JXB Advance Access originally published online on February 13, 2008
Journal of Experimental Botany 2008 59(5):1097-1108; doi:10.1093/jxb/erm334
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REVIEW-ARTICLE |
Mastering ectomycorrhizal symbiosis: the impact of carbohydrates
Universität Tübingen, Botanisches Institut, Physiologische Ökologie der Pflanzen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany
* E-mail: uwe.nehls{at}uni-tuebingen.de
Received 7 August 2007; Revised 20 November 2007 Accepted 30 November 2007
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Abstract
IntroductionMycorrhiza formation is the consequence of a mutualistic interaction between certain soil fungi and plant roots that helps to overcome nutritional limitations faced by the respective partners. In symbiosis, fungi contribute to tree nutrition by means of mineral weathering and mobilization of nutrients from organic matter, and obtain plant-derived carbohydrates as a response. Support with easily degradable carbohydrates seems to be the driving force for fungi to undergo this type of interaction. As a consequence, the fungal hexose uptake capacity is strongly increased in Hartig net hyphae of the model fungi Amanita muscaria and Laccaria bicolor. Next to fast carbohydrate uptake and metabolism, storage carbohydrates are of special interest. In functional A. muscaria ectomycorrhizas, expression and activity of proteins involved in trehalose biosynthesis is mainly localized in hyphae of the Hartig net, indicating an important function of trehalose in generation of a strong carbon sink by fungal hyphae. In symbiosis, fungal partners receive up to
19 times more carbohydrates from their hosts than normal leakage of the root system would cause, resulting in a strong carbohydrate demand of infected roots and, as a consequence, a more efficient plant photosynthesis. To avoid fungal parasitism, the plant seems to have developed mechanisms to control carbohydrate drain towards the fungal partner and link it to the fungus-derived mineral nutrition. In this contribution, current knowledge on fungal strategies to obtain carbohydrates from its host and plant strategies to enable, but also to control and restrict (under certain conditions), carbon transfer are summarized. Key words: Carbohydrate metabolism, ectomycorrhiza, fungi, soil, symbiosis, transport
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Introduction |
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In contrast to arbuscular mycorrhizal fungi, which are obligate biotrophs, ectomycorrhizal (EM) fungi as well as their host plants are not dependent on one another under optimized nutritional conditions.
However, in natural forest ecosystems, major nutrients (nitrogen, phosphate) are fixed in the organic layer or are contained in micro-organisms, and lower animals and trees have only a limited access to this resource (Harley and Smith, 1983; Smith and Read, 1997), making them ecologically dependent on EM fungal partners.
Although litter and humus layers of forest soils are quite rich in complex carbohydrates (e.g. cellulose and lignin), most EM fungi (and a large proportion of other soil microbes) seem to be dependent on simple, readily utilizable carbohydrates which are contained in organisms but are rare in forest soils (Wainwright, 1993). The reason for this is that EM fungi only have a limited capability to degrade complex carbohydrates as a carbon source compared with wood and litter decomposers (Colpaert and van Tichelen, 1996; Read and Perez-Moreno, 2003). In contrast to the soil, plant root exudates can be rich in simple carbohydrates. As EM fungal hyphae cover tree fine roots (see below), they have a direct and privileged access to root exudates. This and the fact that ectomycorrhizal roots gain much more carbon than non-mycorrhizal plant roots help EM fungi to overcome carbohydrate limitation and increase their competitive ability in soil (Smith and Read, 1997; Leake et al., 2001).
While both the fungus and the plant can profit from the interaction, the question of who controls the relationship has been discussed extensively. In the past, this debate was based on ecological observations and experimental modulation of environmental conditions. However, with the power of molecular biological techniques, this debate has recently been revived (Fitter, 2006). Different aspects of symbiosis are often mixed in this discussion, including: the degree of dependency of each partner on a successful symbiosis (reflecting amongst others the current nutritional state of plant and fungus, see above), the developmental control of the partners over the establishment of interacting structures (which is still a black box), and the exchange of nutrients and metabolites at the plant–fungus interface. The focus of this contribution will be on the last point and target the impact of carbohydrates, whose acquisition is presumably the main reason for the fungal partner to enter symbiosis.
