Arbuscular mycorrhiza

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An arbuscular mycorrhiza (plural mycorrhizae or mycorrhizas) is a type of mycorrhiza in which the fungus penetrates the cortical cells of the roots of a vascular plant.

Arbuscular mycorrhizae (AMs) are characterized by the formation of unique structures such as arbuscules and vesicles by fungi of the phylum Glomeromycota (AM fungi). AM fungi help plants to capture nutrients such as phosphorus and micronutrients from the soil. It is believed that the development of the arbuscular mycorrhizal symbiosis played a crucial role in the initial colonisation of land by plants and in the evolution of the vascular plants.^[1]

It has been said that it is quicker to list the plants that do not form mycorrhizae than those that do.^[2] This symbiosis is a highly evolved mutualistic relationship found between fungi and plants, the most prevalent plant symbiosis known,^[3] and AM is found in of 80% of vascular plant families of today.^[4]

The tremendous advances in research on mycorrhizal physiology and ecology over the past 40 years have led to a greater understanding of the multiple roles of AMF in the ecosystem. This knowledge is applicable to human endeavors of ecosystem management, ecosystem restoration and agriculture.

Contents 1 Evolution of mycorrhizal symbiosis 1.1 Paleobiology 2 Physiology 2.1 Presymbiosis 2.2 Symbiosis 2.3 Nutrient uptake and exchange 3 Ecology 3.1 Habitat 3.2 Host range and specificity 3.3 Rhizosphere ecology 4 Phytoremediation 5 Agriculture 5.1 Tillage 5.2 Phosphorus fertilizer 5.3 Perennialized cropping systems 5.4 Soil quality 6 External links 7 Notes 8 References

[edit] Evolution of mycorrhizal symbiosis

[edit] Paleobiology

Both paleobiological and molecular evidence indicate that AM is an ancient symbiosis that originated at least 460 million years ago. AM symbiosis is ubiquitous among land plants, which suggests that mycorrhizae were present in the early ancestors of extant land plants. This positive association with plants may have facilitated the development of land plants.^[3]

The Rhynie chert of the lower Devonian has yielded fossils of the earliest land plants in which AM fungi have been observed.^[5] The fossilized plants containing mycorrhizal fungi were preserved in silica.

The Early Devonian saw the development of terrestrial flora. Plants of the Rhynie chert from the Lower Devonian (400 m.yrs ago) were found to contain structures resembling vesicles and spores of present Glomus species. Colonized fossil roots have been observed in Aglaophyton major and Rhynia, which are ancient plants possessing characteristics of vascular plants and bryophytes with primitive protostelic rhizomes.^[5]

Intraradical mycelium was observed in root intracellular spaces, and arbuscules were observed in the layer thin wall cells similar to palisade parenchyma. The fossil arbuscules appear very similar to those of existing AMF.^[5] The cells containing arbuscules have thickened walls which are also observed in extant colonized cells.

Mycorrhizae from the Miocene exhibit a vesicular morphology closely resembling that of present Glomerales. The need for further evolution may have been lost due to the readily available food source provided by the plant host.^[6] However, it can be argued that the efficacy of signaling process is likely to have evolved and this could be not be easily detected in the fossil record. A fine tuning of the signaling processes would improve coordination and nutrient exchange between symbionts and increasing the fitness of both the fungi and the plant symbionts.

The nature of the relationship between plants and the ancestors of arbuscular mycorrhizal fungi is contentious. Two hypotheses are that:

• Mycorrhizal symbiosis evolved from a parasitic interaction which developed in to a mutually beneficial relationship.
• Mycorrhizal fungi developed from saprobic fungi that became endosymbiotic.^[5]

Both saprotrophs and biotrophs were found in the Rhynie Chert but there is little evidence to support either hypothesis.

There is some fossil evidence that the parasitic fungi did not kill the host cells immediately upon invasion although a response to the invasion was observed in the host cells. This response may have evolved into the chemical signaling processes required for symbiosis.^[5]

In both cases the symbiotic plant-fungi interaction is thought to have evolved from a relationship in which the fungi was taking nutrients from the plant into a symbiotic relationship where the plant and fungi exchange nutrients.

