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Keywords:

  • arbuscular mycorrhizal symbiosis;
  • Glomus;
  • nitrogen;
  • phosphate;
  • signaling

Abstract

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

Contents

  • Summary  35

  • I. 
    Introduction 35
  • II. 
    Presymbiotic dialogue – recognition and anticipation 36
  • III. 
    Early symbiotic phase – contact and penetration 39
  • IV. 
    Mature symbiotic phase – haustoria and mineral nutrition 41
  • V. 
    Concluding remarks 43
  • Acknowledgements  43

  • References  43

Summary

Recent years have seen fascinating contributions to our understanding of the molecular dialogue between fungi and plants entering into arbuscular mycorrhizal (AM) symbioses. Attention has shifted from descriptions of physiological and cellular events to molecular genetics and modern chemical diagnostics. Genes, signal transduction pathways and the chemical structures of components relevant to the symbiosis have been defined. This review examines our current knowledge of signals and mechanisms involved in the establishment of AM symbioses.


I. Introduction

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

The arbuscular mycorrhizal (AM) symbiosis occurs between fungi of the Glomeromycota (Schüssler et al., 2001) and the majority of terrestrial plants. It is the most prevalent mutualistic association between plants and microbial organisms and involves an intimate relationship between plant roots and fungal hyphae. The mutualism of the AM symbiosis is manifested in bidirectional nutrient exchange: the fungus is nourished by plant photosynthates, and plant mineral nutrition – particularly phosphate – is enhanced by the fungus (reviewed in Smith & Read, 1997). AM fungi are obligate biotrophs, depending on living root tissue for carbohydrate supply to complete their asexual life cycle. Although typically the outcome of the AM association is beneficial for both partners, the effectiveness varies in individual plant–fungus combinations (Ravenskov & Jakobsen, 1995; Burleigh et al., 2002; Smith et al., 2003). In natural habitats, this influences ecosystem variability and productivity (van der Heijden et al., 1998). The Glomeromycota consists of approximately 150 isolates, which colonize a wide range of both mono- and dicotyledonous plant species. Under laboratory conditions, single fungal isolates do not exhibit host specificity and will associate with taxonomically distant plants. The widespread distribution of this symbiosis within the plant kingdom has been attributed to its antiquity; fossil records of mycorrhizal land plants place the origin of the AM symbiosis at least 400 million years ago (mya) (Remy et al., 1994), predating the divergence of plant lineages. Nonmycorrhizal plant species arose later in evolution, dating back to 100 mya (Brundrett, 2002). Their occurrence within different plant clades suggests loss of compatibility with AM fungi to be of polyphyletic origin (Brundrett, 2002).

The sequence of steps leading to an AM symbiosis is largely conserved among different combinations of fungal and plant species and appears to be independent of the effectiveness of the symbiosis. The process can be divided into major developmental stages: (i) the presymbiotic phase; (ii) contact and entrance of the fungus into root tissue; (iii) intraradical fungal proliferation; and (iv) cell invagination and nutrient transfer. These stages describe a chronological series of events at an individual infection site. However, establishment of the AM symbiosis in the whole root is highly asynchronous, with the described stages all present simultaneously once the fungus has commenced root penetration.

Recognition in concert with complex morphological and physiological alterations of both symbiotic partners suggests that the AM symbiosis is the result of multifaceted, fine-tuned signaling events. Forward genetic screens have allowed estimation of the scope of processes under plant control, and genes vital to the establishment of the symbiosis have been isolated. Application of genomic tools to molecular studies of AM symbioses has revealed a multitude of potentially relevant plant genes that respond to the development of the symbiosis. The absence of efficient transformation protocols and a lack of genetic tools for asexual fungi have so far hindered the description of signaling events in the fungus. This article summarizes the progress made in understanding AM symbiosis signaling since the reviews by Harrison (2005) and Hause & Fester (2005).

II. Presymbiotic dialogue – recognition and anticipation

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

1. Fungal responses to plant-derived signals

For both symbionts, the period before physical contact (appressoria formation) involves recognition and attraction of appropriate partners and other events promoting an alliance. The survival of the biotrophic fungus is enhanced by ‘economic’ germination and rapid colonization of host plants. Spores of AM fungi persist in the soil and germinate spontaneously, independent of plant-derived signals (Mosse, 1959). However, root exudates and volatiles may promote or suppress spore germination, indicating the existence of spore ‘receptors’ responsive to alterations in the chemical composition of the environment (reviewed in Giovanetti & Sbrana, 1998; Bécard et al., 2004; Harrison, 2005). After germination, the hyphal germ tube grows through the soil. In the absence of a potential host (asymbiotic phase), hyphal growth is limited by the utilization of low amounts of stored carbon (Bécard & Piché, 1989; Bago et al., 1999; Bago et al., 2000) and eventually ceases; however, the spore retains sufficient carbon to allow repeated germination and further possibilities to encounter an appropriate host. The particularly large spores of Gigaspora gigantea can germinate up to 10 times (Koske, 1981).