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The ectomycorrhizal fungal colony |
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EM fungal mycelia can comprise up to 80% of the total fungal biomass and 30% of the microbial biomass in forest soils (Wallander et al., 2001; Högberg and Högberg, 2002; Wallander, 2006) and are regarded as key elements of forest ecosystem processes (e.g. nutrient cycling and carbon entry; for recent reviews see Read et al., 2004; Anderson and Cairney, 2007). Ectomycorrhizal mycelial biomass varies with soil depth and host tree species, but seems to correlate with the distribution of tree roots in the respective soil profile (Wallander et al., 2004; Göransson et al., 2006).
Soil-growing hyphae that explore litter or mineral layers for nutrients constitute a large part of the EM fungal colony (Fig. 1). In contrast to fast growing, saprophytic model fungi such as Aspergillus or Neurospora, different parts of the EM fungal colony remain functionally interconnected (Cairney et al., 1991). In forests, certain EM fungi are spread over areas that are often several square metres, implying that mycelia in the field can extend for considerable distances and persist for several years (Dahlberg and Stenlid, 1990; Baar et al., 1994; Dahlberg, 1997; Anderson et al., 1998). Size of and interconnectivity within the colony seem to depend on the fungal capability to establish specialized long-distance transport hyphae (cords or rhizomorphs, Fig. 1; reviewed by Agerer, 2001). Species that remain non-rhizomorphic are thought to have a limited ability to explore the surrounding soil, while those that possess highly differentiated rhizomorphs are regarded as more adapted to long-distance exploration.
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When soil-growing hyphae recognize an emerging fine root of a plant partner, they direct their growth towards it (Martin et al., 2001) and colonize the root surface, (often) forming a sheath or mantle of hyphae, which encloses the root and isolates it from the surrounding soil (Fig. 1; Blasius et al., 1986). Root hairs, which are normally formed by rhizodermal cells, are suppressed by ectomycorrhiza formation. After or parallel to sheath formation, fungal hyphae grow inside the infected fine root, forming highly branched structures in the apoplast of the rhizodermis or, in the case of gymnosperms in the entire root cortex, the so-called Hartig net (Fig. 1; Kottke and Oberwinkler, 1986).
Both fungal networks of ectomycorrhizas (fungal sheath and Hartig net) have different functions (Harley and Smith, 1983; Kottke and Oberwinkler, 1986; Smith and Read, 1997). The Hartig net serves as an interface between plant and fungus where cells are adapted to the exchange of plant-derived carbohydrates for fungus-derived nutrients. The function of the fungal sheath is that of an intermediate storage for (i) nutrients that are delivered by soil-growing hyphae and are intended for the Hartig net and (ii) carbohydrates that are taken up by hyphae of the Hartig net and are designated for transport towards the soil-growing mycelium (Jordy et al., 1998).
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Fungal carbohydrate nutrition in symbiosis |
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One of the first attempts to assay carbon flow in a mycorrhizal plant was performed by Melin and Nilsson (1957). They showed that feeding [14C]CO2 to leaves resulted in the appearance of labelled carbon in the hyphal mantle within 1 d. These results were confirmed by a number of researchers with different experimental systems later on (Lewis and Harley, 1965b; Cairney et al., 1989; Leake et al., 2001; Wu et al., 2002). Carbon allocation to EM fungi was estimated by different investigators to be as much as 20–25% of net primary production (Söderström, 1992; Högberg and Högberg, 2002; Hobbie, 2006).
