AM fungi are considered to be asexual, although the hyphae of genetically distinct strains can anastomose and exchange genetic material 24 , The very concepts of species and individual are poorly defined in this group of organisms, reflecting a high degree of genetic and functional variability. Even the definition of a cell as a hyphal compartment is inconsistent with the syncytial mycelia of these fungi, in which nuclei are constantly translocated by rapid cytoplasmic streaming Finally, their large asexual spores contain thousands of nuclei, making classical genetic approaches unsuitable 7.
A further level of complexity arises as several Glomeromycota host unculturable endobacteria. All these unorthodox traits have so far limited the possibility of applying standard approaches such as genetic transformation, mutant generation and characterization, as well as large-scale transcriptomic and genomic analyses, to AM fungi. Although sequencing methods are evolving fast, the project to sequence the genome of the AM fungus Glomus intraradices has met a bumpy road At the same time, the lack of a uninucleate cell stage in the life cycle of AM fungi is a major obstacle in obtaining stable transgenic strains.
Nevertheless, the transient expression of an exogenous gene in G. Because of these peculiar traits, transcriptomic 32 and proteomic 33 analyses have so far proven to be more successful in investigating the molecular basis of AM fungal growth and function. In contrast to AM fungi, genetic tools and genomic information have helped in investigating several aspects of AM interactions such as root colonization and communication between symbionts 7 , 27 , Nevertheless, this one-way approach has very likely provided us with a biased picture, in which the plant seems to be the main factor and determining the contribution of each partner to the establishment and functioning of the association is still difficult.
The demonstration that AM fungi possess high-affinity inorganic phosphate Pi transporters provided a breakthrough in the understanding of fungal function. Furthermore, the expression of this Pi transporter was localized to the extraradical hyphae of G. Accumulated as polyphosphate, Pi is then rapidly translocated along the aseptate mycelium to the host plant Nitrogen is another important element taken up by AM fungi, and genes involved in the transport of ammonium 37 and amino acids 38 have been identified, whereas arginine is probably the preferred molecule for long-distance transport to the host plant A glutamine synthase gene of G.
Although carbon transfer from plants to AM fungi was demonstrated in the s 2 , its molecular mechanisms are still unclear. Surprisingly, with the exception of one gene from the non-AM Geosiphon pyriforme 40 , which hosts intracellular cyanobacteria, no hexose transporters responsible for C uptake from host cells have so far been characterized in Glomeromycota.
The availability of expressed sequence tag libraries from different steps of the life cycle of G. A first glimpse has been caught by Seddas et al. The expression of only a few fungal genes is strongly affected by the plant genotype Although there are an increasing number of studies on specific fungal genes, the genetic traits that discriminate an AM fungus from an EM fungus or a pathogen are currently unknown.
Interestingly, a G. Similarly, a gene encoding an Era-like GTPase in the rice pathogen Magnaporthe oryzae and required for virulence was found to be similar to the Gin-N protein from G. These findings suggest that some molecular mechanisms underlying the invasion of plant tissues are shared by pathogenic and symbiotic fungi, in spite of their distant phylogenetic relationships and diverse trophic habits.
The dissection of plant responses illustrates how the mechanisms operating to accommodate the AM fungus inside the plant cell lumen are shared by diverse plants and have been conserved during evolution. Root colonization is vital to AM fungi Fig.
Their spores feed germinating hyphae through the catabolism of storage lipids for just a few days 2. During this period, hyphae explore the soil in search of a host but if they never meet one, they arrest their growth and retract their cytoplasm back into the spore, which may again become dormant and restart the germination process over and over.
This situation is not likely to be very frequent in nature because of the wide host range of these fungi, but is a hallmark of their obligate biotrophy, as well as their endurance.
This strict biotrophy has long frustrated attempts to obtain enough material to perform large-scale nucleic acid extractions or produce sterile inoculum.
The latter was made possible by root organ cultures that serve as a living substrate to grow several species of AM fungi The germination of a resting spore is followed by the production of a short explorative mycelium. The perception of plant exudates, released by the host root, induces recursive hyphal branching, increasing the probability of a direct contact between the symbionts. In the meantime, fungal exudates are perceived by the root, where they trigger calcium spiking through the activation of the common SYM pathway Box 1.
Signal transduction leads to the activation of cellular and transcriptional responses green cells and nuclei. The contact between the plant and fungus is followed by the adhesion of a hyphopodium to the root surface. This triggers the assembly of a broad aggregation of cytoplasm yellow , named the prepenetration apparatus PPA in the contacted epidermal cell and underlying outer cortical cell.