In the vicinity of a host root, fungal morphology shifts towards enhanced hyphal growth and extensive hyphal branching (Fig. 1a) (Giovanetti et al., 1993b; Buee et al., 2000). Such a response can be triggered by host root exudates or volatiles but not by exposure to nonhost roots or their exudates. These observations suggest that the fungus senses a host-derived signal (‘branching factor’), leading to intensified hyphal ramification that is likely to increase the probability of contact with a host root. Hence, distinction between host and nonhost occurs to a certain degree at this early point in the interaction. A recent major breakthrough was the identification of the host branching factor 5-deoxy-strigol, belonging to the strigolactones (Akiyama et al., 2005). Strigolactones have been isolated from a wide range of mono- and dicotyledonous plants and were previously found to stimulate seed germination of parasitic weeds such as Striga and Orobanche (reviewed in Bouwmeester et al., 2003). The concentration of strigolactones in root exudates coincides with the host specificity of AM fungi (Akiyama et al., 2005). The nonmycotrophic Arabidopsis thaliana, for example, produces very low amounts of strigolactones compared with hosts of AM fungi such as carrot and tobacco (Westwood, 2000). The biosynthetic pathway for strigolactones is not well understood. They were previously described as sesquiterpenes (Yokota et al., 1998; Akiyama et al., 2005); however, the use of carotenoid mutants of maize and inhibitors of isoprenoid pathways in maize, sorghum and cowpea showed that strigolactones are derived from the carotenoid biosynthetic pathway, via the plastid, nonmevalonate, methylerythritol phosphate (MEP) pathway (Matusova et al., 2005). Interestingly, the carotenoid cleavage products mycorradicin (‘yellow pigment’) and cyclohexenones specifically accumulate in mycorrhizal roots (Klingner et al., 1995; Maier et al., 1997; Walter et al., 2000). Use of the same maize carotenoid mutations revealed the lack of mycorradicin production and a reduction in mycorrhizal colonization (Fester et al., 2002). These authors examined later stages of the AM interaction. It will now be interesting to analyze the early symbiotic properties of these maize mutants in relation to strigolactone as a stimulant of presymbiotic fungal branching. Nevertheless, the results do indicate that processed carotenoid derivatives are involved at multiple stages in the development of the AM symbiosis, possibly by stimulating intraradical fungal branching.

image

Figure 1. Stages of root colonization by an arbuscular mycorrhizal (AM) fungus. (a) Hyphal branching occurs upon perceiving plant-released strigolactone; (b) pENOD11::GUS expression upon perceiving Myc-factor(s); (c) appressoria formation and passage through outer root cell layers; (d) longitudinal apoplastic fungal spreading; (e) arbuscule formation in the inner cortex. Microphotographs display chlorazole black E stained rice roots colonized by Glomus intraradices. Bars, 25 mm.

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Tomato mutants impaired in the development of AM symbiosis with Gigaspora and Glomus isolates were shown to be affected in the presymbiotic stimulation of spore germination and hyphal growth (David-Schwartz et al., 2001, 2003). The conclusion could be drawn that the lack of a stimulant caused the mutant phenotype. However, the same group observed that exudates of mutant root suppressed spore germination and hyphal tip growth, which they attributed to the presence of an active inhibitory compound (Gadkar et al., 2003).

Although the fungal strigolactone receptor has not yet been isolated, the consequences of strigolactone detection were investigated in Gigaspora rosea and Glomus intraradices exposed to exudates from carrot roots (Tamasloukht et al., 2003). Hyphal branching commenced shortly after initial rapid changes in transcript abundance of putative mitochondrial genes, followed by enhanced oxygen consumption and reducing activity. Hence, induction of a subset of genes appeared to lead to elevated respiratory activity and an energy status necessary for extensive hyphal branching (Tamasloukht et al., 2003). Thus, upon detection of a host root there is vigorous investment in the production of fungal hyphae, which can then rapidly make contact with essential carbon sources (Bécard et al., 2004).

2. Plant responses to fungus-derived signals

The plant responds to the microbial profile of the rhizosphere in different ways, depending upon the type of organism present. Detection of pathogen-derived elicitors triggers plant signaling cascades that lead to a defense response, a phenomenon that has been widely studied (for a recent review, see Glazebrook, 2005). On the other hand, plant defense responses are either not mounted at all or mounted only transiently before being suppressed during AM symbiosis (reviewed in Harrison, 2005; Hause & Fester, 2005). Little is known about AM fungal signal(s), their perception or the consequences triggered in the plant. One study used an inducible transgenic reporter line (Journet et al., 2001) to document the detection of an as yet unknown fungal factor (Kosuta et al., 2003). GUS reporter expression before contact was monitored in root sections adjacent to intensely branching hyphae (Kosuta et al., 2003). A cellophane membrane was placed between the two organisms to prevent physical contact while allowing exchange of signals. The intensity and distribution of GUS expression indicated the detection by the plant of a compound released by the fungus (Fig. 1b). This putative ‘Myc factor’ (in analogy to Nod factor) was produced by the AM fungi tested but was absent from three pathogenic fungi (Kosuta et al., 2003). Interestingly, when contact and penetration were permitted, GUS expression was restricted to infected and associated cells (Chabaud et al., 2002; Genre et al., 2005), indicating the induction of a suppressor activity in noncolonized neighboring cells (Parniske, 2004). Thus, it is possible that a larger region of the plant root becomes primed for an encounter with the fungus by the turning on of a symbiont ‘anticipation’ program that includes MtENOD11 expression. When contact is made and a precise area of penetration and colonization is established, gene expression is restricted to cells in direct contact with the penetrating fungus. Similarly, during preinfection and infection stages in the interaction of Medicago truncatula with nitrogen-fixing Rhizobia, GUS expression was found in the rhizodermis of larger root section before contact and upon subsequent bacterial entrance into the root tissue becomes confined to the area of infection, namely the infection site and the invaded nodule (Journet et al., 2001). This resemblance in expression patterns between the two types of root symbioses suggests that the responses are part of a rather general symbiont ‘anticipation’ program. The M. truncatula mutant Does not make infections 2 (dmi2) does not support fungal penetration (Catoira et al., 2000). However, hyphal branching and MtENOD11 expression before contact is induced to levels comparable to that of wild-type plants, indicating that the presymbiotic properties of dmi2 are not affected (Chabaud et al., 2002). However, no GUS expression was monitored in dmi2 upon contact with the fungus. Therefore while presymbiotic ‘anticipation’ signaling operates independently of MtDMI2 the signaling pathway involved in ‘contact-associated’MtENOD11 expression requires functional MtDMI2.