Potential carbon compounds delivered by the plant partner in symbiosis are soluble sugars, carboxylic acids, and amino acids. Plant cell wall compounds such as pectin, hemicellulose, cellulose, or proteins have also been under discussion (for reviews see Harley and Smith, 1983; Smith and Read, 1997). However, owing to the huge rates of carbon consumption by the fungal partner, cell wall compounds are not likely to constitute a major carbon source. Additionally, even though there are indications that certain EM fungi have some cell wall-degrading activity, the degradation rate is too slow to meet the fungal carbohydrate demand (Trojanowski et al., 1984; Haselwandter et al., 1990; Entry et al., 1991). When grown under axenic conditions, which, however, do not necessarily reflect the situation in ectomycorrhizas, the majority of EM fungi investigated so far grow best on simple sugars such as glucose and fructose (Palmer and Hacskaylo, 1970; Salzer and Hager, 1991). Therefore, it seems likely that soluble sugars and organic acids are the best candidates for plant-derived carbohydrates for fungal nutrition in symbiosis.
It is commonly accepted that sucrose, which is excreted by plant root cells into the common apoplast of the plant–fungus interface, is hydrolysed by a plant-derived invertase in EM symbiosis (Lewis and Harley, 1965a; Salzer and Hager, 1991; Rieger et al., 1992; Schaeffer et al., 1995; Nehls, 2004). The lack of an invertase in (at least many) EM fungi (Palmer and Hacskaylo, 1970; Salzer and Hager, 1991; Hatakeyama and Ohmasa, 2004; Daza et al., 2006) is a profound difference from phytopathogenic (Walters et al., 1996; Voegele et al., 2001) and also ericoid mycorrhizal fungi (Straker et al., 1992; Hughes and Mitchell, 1996). In combination with their low cell wall-degrading activity (compared with wood- and litter-degrading but also ericoid mycorrhizal fungi), lack of invertase activity makes EM fungi dependent on the activity of the plant partner (Smith and Read, 1997), which might be essential for the function of this type of symbiosis.
Compared with regular root exudation, which constitutes 3–5% of carbon fixed in photosynthesis (Pinton et al., 2001), up to 20–25% of net photosynthesis products are transferred towards the fungus in ectomycorrhizal symbiosis (Söderström and Read, 1987; Söderström, 1992; Farrar and Jones, 2000; Högberg and Högberg, 2002; Hobbie, 2006). Thus, plant fine roots lose 6–19 times more carbohydrates in symbiosis (Bevege et al., 1975; Cairney et al., 1989; Wu et al., 2002). Prerequisites for the formation of a strong fungal sink are the ability of Hartig net hyphae to take up carbohydrates speedily from the common apoplast and convert them into fungal metabolites.
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Sugar uptake |
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Two hexose transporter genes from Amanita muscaria (AmMST1, Nehls et al., 1998; AmMST2, Nehls, 2004) and one hexose transporter gene from Tuber borchii (Tbhxt1; Polidori et al., 2007) have been investigated from EM fungi so far. The hexose transporter proteins of both T. borchii and A. muscaria clearly favour glucose uptake over that of fructose. However, while the T. borchii protein revealed a KM value of
38 µM when heterologously expressed in yeast (Polidori et al., 2007), the A. muscaria protein showed a 10 times higher KM value (460 µM; Wiese et al., 2000). Tbhxt1 expression was furthermore enhanced by carbohydrate starvation of Tuber hyphae, while AmMST1/2 (A. muscaria) expression was enhanced by increased external sugar concentrations and in ectomycorrhizas (Fig. 2; Nehls et al., 1998; Nehls, 2004). It was thus concluded that Tbhxt1 is mainly responsible for carbohydrate uptake by soil-growing hyphae and the reduction of sugar leakage from hyphae (Polidori et al., 2007), while the A. muscaria proteins are responsible for carbohydrate uptake in symbiosis (Nehls, 2004).