Subsequent intracellular fungal colonization strictly follows the route of PPAs from the epidermis to the inner cortex. Here, intercellular hyphae can develop along the root axis.
The PPA mechanism is then replicated in the contacted inner cortical cells, both before fungal entry and—on a smaller scale—branching. Eventually, a highly branched arbuscule occupies most of the cell volume, forming an extensive surface for nutrient exchange.
Perception of the host plant by the presymbiotic mycelium is mediated by root exudates. The responsible compounds that are released by the root and diffuse a short distance, before being washed away or degraded, have been identified as strigolactones 45 , They stimulate AM fungal metabolism and branching, a change in mycelial growth pattern that is thought to increase the chances of an encounter with the host.
Strigolactones also have a hormonal role in inhibiting lateral branching of shoots 47 , This direct effect on plant development is considered to be the main function for this class of molecules, which are in fact produced by many plant taxa 45 , 49 , including those not associated with mycorrhizal fungi.
The leakage of strigolactones from roots into the soil and their rapid hydrolysis have in any case made them ideal for signalling root proximity in the rhizosphere 7 , The seeds of parasitic weeds are also stimulated to germinate by strigolactones These multiple functions recall the pleiotropic effects of auxins, and promote consideration of strigolactones as hormones. AM fungi are not inactive during their presymbiotic growth.
A molecular dialogue precedes root colonization, keeping the partners informed about their reciprocal proximity Although the responsible molecules have not yet been identified, AM fungal bioactive molecules were shown to be smaller than 3 kDa, partially lipophilic 51 and suggested to possess a chitin backbone These diffusible signals, often referred to as 'Myc factor' 52 , are known to be perceived by the plant also in the absence of a physical contact with the fungus, inducing, for example, a membrane-steroid-binding protein, which is critical for mycorrhization Plant responses to Myc factors range from the molecular to the organ level and are part of a reprogramming under the control of the so-called common symbiosis SYM pathway Box 2 , the signal-transduction pathway that prepares the plant for successful association with both AM fungi and nitrogen-fixing rhizobia.
The common SYM pathway seems to be primarily involved in controlling early events in AM establishment, and particularly the precontact responses and first steps of root colonization. Mutation of one of these genes blocks fungal colonization at the epidermal or subepidermal cell layer. The central factor of this signalling pathway is the most widespread second messenger in eukaryotic cells: the calcium ion.
In recent years, specific calcium signatures have also been described for AMs. These differences could be the key to understanding one of the central questions in the study of legume symbiosis: as the common pathway is shared by both AM and nodulation, how does the plant determine which microorganism is trying to colonize its tissues?
This is anyway not the case for the majority of AM host plants, which have no obvious relationship with rhizobia.
Once a chemical acquaintance has been made between the fungus and the plant, and roots and hyphae have proliferated and branched in a small volume of the rhizosphere, the presymbiotic phase of the AM interaction culminates in a physical encounter between symbionts, when a hyphal tip touches the surface of a root Figs 4 and 5. AM fungi carefully select the location for starting root penetration. Hyphae can wander for several centimetres along the root surface, forming long, straight or gently curving hyphae; then, unpredictably, they swell, flatten on the cell wall of a few epidermal cells and branch repeatedly to develop what is known as a hyphopodium In the absence of direct evidence, several clues may shed light on this process.
When the plant and fungus are separated by a permeable membrane, AM hyphal branching concentrates in the vicinity of young lateral roots 52 , which are also commonly acknowledged as the primary site of AM colonization, at least in laboratory conditions The transmission electron micrograph in b shows that the hyphopodium strict adhesion to the root is achieved through the formation of several protrusions of the fungal cell wall into the wall of the epidermal cell arrows.
Hyphopodia tightly adhere to the root epidermis and their wall protrudes with many digitations into the outer layers of the plant cell wall Fig. The molecular and developmental mechanisms mediating the switch from linear apical growth to the swollen and branched form of the hyphopodium are still completely obscure. By contrast, hyphopodium development is known to be followed by a pause in fungal growth that can last for 4—6 h before new tip growth is initiated to develop the penetration hypha During this time, plant cells and tissues prepare for colonization.
