Journal of Experimental Botany, Vol. 52, No. 90001, pp. 469-478,
March 2001
© 2001 Oxford University Press
The arbuscular mycorrhizal symbiosis: a molecular review of the fungal dimension
Biotechnology Department, Plant Science Division, Scottish Agricultural College, Kings Buildings, Mains Road, Edinburgh, Scotland, UK
Received 23 March 2000; Accepted 8 August 2000
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Abstract |
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 Top Abstract IntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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Mycorrhizal associations vary widely in structure and function, but the most common interaction is the arbuscular mycorrhizal (AM) symbiosis. This interaction is formed between the roots of over 80% of all terrestrial plant species and Zygomycete fungi from the Order Glomales. These fungi are termed AM fungi and are obligate symbionts which form endomycorrhizal symbioses. This symbiosis confers benefits directly to the host plant's growth and development through the acquisition of P and other mineral nutrients from the soil by the fungus. In addition, they may also enhance the plant's resistance to biotic and abiotic stresses. These beneficial effects of the AM symbiosis occur as a result of a complex molecular dialogue between the two symbiotic partners. Identifying the molecules involved in the dialogue is a prerequisite for a greater understanding of the symbiosis. Ongoing research attempts to understand the underlying dialogue and concomitant molecular changes occurring in the plant and the fungus during the establishment of a functioning AM symbiosis. This paper focuses on the molecular approaches being used to study AM fungal genes being expressed in the symbiotic and asymbiotic stages of its lifecycle. In addition, the importance of studying these fungi, in relation to understanding plant processes, is discussed briefly.
Key words: AM fungi, Zygomycetes, endomycorrhizal symbiosis, fungal genes.
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Introduction |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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Mycorrhizal associations vary widely in structure and function, but the most common interaction is the arbuscular mycorrhizal (AM) association which is formed between the roots of most higher plants and Zygomycete fungi belonging to the order Glomales. It is estimated that more than 80% of all terrestrial plants form this type of association. These include many agriculturally and horticulturally important crop species (Smith and Read, 1997
).
The AM symbiosis represents an ancient symbiosis (Pirozynski and Malloch, 1975; Pirozynski and Dalpe, 1989). Hyphae and arbuscules have been reported in fossils of Aglaophyton, isolated from the Rhynie chert and this evidence has established the existence of AM symbioses in the early Devonian (Remy et al., 1994; Taylor et al., 1995). Furthermore, molecular clock data based on the nucleotide sequence divergence of 18s rDNA suggests that the Glomales arose between 350–460 million years ago and the symbiosis was instrumental for the successful colonization of land by plants (Simon et al., 1993a). During evolution, the AM symbiosis has been lost in about 10% of plants, including whole angiosperm families (Tester et al., 1987).
AM fungi are all members of the class Zygomycota and the current classification (Fig. 1) contains one order, the Glomales, encompassing six genera into which approximately 150 species have been classified (Morton and Benny, 1990). Colonization of the root system by AM fungi confers benefits directly to the hosts plant growth and development, through the acquisition of phosphate and other mineral nutrients from the soil. In addition, colonization may also enhance the plant's resistance to biotic and abiotic stresses (Newsham et al., 1995; Subramanian et al., 1995; Vonreichenbach and Schonbeck, 1995; Ricken and Hofner, 1996). AM fungi also develop an extensive hyphal (extraradical hyphae) network out with the plant root system which makes a significant contribution to the improvement of soil texture and water relations (Bethlenfalvay and Schuepp, 1994). Therefore, these fungi constitute an integral and important component of ecosystems and may have significant applications in sustainable agricultural systems (Schreiner and Bethlenfalvay, 1995).