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The sequenced genomes of ascomycetes contain
20 functional sugar transporter genes (Saccharomyces cerevisiae, Boles and Hollenberg, 1997; Aspergillus niger, Pel et al., 2007) and those of basidiomycetes (Laccaria bicolor, ectomycorrhizal: Martin et al., 2004; Coprinopsis cinerea, saprotroph, http://www.broad.mit.edu/annotation/genome/coprinus_cinereus/Home.html; Phanerochaete chrysosporium, wood decaying: Martinez et al., 2004) 15 putative MST genes (UNehls, unpublished data). The expression of a subset (six out of 15) of the identified Laccaria bicolor genes (belonging to different transporter subgroups) is mycorrhiza enhanced, while one gene (revealing a generally very low transcript level) is suppressed in symbiosis (UNehls, unpublished data). Three of the genes that revealed elevated transcript levels in ectomycorrhizas were specifically induced in symbiosis, while a further three genes also showed an enhanced expression in fruit bodies. Together with the two functionally characterized A. muscaria hexose transporter genes, which also showed strongly enhanced expression upon ectomycorrhiza formation (Nehls et al., 1998; Nehls, 2004), the data from L. bicolor clearly suggest an enhanced fungal sugar uptake capacity in symbiosis. In conclusion, even when the number of, as yet characterized, hexose transporters from EM fungi is rather small compared with the large number of potential sugar transporter genes in their genomes, two important functions are already visible: (i) sugar uptake by soil-growing hyphae and avoidance of monosaccharide leakage under carbohydrate starvation; and (ii) enhanced sugar uptake in symbiosis.
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Fungal sugar metabolism |
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According to investigations by nuclear magnetic resonance (NMR; Martin et al., 1998) and biochemical techniques (Hampp et al., 1995), hexoses that are imported by fungal hyphae are utilized for ATP generation, amino acid biosynthesis, and the formation of (potential) carbohydrate storage compounds. For the maintenance of a strong carbon sink in symbiosis, monosaccharides have to be quickly converted into fungal metabolites, by (i) increased carbon flux through glycolysis and/or (ii) the generation of fungal storage compounds.
Increased flux rates through fungal glycolysis and the tricarboxylic acid cycle (TCA) are indicated by large-scale expression analysis of established Pisolithus microcarpus/Eucalyptus globulus ectomycorrhizas (Duplessis et al., 2005) and supported by investigations of enzyme activities and metabolic regulator content. The enzyme phosphofructokinase performs the rate-limiting step in EM fungal glycolysis (Kowallik et al., 1998). In A. muscaria, this enzyme is activated by fructose 2,6-bisphosphate (F26BP), and symbiotic A. muscaria hyphae have increased amounts of F26BP (Schaeffer et al., 1996), resulting in an increased glycolytic flux in hyphae at the plant–fungus interface. In contrast to data from Pisolithus and A. muscaria, ectomycorrhizas formed by Paxillus involutus showed slightly reduced expression of genes involved in sugar uptake and glycolysis (Le Quere et al., 2005; Wright et al., 2005). This could either indicate species-specific differences of EM fungi upon ectomycorrhiza formation or insufficient experimental data. Analysis of gene expression up to now has covered only a limited number of fungal genes. Furthermore, protein activity is not necessarily reflected by gene expression. Thus, expression data of whole pathways together with analysis of protein function and metabolite content of further EM fungi are necessary to draw sound conclusions.
Two different pools of potential storage carbohydrates can be distinguished in fungi: (i) short chain carbohydrates such as trehalose and polyols; and (ii) the long chain carbohydrate glycogen.
