Mycorrhizal Biology Issues - Research Paper Example

?INTRODUCTION Many dynamic processes occur in the soil. Roots of plants have interactions with several microorganisms that grow and establish colonies within the plant cells. Aside from bacterial endosymbioses, specifically nodule-forming bacterial colonization of roots and Actinorhiza formed by the genus Frankia, fungi interacts with plants to form mycorrhizae. In fact, arbuscular mycorrhizae are the most abundant type of microbial symbiosis present today. Mycorrhizae are symbiotic associations between fungi and vascular plant roots. Certain fungal species, specifically of the phylum Glomeromycota (arbuscular mycorrhizae), Basidiomycetes and Ascomycetes (ectomycorrhizae), beneficially colonize the roots of plants either intracellularly, as in arbuscular mycorrhizal fungi (AMF), or extracellularly, as in ectomycorrhizal fungi. The roots provide the microorganisms a stable access to nutrition. In return, the roots benefit from the high water and mineral absorptive capacity of mycelia resulting from its relatively small size and subsequent better ability to penetrate soil. As a result, mycorrhizal plants are more resistant to lack of water. They are more capable of colonizing barren land or unfamiliar territory than plants without mycorrhizae do. In addition, mycorrhizal fungi process demineralized phosphates such that the minerals will be available for plant use. However, as is the case in all biological interactions, not all mycorrhizae are mutualistic. In cases in which nutrients are abundant in the plant’s environment, association with microorganisms, as is what happens during mycorrhizal formation, may be more parasitic than beneficial (Bucher, 2007). However, current agricultural practices prevent the formation of these mycorrhizae. The pesticides being used have a non-discriminating adverse effect on the microorganisms living in the plants’ ecosystem. As such, despite the prevention of unnecessary nutrient depletion caused by parasitism, the nutrients are not being absorbed optimally because the interactions of plants and microorganisms are prevented. This study provides an overview of mycorrhizal biology. First, the development of mycorrhizae from two separate organisms to a symbiotic interaction is discussed. Next, the morphological and molecular characteristics found only among organisms involved in mycorrhizal interactions. Its functions, particularly in providing nutrients and protecting the plants against salt stress and drought, are then enumerated. Its relationships with various members of its ecosystem are then discussed. Finally, the importance of these knowledge in terms of what aspects should be focused on will be suggested. DEVELOPMENT Endomycorrhizae development Figure 1 illustrates the development of endomycorrhizae. The fungal species associated with endomycorrhizae reproduce asexually. They undergo an asymbiotic phase in which spores germinate and hyphal growth are limited without the nutrients supplied by the host plant. Soon after, hyphal growth begins. This presymbiotic phase is induced by the presence of plant root exudates, which fungal hyphae penetrate to (Bucher, 2007). At the root surface, the fungal hypha develops a set of penetrating cells and is now called a hyphopodium. This now enters the root epidermis, continuing to grow into the outer, and then the inner root cortex. It then spreads intercellular along the longitudinal axis of the root. This structure of the fungus is the one called an arbuscule (Gutjahr et al., 2008). The peak of fungal development is characterized by the development of an extraradical mycelium that is able to produce and exude spores for colonization of other plants (Bucher, 2007; Frey-Klett et al., 2007). However, the development of arbuscular mycorrhizae is not synchronous, in that various colonization stages are present in one plant (Gutjahr et al., 2008). Figure 1, previous page. Development of Endomycorrhizal Development. From Bucher, Marcel, 2007. Tansley review: Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 173, pp. 11-26. Ectomycorrhizae development On the other hand, ectomycorrhizae undergo germination first before sporulation. They then develop sporocarps that release reproductive spores that colonize fine and short roots. As these spores grow into hyphae, they enclose the roots and form what is called as a Hartig net, where nutritional exchange occurs (Frey-Klett et al., 2007). PHYSICAL CHARACTERISTICS OF MYCORRHIZAE Figure 2. Comparison of the morphology of arbuscular mycorrhizae (bottom) and ectomycorrhizae (top). As can be seen, the former has the characteristic tree like structure composed of branches and vesicles, while the latter has the characteristic Hartig net covering the root surface. From