essential for AM symbiosis paved the way for nitrogen-fixing bacteria to form intracellular symbioses with plant cells.     

Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae

Arbuscular mycorrhizal (AM) fungi are a multifaceted group of mutualistic symbionts that are common to terrestrial ecosystems. The interaction between AM fungi and plant roots is of environmental and agronomic importance. Understanding the molecular changes within the host plant upon AM fungal colonisation is a pre-requisite to a greater understanding of the mechanisms underlying the interaction. Differential mRNA display was conducted on leaf tissue of tomato plants colonised and non-colonised by the AM fungus Glomus mosseae and five putative differentially regulated cDNAs were identified. All cDNAs isolated shared high sequence similarity to known plant genes. Differential screening was initially used to establish whether the cDNAs were differentially expressed. Semi-quantitative RT-PCR was used to establish gene expression patterns for all five clones within leaf and root tissue of mycorrhizal and non-mycorrhizal colonised tomato plants. Differential regulation was observed for all five cDNAs. Down-regulation within the leaf tissue of mycorrhizal plants was observed for 4 out of the 5 cDNAs with an up-regulation observed only for one. Tissue specific regulation was observed for several cDNAs, with down-regulation observed in mycorrhizal leaf tissue and up-regulation observed within mycorrhizal root tissue as compared to non-mycorrhizal tissue.     

Ectomycorrhizas Naturally Established in Nothofagus nervosa Seedlings Under Different Cultivation Practices in a Forest Nursery

Mycorrhizas are mutualistic associations between soil fungi and plant roots which usually improve water and nutrient uptake, influencing plant fitness. Nothofagus nervosa (Raulí) is an ecologically and economically important species of South American temperate forests. Since this native tree species yields valuable timber, it was overexploited and its natural distribution area was critically reduced, so it is currently included in domestication and conservation programs. Among the factors that should be considered in these programs are the ectomycorrhizas (EcM), which would be important for the successful establishment and survival of outplanted seedlings. The aim of this work was to analyze the abundance and diversity of EcM in N. nervosa nursery-cultivated seedlings assessed by morphotyping, fungal isolation, and DNA sequencing. Arbuscular mycorrhiza (AM) occurrence was also studied. A 2-year trial was conducted following the cultivation conditions used for domestication programs. Seedlings were cultivated under two different cultivation practices (greenhouse and nursery soil) without artificial inoculation of mycorrhizal fungi. Seedlings’ roots were examined at different times. It was observed that they developed EcM between 6 and 12 months after germination and AMs were not detected in any plant. The most abundant ectomycorrhizal fungi present in seedlings’ roots were Tomentella ellisii (Basidiomycota) and an unidentified fungus named Ascomicetous EcM sp. 1. Abundance and diversity of EcM varied between the two cultivation techniques analyzed in this study, since seedlings that continued growing in the greenhouse had higher colonization values, but those transplanted to the nursery soil were colonized by a higher diversity of fungal taxa.     

Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass

The interaction between mycorrhiza and leaf endophytes (Neotyphodium sp.) was studied in three Poa bonariensis populations, a native grass, differing significantly in endophyte infection. The association between endophytes and mycorrhizal fungi colonisation was assessed by analysing plant roots collected from the field. We found that roots from endophyte-infected populations showed a significantly higher frequency of colonisation by mycorrhizal fungi and that soil parameters were not related to endophyte infection or mycorrhiza colonization. In addition, we did not observe significant differences in the number of AM propagules in soils of the three populations sites. We also report the simultaneous development of Paris-type and Arum-type mycorrhiza morphology within the same root systems of P. bonariensis. The co-occurrence of both colonisation types in one and the same root system found in the three populations, which differed in Neotyphodium infection, suggests that foliar endophytes do not determine AM morphology. The percentage of root length colonised by different types of fungal structures (coils, arbuscules, longitudinal hyphae and vesicles) showed significant and positive differences in arbuscular frequency associated with endophyte infection, whereas the much smaller amounts of vesicles and hyphal coils did not differ significantly.     

植物中丛枝菌根形成的信号途径研究进展

丛枝菌根(arbuscular mycorrhizal,AM)共生是丛枝菌根真菌与大多数陆地植物的根系之间形成的一种互利共生关系。植物给菌根真菌提供碳水化合物;作为回报,菌根真菌能够增强植物对矿质营养元素(尤其是磷)的吸收。菌根的形成过程是一系列信号交换和转导的结果,具有严格并且一致的顺序。本文以植物中菌根形成的信号途径为主线,对菌根真菌的形成过程和信号转导途径及其方式进行了分析和讨论。高等植物中菌根形成的信号途径与豆科植物的结瘤信号途径部分共享,并且与钙离子信号途径相关,但前者更为广泛。尽管该途径中很多过程目前还不十分清楚,但是相信在不久的将来就可以揭开菌根形成过程中的众多谜团。     

植物中丛枝菌根形成的信号途径研究进展

丛枝菌根(arbuscular mycorrhizal, AM)共生是丛枝菌根真菌与大多数陆地植物的根系之间形成的一种互利共生关系。植物给菌根真菌提供碳水化合物; 作为回报, 菌根真菌能够增强植物对矿质营养元素(尤其是磷)的吸收。菌根的形成过程是一系列信号交换和转导的结果, 具有严格并且一致的顺序。本文以植物中菌根形成的信号途径为主线, 对菌根真菌的形成过程和信号转导途径及其方式进行了分析和讨论。高等植物中菌根形成的信号途径与豆科植物的结瘤信号途径部分共享, 并且与钙离子信号途径相关, 但前者更为广泛。尽管该途径中很多过程目前还不十分清楚, 但是相信在不久的将来就可以揭开菌根形成过程中的众多谜团。     

