with legumes and may be at a selective advantage over other strains infecting the same host because they avoid the energetically costly process of N2 fixation. This is important from an agronomic standpoint: non-N2-fixing strains may outcompete mutualistic strains for plant resources, resulting in reduced N2 fixation at the whole plant level. Compounding this issue, tillage can homogenize distributions of rhizo-bial communities, potentially increasing the frequency of crop plants infected by non-N2-fixing strains (West et al., 2002). Plant controls on this interaction are not absent, however; sanctions imposed by the host on these detrimental strains, as a result of reduced O2 supply to non-N2-fixing nodules, limit the fitness of cheating rhizobia and effectively stabilizes the mutualism (Kiers et al., 2003).

interactions among mutualists

None of the groups discussed above occur in isolation with the plant host; the activities of these organisms overlap spatially and temporally. Competition for infection sites, locations on the surface of roots where infection occurs and colonization begins, and for habitat within roots is a likely candidate for direct interactions among symbionts, while enhanced nutritional status of the host as a result of one symbiont may indirectly influence the formation and functioning of other symbioses.

Interactions among symbionts of plants during and following the colonization of root tissue influence the resulting composition of the endophytic microbial community. Plant populations and communities can support high levels of AM fungal species diversity, and multiple AM fungal species can be present on the same plant. However, the presence of more than one AM fungal species on individual root segments is thought to be uncommon (Wilson and Tommerup, 1992) and AM fungal species differ in their ability to colonize host roots in the presence of another AM fungal species (Lopez-Aguillon and Mosse, 1987). These observations suggest that, in addition to a variety of abiotic factors (P concentration, pH, water potential, and temperature), competition may be an important factor structuring AM fungal communities. The degree to which plant nutrition is improved varies among species and isolates of AM fungi (Wilson and Tommerup, 1992); therefore, the results of competitive interactions among AM fungi during the colonization of a host plant will have important consequences for the subsequent health of that individual plant, possibly with implications at community and ecosystem levels.

Klironomos (2003) demonstrated the varying responses of several plant species when individually colonized by different AM fungal species. The growth of individual plant species ranged from highly positive to highly negative relative to uninoc-ulated control plants and was inconsistent across species of AM fungi (Fig. 10.5), suggesting a range of symbiotic outcomes from mutualistic to parasitic in arbuscular mycorrhizas. The mechanism behind this range of functional responses is not understood, but may be related to the degree of colonization and trade-offs associated with the extent of the hyphal network extending into the soil. AM fungal species vary in the biomass of extraradical hyphae produced; fungal associates that produce a larger hyphal network occupy a greater volume of soil and increase the potential for nutrient uptake but demand more photosynthetic C than associates that produce a smaller extraradical hyphal network. Therefore, plant growth responses will depend on the overall benefits of expanding access to nutrients relative to the costs of maintaining the hyphal network. Differences in nutrient requirements and uptake ability among plant species likely contribute to the idiosyncratic nature of this interaction. As a result, stoichiometric responses in plant communities may be indirectly influenced by competitive interactions among AM fungal species during root colonization.

The spatial and temporal succession of EM fungi in a transplanted birch (Betula spp.) forest in Scotland has been well studied and suggests that interactions among EM fungi may influence the structure of EM communities (Deacon and Fleming, 1992). Diversity of fruit bodies increased progressively for up to at least 14 years. Fruiting bodies of EM species, observed near the base of the trees in previous years, appeared farther away from the tree base in successive years, being replaced in their previous distributions by fruiting bodies of previously unobserved species. Lactarius pubescens and Hebeloma velutipes were associated with younger roots and were thus found farther away from the tree base, while a Cortinarius sp. and Russula spp. were found associated with older roots near the tree base. A similar succession may occur within AM fungal communities. Johnson et al. (1991) observed that, along a field-to-forest chronosequence, Acaulospora laevis, Acaulospora scrobiculata, Acaulospora spinosa, Glomus aggregatum, Scutellospora calospora, Scutellospora erythropa, and Scutellospora persica spores were associated with early successional sites, while Acaulospora elegans, Gigaspora gigantea, Glomus ambisporum, Glomus fasciculatum, and Glomus microcarpum spores were associated with late successional sites; however, more study is required to determine if these apparent successional patterns are due to AM fungal interspecific interactions or just a shift of the AM fungal community in response to the changing plant community and/or abiotic characteristics of the chronosequence.