Agarwal, Pragya and Sah, Pankaj, 2009. Ecological importance of ectomycorrhizae in world forest ecosystems. Nature and Science, 7(2), pp. 107-116. Figure 2 illustrates the anatomical differences between arbuscular mycorrhizae and ectomycorrhizae. An in depth discussion of the morphological structures associated with each is provided below. Arbuscular mycorrhizae Arbuscular mycorrhizae are formed by the interaction of plants and Glomeromycots, which are obligate symbionts. Structures of Glomeromycots primarily have arbuscules, or tree branch structures, and vesicles, which are balloon-shaped storage structures. Spores, before its release, have hyphal attachments. They sometimes have a layer of vegetative cells covering them, probably for protection against adverse environmental conditions. Mycelia grows extensively outside the roots to which they are associated with (Redecker and Raab, 2006).. The unique structure of mycorrhizae prevents optimal nutrient exchange without causing the rupture of plasma membrane and mixture of cytosomal components between the microorganism and the plant (Bucher, 2007). Ectomycorrhizae The fungi of Basidiomycetes and Actomycetes grow in between the roots. These type of mycorrhizal associations is the most important in temperate regions. Specificity of fungal species associated with a certain plant is uncommon in this type of association (Agarwal and Sah, 2009). Some extracellular fungi, such as Leccinum and Suillus, only grow together with one particular plant, while others form mycorrhizae with many different plants (Nehls, 2008). The unique structure of ectomycorrhizae is composed of a few hyphae penetrating the outer cortical intercellular spaces and Hartig net, which is an aggregate of fungal cells covering the surface of the lateral roots (Agarwal and Sah, 2009). MOLECULAR CHARACTERISTICS OF MYCORRHIZAE In mycorrhizal formation, interaction does not only involve transfer of resources, but as well as signals specific for these symbiotic relationship. These signals are products of molecular processes that start from gene transcription to the translation of messenger RNAs (mRNA) to their respective protein products. With the advent of molecular biology and the development of various procedures in the field, many of these biomolecules have been related to the identifying functions of several biological groups. In this section, the genetic materials, collectively known as Myc genes, essential to the symbiotic interaction between fungi and plants, and the proteins necessary for mycorrhizal interaction are enumerated. These genes are probably secreted by fungi and are causing further transcription of mycorrhizal-related genes and structural changes in the host tissues (Bucher, 2007). In the study of Gherbi et al. (2008), it was found that Symbiosis Leu-rich Repeat Receptor Kinase (SymRK) in plants is a genetic basis for their microbial interaction, either in root nodulation by rhizobia bacteria and Frankia actinomycetes in legumes (Fabales) or in Glomeromycota fungi-land plant interaction found among endomycorrhiza. This suggests the presence of a common symbiotic pathway shared by interactions forming root nodulation and mycorrhizae (Bucher, 2007). Aside from SymRK, the pathway in mycorrhizae is composed of Does Not Make Infection 2 (DMI 2), CASTOR and PULLOX cation channels (DMI 1), NUP85 and NUP133 nuclear porins. These components have vital roles in inducing increase in calcium levels. The calcium spiking, in turn, induces the activity of Calcium/Calmodulin-Dependent Protein Kinase (CCMK), which phosphorylates CYCLOPS. These signals downstream of calcium spiking are said to be conserved between monocotyledons and dicotyledons (Gutjahr et al., 2008). Interactions among the biomolecules expressed and released by fungus or plant that affects the other have also been reported. A signal from mycorrhizal fungal hyphae induces the expression of ENOD 11 among plants to induce rhizobial root formation. ENOD 11, together with the other nodulins such as ENOD 2, ENOD 5, and ENOD 12, as well as MtN8, transcribe and translate for proteins that have proline-rich amino acid sequences. These proteins are cell wall components, which, due to their structure, probably contributes to the stability of root cells (Manthey, 2004). The ring in the amino acid structure is most likely to contribute to the stabilizing effect that these proteins confer to the cell membranes. Upon colonization by endomycorrhizal fungus Glomus intraradices, tomato (L. esculentum) roots have an increased expression of LIN6, which is an important gene for establishing and maintaining the roots as a carbon sink. In addition, the expression is specific to root cells directly in contact with fungal hyphae and the root’s central cylinder. This modulated expression prevents the presence of surplus carbon that can attract parasitic microorganisms (Schaarschmidt et al., 2006). Among the plants capable of mycorrhizal formation, the presence of strigolactone is essential in causing seed germination and vegetal growth such as root branching (Bucher. 