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The process of AM fungal colonization of host plant roots is characterized by distinct stages involving a series of complex morphogenetic changes in the fungus: spore germination, hyphal differentiation, appressorium formation, root penetration, intercellular growth, arbuscule formation, and nutrient transport. For in-depth discussions on aspects of the development of the arbuscular mycorrhizal symbiosis, readers are referred to a number of comprehensive reviews (Smith and Gianinazzi-Pearson, 1988
; Koide and Schreiner, 1992; Bonfante and Perotto, 1995; Harrison, 1997, 1998, 1999; Hirsch and Kapulnik, 1988; Albrecht et al., 1999).
The AM fungus is a symbiotic organism, however, it also harbours structures called bacterium-like organisms (blos), which have been detected ultrastructurally in spores and germinating and/or symbiotic mycelium (Bianciotto et al., 1996). These bacteria have been shown to be group II Pseudomonads (genus Burkholderia) by DNA sequence analysis of small subunit rRNA genes. However, the significance of these bacteria remains unknown, but indicates that mycorrhizal systems can include plant, fungal and bacterial cells (Bianciotto et al., 1996, 2000).
AM fungi are obligate biotrophs whose completion of their life cycle depends on their ability to colonize a host plant. Furthermore, fungal growth ceases after approximately 25–30 d of culture in the absence of the host plant. Their obligate status, the coenocytic nature of their spores (Becard and Pfeffer, 1993) and recombination (having never been demonstrated (Rosendahl and Taylor, 1997)), are biological aspects of these fungi which have hindered studies on them and on the symbioses they form with plant roots. The latter is particularly important as a mycorrhizal root is the normal state for most plants.
AM fungi have not been cultured in the absence of the host plant and this has hampered their mass production and utilization within crop systems (Jarstfer and Sylvia, 1992). However, it is possible to grow AM fungi in sterile culture with plant root explants (Mosse and Hepper, 1975; Miller-Wideman and Watrud, 1984; Diop et al., 1994) and/or with hairy roots transformed with Agrobacterium rhizogenes (Mugnier and Mosse, 1987; Becard and Fortin, 1988; Diop et al., 1992; Declerck et al., 1996, 1998; Pawlowska et al., 1999). Excised root culture systems have been used to study many aspects of the biology of AM fungi (Balaji et al., 1995; St Arnaud et al., 1995; Bago et al., 1996; Nagahashi et al., 1996; Villegas et al., 1996; Douds et al., 1998; Pfeffer et al., 1999). Furthermore, in vitro culture provides an abundant source of contaminant-free AM fungal hyphal and spore tissue that is a necessary prerequisite for molecular studies.
The understanding of how the AM symbiosis is established and functions is a key issue in plant development, therefore understanding the biology of the fungal partner is a cornerstone of this and of how plant roots function in nature. Since the advent of molecular biology, innovative techniques have been developed which help to overcome some of the problems encountered in the past. Molecular analyses of the fungus in the asymbiotic and symbiotic stages of development are underway.
Study of the AM fungal genome has been modest with the estimated DNA contents of nuclei from spores of different glomalean fungi indicating large genomes as compared to other Zygomycetes, ranging from 0.13 to more than 1.00 pg DNA per nucleus (Bianciotto and Bonfante, 1992; Hosny et al., 1998). Analysis of DNA base composition in nine glomalean species demonstrated a low GC content (at most 35%) with high levels of methylcytosine (Hosny et al., 1997) and, furthermore, the genomes contain extensively repeated DNA sequences (Zeze et al., 1996, 1999).