[edit] Physiology

[edit] Presymbiosis

The development of AM fungi prior to root colonization, known as presymbiosis, consists of three stages: spore germination, hyphal growth, host recognition and appressorium formation.^[7]

Spores of the AM fungi are thick walled multi-nucleate resting structures.^[8] The germination of the spore does not depend on the plant as spores have been germinated under experimental conditions in the absence of plants both in vitro and in soil. However, the rate of germination can be increased by host root exudates.^[7] AM fungal spores germinate given suitable conditions of the soil matrix, temperature, carbon dioxide concentration, pH and phosphorus concentration.^[8]

The growth of AM hyphae through the soil is controlled by host root exudates and the soil phosphorus concentration.

Low phosphorus concentrations in the soil increase hyphal growth and branching as well as induce plant exudation of compounds which control hyphal branching intensity.^[7][9]

The branching of AM fungal hyphae grown in 1 mM phosphorus media is significantly reduced but the length of the germ tube and total hyphal growth was not affected. A concentration of 10 mM phosphorus inhibited both hyphal growth and branching. This phosphorus concentration occurs in natural soil conditions and could thus contribute to reduced mycorrhizal colonization.^[9]

Root exudates from AMF host plants grown in a liquid medium with and without phosphorus have been shown to effect hyphal growth.^[9] Pre-germinated surface-sterilized spores of Gigaspora magarita were grown in host plant exudates. The fungi grow in the exudates from roots starved of phosphorus had increased hyphal growth and produced tertiary branches compared to those grown in exudates from plants given adequate phosphorus. When the growth promoting root exudates were added in low concentration the AM fungi produced scattered long branches. As the concentration of exudates was increased the fungi produced more tightly clustered branches. At the highest concentration arbuscules, the AMF structures of phosphorus exchange were formed.

This chemotaxic fungal response to the host plants exudates is thought to increase the efficacy of host root colonization in low phosphorus soils.^[7] It is an adaptation for fungi to efficiently explore the soil in search of a suitable plant host.^[9]

Further evidence that AM fungi exhibit host specific chemotaxis: spores of Glomus mosseae where separated from the roots of a host plant, non host plants and dead host plant by a membrane only permeable to hyphae. In the treatment with the host plant the fungi crossed the membrane and always emerged within 800 µm of the root. Whereas in the treatments with non host plants and dead plants, the hyphae did not cross the membrane to reach the roots.^[10] This demonstrates that arbuscular mycorrhizal fungi have chemotaxic abilities which enable hyphal growth toward the roots of a potential host plant.

Molecular techniques have been used to further understand the signaling pathways which occur between arbuscular mycorrhizae and the plant roots. In the presence of exudates from potential host plant roots the AM undergoes physiological changes which allow it to colonize its host. AM fungal genes required for the respiration of spore carbon compounds are triggered and turned on by host plant root exudates. In experiments there was an increase in the transcription rate of 10 genes 0.5h after exposure and an even greater rate after 1h. A morphological growth response was observed 4hours after exposure. The genes were isolated and found to be involved in mitochondrial activity and enzyme production. The fungal respiration rate was measured by O₂ consumption rate and increased by 30% 3 hours after exposure to root exudates. This indicates that AMF spore mitochondrial activity is positively stimulated by host plant root exudates. This may be part of a fungal regulatory mechanism that conserves spore energy for efficient growth and the hyphal branching upon receiving signals from a potential host plant.^[11]

When arbuscular mycorrhizal fungal hyphae encounter the root of a host plant an apressorium (an infection structure) is formed on the root epidermis. The apressorium is the structure from which the hyphae can penetrate into the host’s parenchyma cortex.^[12] The formation of apressoria does not require chemical signals from the plant. AM fungi could form apressoria on the cell walls of “ghost” cells in which the protoplast had been removed to eliminate signaling between the fungi and the plant host. However, the hyphae did not further penetrate the cells and grow in toward the root cortex which indicates that signaling between symbionts is required for further growth once appresoria are formed.^[7]

[edit] Symbiosis

Once inside the parenchyma the fungi forms highly branched structures for nutrient exchange with the plant called "arbuscules".^[12] These are the distinguishing structures of arbuscular mycorrhizal fungus. Arbuscules are the sites of exchange for phosphorus, carbon, water and other nutrients.^[8]

The host plant exerts a control over the intercellular hyphal proliferation and arbuscule formation. There is a decondensation of the plant's chromatin which indicates increased transcription of the plant's DNA in arbuscule containing cells.^[12] Major modifications are required in the plant host cell to accommodate the arbuscules. The vacuoles shrink and other cellular organelles proliferate. The plant cell cytoskeleton is reorganized around the arbuscules.