The symbiotic pathway-dependent expression of ENOD11 a gene coding for a putative secreted protein is reported in the hyphopodium area The expression of several other plant genes also changes, many of which are already regulated during the presymbiotic phase New genes also become active on hyphopodium development, including those involved in cell wall remodelling and defence 60 , just at the time when epidermal cells reorganize their cytoplasm to produce an AM-specific structure that is indispensable for successful fungal penetration: the PPA prepenetration apparatus Contacted epidermal cells start to assemble the secretory machinery that builds the interface compartment where the fungus will be hosted.
Cytoplasm becomes aggregated at the contact site, then develops into a thick column that predicts the subsequent route of the hypha across the cell All elements of the secretory pathway are concentrated in the PPA: abundant endoplasmic reticulum, and many Golgi bodies and secretory vesicles But the main factor in this display is the nucleus; at an early stage, its movements to and from the contact site anticipate PPA development Eventually, the PPA is completed and the fungus starts growing again, with a hyphal tip heading through the epidermal cell wall and along the track of the PPA.
At this time, the perifungal membrane is thought to be assembled, as PPA secretory vesicles are expected to fuse to produce an invagination of the plant plasma membrane. Perifungal membrane development marks the appearance of the symbiotic interface, the narrow intracellular compartment that allows AM fungi to grow inside the plant cell without breaking its integrity 5 Figs 4 and 6.
The scheme in a shows how intracellular fungal hyphae are enveloped by the perifungal membrane, an extension of the host cell plasma membrane. This outlines the interface compartment, an apoplastic space that surrounds the fungus and mediates nutrient exchange. The central vacuole is resized into a smaller volume as the fungus develops to occupy most of the cell lumen. The nucleus enlarges and is positioned in the middle of the hyphal branches.
The transmission electron image in b shows the details of the fungal accommodation process inside an arbusculated cell of carrot. The interface compartment uncoloured is clearly visible all around the fungus pink , whereas plant organelles are observed all around the perifungal membrane. All AM fungi are characterized by—and named after—arbuscules from the Latin arbusculum , small tree, Fig.
These structures are formed in the inner root cortex by repeated branching of an intracellular hypha, and considered the site of nutrient exchange The mechanisms controlling arbuscule development are largely unknown. The colonization step is not strictly dependent on the common symbiotic pathway, as, under high inoculum pressure, a few SYM mutants can be forced into AM colonization In most of these cases, the development of arbuscules proceeds normally, although their overall distribution is sometimes reported to be more limited and patchy 7.
Some genes that affect arbuscule development have been recently identified by reverse genetics. RNA interference knockdown of the Vapyrin gene, coding for a cytoplasmic protein with unknown function, induces a marked decrease in epidermal penetration and a total block of arbuscule formation In this case, only intercellular hyphae develop between cortical cells.
This form of hyphal growth also spreads AM infection along the root in wild-type plants and is likely to be less strictly controlled by the plant, as it takes place outside the cells. Similarly, silencing of either a subtilisin protease 65 , a phosphate transporter 66 or two ABC transporters 67 results in arbuscular morphogenetical defects. Taken together, these findings suggest that genes essential for arbuscule development may be independent of the SYM signalling pathway.
Although the regulatory mechanisms leading to fungal branches filling most of the host cell lumen are poorly understood, the process of arbuscule accommodation, which requires a substantial remodelling of the cortical cell, has long been described 5 , 6 , 7.
Similar to any intracellular hypha, all the thin arbuscule branches are enveloped by the perifungal now periarbuscular membrane. This invagination of the host plasmalemma does not simply surround the arbuscule as a whole, but closely follows the surface of each branch, moulded to the arbuscule itself.
The arbusculated cell is where the interface acquires its maximum spatial complexity, with a composition very similar to that of plant primary cell wall 5.
The assembly of this extensive amount of membrane and cell wall material requires the recursive involvement of PPA-like structures, organized both in advance of fungal penetration through the cell wall and along the 'trunk' hypha, as smaller aggregates anticipating the formation of fungal branches The periarbuscular interface assembly also involves the proliferation of endoplasmic reticulum, Golgi apparatus, trans -Golgi network and secretory vesicles 61 , 68 , as well as AM-induced subtilases secreted at the symbiotic interface This is not the only restructuring that the cortical cell undergoes.
Plastids multiply and deploy around the fungus, interconnected by their stromules The nucleus and nucleolus increase in size, whereas chromatin is decondensed 61 , a likely mark of enhanced transcriptional activity. When first the PPA and later the arbuscule occupy a considerable part of the cell volume, the vacuole also has to be reorganized.