Interestingly, an independent report showed induction in the number of lateral roots of M. truncatula in response to perception of a diffusible factor from AM fungi before contact (Olah et al., 2005). Taking under consideration that lateral roots are the preferred site for fungal colonization, it is tempting to speculate that the plant prepares for the association by producing an enhanced amount of favored tissue (Harrison, 2005). How far the fungal factors inducing MtENOD11 expression or lateral root formation relate to the same molecule is not clear. However, in contrast to MtENOD11 expression, lateral root formation was dependent on MtDMI2 (and MtDMI1), which suggests that the two processes are triggered either by different input molecules or by employing different signaling pathways. Evidence for an early and rather broad transcriptional response of the plant to perception of the fungus in its vicinity comes from the recent identification of 11 M. truncatula genes induced by inoculation with Glomus mosseae before contact (Weidmann et al., 2004). Up-regulation of these genes was shown to require DMI3 and gene induction was abolished in dmi3 mutants that do not permit fungal penetration (Catoira et al., 2000). These data indicate that presymbiotic signaling partially depends on the functioning of DMI3, which is further required for penetration of the rhizodermal cell layer.

A different kind of supporting evidence for the concept of a symbiont ‘anticipation’ program comes from the recent finding that higher amounts of starch accumulate in roots of Lotus japonicus following the detection of approaching fungi during the presymbiotic phase (Gutjahr et al., 2005). Such starch accumulation might promote and sustain the symbiosis.

Plant receptors for presymbiotic Myc factor-like signals have not yet been described. However, the absence of appressoria formation on roots of the recently identified maize mutant nope1 indicated a defect in early presymbiotic signaling before physical contact (Paszkowski et al., 2006). The transposon-associated sectorial restoration of wild-type function indicated cell autonomous functioning of ZmNOPE1, arguing against a defect in a plant signal essential for recognition, but pointing towards its involvement in the perception of a fungal component.

III. Early symbiotic phase – contact and penetration

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

1. Appressoria development

The onset of the symbiosis is marked morphologically by the formation of appressoria, the first cell-to-cell contact between fungus and plant and the site of fungal ingress into the host root (Fig. 1c). The development of appressoria can be considered to be the result of successful presymbiotic recognition events when fungal and plant partners are committed to an interaction (Giovanetti et al., 1993a). Structurally, appressoria differ from hyphae by being flattened, elliptical hyphal tips that adhere by unknown means to the surface of host rhizodermal cells (Garriock et al., 1989). This morphological switch is reflected by changes in fungal gene transcription (Breuninger & Requena, 2004). Appressoria do not occur on the rhizodermal cells of nonhosts (Garriock et al., 1989; Giovanetti et al., 1993a) or on artificial surfaces such as cellulose or nylon (Giovanetti et al., 1993a). Interestingly, in a further study, isolated rhizodermal cell walls of a host but not vascular or cortical cell walls of the same origin triggered appressoria development without inducing penetration (Nagahashi & Douds, 1997). Thus, while physical and/or chemical rhizodermal cell wall features are required and sufficient to elicit appressoria formation, penetration needs the support of intact cells, whose coordinated, matching response accommodates the fungus. The phenotypes of numerous plant mutants affected at the stage of penetration following appressoria development fosters this view (reviewed in Marsh & Schultze, 2001). Although ‘penetration’ is compromised in all of these mutants, specific plant-regulated processes associated with penetration have been delineated. In L. japonicus, for example, an epidermal cleft opens between two adjacent rhizodermal cells through which the fungus enters. From here, invasion of the rhizodermal cell(s) is initiated and the fungus trespasses through the underlying exodermal cell (reviewed in Parniske, 2004). Mutations in LjSYM2 (LjSYMRK), LjSYM4 (LjCASTOR) and LjSYM15 affect these processes, specifically the epidermal opening (LjSYM15; Demchenko et al., 2004), the intracellular accommodation of the fungus within rhizo- and exodermal cells (LjSYM2, LjSYM4; Bonfante et al., 2000) and the penetration of cortical cells (LjCASTOR, LjSYM15; Novero et al., 2002). Discovery of the corresponding mutants assisted the definition of these plant-regulated steps (reviewed in Parniske, 2004).

In addition to entering through a rhizodermal cleft, the fungus can also traverse rhizodermal cells directly, as shown in detail for G. gigantea penetrating roots of M. truncatula (Genre et al., 2005). Interestingly, the green fluorescent labeling of cytoskeleton and endoplasmatic reticulum proteins revealed that M. truncatula rhizodermal cells form a prepenetration apparatus after appressoria development (but before fungal invagination of the plant cell) that guides the invading hypha through the cell lumen (Genre et al., 2005). This process commences with nuclear repositioning adjacent to the appressorium. Subsequently, transcellular migration of the nucleus is associated with the formation of a hollow column composed of microtubules, microfilaments and endoplasmic reticulum cisternae connecting the moving nucleus to its previous position below the appressorium. Finally, the fungal hypha enters the preformed channel and follows the route earlier outlined by the plant cell nucleus. Hence, infection only occurs after preparatory activities in the plant cell. These cytological studies illustrate nicely the extensive complementary contribution made by host cell activity to fungal penetration. Moreover, the prepenetration apparatus is not induced in dmi2 and dmi3 in which fungal infection is blocked following appressoria formation. This emphasizes the significance and indispensable participation of plant processes in the coordinated invasion (Genre et al., 2005). It will be important to investigate how far equivalent rearrangements are involved in the accommodation of other endosymbionts. As Genre et al. (2005) show, elaboration of a tunnel for fungal passage through the plant cell is accompanied by the synthesis of a perifungal membrane that encloses the intracellular fungal hypha and confines the apoplastic interface compartment. The formation of a ‘symbiosome membrane’ and an interface matrix have been recognized as features common to biotrophic plant–microbial interactions involving intracellular growth of the microsymbiont (Parniske, 2000). Therefore, it will be an exciting task in the future to elucidate mechanistic conservation among phylogenetically distant but strategically analogous infection forms.