There are two other types of hyphae which originate from the colonized host plant root. Once colonization has occurred short lived runner hyphae grow from the plant root into the soil. These are the hyphae that take up phosphorus and micronutrients which are conferred to the plant. AM fungal hyphae have a high surface to volume ratio making their absorptive ability greater than that of plant roots.^[13] AMF hyphae are also finer than roots and can enter into pores of the soil that are inaccessible to roots.^[14] The third type of AMF hyphae grows from the roots and colonizes other host plant roots. The three types of hyphae are morphologically distinct.^[8]

[edit] Nutrient uptake and exchange

AMF are obligate symbionts. They have limited saprobic ability and are dependent on the plant for their carbon nutrition.^[2] AM fungi take up the products of the plant host’s photosynthesis as hexoses.

The transfer of carbon from the plant to the fungi may occur through the arbuscules or intraradical hyphae.^[15] Secondary synthesis from the hexoses by AM occurs in the intraradical mycelium. Inside the mycelium, hexose is converted to trehalose and glycogen. Trehalose and glycogen are carbon storage forms which can be rapidly synthesized and degraded and may buffer the intracellular sugar concentrations.^[15] The intraradical hexose enters the oxidative pentose phosphate pathway which produces pentose for nucleic acids.

Lipid biosynthesis also occurs in the intraradical mycelium. Lipids are then stored or exported to extraradical hyphae where they may be stored or metabolized. The breakdown of lipids into hexoses, known as gluconeogenesis, occurs in the extraradical mycelium.^[15] Approximately 25% of the carbon translocated from the plant to the fungi is stored in the extraradical hyphae.^[16] Up to 20% of the host plant's photosynthate carbon may be transferred to the AM fungi.^[15] This represents a considerable carbon investment in mycorrhizal network by the host plant and contribution to the below ground organic carbon pool.

An increase in the carbon supplied by the plant to the AM fungi increases the uptake of phosphorus and the transfer of phosphorus from fungi to plant (Bücking & Shachar-Hill 2005). Phosphorus uptake and transfer is also lowered when the photosynthate supplied to the fungi is decreased. Species of AMF differ in their abilities to supply the plant with phosphorus.^[17] In some cases arbuscular mycorrhizae are poor symbionts providing little phosphorus while taking relatively high amounts of carbon.^[17]

The benefit of mycorrhizae to plants is mainly attributed to increased uptake of nutrients, especially phosphorus. This increase in uptake may be due to increase surface area of soil contact, increased movement of nutrients into mycorrhizae, a modification of the root environment and increased storage.^[14] Mycorrhizal can be much more efficient than plant roots at taking up phosphorus. Phosphorus travels to the root or via diffusion and hyphae reduce the distance required for diffusion thus increasing uptake. The rate of inflow of phosphorus into mycorrhizae can be up to six times that of the root hairs.^[14] In some cases the role of phosphorus uptake can be completely taken over by the mycorrhizal network and all of the plant’s phosphorus may be of hyphal origin.^[17]

The available phosphorus concentration in the root zone can be increased by mycorrhizal activity. Mycorrhizae lower the rhizosphere pH due to selective uptake of NH₄⁺ (ammonium-ions) and release of H⁺ ions. Decreased soil pH increases the solubility of phosphorus precipitates. The hyphal uptake of NH₄⁺ also increases the flow of nitrogen to the plant as NH₄⁺ is adsorbed to the soil's inner surfaces and must be taken up by diffusion.^[16]

[edit] Ecology

[edit] Habitat

Arbuscular mycorrhizal fungi are most frequent in plants growing on mineral soils. The populations of AM fungi is greatest in plant communities with high diversity such as tropical rainforests and temperate grasslands where they have many potential host plants and can take advantage of their ability to colonize a broad host range.^[18]. There is a lower incidence of mycorrhizal colonization in very arid or nutrient rich soils. Mycorrhizas have been observed in aquatic habitats; however, waterlogged soils have been show to decrease colonization in some species.^[18]

[edit] Host range and specificity

The specificity, host range and degree of colonization of mycorrhizal fungi is difficult to analyze in the field due to the complexity of interactions between the fungi within a root and within the system. There is no clear evidence that arbuscular mycorrhizal fungi exhibit specificity for colonization of potential AM host plant species as do fungal pathogens for their host plants.^[18] This may be due to the opposite selective pressure involved.