Although a detailed in vivo analysis of tonoplast dynamics and the mechanisms involved is not yet available, it is clear from confocal microscopy that the vacuole is markedly reduced in size 68 , closely following hyphal branches Fig.
Arbuscules are ephemeral structures with an estimated lifespan of 4—5 days. At the end of this cycle, the fungal walls start to collapse in the arbuscule fine branches, as the cytoplasm retracts.
Eventually, this process of senescence extends to the trunk hypha until the whole arbuscule is shrunk to a compact mass of hyphal cell walls. During this process, the periarbuscular membrane rearranges once more to adapt to its changing content. The fungus eventually disappears and the host cell regains its previous organization with a large central vacuole 70 and can undergo new colonization.
In fact, root infection by AM fungi is not a linear or synchronous event. As the fungus repeatedly attempts cell and root colonization, arbuscules of very different ages coexist in neigbouring cells, and early structures, such as young hyphopodia, can develop on already colonized roots.
The significant cell reorganization during root colonization is associated with important changes in the transcriptomic profile of AM roots. Several model plants have been investigated, including M. In all cases, expression level was significantly altered for genes, including those for nutrient transporters, transcription factors and proteins involved in cellular dynamics and cell wall synthesis.
A mycorrhiza-specific plant phosphate transporter, which is localized on the periarbuscular membrane 6 Fig.
Among the regulated L. The strongest upregulated gene of the array is a putative ammonium transporter 76 , the transcripts of which have been quantified and specifically localized in arbusculated cells using laser microdissection. The availability of microarrays and novel molecular tools has stimulated questions on the systemic effects of AM fungi 77 in plants of agronomic interest as well. Significant gene modulation was reported in shoots of mycorrhizal tomato The knockdown of sucrose synthase affects arbuscule development, and also reduces plant height, shoot weight and seed yield All these data support the idea that, on colonization, plants activate an organism-wide reprogramming of their major regulatory networks and argue that mobile factors of fungal or plant origin are involved in a generalized metabolic change; in this context, hormones 80 , 81 and microRNA 82 , 83 may be good candidates.
At present, experimental data—for example, for jasmonic acid—are still highly controversial 80 , Analysis of ethylene, abscisic acid, salicylic acid and jasmonate-related compounds coupled to transcriptional profiling have documented both common and divergent responses of tomato roots to G.
The emerging picture looks complicated: symbiosis changes the levels of several hormones, in parallel with changes in the expression of their biosynthetic enzymes, also highlighting a role for oxylipins in AM Oxylipin regulation shows parallels with plant—pathogen interactions; as resistance to Phytophthora parasitica is known to depend partly on oxylipin synthesis in tobacco 85 , oxylipin regulation might shed light on the enhanced resistance of AM plants to pathogens In conclusion, the plant processes that permit the accommodation of fungal structures are active in epidermal, outer and inner cortical cells.
Their seeds will not germinate without a mycorrhizal partner usually a Basidiomycete. After nutrients in the seed are depleted, fungal symbionts support the growth of the orchid by providing necessary carbohydrates and minerals.
Some orchids continue to be mycorrhizal throughout their life cycle. If symbiotic fungi were absent from the soil, what impact do you think this would have on plant growth? Addition of fungal spores to sterile soil can alleviate this problem.
The a infection of Pinus radiata Monterey pine roots by the hyphae of Amanita muscaria fly amanita causes the pine tree to produce many small, branched rootlets. The Amanita hyphae cover these small roots with a white mantle. Endophytes release toxins that repel herbivores, or confer resistance to environmental stress factors, such as infection by microorganisms, drought, or heavy metals in soil. Coevolution of Land Plants and Mycorrhizae As we have seen, mycorrhizae are the fungal partners of a mutually beneficial symbiotic association that coevolved between roots of vascular plants and fungi.
A well-supported theory proposes that fungi were instrumental in the evolution of the root system in plants and contributed to the success of Angiosperms. The bryophytes mosses and liverworts , which are considered the most ancestral plants and the first to survive and adapt on land, have simple underground rhizoids, rather than a true root system, and therefore cannot survive in dry areas. However, some bryophytes have arbuscular mycorrhizae and some do not. True roots first appeared in the ancestral vascular plants: Vascular plants that developed a system of thin extensions from their roots would have had a selective advantage over nonvascular plants because they had a greater surface area of contact with the fungal partners than did the rhizoids of mosses and liverworts.
The first true roots would have allowed vascular plants to obtain more water and nutrients in the ground.