When grown in the presence of a rich carbon source but also in functional ectomycorrhizas, EM fungi produce a series of sugars and sugar alcohols (mannitol, arabitol, erythritol) among which trehalose and mannitol dominate (Table 1). Amanita muscaria growth in axenic culture on glucose as a carbon source results in an increase in trehalose content over time, which is later continuously depleted again under glucose starvation (Wallenda, 1996). Furthermore, trehalose dominates in the most intense plant–fungus interaction zone of functional mycorrhizas, indicating a conversion of glucose into this compound (Rieger et al., 1992). In accordance with this, trehalose biosynthesis occurs mainly in hyphae of the plant–fungus interface and is strongly increased upon ectomycorrhiza formation (Fig. 3; Fajardo López et al., 2007). Together, these data indicate that in A. muscaria trehalose might function as a storage carbohydrate. In contrast to trehalose, mannitol is rarely found in A. muscaria. Only fruiting bodies contain larger mannitol concentrations (Wallenda, 1996). With the exception of Hygrophorus pustulatus, trehalose is clearly dominant in substrate mycelia, ectomycorrhizas, and fruit bodies of investigated ectomycorrhizal basidiomycetes belonging to the order Agaricales (Table 1). However, in the non-mycorrhizal fungus Agaricus bisporus (belonging to same order), mannitol is found in higher concentrations than trehalose in hyphae grown on straw and fruiting bodies. The situation is even more puzzling in the order Boletales, where in relatively closely related EM fungi sometimes mannitol and sometimes trehalose dominates. Members of other orders of ectomycorrhizal basidiomycetes are only rarely investigated and here trehalose or mannitol could dominate. For ascomycotic EM fungi the situation seems to be clearer. Mannitol (sometimes also arabitol) is clearly dominant in substrate mycelia and mycorrhizas, while trehalose is rarely found (Table 1). However, in hyphae of the non-mycorrhizal ascomycete Cordyceps bassiana, trehalose dominates. Together with the small number of species of ascomycotic EM fungi investigated, this might indicate a similar situation to that in basidiomycetes.
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With the exception of a few models, the functional interpretation of published data is generally difficult for most of the investigated EM fungi due to missing knowledge about fungal physiology. It is further complicated by the fact that trehalose (for a review see Crowe, 2007) and polyols (for a review see Solomon et al., 2007) could act as osmo-, cryo-, heat, and drought protectants and as scavengers for radical oxygen species in certain fungi, in addition to their postulated function in carbohydrate storage and distribution (see below). Thus, in future more detailed investigations on fungal physiology together with manipulation of carbon metabolism in model fungi are necessary.
In Lactarius, glycogen content is high during winter, declines due to strong fungal propagation until summer, and is restored during autumn (Genet et al., 2000). In contrast, short-term (up to 3 weeks) exposure of A. muscaria hyphae in the presence or absence of a carbon source had nearly no effect on glycogen content (Wallenda, 1996). Nevertheless, Jordy et al. (1998) observed changes in glycogen content and localization during ectomycorrhiza formation. While glycogen was initially found in Hartig net hyphae, it was later (in agreement with a potential function in long-term storage) observed exclusively in hyphae of the fungal sheath. The initial occurrence of glycogen in Hartig net hyphae could, however (like temporal starch formation in leaves), be interpreted as a flux control mechanism. When carbohydrate import into hyphae exceeds its export to other parts of the fungal colony, long-term storage pools are filled to ensure continuous fungal carbohydrate sink strength in symbiosis. Together these data thus indicate a potential function of glycogen (like starch in plants) in long-term carbohydrate storage, which is usually only mobilized when the short-term pools (e.g. trehalose and polyols) are empty.
Because EM fungi commonly form an extensive external mycelium, and soil-growing hyphae are dependent on carbohydrate support by mycorrhizas (Cairney and Burke, 1996; Leake et al., 2001), long-distance transport of carbon is of great importance for fungal physiology. Since glycogen is stored in the cytoplasm as large, non-mobile granules, it is rather unlikely that it (similar to starch in plants) serves as the long-distance carbohydrate transport form in fungi. In contrast, polyols and trehalose are present in large quantities in fungal hyphae and are (like sucrose in plants) quite mobile, making them good candidates for long-distance transport carbohydrates. However, further investigations, including the generation of mutants in certain pathways, are necessary to support this hypothesis.