In parasitic relations, the host plant benefits from mutations which prevent colonization whereas in a symbiotic relationship, the plant benefits from mutation that allow for colonization by AMF.^[18] However, plant species differ in the extent and dependence on colonization by certain AM fungi and some plants may be facultative mycotrophs while others may be obligate mycotrophs.^[18]

The ability of the same AM fungi to colonize many species of plants has ecological implications. Plants of different species can be linked underground to a common mycelial network.^[18] One plant may provide the photosynthate carbon for the establishment of the mycelial network which another plant of a different species can utilize for mineral uptake. This implies that arbuscular mycorrhizae are able to balance below ground intra – and interspecific plant interactions.^[18]

[edit] Rhizosphere ecology

The rhizosphere is the soil zone in the immediate vicinity of a root system.

Arbuscular mycorrhizal symbiosis affects the community and diversity of other organisms in the soil. This can be directly seen by the release of exudates, or indirectly by a change in the plant species and plant exudates type and amount.^[19]

Mycorrhizae diversity has been shown to increase plant species diversity as the potential number of associations increases. Dominant arbuscular mycorrhizal fungi can prevent the invasion of non-mycorrhizal plants on land where they have established symbiosis and promote their mycorrhizal host.^[20]

Recent research has shown that AM fungi release a diffusional factor, known as the myc factor, which activates the nodulation factor's inducible gene mtENOD11. This is the same gene involved in establishing symbiosis with the nitrogen fixing bacteria, rhizobium (Kosuta et al. 2003). When rhizobium bacteria are present in the soil, mycorrhizal colonization is increased due to an increase in the concentration of chemical signals involved in the establishment of symbiosis (Xie et al. 2003). Effective mycorrhizal colonization can also increase the nodulations and symbiotic nitrogen fixation in mycorrhizal legumes.^[16]

The extent of arbuscular mycorrhizal colonization and species affects the bacterial population in the rhizosphere. Bacterial species differ in their abilities to compete for carbon compound root exudates. A change in the amount or composition of root exudates and fungal exudates due to the existing AM mycorrhizal colonization determines the diversity and abundance of the bacterial community in the rhizosphere.^[19]

The influence of AM fungi on plant root and shoot growth may also have indirect effect on the rhizosphere bacteria. AMF contributes a substantial amount of carbon to the rhizosphere through the growth and degeneration of the hyphal network. There is also evidence that AM fungi may play an important role on mediating the plant species' specific effect on the bacterial composition of the rhizosphere.^[19]

[edit] Phytoremediation

The use of arbuscular mycorrhizal fungi in ecological restoration projects has been shown to enable host plant establishment on degraded soil and improve soil quality and health (phytoremediation).^[21]

Disturbance of native plant communities in desertification-threatened areas is often followed by degradation of physical and biological soil properties, soil structure, nutrient availability and organic matter.

When restoring disturbed land it is essential to not only replace the above ground vegetation but also the biological and physical soil properties.^[21]

A relatively new approach to restore land and protect against desertification is to inoculate the soil with arbuscular mycorrhizal fungi with the reintroduction of vegetation. A long term study demonstrated that a significantly greater long term improvement in soils' quality parameters was attained when the soil was inoculated with a mixture of indigenous arbuscular mycorrhizal fungi species compared to the non inoculated soil and soil inoculated with a single exotic species of AM fungi (Figure 2).^[21] The benefits observed were an increased plant growth and soil nitrogen content, higher soil organic matter content and soil aggregation. The improvements were attributed to the higher legume nodulation in the presence of AMF, better water infiltration and soil aeration due to soil aggregation.

Inoculation with native AM fungi increased plant uptake of phosphorus, improving plant growth and health. The results support the use of AM fungi as a biological tool in the restoration of biotopes to self-sustaining ecosystems.^[21]

[edit] Agriculture

Many modern agronomic practices are disruptive to mycorrhizal symbiosis. There is great potential for low input agriculture to manage the system in a way that promotes mycorrhizal symbiosis.

Conventional agriculture practices, such as tillage, heavy fertilizers and fungicides, poor crop rotations and selection for plants which survive these conditions, hinder the ability of plants to form symbiosis with arbuscular mycorrhizal fungi.