2. The common SYM pathway

All of the legume mutants described so far are common sym mutants impaired in root endosymbioses, mycorrhiza and nodulation. These mutants indicate the existence in legumes of partially shared genetic programs required for successful interaction with fungal and bacterial symbionts. A large number of legume mutants, including dmi1, dmi2 and dmi3 mutants (Catoira et al., 2000), and one tomato mutant (Barker et al., 1998), have been identified, which support appressoria formation but are compromised in intraradical invasion (reviewed in Marsh & Schultze, 2001). While in M. truncatula, three classes of mutants (dmi1, dmi2 and dmi3) have been reported, seven genes (LjSYMRK, LjCASTOR, LjPOLLUX, LjSYM3, LjSYM6, LjSYM15, LjSYM24) were found to be required for fungal penetration in L. japonicus (reviewed in Harrison, 2005; Kistner et al., 2005). The use of model legumes paved the way for isolating corresponding genes from mutant backgrounds and defining a signal transduction pathway essential for the two root symbioses (Fig. 2). As several authors have discussed this topic in detail (Parniske, 2004; Harrison, 2005; Hause & Fester, 2005; Oldroyd et al., 2005; Oldroyd & Downie, 2006), this article will only briefly summarize the current knowledge and describe recent progress taking a ‘mycocentric’ view. The genes revealed by these mutations all control fungal passage through the outer cell layers. The corresponding proteins, namely the Leu-rich repeat receptor-like kinase LjSYMRK/MsNORK/MtDMI2 (Endre et al., 2002; Stracke et al., 2002) as well as the plastid ion channels LjCASTOR/LjPOLLUX/MtDMI1 (Ane et al., 2004; Imaizumi-Anraku et al., 2004) and the nuclear localized calcium- and calmodulin-dependent protein kinase MtCCamK/MtDMI3 (Levy et al., 2004; Mitra et al., 2004), are needed for the early steps in Nod factor signaling and are probably also involved in signaling during the early stages of mycorrhizal colonization. The first genes isolated encoded the LjSYMRK/MsNORK/MtDMI2 receptor-like kinases (Endre et al., 2002; Stracke et al., 2002). The structure of the protein with an extensive extracellular domain suggests it is involved in the extracellular binding of a ligand and the intracellular transduction of the signaling event via its protein kinase domain. At present, however, it is not clear if these proteins in fact operate as primary receptors for a compound released by AM fungi. It is equally plausible that additional receptors are involved in the perception of a ‘Myc factor’ as was shown for the Nod factor receptors LjNFR1/MtLYK3 and LjNFR5 (Limpens et al., 2003; Madsen et al., 2003; Radutoiu et al., 2003). One of the early responses of legume root hair cells to the perception of Rhizobia or purified Nod factors is intracellular calcium oscillation (for a recent review, see Oldroyd & Downie, 2006). During Nod factor signaling, DMI1 (LjCASTOR and LjPOLLUX) and MtDMI2 (LjSYMRK, MsNORK) type proteins are necessary for the induction of calcium spiking, while MtDMI3 (MtCCamK) type proteins are assumed to be involved in deciphering the calcium signal (Fig. 2) (Levy et al., 2004; Mitra et al., 2004). Although calcium oscillation has not been shown for mycorrhizal signaling, the participation of proteins associated with calcium signaling suggests calcium also functions as a second messenger within the fungus-related signaling pathway. Recently, another member of the SYM pathway required for calcium spiking during nodulation has been discovered: the gene affected in the L. japonicus sym3 mutant encodes a homologue of the mammalian nucleoporin NUP133 and was therefore termed Lotus NUP133 (Kanamori et al., 2006). Consistent with a function as a nucleoporin, an eYFP-NUP133 fusion protein localized to the nuclear rim assembly with the nuclear pore complex. The absence of pleiotropic phenotypes of Lotus nup133 mutant plants indicates the specific involvement of the LjNUP133 protein in root symbioses. Although its function during symbiosis is not clear, it is intriguing that the early symbiotic signal transduction pathway includes ion fluxes, plastid ion channels and nuclear pore complexes. Cloning of the mutated genes from the remaining Lotus sym mutants is currently in progress in different laboratories. The establishment of a comprehensive picture of how the individual components of the SYM pathway tie up should be possible in the near future. Furthermore, because of the ancient nature of the AM symbiosis, a high degree of functional conservation of these SYM factors among members of plant families other than legumes can be anticipated. Noticeably, a first supporting example showed that the nodulation phenotype of the M. truncatula dmi3 mutant can be rescued by introducing a rice gene putatively orthologous to the leguminous CCamK (Godfroy et al., 2006). It will be important to verify complementation of the mycorrhizal mutant phenotype of the transformed dmi3 line and also to address the function of this gene for the interaction of rice with AM fungi. Similarly, for other putative SYM factor orthologs from non-leguminous dicotyledonous or from monocotyledonous plants (Zhu et al., 2006), the relevance for the AM symbiosis can be addressed via reverse genetics.

image

Figure 2. A ‘mycocentric’ view of the common SYM/DMI signaling pathway. The signaling pathway as it appears in this figure has emerged from genetic investigations on Medicago truncatula, Lotus japonicus and Medicago sativa. Abbreviations in squares refer to identified genes. The Myc factor(s) released by arbuscular mycorrhizal (AM) fungi has not been identified and also the link (possibly a transcription factor, TF) between DMI3 and mycorrhiza-induced alterations in gene expression is unknown. (Modified after Oldroyd et al. (2005).)

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The identification of additional components within the symbiotic nitrogen fixation signaling cascade indicates that proteins with related functions might be involved in mycorrhizal signaling. For example, a functional equivalent of the putative Nod factor receptors LjNFR1 and LjNFR5 (reviewed in Oldroyd et al., 2005; Oldroyd & Downie, 2006) could exist for ‘Myc factor’ perception (Fig. 2). It is also likely that components corresponding to the GRAS transcription factors MtNSP1 and MtNSP2 (Kalo et al., 2005; Smit et al., 2005) are present to modulate gene expression in response to calcium oscillation during mycorrhizal signaling (Fig. 2). In summary, genetically dissecting the common SYM signal transduction pathway required for bacterial and fungal root endosymbiosis not only unraveled the players involved but also provided a first glimpse at conservation and specialization of signaling cascades essential for nodulation and mycorrhiza development.