Molecular-based technologies have been particularly successful for studying ribosomal DNA sequences from AM fungi (Simon et al., 1992a, b; Clapp et al., 1995; Sanders et al., 1995; Abbas et al., 1996; Lloyd-Macgilp et al., 1996; Simon, 1996; Redecker et al., 1997, 1999, 2000a; Pringle et al., 2000). Ribosomal-based DNA sequence analysis has revealed genetic variation both within and between AM fungal species (Sanders et al., 1995; Lloyd-Macgilp et al., 1996; Vandenkoornhuyse and Leyval, 1998; Bago et al., 1998; Clapp et al., 1999; Hosny et al., 1999a; Lanfranco et al., 1999a), with in situ hybridization of spore interphasic nuclei with ribosomal DNA, demonstrating an internuclear variability in the number of rDNA loci in AM fungi (Trouvelot et al., 1999). Likewise, isolation and study of these sequences have led to the initial molecular phylogenetic characterization of the Glomales (Bruns et al., 1992; Redecker et al., 2000b; Tehler et al., 2000). Furthermore, these ribosomal DNA sequences have permitted the detection of AM fungi in mycorrhiza from various host plants and within soil ecosystems (Simon et al., 1993b; Clapp et al., 1995; Di Bonito et al., 1995; Claassen et al., 1996; van Tuinen et al., 1997; Helgason et al., 1998; Millner et al., 1998).
Alternative PCR strategies employed to study AM fungi include random amplified polymorphic DNA (RAPD) (Wyss and Bonfante, 1993; Lanfranco et al., 1995; Gadkar et al., 1997) and amplification of satellite regions (Longato and Bonfante, 1997; Zeze et al., 1997). The study of the functional non-ribosomal AM fungal genes falls within two categories—untargeted and targeted approaches for isolation.
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Targeted molecular approaches |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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Targeted approaches involve investigating molecules with known gene sequences and/or protein functions. Utilizing targeted approaches, the range of fungal genes isolated to date is modest, but range from nutritionally to morphologically important functional genes (Harrison and van Buuren, 1995
; Ferrol et al., 2000; Kaldorf et al., 1994, 1998; Lanfranco et al., 1999b, c).
One of the major benefits associated with a AM symbiosis is the enhanced P status of mycorrhizal plants. The enhancement is due to the uptake of P from the soil by the AM fungus and then its subsequent translocation and transfer to the host plant (Smith and Smith, 1989). The phosphate flux has been estimated at 13 nmol m-2 s-1 across the arbuscule in the mycorrhiza, although this rate can increase if exogenous phosphate is supplied (Cox and Tinker, 1976; Smith et al., 1994). A high affinity phosphate transporter has been cloned from Glomus versiforme, however, the gene transcripts corresponding to the transporter are only detected in the extraradical mycelium and not in the fungal structures within the root (Harrison and van Buuren, 1995). This suggests that this transporter must be responsible for the initial uptake from the soil matrix but the mechanisms for the transfer of P to the host plant have yet to be identified (Harrison and van Buuren, 1995).
The arbuscule is thought to be the major site for nutrient exchange between the two symbiotic partners. Therefore, mechanisms should be present to facilitate the transport of these compounds. Membrane H+-ATPases are considered the major transport proteins controlling ionic and molecular transport processes at the cellular level in plants and fungi. Studies have revealed changes in distribution and activation of particular H+-ATPases in the peripheral, peri-arbuscular and arbuscular membranes of functional AM interfaces (Marx et al., 1982; Gianinazzi-Pearson et al., 1991; Bago et al., 1997). Utilizing a PCR cloning approach based on the use of highly degenerate primers, five partial genomic clones encoding P-type ATPases (GmHA1-5), were isolated from the AM fungus, G. mosseae (Ferrol et al., 2000). These clones represent putative isoforms, whose function remains to be analysed, but expression analysis of GmHA1 and GmHA2 demonstrated that the former was expressed in the intraradical hyphae and the latter in the extraradical hyphae (Ferrol et al., 2000).
Another nutritionally-important AM fungal gene to be isolated was an assimilatory nitrate reductase (NR) gene. This NR was identified in DNA from spores of Glomus using a PCR based strategy (Kaldorf et al., 1994). Moreover in situ hybridization located the fungal NR in arbuscules but not in vesicles, suggesting differential fungal gene expression in the symbiotic state (Kaldorf et al., 1998).