Most agricultural crops can perform better and are more productive when well colonized by AM fungi. AM symbiosis increases the phosphorus and micronutrient uptake and growth of their plant host (George et al. 1992).

Management of AM fungi is especially important for organic and low input agriculture systems where soil phosphorus is generally low, although all agroecosystems can benefit by promoting arbuscular mycorrhizae establishment.

Some crops that are poor at seeking out nutrients in the soil are very dependent on AM fungi for phosphorus uptake. For example flax, which has poor chemotaxic ability, is highly dependent on AM mediated phosphorus uptake at low and intermediate soil phosphorus concentrations (Thingstrup et al. 1998).

Proper management of AMF in the agroecosystems can improve the quality of the soil and the productivity of the land. Agricultural practices such as reduced tillage, low phosphorus fertilizer usage and perennialized cropping systems promote functional mycorrhizal symbiosis.

[edit] Tillage

Tillage reduces the inoculation potential of the soil and the efficacy of mycorrhizaes by disrupting the extraradical hyphal network (Miller et al. 1995, McGonigle & Miller 1999, Mozafar et al. 2000).

By breaking apart the soil macro structure the hyphal network is rendered non-infective (Miller et al. 1995, McGonigle & Miller 1999). The disruption of the hyphal network decreases the absorptive abilities of the mycorrhizae because the surface area spanned by the hyphae is greatly reduced. This in turn lowers the phosphorus input to the plants which are connected to the hyphal network (Figure 3, McGonigle & Miller 1999).

In reduced tillage system heavy phosphorus fertilizer input may not be required as compared to heavy tillage systems. This is due to the increase in mycorrhizal network which allows mycorrhizae to provide the plant with sufficient phosphorus (Miller et al. 1995).

[edit] Phosphorus fertilizer

The benefits of AMF are greatest in systems where inputs are low. Heavy usage of phosphorus fertilizer can inhibit mycorrhizal colonization and growth.

As the soil's phosphorus levels available to the plants increases, the amount of phosphorus also increases in the plant's tissues, and carbon drain on the plant by the AM fungi symbiosis become non-beneficial to the plant (Grant 2005).

A decrease in mycorrhizal colonization due to high soil phosphorus levels can lead to plant deficiencies in other micronutrients that have mycorrhizal mediated uptake such as copper (Timmer & Leyden 1980).

[edit] Perennialized cropping systems

Cover crops are grown in the fall, winter and spring, covering the soil during periods when it would commonly be left without a cover of growing plants.

Mycorrhizal cover crops can be used to improve the mycorrhizal inoculum potential and hyphal network (Kabir and Koide 2000, Boswell et al.1998, Sorensen et al 2005).

Since AM fungi are biotrophic, they are dependent on plants for the growth of their hyphal networks. Growing a cover crop extends the time for AM growth into the autumn, winter and spring. Promotion of hyphal growth creates a more extensive hyphal network. The mycorrhizal colonization increase found in cover crops systems may be largely attributed to an increase in the extraradical hyphal network which can colonize the roots of the new crop (Boswell et al. 1998). The extraradical mycelia are able to survive the winter providing rapid spring colonization and early season symbiosis (McGonigle and Miller 1999). This early symbiosis allows plants to tap into the well established hyphal network and be supplied with adequate phosphorus nutrition during early growth which greatly improves the crop yield.

[edit] Soil quality

Restoration of native AM fungi increases the success of ecological restoration project and the rapidity of soil recovery.^[21] There is evidence that this enhancement of soil aggregate stability is due to the production of a soil protein known as glomalin.

Glomalin related soil proteins (GRSP) have been identified using a monoclonal antibody (Mab32B11) raised against crushed AMF spores. It is defined by its extraction conditions and reaction with the antibody Mab32B11.