3. Apoplastic fungal spread

Transcellular passage of the outer root cell layers appears to be a bottleneck in the development of the AM symbiosis, while entrance to the cortex apoplast permits rapid spread of the fungus along the axes of the root (Fig. 1d, Parniske, 2004). In the maize mutant taci1, the fungus enters the apoplast and initiates hyphal growth along the longitudinal axes of the root. However, these hyphae become septate and die, and horizontal spreading is not accomplished (Paszkowski et al., 2006). Furthermore, silencing of the M. truncatula CDPK1 gene, which encodes a calcium-dependent protein kinase required for root development, led to significantly reduced longitudinal spread of the fungus and similarly decreased progression of nodulation-associated infection threads through cortical cells (Ivashuta et al., 2005). Reduced microbial growth was suggested to occur as a result of altered cell wall composition and cytoskeleton organization of silenced CDPKi lines. The phenotypes of taci1 and CDPKi provide evidence that plant-encoded factors are required for apoplastic proliferation of the fungus.

IV. Mature symbiotic phase – haustoria and mineral nutrition

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

1. Arbuscule development

Arbuscules are the key feature of the AM symbiosis as they represent an extreme form of intimacy and compatibility. Formation of arbuscules within host cells is associated with dramatic morphological and physiological changes in both symbiotic partners. The fungus invaginates inner cortex cells where it undergoes extensive dichotomous branching into a tree-like fungal structure that may entirely fill the living cortical cell (Fig. 1e). Consequently the architecture of the host cell undergoes remarkable changes: for example, the nucleus moves from a peripheral to a central position, the vacuole becomes fragmented and an extensive periarbuscular membrane is synthesized that is in continuum with the plant plasma membrane (reviewed in Harrison, 1999). Despite this intense activity of both partners leading towards arbusculated cells, arbuscules collapse after several days, leaving an intact cortical cell that is then able to host another arbuscule. It is not known what triggers fungal entrance into the cell but the perception of a radial sugar gradient between the vascular tissue and the outer cell layers may be involved in induction of arbuscule formation (Blee & Anderson, 1998). The signals that induce intracellular fungal branching or arbuscule decay have also not been identified. However, as mentioned in Section II.1, the recent identification of strigolactone as a stimulant for presymbiotic fungal branching (Akiyama et al., 2005), combined with the finding that part of its putative biosynthetic pathway is activated in colonized roots (Maier et al., 1997; Walter et al., 2000; Matusova et al., 2005), indicates that related molecules may elicit intracellular hyphal branching. It has been suggested that arbuscule senescence is a result of plant responses countering intracellular colonization (Salzer et al., 1999; Walter et al., 2000). Alternatively, the initiation of arbuscule collapse may be caused by endogenous fungal signaling or coordinated signaling cross-talk.

Development of arbuscules is at least partially under the control of the host genetic program. So far, one legume mutant has been described (pea sym36) in which reduced arbuscules with fewer and shorter branches are formed (Engvild, 1987; Gianinazzi-Pearson et al., 1991). In addition, proteins of the SYM pathway are either required for arbuscule development, such as LjCASTOR, LjSYM15 and likely LjSYM6, or contribute to arbuscule formation, such as LjPOLLUX, LjNup133 and LjSYM24 (Kistner et al., 2005). The recovery of further mutants in forward genetic screens is an urgent task in order to unravel plant factors essential to the formation of this key structure of the AM symbiosis. In recent years, several laboratories have undertaken global gene expression profiling to identify AM regulated genes (Martin-Laurent et al., 1997; Lapopin et al., 1999; van Buuren et al., 1999; Journet et al., 2002; Liu et al., 2003; Taylor & Harrier, 2003; Wulf et al., 2003; Brechenmacher et al., 2004; Grunwald et al., 2004; Weidmann et al., 2004; Guimil et al., 2005; Hohnjec et al., 2005). In many cases gene expression was monitored at the stage of a mature symbiosis and long lists of induced and suppressed genes have been created. Reporter lines using the promoters of up-regulated genes in conjunction with GUS or GFP revealed either exclusive expression in arbusculated cells or expression in tissue patches including cells with arbuscules and cells in the vicinity of arbuscules (reviewed in Harrison, 2005; Hohnjec et al., 2005). The list of candidate genes probably includes those essential for signaling during the initiation and formation of arbuscules.

With the help of reverse genetics it is possible to determine the relevance of differentially regulated genes for the development of an AM symbiosis, especially where extensive resources are available, such as L. japonicus, M. truncatula and rice (Perry et al., 2003; Hirochika et al., 2004; Tadege et al., 2005). Alternatively, efficient transformation protocols can be applied to RNAi (or antisense)-mediated gene silencing in a variety of AM host plants. Knock-down of the expression of a M. truncatula gene encoding the jasmonic acid-biosynthetic enzyme allene oxide cyclase by transformation with antisense cDNA resulted in lower amounts of jasmonic acid (Isayenkov et al., 2005). A delay in colonization, accompanied by reduced arbuscle formation was observed indicating that jasmonic acid plays a role during the development of an AM symbiosis. Further exciting discoveries facilitated by the availability of these resources can be predicted in the near future in various AM host plants.