During the asymbiotic and symbiotic development of AM fungi they undergo extensive morphogenesis. Chitin synthases (chs) play key roles in fungal morphogenetic processes catalysing the transfer of N-acetylglucosamine from UDP-N-acetylglucosamine into a chitin chain. Chitin is a constant component of AM fungi during these morphogenetic events and is accompanied by modifications in the chitin architecture during these processes (Bonfante, 1988). Therefore, an understanding of the basis of chitin synthesis in these symbionts may be a prerequisite for a better understanding of both the AM fungal morphogenetic events and its interaction with a host plant. Targeted approaches have been undertaken to amplify chs genes from AM fungi by utilizing degenerate primers designed on highly conserved chs domains (Lanfranco et al., 1999b, c). Two chs genes from class I and class IV have been isolated from Glomus versiforme (Lanfranco et al., 1999b), while one class II (Gimchs1) and two class IV (Gimchs2 and Gimchs3) chs genes have been isolated from Gigaspora margarita (Lanfranco et al., 1999c). Expression analysis of the latter chs genes in G. margarita demonstrated that Gimchs1 and Gimchs3 transcripts were detected during AM fungal root colonization, while none of the three transcripts were detected during spore germination. These results demonstrated that chitin synthesis in AM fungi is complex and involves multiple chs genes with transcriptional and/or post transcriptional regulation (Lanfranco et al., 1999b, c).
The first report of a targeted study of gene expression in the spores of the AM fungus was completed by Franken et al. (Franken et al., 1997). PCR based approaches demonstrated the presence of mRNA from genes encoding glyceraldehyde-3-phosphate dehydrogenase, ß-tubulin and P-type ATPases in the AM fungus Gigaspora rosea. The further use of ß-tubulin as a reference to quantify fungal material in the symbiotic and asymbiotic stages of development of the AM fungus G. mosseae has been reported (Butehorn et al., 1999). However, further analysis is necessary to determine how different copies of ß-tubulin are distributed among isolates of AM fungal species and how many copies are transcribed at different developmental stages.
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Untargeted molecular approaches |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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Untargeted approaches to isolating AM fungal genes have included differential display (DD) and differential screening (DS). These molecular techniques involve investigating the presence and/or absence of random untargeted gene products. The advantages of using these types of approaches is that no information on specific sequence information is required.
The DD method (Fig. 2) offers an opportunity whereby it is possible to compare simultaneously the mRNA transcripts present in a colonized and non-colonized root system, but, it also allows for the isolation of mRNA transcripts of genes being expressed within the fungus during a functional symbiotic relationship. DD has been used successfully to isolate fungal genes expressed during a functioning symbiosis (Harrier et al., 1998; Delp et al., 2000), but also in its asymbiotic growth stage, in response to the rhizobacterium Bacillus subtilis (Requena et al., 1999). Delp et al. isolated three partial cDNAs (GINMYC1, GINMYC2 and GINHB1) from the fungus G. intraradices (Delp et al., 2000). GIMYC1 and GINHB1 are expressed predominantly in external hyphae whereas GIMYC2 is expressed equally in the symbiotic state as compared to the external hyphae. Analysis of the deduced amino acid sequence of these transcripts demonstrated homology to known eukaryotic genes with GIMYC1 sharing homology to TRIP15, a human protein that interacts in a hormone-dependent manner with the thyroid receptor and ALIEN from Drosophila a protein that is regulated in a developmentally controlled manner. GINMYC2 shares homology to O-linked N-acetylglucosamine transferases from vertebrates and GINHB1 contains a putative leucine zipper and a homeodomain which indicates that it binds DNA and may act as a transcriptional regulator.