There is other circumstantial evidence that glomalin is of AM fungal origin. When AM fungi are eliminated from soil through incubation of soil without host plants the concentration of GRSP declines. A similar decline in GRSP have also been observed in incubated soils from forested, afforested and agricultural land^[22] and grasslands treated with fungicide.^[23]

Glomalin is hypothesized to improve soil aggregate water stability and decrease soil erosion. A strong correlation has been found between GRSP and soil aggregate water stability in a wide variety of soils where organic material is the main binding agent, although the mechanism is not known.^[23] The protein glomalin has not yet been isolated and described, and the link between glomalin, GRSP and arbuscular mycorrhizal fungi is not yet clear.^[23]

[edit] External links

• CSIRO: Arbuscular Mycorrhizas
• INVAM: International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi
• Phylogeny and taxonomy of Glomeromycota
• Mycorrhizal Literature Exchange
• Information on VAM
• Janusz Blaszkowski - Information on AMF

[edit] Notes

[edit] References

• Boswell, E. P., R.T. Koide, D.L. Shumway, H.D. Addy. (1998). "Winter Wheat cover cropping, VA mycorrhizal fungi and maize growth and yield". Agriculture, Ecosystems and Environment 67: 55-65. doi:10.1016/S0167-8809(97)00094-7. 
• Bucking H., Shacker-Hill Y. (2005). "Phosphate uptake, transport and transfer by arbuscular mycorrhizal fungus is increased by carbohydrate availability". New Phytologist 165: 889-912. doi:10.1111/j.1469-8137.2004.01274.x. 
• George E., K. Haussler, S.K. Kothari, X.L. Li and H. Marshner,1992 Contribution of Mycorrhizal Hyphae to Nutrient and Water Uptake of Plants. In Mycorrhizas in Ecosystems, ed., D.J. Read, D.H. Lewis, A.H. Fitter, I.J. Alexander. United Kingdom: C.A.B. International, pp.42-47.
• Grant, C. Bitman, S., Montreal, M., Plenchette, C., Morel, C.. "Soil and fertilizer phosphorus: effects on plant supply and mycorrhizal development". Canadian Journal of Plant Science 85: 3-14. 
• Kosuta, S., Chabaud, M., Lougnon, G., Gough, C., Denarie, J., Barker, D., Bacard, G. (2003). "A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific mtENOD11 expression in roots of Medicago truncatula". Plant Physiology 131: 952-962. doi:10.1104/pp.011882. 
• Kabir, Z. and R.T. Koide (2000). "The effect of dandelion or a cover crop on mycorrhiza inoculum potential, soil aggregation and yield of maize". Agriculture, Ecosystems and Environment 78: 167-174. doi:10.1016/S0167-8809(99)00121-8. 
• McGonigle, T.P. and M.H. Miller (1999). "Winter survival of extraradical hyphae and spores of arbuscular mycorrhizal fungi in the field". Applied Soil Ecology 12: 41-50. doi:10.1016/S0929-1393(98)00165-6. 
• Miller, M.H., McGonigle T.P., Addy, H.D. (1995). "Functional ecology if vesicular arbuscular mycorrhizas as influenced by phosphate fertilization and tillage in an agricultural ecosystem". Critical Reviews in Biotechnolgy 15: 241-255. doi:10.3109/07388559509147411. 
• Mozafar, A., Anken, T., Ruh, R., Frossard, E. (2000). "Tillage intensity, Mycorrhizal and non mycorrhizal fungi and nutrient concentrations in maize, wheat and canola". Agronomy Journal 92: 1117-1124. 
• Sorensen, J.N., J Larsen and I. Jakobsen (2005). "Mycorrhizae formation and nutrient concentration in leeks (Allium porrum) in relation to previous crop and cover crop management on high P soils". Plant and Soil 273: 101-114. doi:10.1007/s11104-004-6960-8. 
• Thingstrup, I., G. Rubaek, E. Sibbensen and I. Jakobsen (1999). "Flax (Linum usitatissimum L.) depends on arbuscular mycorrhizal fungi for growth and P uptake at intermediate but not high soil P levels in the field". Plant and Soil 203: 37-46. doi:10.1023/A:1004362310788. 
• Timmer, L., Leyden, R. (1980). "The relationship of mycorrhizal infection to phosphorus-induced copper deficiency in sour orange seedlings". New Phytologist 85: 15-23. doi:10.1111/j.1469-8137.1980.tb04443.x. 
• Xie, Z., Staehelin, C., Vierheilig, H., Weimken, A., Jabbouri, S., Broughton W., Vogeli-Lange, R., Thomas B. (1995). "Rhizobial Nodulation Factors Stimulate Mycorrhizal Colonization of Nodulation and Nonnodulating Soybeans". Plant Physiology 108: 1519-1525.