2. Symbiotic phosphate and nitrogen acquisition

Arbuscular mycorrhizal fungi obtain carbohydrates from their hosts and simultaneously improve plant acquisition of mineral nutrients, in particular phosphate (Pi). It was recently shown that, depending on the particular plant–fungus combination, symbiotic phosphate uptake may partially participate in, or even dominate, overall plant Pi acquisition (Smith et al., 2003). The proposed metabolic route of symbiotic Pi acquisition starts with the assimilation of inorganic Pi at the hyphal–soil interface by fungal high-affinity transporters (Harrison & van Buuren, 1995; Maldonado-Mendoza et al., 2001; Benedetto et al., 2005). Inside the fungus, inorganic Pi is translocated in the form of polyphosphate from fungal structures outside of the root to those inside (Solaiman et al., 1999; Ohtomo & Saito, 2005). Before release into the periarbuscular interface, phosphate becomes depolymerized to inorganic Pi (Ohtomo & Saito, 2005). Pi is acquired from the interface by plant-encoded phosphate transporters. Such transporters have been identified from several plant backgrounds and were shown to be transcriptionally induced during the development of the AM symbiosis (Rausch et al., 2001; Harrison et al., 2002; Paszkowski et al., 2002; Glassop et al., 2005; Nagy et al., 2005). While only one mycorrhiza-induced Pi transporter coding gene has currently been identified from M. truncatula (MtPT4; Harrison et al., 2002), three have been found in solanaceous species (StPT3/LePT3, StPT4/LePT4, and StPT5/LePT5; Karandashov & Bucher, 2005; Nagy et al., 2005), two in rice (OsPT11 and OsPT13; Paszkowski et al., 2002; Guimil et al., 2005) and one in maize, barley and wheat (Glassop et al., 2005). The mycorrhiza-specific subfamily comprises the orthologous monocot proteins OsPT11 and TaPT1, and the dicot proteins MtPT4, StPT4/LePT4 and StPT5/LePT5 (Table 1), indicating a gene duplication event in the case of the solanaceous transporters (Nagy et al., 2005). The StPT3 protein is nonorthologous to the MtPT4 type proteins and to OsPT13. While OsPT13 is weakly expressed in mycorrhizal roots (Guimil et al., 2005), StPT3 exhibits a strong up-regulation (Rausch et al., 2001). One of these mycorrhiza-induced Pi transporters has been localized to the periarbuscular membrane, consistent with a function in plant uptake of Pi from the interface between fungus and plant (Harrison et al., 2002). A pressing project is to confirm the function of these transporter proteins in symbiotic Pi acquisition and to examine their influence on the establishment of the symbiosis. The fact that mycorrhiza-induced Pi transporters in some plant species are present in small gene families has so far hampered approaches to this question because of functional redundancy (Nagy et al., 2005). Moreover, it is of great interest to elucidate the nature of the signal specifically inducing symbiotic Pi transporter genes and also to determine the mechanism leading to the periarbuscular membrane localization of the corresponding Pi transporter proteins.

Table 1.  Mycorrhiza-specific plant phosphate transporters
Gene namePlant speciesReference
MtPT4Medicago truncatulaHarrison et al. (2002)
LePT4TomatoKarandashov et al. (2004)
LePT5TomatoNagy et al. (2005)
StPT4PotatoKarandashov & Bucher (2005)
StPT5PotatoNagy et al. (2005)
OsPT11RicePaszkowski et al. (2002)
TaPT1WheatGlassop et al. (2005)

It has been long recognized that in addition to Pi, AM fungi also promote nitrogen nutrition of their hosts (Raven et al., 1978). Until recently, very little was known about how AM fungi take up nitrogen from the environment and enable transfer of a portion to the plant. Stable isotope labeling has now suggested that inorganic nitrogen is taken up by the extraradical mycelium, incorporated into amino acids, translocated from extra- to intraradical fungal structures as arginine and then released as ammonium to the plant (Govindarajulu et al., 2005; Jin et al., 2005). Further support for this uptake route comes from the finding that transcript abundance of key enzymes of nitrogen assimilation and of arginine breakdown preferentially accumulate in extra- or intraradical mycelium, respectively (Govindarajulu et al., 2005). In analogy to the path of symbiotic Pi uptake, the arbuscule may be the site of symbiotic nitrogen uptake involving plant-encoded nitrogen transporters located within the periarbuscular plant membrane. Promising candidates such as mycorrhiza-induced nitrate and ammonium transporters have been identified in transcriptome analyses of mycorrhizal M. truncatula and rice (Frenzel et al., 2005; Guimil et al., 2005; Hohnjec et al., 2005). It will be interesting to investigate their role in symbiotic nitrogen uptake to determine the contribution of AM symbioses to nitrogen acquisition of plants.

V. Concluding remarks

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

Although our understanding of molecular mechanism and signaling pathways coupled to AM symbioses need further refinement, the past few years have brought exciting discoveries in this area. Elucidation of molecular events associated with signaling and nutrient acquisition processes have moved rapidly forward. It is foreseeable that the availability of forward and reverse genetics resources as well as established transformation protocols will stimulate further work towards identification and characterization of plant (and fungal) factors relevant to AM symbioses. Furthermore, central questions concerning their conservation among mono- and dicotyledonous plants, and also their relevance in other plant–microbial interactions, can be addressed in the near future.

Acknowledgements

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References

I apologize to all those researchers whose work I have overlooked or could not include because of space considerations. I am grateful to Patrick King, Caroline Gutjahr and Ruairidh Sawers for critical reading of the manuscript and to the University of Geneva and Swiss National Science Foundation for funding (grant 3100A0-104132).

