Plant Cell Responses to Arbuscular Mycorrhizal Fungi: Getting to the Roots of the Symbiosis.

Since their colonization of terrestrial ecosystems, plants have developed numerous strategies to cope with the diverse bi? otic and abiotic challenges that are a consequence of their sedentary life cycle. One of the most successful strategies is the ability of root systems to establish mutualistic and reciprocally beneficial symbiotic relationships with microorganisms. Mycorrhizas, the intricate associations roots form with specific fungal groups, are by far the most frequent of these and rep? resent the underground absorbing organs of most plants in nature (Gianinazzi-Pearson, 1984). Through their function in the efficient exploitation of soil mineral resources and their bioprotective role against a number of common soilborne pathogens, mycorrhizas are instrumental in the survival and fitness of many plant taxa in diverse ecosystems, including many crop species (reviewed in Allen, 1991; Bethlenfalvay and Linderman, 1992). Several kinds of mycorrhizal associations can be distin? guished according to their morphology and the plant and fungal taxa concerned. They fail almost exclusively into two broad groups: (1) the ectomycorrhizas of woody Angiosperms and Gymnosperms, in which Basidiomycetes, Ascomycetes, or Zygomycetes develop intercellular hyphae from a mycelial sheath covering the surface of short lateral roots; and (2) the endomycorrhizas, characterized by intraradical mycelium growth and intracellular fungal proliferation, which are formed by Basidiomycetes in the Orchidaceae (orchidoid mycorrhiza), Ascomycetes in the Ericales (ericoid mycorrhiza), and Zygomy? cetes in most other terrestrial plant taxa (arbuscular mycorrhiza; reviewed in Harley and Smith, 1983). Plant compatibility with mycorrhizal fungi is a generalized and ancient phenomenon. Species in >80? /o of extant plant families are capable of establishing arbuscular mycorrhiza (AM), and fossil evidence suggests that symbioses of this kind existed >400 million years ago in the tissues of the first land plants (Pirozynski and Dalpe, 1989; Remy et al., 1994). As such, the ability of plants to form AM must be under the control of mechanisms that have been conserved in new plant taxa as they appeared during evolution. This compatibility also implies that selective recognition processes in plants discriminate be? tween beneficial and harmful microorganisms and that the essential genetic determinants for AM establishment are com? mon to an extensive part of the plant kingdom. In contrast to their extremely wide host range and despite their ancient origins, only six genera of fungi belonging to the order Glomales of the Zygomycetes have evolved the ability to form AM (Morton and Benny, 1990). Interactions between an AM fungus and a plant begin when a hypha from a ger? minating soilborne spore comes into contact with a host root. Thi step is followed by induction of an appressorium, from which an infection hypha penetrates deep into the parenchyma cortex (Figure 1A), where interand intracellular proliferation of mycelium is intense. Here, fungal development culminates in the differentiation of intracellular haustoria, known as arb scules (Figure 1B). These fungal structures, which establish large surface of contact with the plant protopiast, are attrib? uted a key role in reciprocal nutrient exchange between the plant cells and the AM fungal symbionts (Smith and Smith, 1990). However, arbuscules are ephemeral structures, and an individual arbuscule reaches full development within several days, after which it begins to senesce (Alexander et al., 1988). AM development continues within a root system as the fungus spre ds to newly emerging roots. In this way, fungal coloniza? tion occurs concomitantly in different roots in an unsynchronized manner.