Competition among rhizobia has been studied with the goal of determining the necessary conditions for inoculant strains to nodulate hosts in the presence of indigenous strains, which may be inferior N2 fixers. Several factors affect the outcome of competition for nodulation, including abundance; soil fertility, pH, temperature, and moisture; presence of predators, parasites, and antagonists; and pesticide use (Dowling and Broughton, 1986). The relative attractiveness of specific sugars, amino acids, and other components of the root exudates from host and nonhost plants differs among species of rhizobia. Strains also differ in motility, affecting the speed at which individual rhizobia encounter and nodulate the host. The presence of blocking strains, those that initiate infection thread formation and root hair curling but do not complete nodulation, can prevent competent rhizobia from nodulating the host plant.

Dual colonization of plants by AM fungi and rhizobia, in legumes, or Frankia, in nonlegumes, is common and has additive effects on nodulation, AM fungal colonization, and plant nutrition (Azcon-Aguilar and Barea, 1992; Dar et al., 1997; Jha et al., 1993; Siddiqui and Mahmood, 1995). The high P requirements in nodules during N2 fixation (due to the upward of 25 to 30 mol of ATP required per mole of N2 fixed) and the N demanded by AM fungi during chitin synthesis suggest a physiological basis for this correlation between the presence of nodules and arbuscular mycorrhizas in root systems. Kucey and Paul (1982) observed that AM beans supported greater nodule biomass and greater rates of N2 and CO2 fixation than nonmycorrhizal beans. The greater rate of C utilization by nodules in AM beans (12% of total fixed C vs 6% in nonmycorrhizal beans) was offset by enhanced CO2 fixation. Therefore, requirements for potentially limiting nutrients (C, N, P) in each individual symbiosis may be overcome by the presence of additional symbioses on the same host, enhancing the levels at which all processes occur and increasing the benefits to all participants in the tripartite symbiosis. The consequence of this tripartite symbiosis for the outcome of competitive interactions with plant species that participate in only one symbiosis is currently not known.

Molecular and biochemical investigations of tripartite symbioses have revealed a great deal of similarity between mycorrhizal and rhizobial symbioses, despite differences in morphological characteristics. Prior to colonization, signaling molecules derived from the AM fungal mycelium (putative "Myc factors") trigger similar responses in plants as to analogous molecules of rhizobial origin ("Nod factors"), as indicated by patterns of flavonoid accumulation (Vierheilig, 2004). In legumes, several of the same genes are induced during interactions with either rhizobia or AMF, and most nonnodulating mutants are also unable to form symbioses with AM fungi (Albrecht et al., 1999). Recent research has uncovered divergence between AM fungi and rhizobia in terms of plant gene regulation, but also common patterns of gene induction between an AM fungus, G. mosseae, and an endophytic, plant-growth-promoting bacterium, Pseudomonasfluorescens (Sanchez et al., 2004). The authors suggested that the observed patterns of divergence and similarity may be due to anatomical aspects of the symbioses, with nodule formation initiated by Sinorhizobium melloti requiring much more reorganization of root structures than during colonization by G. mosseae and P. fluorescens.

interactions with pathogens

A disease is a deviation from the normal physiological status of an organism or its parts, resulting from the activity of biotic and abiotic factors, such that its vital functions are impaired. A variety of pathogenic soil microorganisms can cause diseases in plants, including viruses, bacteria, fungi, oomycetes, and nematodes. The interactions between several pathogens and plants are similar to the mutualisms discussed above in that they represent intimate relationships between organisms in which one colonizes the intra- or intercellular space within the roots, they can involve significant structural reorganization of root anatomy, and they require molecular signaling by both of the participants during the processes of recognition, infection, and colonization of roots. However, interactions resulting in disease are geared toward maximizing the fitness of one group while negatively affecting the host. Given the diversity of plant pathogens, no attempt will be made here to discuss their individual life history characteristics, except in the context of their interactions with mutualistic plant associates and the resultant effects on plant population and community dynamics. For an introduction to these pathogens and their importance in plant pathology see Bruehl (1987).

Biological control of disease-causing organisms using plant mutualists has been, and continues to be, a goal of some researchers studying these mutualisms. As with most biological control agents, field trials frequently provide inconsistent and/or inconclusive results, although there have been several observations of reductions in disease-causing organisms and disease levels in crop plants following inoculation with plant mutualists. Laboratory studies suggest several mechanisms by which mutualists of plants reduce disease in plant hosts: directly, via antagonism or antibiosis, or indirectly, via enhanced nutritional status of the host, competition for infection sites or limiting nutrients in the rhizosphere, alteration of root morphology, and induction of host defenses. Most studies investigating interactions between disease-causing organisms and plant associates and their consequences for host health have focused on plant-pathogenic (PP) fungi and nematodes. Few studies have focused on interactions with bacterial and viral pathogens or root herbivores. Some AM fungi have been observed to reduce infection of soybean, eggplant, cucumber, mulberry, and grape by Pseudomonas spp. AM hosts tend to exhibit elevated viral loads and greater levels of viral diseases, hypothesized to be due to higher P levels in AM plant tissue improving host quality and facilitating viral growth (Xavier and Boyetchko, 2002). In addition, a few studies have shown reduced survivorship of larval insects feeding on AM roots relative to those feeding on nonmycorrhizal roots (see Gange and Bower, 1996, for a brief review).