Fossil records indicate that fungi actually preceded the invasion of ancestral freshwater plants onto dry land. The first association between fungi and photosynthetic organisms on land involved moss-like plants and endophytes.
These early associations developed before roots appeared in plants. The fungi involved in mycorrhizae display many characteristics of ancestral fungi; they produce simple spores, show little diversification, do not have a sexual reproductive cycle, and cannot live outside of a mycorrhizal association. The plants benefited from the association because mycorrhizae allowed them to move into new habitats and allowed the increased uptake of nutrients, which gave them an enormous selective advantage over plants that did not establish symbiotic relationships.
Lichens display a range of colors and textures Figure and can survive in the most unusual and hostile habitats. They cover rocks, gravestones, tree bark, and the ground in the tundra where plant roots cannot penetrate. Lichens can survive extended periods of drought, when they become completely desiccated, and then rapidly become active once water is available again. Explore the world of lichens using this site from Oregon State University. It is important to note that lichens are not a single organism, but rather another wonderful example of a mutualism, in which a fungus usually a member of the Ascomycota or Basidiomycota lives in a physical and physiological relationship with a photosynthetic organism a eukaryotic alga or a prokaryotic cyanobacterium Figure.
Generally, neither the fungus nor the photosynthetic organism can survive alone outside of the symbiotic relationship. The body of a lichen, referred to as a thallus, is formed of hyphae wrapped around the photosynthetic partner. The photosynthetic organism provides carbon and energy in the form of carbohydrates. Some cyanobacteria additionally fix nitrogen from the atmosphere, contributing nitrogenous compounds to the association.
In return, the fungus supplies minerals and protection from dryness and excessive light by encasing the algae in its mycelium.
The fungus also attaches the lichen to its substrate. The thallus of lichens grows very slowly, expanding its diameter a few millimeters per year. Both the fungus and the alga participate in the formation of dispersal units, called soredia—clusters of algal cells surrounded by mycelia. Soredia are dispersed by wind and water and form new lichens. Lichens are extremely sensitive to air pollution, especially to abnormal levels of nitrogenous and sulfurous compounds.
The U. Forest Service and National Park Service can monitor air quality by measuring the relative abundance and health of the lichen population in an area. Lichens fulfill many ecological roles.
Caribou and reindeer eat lichens, and they provide cover for small invertebrates that hide in the mycelium. In the production of textiles, weavers used lichens to dye wool for many centuries until the advent of synthetic dyes. The pigments used in litmus paper are also extracted from lichens. The benefit to fungi is that they can obtain up to 20 percent of the total carbon accessed by plants.
Mycorrhizae function as a physical barrier to pathogens. They also provides an induction of generalized host defense mechanisms, which sometimes involves the production of antibiotic compounds by the fungi. Fungi have also been found to have a protective role for plants rooted in soils with high metal concentrations, such as acidic and contaminated soils. There are two types of mycorrhizae: ectomycorrhizae and endomycorrhizae. Ectomycorrhizae form an extensive dense sheath around the roots, called a mantle.
Hyphae from the fungi extend from the mantle into the soil, which increases the surface area for water and mineral absorption.
Once smaller sugar molecules are produced and consumed by the fungi, the fungi in turn become a meal for the ants. The insects also patrol their garden, preying on competing fungi. Both ants and fungi benefit from the association. The fungus receives a steady supply of leaves and freedom from competition, while the ants feed on the fungi they cultivate.
Learning Objectives Describe mutualistic relationships with fungi. Key Points Mutualistic relationships are those where both members of an association benefit; Fungi form these types of relationships with various other Kingdoms of life. In lichen, fungi live in close proximity with photosynthetic cyanobateria; the algae provide fungi with carbon and energy while the fungi supplies minerals and protection to the algae.
Mutualistic relationships between fungi and animals involves numerous insects; Arthropods depend on fungi for protection, while fungi receive nutrients in return and ensure a way to disseminate the spores into new environments. Key Terms mycorrhiza : a symbiotic association between a fungus and the roots of a vascular plant lichen : any of many symbiotic organisms, being associations of fungi and algae; often found as white or yellow patches on old walls, etc.
Mutualistic Relationships Symbiosis is the ecological interaction between two organisms that live together. Figure: Mycorrhizal fungi : a Ectomycorrhiza and b arbuscular mycorrhiza have different mechanisms for interacting with the roots of plants.
Lichens Lichens display a range of colors and textures. Figure: Lichen: fungi and cyanobateria : Lichens have many forms. They may be a crust-like, b hair-like, or c leaf-like.
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