2007). In the plasma membrane, H-ATPase pump generates an electrochemical gradient needed to drive the inorganic phosphate intake. (Bucher, 2007). The transfer of phosphate from fungi to plants is facilitated by symbiosis-induced expression of membrane spanning inorganic phosphate (Pi) transporter proteins. StPT3 was identified from potato, LePT4 and StPT3-homologue StPT4 were isolated from tomato (Lycopersicon esculentum) (Nagy et al., 2005). As may have already been obvious, the molecules expressed by plants or fungi involved in a mycorrhizal interaction contribute to causing the physical and functional changes observed among these symbioses. MtC50410.1 is a gene found specifically to be activated in plants with arbuscular mycorrhizae. It codes for a DELLA protein, which is related to the regulators in other plant species that inhibit giberellin (GA) response and subsequently decrease GA-related growth effects. Without the supposed growth effects, the increased GA concentration in mycorrhizal roots results to a deeper carbohydrate sink that sustains the demands of the related fungal growth. Mtha1 is also found to control transport processes across periarbuscular membranes. MtC10430, related to nodulin 26 of bacteria-made root nodules, codes for a membrane-bound protein that acts as a water transporting channel that improves osmoregulation. This protein is activated by calcium-dependent kinases that in turn is activated by negative water pressures such as during drought. On the other hand, for defense, the expression of MtC genes are upregulated in plants involved in mycorrhizal interactions (Manthey et al., 2004). The hyphae of arbuscular mycorrhizal fungi produce the organic compound, glomalin, which is a glycoprotein that can serve as a carbon storage for the organism (Auge, 2001). Trehalose, a carbohydrate, is synthesized in Hartig nets of ectomycorrhizae (Nehls, 2008). Ectomycorrhizal fungi, because of the greater biomass of their umbrella-shaped fruiting bodies and the resulting increase in respiration rates, require more photosynthetic products their hosts. To facilitate this transfer and convert the plant sugars to storage sugars, these organisms produce hormones that affect the associated plants (Agarwal and Sah, 2009). FUNCTION Figure 3. Schematic Diagram of the Various Effects of Mycorrhizae. From Finlay, Roger D., 2008, Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. Journal of Experimental Botany, 59(5), pp. 1115-1126. Figure 3 summarizes the many effects of mycorrhizae on the ecosystem. This is discussed in greater detail in the following sections below. Increase in nutrient and sunlight supply 1. Mobilization of minerals Phosphorus (P) is one of the essential elements needed by a biological system. One of its most elucidated role is in bioenergetics, wherein phosphorous-containing molecules such as Adenosine Troposphere (ATP) is the working high-energy molecule utilized by the body. In addition, nicotinamide adenine dinucleotide phosphate (NADPH) activates kinases that catalyze many chemical reactions in the body. Of course, phosphorus helps stabilize the structure of nucleic acids and phospholipids. Aside from Phosphorus, Nitrogen (N) is an important part of an organism, because it is needed to produce amino acids, the building blocks of proteins, and nucleotide bases, which make up the nucleic acids. In plants, they are not as readily available as other minerals because of its low mobility due to its strong and almost spontaneous association with other ions, producing polymers that are not readily available for plant use. Usual sources of P and N include pollen and dead nematodes. The availability of P and N affects the plants in such a way that roots grow undergo modification to allow optimum absorption of these minerals. One of the ways by which this is achieved is acquiring mycorrhizae, whose fungal component mechanically break down the soil (Finlay, 2008). Aside from N and P, Auge (2001) also reported that differences in nutrient concentrations during drought were also observed by several studies. Copper and Zinc concentrations in leaves are higher among mycorrhizal plants than among non-mycorrhizal ones. Manganese and boron concentrations, on the other hand, were lower. 