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The obligately biotrophic relationship of the arbuscular mycorrhizal (AM) fungus in the root cortex and the regulation of colonization by carbon supply are strongly suggestive that mycorrhizas interact directly with root pathogens that have similar trophic requirements. Aphanomyces euteiches is a biotrophic pathogen that attacks root cortical tissues of pea and other legumes. The potential exists for resource competition between the symbiotic fungus and pathogen, leading to the reduction of each other’s colonization and reproduction when they coinhabit roots. Larsen & Bodker (2001) use fungal specific neutral lipid fatty acids as indicators of infection and energy status of Glomus mosseae and A. euteiches in pea roots to measure the interaction of these trophically similar fungi. The presence of G. mosseae does not affect root rot severity of A. euteiches but reduces the level of energy reserves and sporulation of the pathogen in the root cortex. Concomitantly, the biomass and energy reserves of the AM fungus are reduced as well. In many studies, mycorrhizal mediated effects on host nutrition indirectly influence the outcome of these interactions because they have been often studied in phosphorus-deficient soils. Larsen & Bodker’s (2001) study is one of the first attempts to resolve the direct trophic interactions based on competition for C and possibly other nutrients between the symbiont and other organisms colonizing the root cortex and mycorrhizosphere.
‘In 1981, Schenck commented that the answer as to whether or not mycorrhizas can control root diseases would “require a crystal ball”’
Can mycorrhizas control root diseases?
Modern study of arbuscular mycorrhizas began with plant pathologists, who viewed roots primarily as hosts for parasitic and pathogenic fungi and nematodes. Their research was among the first to define the normative state of the root cortex as the colonization site for ‘vesicular–arbuscular’ mycorrhizal fungi, as well as soilborne fungi, bacteria and nematodes. J. W. Gerdemann and his students (Gerdemann, 1975) conducted pioneering studies in the 1960s to demonstrate the functional role of external hyphae of these fungi in the acquisition of plant nutrients, especially in low P availability soils. Plant growth response to inoculation at low nutrient supply soon stimulated interest in AM fungi as biocontrol and stress-reducing agents, especially after initial studies showed heightened resistance of roots to infection by fungal pathogens, such as Thielaviopsis basicola, and the root knot nematode, Meloidogyne incognita (Schoenbeck, 1979). In sharp contrast to the positive benefits in these pathosystems, susceptibility to some pathogens (e.g. Phytophthora spp.) was increased for certain hosts (Ross, 1972).
Only limited evidence has emerged that the AM fungi compete directly with other biotrophic organisms for the same cortical space and resources. Other mechanisms invoked are as diverse as the results of the interactions, but are often cited as structural and biochemical resistances induced by the AM fungus in the root cortex, or as attributable to alterations in the mycorrhizosphere microflora (Lindermann, 1994). In a definitive review of the early literature on ‘VA mycorrhizas’, Gerdemann (1975) issued a caveat: ‘in studies of the effect of VA mycorrhizas on disease it should be determined whether changes in resistance are caused by increased nutrient absorption or if the effect is more direct’. In the 1970s, Gerdemann’s student, Schenck (1981), conducted research on mycorrhizal interactions with a diversity of root-infecting fungi and nematodes. But by 1981, Schenck remarked in apparent frustration: ‘the answer to “can mycorrhizas control root diseases” would require a crystal ball or a soothsayer!’
Another of Gerdemann’s students, Rhodes (1980) wrote in a prescient review of the benefits of AM fungi in agricultural systems that ‘root pathogens should in most instances be regarded as pathogens of mycorrhizae, since it is the mycorrhizal root that is encountered by pathogens in most cases. Pathogenic microorganisms have coevolved with VA fungi and have been exposed to the mycorrhizal condition of roots over thousands of centuries. The very fact that root diseases still occur indicates that such pathogens have successfully adapted to parasitize mycorrhizal hosts. Nevertheless, any role that mycorrhizal fungi may play in restricting or enhancing disease development is deserving of attention.’
Defining mechanisms unrelated to improved phosphorus nutrition
Molecular probes provide unprecedented opportunity for comparative study of expression of plant resistance in AM fungal vs pathogen interactions. Thus far, the evidence that arbuscular mycorrhizal colonization conditions systemic resistance to other pathogens, such as through up-regulation of pathogenesis-related proteins, remains controversial (Blee & Anderson, 2000). Apparently, the expression of genes encoding plant defenses is weak when AM fungi colonize roots and, at later stages, colonization even suppresses plant defense-related genes. Given the low specificity of AM fungi, it is not unreasonable to expect suppression of general host defenses. Systemic priming of root tissues to form structural and biochemical barriers is usually dependent on a high level of root colonization and cannot always be verified as mycorrhiza specific because the P status of the plant before pathogen challenge is unknown (Cordier et al., 1998).