H2O2参与AM真菌与烟草共生过程

以烟草((Nicotiana tabacum,品种CF90NF)为寄主,苗期接种丛枝菌根(AM)真菌摩西球囊霉(Glomus mosseae,G.m),测定G.m与烟草共生过程中烟草根部H2O2含量以及多胺氧化酶(PAO)和过氧化物酶(POD)活性;研究外源H2O2对G.m侵染烟草的影响以及H2O2清除剂和合成抑制剂对烟草侧根H2O2含量及烟草侧根和菌丝中H2O2荧光强度的影响,以探究H2O2在AM真菌侵染烟草过程中的作用。结果表明,接种G.m 20d后烟草侧根中出现H2O2含量的猝发,一定浓度的外源H2O2促进G.m对烟草的侵染,而H2O2清除剂抗坏血酸(AsA)显著削弱烟草侧根和菌丝中的H2O2荧光强度,降低G.m对烟草的侵染率,表明H2O2参与G.m与烟草共生过程;在G.m与烟草共生过程中,PAO和POD活性显著升高,PAO抑制剂二氨基十二烷(DADD)和POD抑制剂水杨羟肟酸(SHAM)显著降低烟草侧根中H2O2荧光强度,对菌丝中H2O2荧光强度无显著影响,表明烟草根部和G.m均可产生H2O2,PAO和POD参与烟草侧根中H2O2的合成,菌丝中可能存在其他来源的H2O2。     

Mycorrhizal C costs and nutritional benefits in developing grapevines

Arbuscular mycorrhizal (AM) C-costs in grapevines were investigated. Dormant vines rely on stored C for initial growth. Therefore AM colonisation costs would compete with plant growth for available C reserves. One-year-old grapevines, colonised with Glomus etunicatum (Becker and Gerdemann), were cultivated under glasshouse conditions. The C-economy and P utilisation of the symbiosis were sequentially analysed. AM colonisation, during the 0–67 day growth period, used more stem C relative to root C, which resulted in lower shoot growth. The decline in AM colonisation during the period of 67–119 days coincided with stem C replenishment and higher shoot growth. Construction costs of AM plants and root C allocation increased with root P uptake. The efficiency of P utilisation was lower in AM roots. The reliance of AM colonisation on stem C declined with a decrease in colonisation, providing more C for the refilling of stem carbohydrate reserves and shoot growth. Once established, the AM symbiosis increased P uptake at the expense of refilling of root C reserves. Although higher root C allocation increased plant construction costs, AM roots were more efficient at P utilisation.     

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。     

The Ecology of Arbuscular Mycorrhizal Fungi

Arbuscular mycorrhiza is a mutually beneficial biological association between species in the fungal phylum Glomeromycota and higher plants roots. The symbiosis is thought to have afforded green plants the opportunity to invade dry land ca 450 Ma ago and the vast majority of extant terrestrial plants retain this association. Arbuscular mycorrhizal (AM) fungi perform various ecological functions in exchange for host photosynthetic carbon that almost always contribute to the fitness of hosts from an individual to community level. Recent AM fungal research, increasingly delving into the ‘Black Box’, suggests that species in this phylum may play a key facilitative role in below-ground micro- and meso-organism community dynamics, even more perhaps, that of a bioengineer. The ubiquitous nature of the symbiosis in extant flora and the fact that variations from the AM symbiosis are recent events suggest that Glomeromycota and plant roots coevolved. This review considers aspects of AM fungal ecology emphasizing past and present importance of the phylum in niche to global ecosystem function. Nutrient exchange, evolution, taxonomy, phenology, below-ground microbial interaction, propagule dissemination, invasive plants interactions, the potential role in phytoremediation and some of the factors affecting AM fungal biology are discussed. We conclude that it is essential to include AM association in any study of higher plants in natural environments in order to provide an holistic understanding of ecosystems.     

Spatial changes of arbuscular mycorrhizal fungi in peach and their correlation with soil properties

Arbuscular mycorrhizal (AM) fungi have beneficial effects on host plants, but their growth is influenced by various factors. This study was carried out to analyze the variation of AM fungi in soils and roots of peach (Prunus persica L. var. Golden Honey 3, a yellow-flesh variety) trees in different soil layers (0–40 cm) and their correlation with soil properties. The peach tree could be colonized by indigenous AM fungi (2.2–8.7 spores/g soil and 1.63–3.57 cm hyphal length/g soil), achieving 79.50–93.55% of root AM fungal colonization degree. The mycorrhizal growth, root sugars, soil three glomalins, NH₄⁺-N, NO₃⁻-N, available P and K, and soil organic matter (SOM) had spatial heterogeneity. Soil spores, but not soil hyphae contributed to soil glomalin, and soil glomalin also contributed to SOM. There was a significant correlation of soil hyphae with spore density, soil NO₃⁻-N, and SOM. Root mycorrhiza was positively correlated with spore density, NH₄⁺-N, NO₃⁻-N, and easily extractable glomalin-related soil protein. Notably, spore density positively correlated with NO₃⁻-N, available K, SOM, and root fructose and glucose, while negatively correlated with available P and root sucrose. These findings concluded that mycorrhiza of peach showed spatial distribution, and soil properties mainly affected/altered based on the soil spore density.