References

  1. Top of page
  2. Abstract
  3. I. Introduction
  4. II. Presymbiotic dialogue – recognition and anticipation
  5. III. Early symbiotic phase – contact and penetration
  6. IV. Mature symbiotic phase – haustoria and mineral nutrition
  7. V. Concluding remarks
  8. Acknowledgements
  9. References
  • Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824827.
  • Ane JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Levy J, Debelle F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Denarie J, Cook DR. 2004. Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 13641367.
  • Bago B, Pfeffer PE, Douds DD Jr, Brouillette J, Becard G, Shachar-Hill Y. 1999. Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiology 121: 263272.
  • Bago B, Pfeffer PE, Shachar-Hill Y. 2000. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiology 124: 949958.
  • Barker S, Stummer B, Gao L, Dispain I, O’Connor P, Smith S. 1998. A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterization. Plant Journal 15: 791797.
  • Bécard G, Kosuta S, Tamasloukht M, Séjalon-Delmas N, Roux C. 2004. Partner communication in the arbuscular mycorrhizal interaction. Canadian Journal of Botany 82: 11861197.
  • Bécard G, Piché Y. 1989. New aspects on the acquisition of biotrophic status by a vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytologist 112: 7783.
  • Benedetto A, Magurno F, Bonfante P, Lanfranco L. 2005. Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15: 620627.
  • Blee K, Anderson A. 1998. Regulation of arbuscule formation by carbon in the plant. The Plant Journal 16: 523530.
  • Bonfante P, Genre A, Faccio A, Martini I, Schauser L, Stougaard J, Webb J, Parniske M. 2000. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Molecular Plant–Microbe Interactions 13: 11091120.
  • Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH. 2003. Secondary metabolite signalling in host–parasitic plant interactions. Current Opinions in Plant Biology 6: 358364.
  • Brechenmacher L, Weidmann S, Van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V. 2004. Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula–Glomus mosseae interactions. Mycorrhiza 14: 253262.
  • Breuninger M, Requena N. 2004. Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genetics Biology 41: 794804.
  • Brundrett M. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytologist 154: 275304.
  • Buee M, Rossignol M, Jauneau A, Ranjeva R, Becard G. 2000. The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Molecular Plant–Microbe Interactions 13: 693698.
  • Burleigh SH, Cavagnaro T, Jakobsen I. 2002. Functional diversity of arbuscular mycorrhizas extends to the expression of plant genes involved in P nutrition. Journal of Experimental Botany 53: 15931601.
  • Van Buuren ML, Maldonado-Mendoza IE, Trieu AT, Blaylock LA, Harrison MJ. 1999. Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Molecular Plant–Microbe Interactions 12: 171181.
  • Catoira R, Galera C, De Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J. 2000. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12: 16471666.
  • Chabaud M, Venard C, Defaux-Petras A, Becard G, Barker D. 2002. Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbucular mycorrhizal fungi. New Phytologist 156: 265273.
  • David-Schwartz R, Badani H, Smadar W, Levy AA, Galili G, Kapulnik Y. 2001. Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant Journal 27: 561569.
  • David-Schwartz R, Gadkar V, Wininger S, Bendov R, Galili G, Levy AA, Kapulnik Y. 2003. Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Molecular Plant–Microbe Interactions 16: 382388.
  • Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowska K. 2004. Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytologist 163: 381392.
  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB. 2002. A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962966.
  • Engvild K. 1987. Nodulation and nitrogen fixation mutants of pea, Pisum sativum L. Theoretical and Applied Genetics 74: 711713.
  • Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D. 2002. Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216: 148154.
  • Frenzel A, Manthey K, Perlick AM, Meyer F, Puhler A, Kuster H, Krajinski F. 2005. Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Molecular Plant Microbe–Interactions 18: 771782.
  • Gadkar V, David-Schwartz R, Nagahashi G, Douds DD Jr, Wininger S, Kapulnik Y. 2003. Root exudate of pmi tomato mutant M161 reduces AM fungal proliferation in vitro. FEMS Microbiological Letters 223: 193198.
  • Garriock M, Peterson R, Ackerley C. 1989. Early stages in colonization of Allium porrum (leek) roots by the vesicular-arbucular mycorrhizal fungus, Glomus versiforme. New Phytologist 112: 8592.
  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG. 2005. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17: 34893499.
  • Gianinazzi-Pearson V, Gianinazzi S, Guillemin J, Trouvelot A, Duc G. 1991. Genetic and cellular analysis of resistance to vesicular arbuscular (VA) mycorrhizal fungi in pea mutants. In: VermaHHAD, ed. Advances in molecular genetics of plant–microbe interactions. Dordrecht, the Netherlands: Kluwer Academic Publishers, 336342.
  • Giovanetti M, Avio L, Sbrana C, Citernesi A. 1993a. Factors affecting appressoria development in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd. and Trappe. New Phytologist 123: 114122.
  • Giovanetti M, Sbrana C. 1998. Meeting a non-host: the behaviour of AM fungi. Mycorrhiza 8: 123130.
  • Giovanetti M, Sbrana C, Avio L, Citernesi A, Logi C. 1993b. Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytologist 125: 587593.
  • Glassop D, Smith SE, Smith FW. 2005. Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222: 688698.
  • Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205227.
  • Godfroy O, Debelle F, Timmers T, Rosenberg C. 2006. A rice calcium- and calmodulin-dependent protein kinase restores nodulation to a legume mutant. Molecular Plant–Microbe Interactions 19: 495501.
  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y. 2005. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435: 819823.
  • Grunwald U, Nyamsuren O, Tamasloukht M, Lapopin L, Becker A, Mann P, Gianinazzi-Pearson V, Krajinski F, Franken P. 2004. Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Molecular Biology 55: 553566.
  • Guimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ionnidis V, Oakeley E, Docquier M, Descombes P, Briggs S, Paszkowski U. 2005. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proceedings of the National Academy of Sciences, USA 102(22): 80668070.
  • Gutjahr C, Novero M, Genre A, Welham T, Wang T, Bonfante P. 2005. Prior to colonization Gigaspora margarita induces starch accumulation in Lotus japonicus roots. In: 12th International Conference on Molecular Plant–Microbe Interactions, Merida, Mexico. (In press.)
  • Harrison MJ. 1999. Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiological Plant Molecular Biology 50: 361389.
  • Harrison M. 2005. Signaling in the arbuscular mycorrhizal symbiosis. Annual Review of Microbiology 59: 1942.
  • Harrison MJ, Dewbre GR, Liu J. 2002. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14: 24132429.
  • Harrison MJ, Van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378: 626629.
  • Hause B, Fester T. 2005. Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221: 184196.
  • Heijden MVD, Klironomos J, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders I. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 6972.
  • Hirochika H, Guiderdoni E, An G, Hsing YI, Eun MY, Han CD, Upadhyaya N, Ramachandran S, Zhang Q, Pereira A, Sundaresan V, Leung H. 2004. Rice mutant resources for gene discovery. Plant Molecular Biology 54: 325334.
  • Hohnjec N, Vieweg MF, Puhler A, Becker A, Kuster H. 2005. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiology 137: 12831301.
  • Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Allan Downie J, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M. 2004. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433(7025): 527531.
  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B. 2005. Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiology 139: 14011410.