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Carbohydrates as a signal for the regulation of fungal physiology in ectomycorrhizas |
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Sugar-dependent regulation of gene expression was investigated in functional A. muscaria ectomycorrhizas using hexose importer genes (Nehls et al., 1998; Nehls, 2004) and a phenylalanine ammonium lyase (AmPAL; Nehls et al., 1999). In axenic culture, the expression of these genes is regulated by a threshold response mechanism dependent on the extracellular monosaccharide concentration (Nehls et al., 2001a). In functional ectomycorrhizas, AmPAL was only detectable in hyphae of the fungal sheath, while elevated hexose transporter gene expression was exclusively observed in hyphae of the Hartig net (Nehls et al., 2001a). Owing to the opposing (sugar-dependent) regulation of these genes in both hyphal networks, hexose (glucose or fructose) concentrations >2 mM can be expected in the apoplast of the root region containing the Hartig net, while lower concentrations are probably present in the apoplast of hyphae of the fungal sheath (Nehls et al., 2001b). Basidiomycotic EM fungi (Salzer and Hager, 1993; Stülten et al., 1995; Nehls et al., 2001b) and also most investigated plant monosaccharide transporters (Büttner and Sauer, 2000) strongly favour glucose over fructose import. Since sucrose is hydrolysed at the plant–fungus interface into equimolar amounts of glucose and fructose, preferential glucose uptake would result in increased apoplastic fructose concentrations, which could trigger fungal physiology in symbiosis (Fig. 4; Nehls, 2004; see below).
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‘Metabolic zonation’ and ‘physiological heterogeneity’ have been discussed as important concepts for a functional understanding of EM symbiosis (Cairney and Burke, 1996; Timonen and Sen, 1998). Differences in the apoplastic hexose concentration at the Hartig net versus the fungal sheath could be a signal that regulates fungal physiological heterogeneity in ectomycorrhizas (Nehls et al., 2001b; Nehls, 2004). To investigate the general effect of the external sugar concentration on A. muscaria gene expression, microarray hybridization (800 tentative genes) was performed with probes from mycelial samples grown under axenic conditions with either 1 mM or 25 mM glucose as carbon source. For
5% of the investigated genes an at least 2-fold difference in gene expression was observed (Nehls et al., 2007; UNehls, unpublished data). This indicates that (for A. muscaria) sugar-dependent regulation of fungal gene expression caused by differences in the apoplastic hexose concentration at the plant–fungus interface versus the fungal sheath may explain some of the local adaptations of fungal physiology in functional ectomycorrhizas. In yeast and filamentous ascomycetes the external sugar concentration is sensed by monosaccharide transporter-like proteins that regulate sugar-dependent gene induction. In addition to external sugar sensors, monosaccharide-dependent gene repression is regulated via a hexokinase-dependent signalling pathway (Özcan and Johnston, 1995). As in ascomycetes, hexokinase obviously acts as a regulator of sugar-dependent gene repression in the EM fungus A. muscaria (Nehls et al., 1999). However, in contrast to ascomycetes, the sugar-dependent induction of A. muscaria sugar transporter genes seems to be regulated by an internal sensor located either further downstream from hexokinase in glycolysis or in storage carbohydrate biosynthesis (Nehls et al., 1998, 2001a; Nehls, 2004).
In contrast to the situation in A. muscaria, mycorrhiza-induced sugar transporter gene expression was not regulated in a sugar-dependent manner in L. bicolor (UNehls, unpublished data). However, also in A. muscaria, genes involved in sugar metabolism (e.g. trehalose biosynthesis) are regulated in a sugar-independent manner (Fajardo López et al., 2007). Thus, the extent of fine-tuning of EM fungal physiology by sugar regulation might be species dependent and has to be further addressed in the future.