2. Water movement Several effects of mycorrhizae on plant growth and physiology have been collated by Auge (2001). Most studies reporting differences on stomatal conductance and transpiration between mycorrhizal and non-mycorrhizal plants found that the presence of symbiotic fungi increases the transpiration and stomatal conductance. This means that the water potential of plants in symbioses with fungi have water content enough to keep open the water potential-driven stomata. These leaf structures are openings on the underside of the leaves that allows the intake of carbon dioxide (CO2) and the release of oxygen (O2). Because this unavoidably exposes the water-rich mesophyll to the relatively water-poor atmosphere, stomata also allows the transpiration of water from the plant to the atmosphere. Stomata are thus regulated by water levels, in which low water levels absorbed by the plants causes stomatal closing, while high water levels result to stomatal opening. Increased transpiration may also be observed in mycorrhizal plants, indirectly through the faster rate at which it dries the soil, as compared to that of non-mycorrhizal plants with comparable size as that of those with mycorrhiza. Of course, in optimal setting, an open stomata is much more preferred because this means the plant can produce food and O2. With this in mind, it can now be said that because mycorrhiza increases transpiration and stomatal conductance in plants, parameters that suggest prolonged stomatal opening, then water content and food production or photosynthesis are greater in mycorrhizal plants. In addition, fungi symbiotic to plants are said to get 5-20% of the plants produce. Since mycorrhizal fungi depends on the plants to provide them carbon, the root system serves as a greater carbon sink, which drives the net movement of carbon from leaves to roots. During times when photosynthesis is not optimal, lower carbon concentrations in the leaf mesophyll is expected. This will then stimulate stomata opening to allow atmospheric CO2 uptake (Auge, 2001). Protection Several evidences on the protective effect of mycorrhizal fungi on plants exposed to non-optimal conditions have already been published. However, in spite of 80% of vascular plants infected with mycorrhizal fungi, not all of these plants reported to have such improvements. The study of the effects of mycorrhiza must thus be from case to case basis. 1. Salt stress In the study of Al-Karaki (2000), the effects of varying salt concentrations on the several growth parameters of greenhouse-grown tomato (L. esculentum) that mutually interacts with the mycorrhizal fungi Glomus mosseae. High salt concentrations occur in the environment, especially in arid and semi-arid regions, as water evaporates out of the soil. Since the salts are left behind, then their concentration increase significantly. This leads to a higher oncotic pressure in the salt, driving osmosis, or the movement of water, more toward the soil than to the roots. Thus high salt concentrations in the soil decreases the water needed for the optimal growth of plants. The salt concentrations used in the study were 1.4 dS/m for the control, 4.7 dS/m for medium salt stress, and 7.4 dS/m for high salt stress. To prevent other factors from contributing to or decreasing the effects of salt, if any, a sterilized, low Phosphorus-containing soil was used. 35-day old seedlings of similar sizes were exposed to the set-ups for six weeks, after which the growth of the plant and fungi were observed. After six weeks, it was seen that, as expected, the increase in salt levels lead to a decrease in plant and fungal growth. However, the presence of mycorrhiza improves the plant’s response on salt stress as, at all salt levels, aerial and root dry masses were higher in plants that interacted with mycorrhiza than those that did not. In addition, mycorrhiza improved the uptake of Phosphorus, Sodium, Potassium, Iron, Copper, and Zinc even at salt stress (Al-Karaki, 2000). 2. Drought In the effect of mycorrhiza on soil drying, some studies reported that if the plants started out as seedlings of similar sizes, then differences between mycorrhizal and non-mycorrhizal plants in terms of the rate it dries up the soil are caused by the resulting differences in size, in which the shoots and roots of mycorrhizal plants grew up to have larger surface areas, evaporative and absorptive surface areas, respectively. When these episodes of soil drying happen, shoot growth is inhibited to prevent excessive water loss. This was found to be effected by a root-to-shoot non-hydraulic signaling system (Auge, 2001; Finlay 2008). Finally, Auge (2001) and Finlay (2008) reported the possible mechanisms explaining the improved drought tolerance among mycorrhizal plants. It has been suggested that the extra radical hyphae observed among arbuscular mycorrhizae may contribute to a plant’s water absorption. Minerals also contribute to the positive effects on the water absorption of mycorrhizal fungi in plants. The increased Phosphorus (P) concentration in leaves is one of the factors that improve energetics. In addition, P makes stomata more sensitive to ABA, which is a root-to-shoot signal of water availability. Thus, the mineral indirectly influences stomatal behavior, and water availability. 