  • Ivashuta S, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS. 2005. RNA interference identifies a calcium-dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17: 29112921.
  • Jin H, Pfeffer PE, Douds DD, Piotrowski E, Lammers PJ, Shachar-Hill Y. 2005. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytology 168: 687696.
  • Journet EP, El-Gachtouli N, Vernoud V, De Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V. 2001. Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Molecular Plant–Microbe Interactions 14: 737748.
  • Journet EP, Van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O, Godiard L, Micheli F, Kahn D, Gianinazzi-Pearson V, Gamas P. 2002. Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Research 30: 55795592.
  • Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE. 2005. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 17861789.
  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. 2006. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Sciences, USA 103: 359364.
  • Karandashov V, Bucher M. 2005. Symbiotic phosphate transport in arbuscular mycorrhizas. Trends in Plant Science 10: 2229.
  • Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M. 2004. Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 101: 62856290.
  • Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M. 2005. Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17: 22172229.
  • Klingner A, Bothe H, Wray V, Marner FJ. 1995. Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38: 5355.
  • Koske R. 1981. Multiple germination by spores of Gigaspora gigantea. Transactions of the British Mycological Society 76: 328330.
  • Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G. 2003. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 131: 952962.
  • Lapopin L, Gianinazzi-Pearson V, Franken P. 1999. Comparative differential RNA display analysis of arbuscular mycorrhiza in Pisum sativum wild type and a mutant defective in late stage development. Plant Molecular Biology 41: 669677.
  • Levy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T, Denarie J, Rosenberg C, Debelle F. 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 13611364.
  • Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R. 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630633.
  • Liu J, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ. 2003. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15: 21062123.
  • Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J. 2003. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637640.
  • Maier W, Hammer K, Dammann U, Schulz B, Strack D. 1997. Accumulation of sesquiterpenoid cyclohexonone derivatives induced by an arbuscular mycorrhizal fungus in members of the Poaceae. Planta 202: 3642.
  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ. 2001. A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Molecular Plant–Microbe Interactions 14: 11401148.
  • Marsh J, Schultze M. 2001. Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytologist 150: 525532.
  • Martin-Laurent F, Van Tuinen D, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S, Franken P. 1997. Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosis-regulated plant gene. Molecular General Genetics 256: 3744.
  • Matusova R, Rani K, Verstappen FW, Franssen MC, Beale MH, Bouwmeester HJ. 2005. The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiology 139: 920934.
  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GE, Long SR. 2004. A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proceedings of the National Academy of Sciences, USA 101: 47014705.
  • Mosse B. 1959. The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Transactions of the British Mycological Society 42: 273286.
  • Nagahashi G, Douds D. 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytologist 136: 299304.
  • Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M. 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. Plant Journal 42: 236250.
  • Novero M, Faccio A, Genre A, Stougaard J, Webb K, Mulder L, Parniske M, Bonfante P. 2002. Dual requierment of the LjSYM4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. New Phytologist 154: 741749.
  • Ohtomo R, Saito M. 2005. Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. New Phytology 167: 571578.
  • Olah B, Briere C, Becard G, Denarie J, Gough C. 2005. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant Journal 44: 195207.
  • Oldroyd GE, Downie JA. 2006. Nuclear calcium changes at the core of symbiosis signalling. Current Opinion in Plant Biology 9(4): 351357.
  • Oldroyd GE, Harrison MJ, Udvardi M. 2005. Peace talks and trade deals. Keys to long-term harmony in legume-microbe symbioses. Plant Physiology 137: 12051210.
  • Parniske M. 2000. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Current Opinion in Plant Biology 3: 320328.
  • Parniske M. 2004. Molecular genetics of the arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 7: 414421.
  • Paszkowski U, Jakovleva L, Boller T. 2006. Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. The Plant Journal 47(2): 165173.
  • Paszkowski U, Kroken S, Roux C, Briggs SP. 2002. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences, USA 99: 1332413329.
  • Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, Yoshida S, Parniske M. 2003. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiology 131: 866871.
  • Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585592.
  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M. 2001. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414: 462470.
  • Raven J, Smith S, Smith F. 1978. Ammonium assimilation and the role of mycorrhizas in climax communities in Scotland. Botanical Society of Edinburgh 43: 2735.
  • Ravenskov S, Jakobsen I. 1995. Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytologist 129: 611618.
  • Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million- year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences, USA 91: 1184111843.
  • Salzer P, Corbiere H, Boller T. 1999. Hydrogen peroxide accumulation in Medicago truncatula root colonized by the arbuscular mycorrhiza-forming fungus. Planta 208: 319325.
  • Schüssler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 14131421.
  • Smit P, Raedts J, Portyanko V, Debelle F, Gough C, Bisseling T, Geurts R. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 17891791.
  • Smith SE, Read DJ. 1997. Mycorrhizal symbiosis. San Diego: Academic Press.
  • Smith SE, Smith FA, Jakobsen I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133: 1620.
  • Solaiman MZ, Ezawa T, Kojima T, Saito M. 1999. Polyphosphates in intraradical and extraradical hyphae of an arbuscular mycorrhizal fungus, Gigaspora margarita. Applied Environmental Microbiology 65: 56045606.
  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M. 2002. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417: 959962.
  • Tadege M, Ratet P, Mysore KS. 2005. Insertional mutagenesis: a Swiss Army knife for functional genomics of Medicago truncatula. Trends in Plant Science 10: 229235.
  • Tamasloukht M, Sejalon-Delmas N, Kluever A, Jauneau A, Roux C, Becard G, Franken P. 2003. Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiology 131: 14681478.
  • Taylor J, Harrier LA. 2003. Expression studies of plant genes differentially expressed in leaf and root tissues of tomato colonised by the arbuscular mycorrhizal fungus Glomus mosseae. Plant Molecular Biology 51: 619629.
  • Walter MH, Fester T, Strack D. 2000. Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the ‘yellow pigment’ and other apocarotenoids. Plant Journal 21: 571578.
  • Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V. 2004. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Molecular Plant–Microbe Interactions 17: 13851393.
  • Westwood J. 2000. Characterization of the Orobanche-Arabidopsis system for studying parasite–host interactions. Weed Science 48: 742748.
  • Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F. 2003. Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Molecular Plant–Microbe Interactions 16: 306314.
  • Yokota T, Sakal H, Okuno K, Yoneyama K, Takeucji Y. 1998. Alectrol and Orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49: 19671973.
  • Zhu H, Riely BK, Burns NJ, Ane JM. 2006. Tracing non-legume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 172(4): 24912499.