Smith (1988) provided the first well defined framework for predicting interactions in the host–mycorrhiza–pathogen triangle based on trophic relationships. He proposed that the potential for AM fungi to affect host–pathogen relationships by mechanisms unrelated to improved P nutrition is greatest for obligate biotrophs (e.g. endoparasitic nematodes) and least for facultative saprotrophic fungi (e.g. certain species of Fusarium, Phytophthora and Rhizoctonia). In most instances, direct mycorrhizal effects are most clearly evident for measurements of parasitic nematode development. He judged that AM fungi are probably affecting host–pathogen relations by physiologically altering the host or competing for space or host resources. Smith noted that experimental data are scant for host resource competition between pathogens and AM fungi and encouraged investigations of C as well as P flow between root-inhabiting organisms that have obligate requirements for host-derived C.
Resource availability in the root cortex vs the mycorrhizosphere
More evidence is emerging that intraradical hyphae of AM fungi efficiently take up sugars from the root apoplast and, conversely, the host functionally regulates colonization through resource availability in the root cells and rhizosphere (Graham, 2000). Studies utilizing nuclear magnetic resonance (NMR) spectroscopy confirm that intercellular AM hyphae rapidly assimilate hexoses, but extramatrical hyphae are incapable of taking up sugars (Douds et al., 2000). Inadequate P nutrition in the roots increases C-release into the apoplast from root cells because of altered plasmalemma structure as a consequence of phospholipid depletion (Ratnayake et al., 1978). Mycorrhizal colonization becomes self-limiting because improved phosphate availability in roots provided by the mutualistic response restores membrane integrity and even restricts C flux into the root apoplast and rhizosphere (Graham et al., 1981, J. H. Graham, unpublished) (Fig. 1). Intercellular mycorrhizal colonization acts further to reduce sugar leakage from the root cortex compared with the cortex of nonmycorrhizal roots below the critical P concentration in tissues that affects membrane permeability (Fig. 1: ≤ 0.11% P in citrus leaves; Ratnayake et al., 1978). With attainment of P sufficiency in tissues, mycorrhizal mediated decrease in sugar availability from roots is coincident with reduction in pathogen colonization and damage (Graham & Menge, 1982; Graham & Egel, 1988).
The inability of external hyphae to assimilate sugars diminishes the role of extramatrical hyphae as sites for C interactions. Only a small fraction (< 2%) of the total below-ground labelled 14C in mycorrhizal citrus roots is released into the rhizosphere and an even smaller fraction (< 0.2%) is attributable to release into the mycorrhizosphere (Eissenstat et al., 1993). Populations and metabolic activity of Pseudomonas fluorescens are reduced in the hyphosphere of G. intraradices compared to nonrhizosphere soil (Ravnskov et al., 1999). Thus, microorganisms compete intensely for C in the hyphosphere as this arena is perhaps even more growth-limiting than rhizosphere soil.
Functional role of mycorrhizas in relation to root pathogens in the field
Field evidence remains unconvincing that AM fungi substantially improve P relations and growth of temperate crops in agroecosystems (McGonigle & Miller, 1996). Even in natural systems, plants with fibrous root architecture show only marginal reduction in P acquisition when their mycorrhizas are impaired by fungicides (West & Fitter Watkinson, 1993). This directs attention to other functional attributes of mycorrhizas that might confer competitive advantage for plants to maintain the symbiosis in the absence of substantial P benefit. In a temperate grassland ecosystem, direct interaction of AM fungi, not P uptake, reduces the deleterious effects of the root pathogenic fungi and thereby may increase plant fecundity (Newsham et al., 1994). Newsham et al. (1995) propose that root protection by AM fungi may be as important as nutritional benefits in natural systems, though they do not specify a mechanism for the interaction of mycorrhizas and root-infecting fungi. Their conclusion is derived from study of AM function in only a few plant species under natural conditions, thus, the broader significance of direct mycorrhiza–pathogen interactions requires much greater support from field experimentation.
Refined understanding of the exchanges of P, C and other nutrients in arbuscular mycorrhizas and the mycorrhizosphere permits us better to answer the question ‘what do root pathogens see in mycorrhizas?’Larsen and Bodker (1994) employ neutral lipid fatty acids for more precise quantification of the interaction of a root pathogen and an AM fungus than here-to-fore possible. Moreover, these fatty acids give estimates of the ‘energy status’ of the interacting fungi, as the signature acids comprise more than 50% of the storage lipid in each fungus. The concomitant reduction in each fungus’s biomass and energy status provides preliminary evidence for competition for resources between the obligate symbiont and the biotrophic pathogen. The specificity of signature fatty acids for evaluation of direct interactions of selected microbes and plant species should greatly facilitate studies, particularly under field conditions.
Florida Experiment Station Journal Series No. R-07911