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The host plant |
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McDowell et al. (2001) report that 47–59% of plant photosynthates are allocated to ectomycorrhizas, and several authors estimate that 20–25% of the net photosynthesis rate is used for fungal support (Söderström and Read, 1987; Söderström, 1992; Farrar and Jones, 2000; Högberg and Högberg, 2002; Hobbie, 2006). Together these data indicate, that (i) both the fungus and infected roots consume similar amounts of fine root-allocated carbohydrates and (ii) carbohydrate uptake by both partners must be strongly increased in symbiosis. In agreement with this, sugar transporter gene expression is significantly enhanced in fungal hyphae (see above) and root cells (see below, Fig. 2). In response to the huge carbohydrate drain in symbiosis, the plant can (i) increase its photosynthetic efficiency and (ii) control carbohydrate loss toward the fungus to avoid fungal parasitism.
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Increased host photosynthesis in EM symbiosis |
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A constant sugar supply towards the fungus by the host plant is essential for mycorrhizal functioning and seems to be tightly coupled to photosynthetic activity (Högberg et al., 2002; van Hees et al., 2005). Direct and indirect observations indicate that mycorrhization can up-regulate the net photosynthesis rate of the host plant to meet the increased carbohydrate demand in symbiosis. Vodnik and Gogala (1994) found increased chlorophyll and carotenoid contents in needles of spruce seedlings mycorrhized with different EM fungi. Mycorrhized Castanea sativa plants have decreased respiration rates, resulting in a lower CO2 compensation point and an increased amount of ribulose bisphosphate carboxylase (Martins et al., 1997). Gas exchange measurements revealed an increased CO2 fixation rate for mycorrhized Norway spruce, poplar, and birch (Friedrich, 1998; Loewe et al., 2000; Wright et al., 2000). Furthermore, Lamhamedi et al. (1994) demonstrated that the removal of L. bicolor fruiting bodies, which form a huge extra carbon sink generated by EM fungi, resulted in a rapid decrease in net photosynthesis of host plants.
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Control of local carbohydrate loss by plant roots |
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The first hints of a control of carbon drain towards the fungal partner in symbiosis came from fertilization experiments, showing that increased soil nitrogen availability is often associated with decreased production of extraradical hyphae, reduced colonization intensity of fine roots, and decreased fruiting body formation by EM fungi (Wallenda and Kottke, 1998; Nilsson and Wallander, 2003; Nilsson et al., 2005; Hendricks et al., 2006). Decreased fungal growth rates under elevated soil nitrogen content indicate a reduction in the carbohydrate flux towards the fungus, caused by a diminished dependency of the host plant on the fungal partner.
The prevention of a carbohydrate drain from the plant towards the fungus can occur at several levels, including (i) the control of sucrose export into the common apoplast (that is still largely unknown); (ii) the control of sucrose hydrolysis, and (iii) competition between root cells and fungal hyphae for hexoses present in the apoplast of the root region containing the Hartig net.
Root exudation of non-charged molecules (sucrose, hexoses) occurs mainly passively, aided by the concentration gradient between plant cells and the apoplast. This makes it difficult for plants to exert direct control over many components of their C efflux (Jones and Darrah, 1996), but sugar re-import by root cells can be directly up-regulated to help alleviate stress (Jones et al., 2004). Thus, root sink strength, rates of local sucrose hydrolysis, and hexose re-uptake by root cells are thought to regulate fungal carbohydrate nutrition in ectomycorrhizas.
Apoplastic sucrose hydrolysis by plant-derived cell wall acid invertases is a prerequisite for fungal carbohydrate support in ectomycorrhizal (Salzer and Hager, 1991; Salzer and Hager, 1993; Schaeffer et al., 1995) and arbuscular (Wright et al., 1998; Schaarschmidt et al., 2006) mycorrhiza symbiosis. While acid invertase activity seems not to be a rate-limiting step in Medicago truncatula (arbuscular mycorrhiza symbiosis; Schaarschmidt et al., 2007) and Norway spruce (ectomycorrhiza; Schaeffer et al., 1995), enzyme activity is increased upon ectomycorrhizal symbiosis in Betula (Wright et al., 2000) and poplar (UNehls, unpublished data). This indicates that invertase activity might be a checkpoint for fungal carbohydrate support in some plants.