There are several papers that chronicle the effects of EM and AM fungi on populations of PP fungi and disease severity. Dehne (1982) summarized the literature pertaining to the impact of mycorrhizal fungi on PP fungi and found that there was evidence for both increased and decreased levels of PP fungi and plant disease in the presence of mycorrhizal fungi. Increased disease levels were suggested to be due to enhanced nutritional status of the host, making it a higher quality resource for the pathogenic fungus. Reduced disease levels might be explained by enhanced host vigor, interference with pathogen infection, or competition for habitat within roots. For EM fungi, there is also the possibility of direct chemical antagonism of pathogenic fungi (Duchesne et al., 1988).

Interactions between AM fungi and PP nematodes appear to be symmetrical, with the outcome dependent on the order of infection. The two groups appear to be incompatible, competing for habitat within the roots or indirectly altering the quality and/or quantity of habitat available for the other group. AM fungi are unable to colonize root segments parasitized by endoparasitic nematodes. AM structures are usually not found in galled tissues inhabited by galling nematodes, whether live, inactive, or dead, suggesting that physiological changes involved in the formation of root galls make these roots inhospitable to AM fungi. Ectoparasitic nematodes inflict damage to root tissue such that AM fungal colonization of these damaged roots is reduced.

PP nematodes have, on occasion, been observed to infect AM roots. The colonization of roots by AM fungi can lead to reduced populations of PP nematodes and lowered disease severity, although this interaction is often cultivar-specific and dependent on soil nutrient levels. Nematode life history is also important in this interaction, with AM fungi reducing population growth of sedentary endoparasitic nematodes but not migratory endoparasitic nematodes in a meta-analysis of 17 independent studies (Borowicz, 2001). AM fungi may increase plant tolerance of PP nematodes; nematode infection results in local alterations to root architecture that interfere with nutrient uptake, which may be mediated at the whole plant level by AM fungal colonization of other parts of the root system. However, at least some benefits of AM fungal colonization are likely associated with mechanisms other than increased plant vigor since benefits to plants in the presence of AM fungi are not negated by increasing nutrient availability (Ingham, 1988). In a few cases, increased populations of PP nematodes were observed to be associated with AM fungal colonization; this positive response may be a result of AM fungi increasing root mass and, thus, habitat availability for PP nematodes. Therefore, to properly interpret the impact of AM fungal colonization on root pathogens, estimates of PP nematode abundance need to be standardized with estimates of root mass.

Newsham et al. (1995) proposed a dichotomy in the type of benefit derived by plants from AM symbioses based on root system architecture (Fig. 10.8). Highly branched root systems, which are highly susceptible to pathogen infection, benefit from AM fungi occupying locations in the roots where pathogens could otherwise

Poorly branched

Root system architecture *- Intermediate -

Highly branched

Poorly branched

Highly branched

FIGURE 10.8 Hypothetical P uptake (dashed diagonal line) and pathogen protection (solid diagonal line) benefits of AM fungi for plant species with poorly branched to highly branched root system architectures. The dashed horizontal line represents other functions of the AM association not defined by root system architecture. (Reprinted from Newsham, Fitter, and Watkinson, 1995, copyright 1995, with permission from Elsevier.)

FIGURE 10.8 Hypothetical P uptake (dashed diagonal line) and pathogen protection (solid diagonal line) benefits of AM fungi for plant species with poorly branched to highly branched root system architectures. The dashed horizontal line represents other functions of the AM association not defined by root system architecture. (Reprinted from Newsham, Fitter, and Watkinson, 1995, copyright 1995, with permission from Elsevier.)

colonize. Poorly branched root systems, which are less susceptible to pathogen infection, but occupy a relatively low volume of soil, benefit primarily as a result of P uptake by AM fungi. The authors use three pieces of evidence to support their model: (1) a positive correlation between P inflow and specific root tip number (a measure of root system branching) for seven forb and grass species; (2) a positive correlation between P uptake and percentage root length colonized by AM fungi in two plant species with poorly branched root systems, Hyacinthoides non-scripta and Ranunculus adoneus; and (3) the observation that a Glomus sp. provides pathogen protection to Vulpia ciliata, an annual grass with a highly branched root system, yet does not enhance P uptake. However, further tests of this model have not been conducted.