3. Toxic substances Mycorrhizal fungi have been shown by several studies to degrade toxic substances. In 1993, 2, 4-dichlorophenoxyacetic acid and atrazine, chlorinated aromatic herbicides, were shown to be degraded by ectomycorrhizal fungi. In 1997, better degradation of 2, 4-dichlorophenol was recorded from two ectomycorrhizal fungi, Paxillus involutus and Suillus variegatus in association with Pinus sylvestris than when they are in pure culture. In addition, S. variegates was also determined to be effective against 2, 4, 6-trinitrotoluene. Aside from producing the degrading factors themselves, they can also provide carbon sources to bacteria that have boremediation effects. These recruitment thus make bioremediation easier and more efficient (Finlay, 2008). Carbon sink It was said earlier that mycorrhizal fungi get 5-20% of the carbohydrates produced by the plants. These, in turn, are used by these microorganisms to produce enzymes, organic acids and compounds which may chemically breakdown the P and N containing polymers, again making these minerals much more available for use (Finlay, 2008). MYCORRHIZA IN ENVIRONMENT Relationships with other organisms Aside from the interactions between members of Glomeromycota/Basidiomycetes/Actomycetes and vascular plants, mycorrhizae themselves interact with microorganisms found in their habitat. These microorganisms help mycorrhizae, especially the ones made by Basidiomycetes and Ascomycetes, either by releasing growth factors that increases the mycelial surface area and increases plant root branching thus improving nutritional intake, or protection by detoxifying antagonistic substances and inhibition of organisms that competes with the plant or fungus involved in a mycorrhizal interaction. For example, mycorrhizae with Tuber melanosporum, an Ascomycete, are protected by pseudomonads against soil-borne competitors (Frey-Klett et al., 2007). Fungi such as soil yeasts release volatiles that improve spore germination and hyphen growth in G. mosseae (Tarkka and Piechulla, 2007). 1. Bacterial-induced mycorrhizal fungus specificity The specificity of fungi interacting symbiotically with plants may have been a result of the activity of bacteria present in its habitat. For example, Streptomyces sp. strain ACH 505 is generally toxic against Heterobasidion sp. fungi strains. However, one strain, Heterobasidion abietinum 331, was observed by Lehr et al. (2007) to be resistant to the effects of Streptomyces sp. ACH 505. This strain of fungi is thus the one which was able to have a symbiotic interaction with the Norway spruce (Picea abies) plant. The factor that was identified as the contributor to this selection is the antifungal toxins released by the bacteria. H. abietinum 331 is thus resistant to this toxins. In addition, Streptomyces sp. ACH 505 may be releasing toxins that specifically acts onto the root, breaking down the defense mechanisms set up by plants, specifically the peroxidase activity and PaSpi2 gene expression, which results to the production of peroxidase enzyme. This results to an increased H. abietinum 331 colonization. 2. Symbiotic relationships The relationship of mycorrhizae with other microorganisms has also been shown to be symbiotic. The survival of the bacterium Pseudomonas fluorescens strain BBc6R8 has been established to be dependent on mycorrhizal Douglas fir roots. The arbuscular mycorrhizal fungus Glomus mosseae, which interacts with L. esculentum (tomato) improves the survival of P fluorescens 92rk. The trehalose, the carbon storage form in fungi, is said to be its link to bacteria associated with mycorrhizae. Thus, bacteria that can only digest trehalose are probably the ones that can interact with mycorrhizae (Frey-Klett et al., 2007). 3. Antagonistic relationships If there are microorganisms that improves mycorrhizal growth, there are also some which do not. For example, volatiles from Trichoderma pseudokoningii (Saprophytic fungi) inhibit Gigaspora rosea spore germination and subsequent mycorrhizal development in Glycine max (soybean) (Tarkka and Piechulla, 2007). 