In A. muscaria/P. tremulaxtremuloides ectomycorrhizas, expression of monosaccharide importer genes of both fungal and plant origin is strongly enhanced compared with non-mycorrhizal fine roots (Fig. 2). Three out of a total of 24 potential monosaccharide transporter genes present in the poplar genome (Tuskan et al., 2006) are up-regulated by ectomycorrhiza formation (Grunze et al., 2004; Nehls et al., 2007; UNehls, unpublished data), and one of them (PttMST3.1) is at least 10 times more highly expressed in roots than any other hexose transporter gene. As a consequence, intense competition for apoplastic hexoses can be supposed to occur at the plant–fungus interface. This raises the question of how the observed net transfer of large amounts of carbohydrates towards the fungus can occur under these conditions. A hint of how the increased plant hexose transporter gene expression and an efficient fungal sugar support could fit together came from attempts to express the poplar sugar transporter PttMST3.1 in yeast or Xenopus laevis oocytes. As heterologous expression of the entire cDNA failed in both experimental systems, Grunze et al. (2004) speculated that this transporter may also be regulated at the post-translational level (e.g. by phosphorylation). Indeed, potential phosphorylation sites are present in the deduced PttMST3.1 protein sequence (Grunze, 2004). This feedback control mechanism would allow a fine-tuning of the activation status of selected transporters in root cells as a reaction to the amount of nutrients delivered by the fungus. If the fungus provides sufficient nutrients, the activity of PttMST3.1 would be shut off, while the protein would be activated as soon as the nutrient transfer is insufficient (Fig. 5). To test this hypothesis, transgenic poplar plants were generated that overexpress an additional hexose importer gene under conditions that cannot be controlled by the plant (UNehls, unpublished data). In agreement with the assumption by Grunze et al. (2004), these transgenic plants reveal a reduced mycorrhizal infection capability and an abnormal termination of the symbiosis (UNehls, unpublished data).
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Summary and outlook |
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Together with their fungal partners, root systems of EM forest trees receive about half of the photosynthetically fixed carbon. This carbohydrate demand is the consequence of a plant nutritional strategy that is in large part dependent on microbial partners. On the other hand, plant-derived carbohydrate input into EM fungi is driving a microbial-based recycling machinery which is essential for the establishment of forest ecosystems and sustainable tree growth.
To enable a strong carbohydrate sink at the plant–fungus interface, most investigated model fungi increase monosaccharide uptake capacity and carbohydrate flux through glycolysis and the TCA cycle (energy production for transport and metabolic processes). Furthermore, increased contents of trehalose and/or mannitol in functional ectomycorrhizas indicate that these compounds are potential intermediate carbohydrate stores, which are perhaps also involved in long-distance transport of carbon within the fungal colony. The relevance of trehalose and polyols for fungi is, however, controversially discussed. Only in some ascomycotic fungi (basidiomycotic fungi are only rarely investigated) could a function for these compounds as carbohydrate storage be confirmed by genetic approaches. The situation is further complicated by the fact that trehalose and mannitol could act as stress protectants in some fungi. Thus, genetic approaches to verify the particular function of these compounds in EM fungi are necessary.
Regulation and fine-tuning of fungal physiology in EM fungal networks seems to be controlled by developmental mechanisms and sugars. To what extent sugars play a role in gene regulation seems to be dependent on the fungal species. However, further EM fungi have to be investigated to draw a more general picture.
Host trees increase their photosynthetic capacity in symbiosis, but indications were found that they also control and restrict carbohydrate flux towards their partners to avoid fungal parasitism. The mechanisms by which this occurs are still unclear, and further investigations are needed.
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Acknowledgements |
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The author is indebted to Dr Nina Grunze and Dr Sylvia Schrey for critical reading of the manuscript. This work was financed by the German Science Foundation (DFG).
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