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The Ecology of Plant-Microbial Mutualisms

Jeff Powell John Klironomos

Introduction

Roots as an Interface for Plant-Microbial Mutualisms

Mycorrhizal Symbioses

Symbioses Involving N-Fixing Organisms

Interactions among Mutualists

Interactions with Pathogens

Implications for Plant Populations and Communities Challenges in the Study of Interactions Conclusions

References and Suggested Reading introduction

Plants interact with a multitude of soil microorganisms in many different ways that have important consequences for plant growth and fitness. When microorganisms colonize and live within a host plant, these interactions are called "symbioses." In mutualistic symbioses, in which all partners benefit, the plant generally supplies its symbiont with photosynthetic C in exchange for a limiting resource (such as a nutrient or water) or protection from antagonists. Mycorrhizal fungi, the most ubiquitous of root-associated plant symbioses, attain photosynthetic C from the plant partner in return for enhanced nutrient and water uptake, resulting from an increased effective root surface area or increased uptake efficiency of certain nutrients. Mycorrhizal plants can have enhanced growth compared to uncolonized plants under low nutrient concentrations and under conditions where movement of nutrients in soil is reduced (e.g., drought). Leguminous plants form rhizobial symbioses with N2-fixing bacteria. Rhizobia infect the roots of the host plant, which then initiate the development of root nodules where rhizobia fix atmospheric N in exchange for photosynthetic C. Other N2-fixing bacteria, such as Frankia spp., enter into the same type of symbiosis as rhizobia, but only with a small group of nonleguminous plant species.

In practice, however, it is not always easy to observe benefit for all partners. The outcome of the symbiosis can range from mutualism to parasitism, and this can depend on interactions with the environment along spatial and temporal scales. One reason for this apparent contradiction is that we are not fully aware of the complete spectrum of ecological and evolutionary consequences of these so-called mutualistic relationships. Plants could derive indirect benefits from their microbial partners via effects on physical and biotic soil components, interactions with pathogenic microorganisms, or mediation of competition or herbivory. The long-term benefits of the symbiosis, derived at times of stress or disturbance, may outweigh negative consequences that are transient in nature.

In this chapter, we will continue to refer to symbioses, in general, that have potential to be mutualistic (mycorrhizal, rhizobial, and actinorrhizal symbioses) as "mutualistic," to distinguish them from symbioses that are obviously parasitic (involving plant pathogens). However, when describing specific types of mutualistic symbioses, they will be referred to as "symbioses."

roots as an interface for plant-microbial mutualisms

Mutualisms among plants and microorganisms are much more common below ground than above ground, even though diverse interactions between plants and microorganisms occur in both realms. Saprotrophs and plant-pathogenic microbes dominate in the phyllosphere and their community composition differs considerably from that of the rhizosphere (Lindow and Brandl, 2003). Mutualisms among plants and microorganisms are not entirely absent in the phylloplane but appear to be limited to a few that influence plant-herbivore interactions (e.g., Clay, 1990). Functional aspects might explain the apparent difference in the prevalence of mutualisms in the two environments. Soil is a heterogeneous environment in which mutualists aid plants in exploiting ephemeral resource patches by converting organic nutrients into usable inorganic forms and through the production of structures that extend the effective zone of water and nutrient uptake by roots. Above ground, the primary resources for which plants compete are light, pollinators, and seed dispersal agents. Some fungi manipulate plant morphology and, indirectly, pollinator behavior in order to facilitate dispersal of fungal gametes, but this interaction is detrimental to plant fitness (Roy, 1993). We are not aware of any evidence that the ability of plants to capture light is enhanced through the production of specialized structures by phyllosphere microorganisms. Plants that form mutualistic symbioses with soil microorganisms, however, can grow larger as a result of enhanced nutrient uptake, allowing these plants to compete more vigorously for light and, possibly, achieve greater fitness.

mycorrhizal symbioses

Mycorrhizas are symbioses between nonpathogenic fungi and the roots of the host plant. The mycorrhizal symbiosis is ubiquitous, is present in nearly all plant species, and can provide mutual benefits to the participants. Mycorrhizal classification is based on anatomical features of the root-fungus interface and the taxonomic classification of the fungus and host plant (Table 10.1). Peterson et al. (2004) presented a detailed overview of the different mycorrhizal types and many spectacular images of plant, fungal, and mycorrhizal structures. Arbuscular mycorrhizal (AM) fungi occur in symbioses with plant taxa belonging to >90% of vascular and nonvascular plant families. The taxonomic diversity of AM fungal species is relatively low (estimates range from ~150 to 200 spp.) and confined to the Phylum Glom-eromycota (formerly the Order Glomales within the Zygomycota) based on 18S rRNA sequence data. Ectomycorrhizal (EM) fungi form symbioses with several gymnosperm and angiosperm species and are taxonomically diverse, with approximately 6000 species; Kendrick (2001) notes 74 genera in the Basidiomycota and 16 genera in the Ascomycota. Other types of mycorrhizas are more restricted with regard to the phylogenetic diversity of the plant species in which associations are formed. Ectendomycorrhizas can be found in roots of the conifer genera Larix and Pinus. Arbutoid and ericoid mycorrhizas occur for ericaceous plants, although the former can be found in some of the Pyrolaceae (wintergreen family) and the latter can also occur in some bryophytes (nonvascular plants such as mosses, liverworts, and hornworts). Monotropoid and orchid mycorrhizas form only in roots of the plant families Monotropaceae (e.g., Indian pipe, pinedrops) and Orchidaceae, respectively; the fungal partner, however, may be able to form other types of mycorrhizal associations with other plants. Plants that associate in monotropoid mycorrhizas are achlorophyllous and nonphotosynthetic (termed mycoheterotrophic) and rely on the fungus to form additional mycorrhizal associations, often of different types, with other plants in order to attain photosynthate. Orchid mycorrhizas function in a similar way and the presence of the fungal symbiont is required prior to seed germination and seedling establishment.

The formation of mycorrhizal symbioses is complex and involves recognition, infection, and then internal colonization of roots. The process differs depending on the type of mycorrhiza (Figs. 10.1 and 10.2). AM fungi can colonize host plants via intact mycelial networks, hyphal fragments, or individual spores. Root exudates stimulate hyphal branching and directed growth. Once a hypha contacts a root, the fungus forms an appressorium from which it attempts infection. If successful, hyphae penetrate epidermal cells, enter the cortex, and grow intercellularly (or intracellularly

TABLE 10.1 The Classification of Mycorrhizal Associations Based on Fungal Morphology (Modified from Dalpe, 2003)
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