4. Plant response The plants respond to these interactions by physiological changes. In response to the increased root carbohydrate drain caused by the presence of mycorrhizal fungi, plants either increase their photosynthetic efficiency or prevent fungal parasitism by restricting carbohydrate flux to the interacting hyphae (Nehls, 2008). Ecological importance Ectomycorrhizae has an important role as it improves the growth of big, dominant trees, such as Dipterocarps, growing in temperate regions, where climate conditions are growth-limiting. In this environment, sunlight penetrating the surface is low. Growth of seedlings are thus dependent on the aid of mycorrhizal fungi to provide them enough resources for growth. It is one of the factors that lead to survival of forest ecosystem. The vitality of the presence of mycorrhiza was elucidated in 1973 when Pines and Oaks were planted in the tropics and grasslands, where the fungi species associated with them are absent. This resulted in seedling death or poor growth (Agarwal and Sah, 2009). In other members of the ecosystem, mycorrhizal interactions are important because the fungal hyphae, through its weathering effectss on soil, mobilizes the nutrients from their respective organic polymers. These released nutrients are then used up by other non-mycorrhizal plants and microorganisms present within the ecosystem. In addition, the presence of various mycorrhizal fungi was observed to contribute to the diversity of environmental organisms (Finlay, 2008). FUTURE ADVANCES Nowadays that the population is progressively increasing, efforts on increasing food producing efficiency has been steadily increasing as well. As already discussed, mycorrhizae can increase food productivity of plants, which is a natural source of food for animals and humans. Because of its protective roles against pathogens, drought and salt stress, it may be tapped as an alternative to fertilizers and pesticides, which cause adverse effects toward other members of its ecosystem or to the consumers of the plant products. As can be deduced from the discussion above, not a lot of plants are involved in the study. However, as mentioned earlier, different plants respond to the presence of mycorrhizal fungi in different manner. Researches surveying the mycorrhizal interactions in other plants not previously studied should be performed. The data can be collated through an online database available for all countries. References Agarwal, Pragya and Sah, Pankaj, 2009. Ecological importance of ectomycorrhizae in world forest ecosystems. Nature and Science, 7(2), pp. 107-116. Al-Karaki, Ghazi N., 2000. Growth of micorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza, 10, pp. 51-54. Auge, Robert M., 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, pp. 3-42. Bucher, Marcel, 2007. Tansley review: Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist, 173, pp. 11-26. Finlay, Roger D., 2008, Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. Journal of Experimental Botany, 59(5), pp. 1115-1126. Frey-Klett, P. , Garbaye, J., and Tarkka, M., 2007. Tansley review: The mycorrhiza helper bacteria revisited. New Phytologist, 176, pp. 22-36. Gherbi, Hassen, Markmann, Katharina, Svistoonoff, Sergio, Estevan, Joan, Autran, Daphne, Giczey, Gabor, Auguy, Florence, Peret, Benjamin, Laplaze, Laurent, Franche, Claudine, Parniske, Martin, and Bogusz, Didier, 2008. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. PNAS, 105(12), pp. 4928-4932. Gutjahr, Caroline, Banba, Mari, Croset, Vincent An, Kyungsook, Miyao, Akio, An, Gynheung, Hirochika, Hirohiko, Imaizumi-Anraku, Haruko, and Paszkowski, Uta, 2008. Arbuscular Mycorrhiza–Specific Signaling in Rice Transcends the Common Symbiosis Signaling Pathway. The Plant Cell, 20, pp. 2989-3005. Lehr, Nina A., Schrey, Silvia D., Bauer, Robert, Hampp, Rudiger, and Tarkka, Mika T., 2007. Suppression of plant defence response by a mycorrhiza helper bacterium. New Phytologist, 174, pp. 892-903. Manthey, Katja, Krajinski, Franziska, Honhnjec, Natalija, Firnhaber, Christian, Puhler, Alfred, Perlick, Andreas M., and Kuster, Helge, 2004. Transcriptome Profiling in Root Nodules and Arbuscular Mycorrhiza Identifies a Collection of Novel Genes Induced During Medicago truncatula Root Endosymbioses. MPMI. 17(10), pp. 1063-1077. Nagy, Reka, Karandashov, Vladimir, Chague, Veronique, Kalinkevich, Katsiaryna, Tamasloukht, M’Barek, Xu, Guohua, Jakobsen, Iver, Levy, Avraham A., Amrhein, Nikolaus, and Bucher, Marcel, 2005. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. The Plant Journal. 42, pp. 236-250. Nehls, Uwe, 2008. Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. Journal of Experimental Botany. 59(5), pp. 1097-1108. Redecker, Dirk and Raab, Philipp, 2006. Phyloheny of the Glomeromycota (arbuscular mycorrhizal fungi: recent developments and new gene markers. Mycologia. 98(6), pp. 885-895. Schaarschmidt, Sara, Roitsch, Thomas and Hause, Bettina, 2006. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. Journal of Experimental Botany, 57(15), pp. 4015-4023. Tarkka, Mikka T. and Piechulla, Birgit, 2007. Aromatic weapons: truffles attack plants by the production of volatiles. New Phytologist, 175, pp. 381-383. Read More