J. M. Barea

Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved

Abstract Biological control of plant pathogens is currently accepted as a key practice in sustainable agriculture because it is based on the management of a natural resource, i.e. certain rhizosphere organisms, common components of ecosystems, known to develop antagonistic activities against harmful organisms (bacteria, fungi, nematodes etc.). Arbuscular mycorrhizal (AM) associations have been shown to reduce damage caused by soil-borne plant pathogens. Although few AM isolates have been tested in this regard, some appear to be more effective than others. Furthermore, the degree of protection varies with the pathogen involved and can be modified by soil and other environmental conditions. This prophylactic ability of AM fungi could be exploited in cooperation with other rhizospheric microbial angatonists to improve plant growth and health. Despite past achievements on the application of AM in plant protection, further research is needed for a better understanding of both the ecophysiological parameters contributing to effectiveness and of the mechanisms involved. Although the improvement of plant nutrition, compensation for pathogen damage, and competition for photosynthates or colonization/infection sites have been claimed to play a protective role in the AM symbiosis, information is scarce, fragmentary or even controversial, particularly concerning other mechanisms. Such mechanisms include (a) anatomical or morphological AM-induced changes in the root system, (b) microbial changes in rhizosphere populations of AM plants, and (c) local elicitation of plant defence mechanisms by AM fungi. Although compounds typically involved in plant defence reactions are elicited by AM only in low amounts, they could act locally or transiently by making the root more prone to react against pathogens. Current research based on molecular, immunological and histochemical techniques is providing new insights into these mechanisms.

Vesicular-Arbuscular Mycorrhizae as Modifiers of Soil Fertility

It has become clear that microbial activity must be considered a key component among those conferring “soil fertility,” i.e., the ability of a given soil to support plant development and nutrition (Pauli, 1967). The major components interacting to determine “soil fertility” are depicted in Figure 1. Accordingly, “fertility” can be considered an inherent property of a given soil. However, the plant itself is able to modify soil fertility in two different ways. One is based on the “rhizosphere effect” exerted by the plant, which can alter the fluxes of energy and the supply of substrates for soil microorganisms. The other way is based on the inherently different growth rates and metabolism of the different plant species that are known to “change” the capacity of the soil to provide each particular plant with nutrients (Hayman, 1975).

Arbuscular Mycorrhizas in Sustainable Soil-Plant Systems

The significance of mycorrhizas in sustainable agriculture was highlighted several years ago (Mosse 1986) when it was realized that the stability of these systems was endangered. More recently, Bethlenfalvay and Linderman (1992) have re-emphasized the importance of this plant-fungus symbiosis in the maintenance of sustainability in agricultural production. Due to their ability to alleviate the effects of plant stress (Jeffries 1987; Barea 1991), in this review we wish to discuss the role of arbuscular mycorrhizas as essential components of sustainable ecosystems in general, including agriculture. We will also consider some of the constraints on the practical application of mycorrhizal technology in these situations, but first it is necessary to briefly define the concept of sustainability and the problems endangering sustainable systems.

Stimulation of Plant Growth and Drought Tolerance by Native Microorganisms (AM Fungi and Bacteria) from Dry Environments: Mechanisms Related to Bacterial Effectiveness

In this study we tested whether rhizosphere microorganisms can increase drought tolerance to plants growing under water-limitation conditions. Three indigenous bacterial strains isolated from droughted soil and identified as Pseudomonas putida, Pseudomonas sp., and Bacillus megaterium were able to stimulate plant growth under dry conditions. When the bacteria were grown in axenic culture at increasing osmotic stress caused by polyethylene glycol (PEG) levels (from 0 to 60%) they showed osmotic tolerance and only Pseudomonas sp. decreased indol acetic acid (IAA) production concomitantly with an increase of osmotic stress (PEG) in the medium. P. putida and B. megaterium exhibited the highest osmotic tolerance and both strains also showed increased proline content, involved in osmotic cellular adaptation, as much as increased osmotic stress caused by NaCl supply. These bacteria seem to have developed mechanisms to cope with drought stress. The increase in IAA production by P. putida and B. megaterium at a PEG concentration of 60% is an indication of bacterial resistance to drought. Their inoculation increased shoot and root biomass and water content under drought conditions. Bacterial IAA production under stressed conditions may explain their effectiveness in promoting plant growth and shoot water content increasing plant drought tolerance. B. megaterium was the most efficient bacteria under drought (in successive harvests) either applied alone or associated with the autochthonous arbuscular mycorrhizal fungi Glomus coronatum, Glomus constrictum or Glomus claroideum.B. megaterium colonized the rhizosphere and endorhizosphere zone. We can say, therefore, that microbial activities of adapted strains represent a positive effect on plant development under drought conditions.

Saprophytic Growth of Arbuscular Mycorrhizal Fungi

Strictly speaking the title of this chapter is a contradiction. If “saprophytic growth” is growth exhibited by an organism in a free-living status, it is obvious that this term cannot apply to arbuscular mycorrhizal fungi (AMF) as none of the 130 species of AMF (Walker 1992) have yet been successfully cultured axenically. These fungi have a low, or negligible, saprophytic ability and can apparently produce viable propagules only upon the biotrophic colonization of a susceptible host root. They are thus considered physiologically obligate symbionts and the related literature reflects the failure to grow them on synthetic media (Azcon-Aguilar and Barea 1992). There are descriptions, however, of limited saprophytic development of AMF which takes place either in soil, prior to any contact with the host root, or even “in vitro” (Azcon-Aguilar and Barea 1985; Koske and Gemma 1992). It is this saprophytic growth which will be discussed in this chapter.

The rhizosphere of mycorrhizal plants

Providing that appropriate carbon substrates are available, microbial communities are able to develop a range of activities which are crucial in maintaining a biological balance in soil (Bowen and Rovira 1999), a key issue for the sustainability of either natural ecosystems or agroecosystems (Kennedy and Smith 1995). Soil-borne microbes have a particular microhabitat in which to flourish. In particular, they are bound to the surface of soil particles or found in soil aggregates, while others interact specifically with the plant root system (Glick 1995). The root-soil interface is actually a dynamic changing environment, a microcosm where microorganisms, plant roots and soil constituents interact (Lynch 1990; Azcon-Aguilar and B area 1992; Linderman 1992; B area 1997, 2000, Kennedy 1998; Bowen and Rovira 1999; Gryndler 2000), to develop what is known as the rhizosphere (Hiltner 1904). The rhizosphere, therefore, is the zone of influence of plant roots on the associated microbiota and soil components, and is clearly a different physical, chemical and biological environment from the bulk soil (Bowen and Rovira 1999), where an altered microbial diversity and increased activity and number of microorganisms is characteristic (Kennedy 1998).Actually, the structure and diversity of populations of fluorescent pseudomonads associated with roots were shown to differ significantly from those of soil populations. Rhizosphere and non-rhizosphere populations could be discriminated on the basis of their ability to use specific organic compounds (Lemanceau et al. 1995; Latour et al. 1996), to mobilize ferric iron (Lemanceau et al. 1988) or to reduce nitrogen oxides (Clays-Josserand et al. 1995).