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AM fungi receive a carbon source from the host plant. It has been suggested that the fungus prefers to utilize glucose (Shachar-Hill et al., 1995
). The underlying mechanisms of carbon sensing and utilization by AM fungi in the symbiosis is not very well understood. Enzymatic activities of glycolytic enzymes during symbiotic and asymbiotic growth of G. mosseae (Macdonald and Lewis, 1978) and G. margarita (Saito, 1995) have been detected. But, to date only the cDNA corresponding to the phosphoglycerate kinase (PGK) gene has been isolated from G. mosseae, which is a key enzyme in the glycolytic pathway (Harrier et al., 1998). This gene was isolated by DD and expression analysis has demonstrated that this gene is expressed in both the symbiotic and asymbiotic stages of development. However, quantitative differences in the expression were delimited by quantitative immunoblotting using a polyclonal ab specific to the G. mosseae PGK protein (Harrier and Sawczak, 2000). This demonstrated that there was a significant increase in PGK protein levels in the symbiotic as compared to the asymbiotic stage of development. These results suggest that there is differential regulation of genes in the AM fungus during the symbiosis.
Requena et al. isolated the FOX2 gene from G. mosseae (Requena et al., 1999). This highly conserved gene encodes a multifunctional protein of the peroxisomal ß-oxidation pathway. Expression studies of this gene in the presence/absence of B. subtilus demonstrated a 5-fold down-regulation of the transcript and this demonstrates that AM fungi are able to change its gene expression in response to stimuli other than the host plant.
Differential screening is based on differences in the concentration of nucleic acid species between two or more samples (i.e. mycorrhizal and non-mycorrhizal) and is aimed at isolating differentially transcribed mRNAs (Sabelli, 1996). This is a powerful technique which has been used extensively in plant studies and has been used successfully to isolate novel plant and AM fungal genes differentially expressed during the AM symbiosis (Tahiri-Aloui and Antoniw, 1996; Burleigh and Harrison, 1997; Murphy et al., 1997; van Buuren et al., 1999b), in particular, a cDNA from the arbuscular mycorrhizal fungus, G. versiforme, with homology to a cruciform DNA-binding protein from Ustilago maydis (Burleigh and Harrison, 1998).
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Study of gene regulatory elements in AM fungi |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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The isolation and study of the regulatory elements of the AM fungal genes is a necessity for a greater understanding of the factors which control gene expression. The construction of prokaryotic-free representative genomic libraries is mandatory for the isolation of these regulatory elements. The construction of AM fungal libraries has been well documented (Franken and Gianinazzi-Pearson, 1996
; Hosny et al., 1999b; van Buuren et al., 1999a) and will be a fundamental tool for AM fungal studies in the future. To date, there is a paucity of data regarding regulatory elements of AM fungal genes, with the promoter region corresponding to the G. mosseae PGK gene having recently been isolated (Harrier, 2001). The study of this promoter is enhanced by the PGK promoter regions of several fungi having already been studied in detail (Vanhanen et al., 1991; Goldman et al., 1992; Takaya et al., 1995; Le Dall et al., 1996). This provides an excellent framework for a comparative study. Within the G. mosseae PGK promoter region several regulatory motifs have been identified. These include heat shock elements and upstream-activating sequences (UAS) similar to those located in Saccharomyces cerevisiae and Rhizopus niveus. These UAS elements have been shown in these organisms to be key regulators in response to carbon sources. Furthermore the G. mosseae promoter region contains homologous sequences to three elements of the S. cerevisiae UAS. This may be an important feature in the biology of AM fungi, since all the other fungal species PGK promoter regions studied so far, the UAS is either absent and/or only one segment of the S. cerevisiae UAS sequence is present. The importance of all three segments may arise from AM fungi being obligate symbionts, who receive a carbon source from the host plant, as they must have the mechanisms in place to respond when a carbon source becomes available to them through their symbiotic interaction or by the utilization of storage compounds. The appropriate response to carbon availability by AM fungi may be enhanced further by the presence of a second UAS sequence homologous to the one found in R. niveus. The presence of the two UAS sequences may play a key role in the two different stages of AM fungal development, i.e. asymbiotic and symbiotic. However, further research is required to validate the role of the UAS sequences in the response of AM fungi to carbon.