Although less studied than mycorrhizal fungi for their potential to reduce pathogen loads on host plants, rhizobia can reduce infection rates by, and enhance host tolerance to, pathogenic fungi. This enhanced tolerance is probably due to greater plant health and the stimulation of defense compounds, but possibly also to production of antifungal compounds. For instance, rhizobitoxine plays a role in nodule development, but has also been observed to inhibit growth of Macrophomina phaseolina in culture plates (Chakraborty and Purkayastha, 1984). Field trials using selected species of Rhizobium and Bradyrhizobium resulted in reduced infection rates of host and nonhost crops (including nonleguminous crops) by M. phaseolina, Rhizoctonia solani, and Fusarium spp. (Ehteshamul-Haque and Ghaffar, 1993). Fungal growth was reduced in culture, suggesting that competitive or antagonistic interactions between rhizobia and fungi may have played an important role in reducing infection rates. Rhizobia have been observed to be stimulated by and migrate toward roots of nonlegumes, perhaps explaining the reduced infection rates of non-leguminous crops.

implications for plant populations and communities

Much of the study of plant-microbial mutualisms has focused on interactions at the level of individual plants, yet the effects of these mutualisms are also observed in plant populations and communities. Plant population dynamics are driven by a number of factors (e.g., competition with other plants, herbivory, resource availability) that are mediated or strengthened by mycorrhizal fungi and rhizobia. Plants that engage in symbioses with N-fixing bacteria are able to thrive under conditions of low N availability but also foster conditions, through the process of N2 fixation, that eventually allow for the growth of other plant species and facilitate succession. Complex interactions among plants and AM fungi influence the structure of plant communities; increasing AM fungal species diversity enhanced plant species diversity in abandoned agricultural fields, likely due to interactions between individual plant and fungal species modifying competitive interactions among plants (van der Heijden et al., 1998).

Recent research has been focused on elucidating the roles of plant-microbial mutualisms in invasion by nonnative species. Nonnative plant species can use mycorrhizal fungi to facilitate invasion of plant communities. For example, AM fungi improve the competitive ability of invasive spotted knapweed (Centaurea maculosa) against some native grass and forb species (Callaway et al., 2004). Other nonnative plants disrupt mycorrhizal mutualisms to prevent recruitment of native plants. For example, garlic mustard (Alliaria petiolata) produces allelochemicals that have negative effects on AM fungal communities, reducing growth of native seedlings (Stinson et al., 2006). In some cases, the establishment of nonnative plants is limited by the absence of mutualists in the nonnative range. Establishment in New Zealand and South Africa of nonnative Pinus spp. is limited to areas where suitable EM fungi have either invaded or been introduced, and invasiveness of actin-orrhizal plants is linked to their ability to form symbioses with native Frankia spp. (Richardson et al., 2000).

In some cases, our basic understanding of plant-microbial mutualisms has already been applied for practical purposes. There has been some success in the use of these organisms, either inundatively in small-scale plantings or as inoculants prior to the distribution of seedlings or rootstock to growers. Strains of Bradyrhizobium japonicum are commercially available as an inoculant to promote nodulation of legume field and greenhouse crops. Inoculation of plant seedlings with mycorrhizal fungi prior to transplantation can be a useful technique to enhance productivity of orchard crops and to promote reforestation and revegetation efforts, such as those for mine spoils. Also, with a greater understanding of how symbionts of plants respond to disturbances of anthropogenic origin (e.g., climate change, N deposition, introduction of invasive plant species), it may be possible to predict how the structure and functioning of natural and agricultural ecosystems will be influenced by these disturbances and to take the appropriate steps to prevent or mediate their effects.

challenges in the study of interactions

A major problem associated with studying interactions involving plant-microbial mutualisms is our inability to monitor accurately and precisely the population dynamics of soil and root-associated microorganisms (see Chaps. 3 and 4). Indirect measures of interaction strength focus on functional responses, such as disease severity or growth response of the plant following inoculation with different combinations of microbes. Direct measures, such as counting bacteria or measuring fungal biomass, are problematic because they tend to overestimate viable population size. Culture-dependent methods work only for the small fraction of soil microorganisms that can be cultured on artificial media. AM fungi are obligate symbionts and can be cultured only on living roots, so abundance is estimated by the extent to which fungi colonize roots, which provides no means of determining the actual

TABLE 10.2 Comparison of Culture-Based and Molecular Techniques for Estimating the Effect of Glomus intraradices on the Abundance of Fusarium solani f. sp. phaseoli

Soil compartment


F. solani abundance (CFU X 1000/g soil)

F. solani abundance (^g DNA/g soil)


Glomus present



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