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AM fungal proteome analysis |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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A substantial quantity of research has focused on the isolation and study of AM fungal genes. However, there has been a modest amount of research on AM fungal proteins. A problem associated with studing proteins of AM fungi during the symbiotic state is differentiating them from proteins of plant origin. Moreover, with the recent advances in proteomics, analysis of polypeptides by mass spectrometry may result in the identification of important AM fungal proteins.
Specific fungal enzymes, which may aid the penetration of the outer root tissues have been studied, with small amounts of cell-degrading enzymes such as pectinase, cellulases, endo- and exoglucanases, and xyloglucanases (Garcia-Romera, 1991a, b; Garcia-Garrido et al., 1992a, b, 1996a, b, 1999) have been localized to the colonizing AM fungus. In addition, phosphatase activity has been localized within the phosphate accumulating vacuoles of hyphae and along the fungal tonoplast (Gianinazzi-Pearson and Gianinazzi, 1976, 1978; Gianinazzi et al., 1979). Moreover, the activity of this enzyme can be detected and measured in an mycorrhizal root system (Tisserant et al., 1993).
Antibodies corresponding to fungal proteins have been utilized in an attempt to identify specific fungal species (Aldwell et al., 1983, 1985; Kough et al., 1983; Wilson et al., 1983; Wright et al., 1987; Hahn et al., 1993; Hahn and Hock, 1994; Göbel et al., 1995), and/or detect AM fungi in plant root and soil systems (Aldwell et al., 1986; Wright and Morton, 1989; Friese and Allan, 1991; Cordier et al., 1996).
Overall there is a lack of data on proteins corresponding to specific functional metabolic genes (Anstrom et al., 1994, reviewed in Hahn et al., 1994; Gianinazzi-Pearson and Gianinazzi, 1995) with the majority of research focusing on antibodies to determine modifications in fungal cell components related to infection and development.
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AM fungal transformation technology |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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The study by Forbes et al. demonstrated that it was possible to introduce foreign DNA into spores of Gigaspora rosea and detect transient gene expression (Forbes et al., 1998b
). Moreover, after the first generation spores were harvested, it was possible to detect the presence of the GUS gene by PCR and also to detect the protein by immunoblotting, thus suggesting a stable transformation (Forbes et al., 1998a). The underlying biology of the transformation is not understood and future work should aim to answer these questions. |
Conclusions |
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TopAbstractIntroductionTargeted molecular approachesUntargeted molecular approachesStudy of gene regulatory...AM fungal proteome analysisAM fungal transformation...ConclusionsReferences |
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In the future, studies on the AM symbiosis will benefit from the developing molecular techniques. These coupled with traditional physiological experimentation and mycorrhizal plant mutants, will aid the understanding of this dynamic interaction between plants and fungi. In particular, strategies, such as expressed sequence tags (ESTs) (Adams et al., 1991
) and serial analysis of gene expression (SAGE) (Velculescu et al., 1995) will allow the rapid and detailed analysis of thousands of transcripts. Strategies utilizing ESTs, for example, subtractive hybridization and/or suppressive subtractive hybridization, which allow comparisons to be made between different developmental stages of AM fungi are currently being developed (Lanfranco et al., 2000; Requena et al., 2000). These studies may shed light on the key pathways regulating the development of AM fungi. Moreover, the utilization of microarray technology (DeRisi et al., 1997) will allow the simultaneous comparisons of the different stages of the AM fungal lifecycle, and will also permit comparisons between other plant-pathogenic and/or symbiotic interactions with the AM fungal–plant symbiosis.
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Acknowledgments |
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Financial support was provided by the Scottish Executive Rural Affairs Division (SERAD).
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Notes |
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1 Fax: +44 131 6672601. E-mail: L.Harrier{at}ed.sac.ac.uk
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