Abstract
The mutualistic symbiosis of most land plants with arbuscular mycorrhizal (AM) fungi has been shown to favor mineral and water nutrition and to increase resistance to abiotic and biotic stresses. The main mechanisms involved in the control of the disease symptoms and intraradical proliferation of soilborne phytopathogens are due to root colonization with AM fungi. The role of the rhizobacteria is shown to be specifically associated with extraradical network of the AM and mycorrhizosphere. The mycorrhizosphere can form a favorable environment for microorganisms which have potentiality to act antagonistic to pathogen abundance. It makes an additional advantage in identifying rhizobacteria from AM fungi structures or mycorrhizosphere, which often lead to the isolation of organisms having strong properties of antagonism on various soilborne pathogens. The ability of AM fungi to control soilborne diseases is mainly related to their capacity to stimulate the establishment of rhizobacteria against the favorable environment of pathogen within the mycorrhizosphere prior to the root infection. Recent advancement in scientific research has provided more clear picture in understanding the mechanisms involved in AM fungi/rhizobacteria interactions. Herein, this chapter includes the mechanisms of the AM fungi-mediated biocontrol, interactions between AM-associated bacteria and AM fungus extraradical network, AM-associated bacteria and biocontrol activities and unfavorable zone to pathogen development: the mycorrhizosphere.
Keywords
- AM-associated bacteria (AMB)
- arbuscular mycorrhizal fungi
- biocontrol
- mycorrhizosphere
- soilborne pathogens
1. Introduction
A majority of land plants in nature are growing symbiotically in relationship with AM fungi. This relationship is well established with the roots of these plants. Soil exploration by the external mycelium of AM fungi increases the nutrient absorptive root surface area and thus favors the host plant in access to nutrients and water [1, 2]. Moreover, as the largest component of the soil microbial biomass [3, 4], AM fungi form widespread mycelial networks within the soil atmosphere, and hyphae harbour important sites for interactions with other soilborne microorganisms. The constricted zone adjacent to soil-living roots is called the rhizosphere [5]. It is characterized by increased microbial activity and by a specific microbial community structure [6, 7]. Along with root-AM fungi associations, factors influencing the community structure and the biomass of soil microorganisms lead to the establishment of a zone called mycorrhizosphere [8, 9, 10, 11, 12]. The zone of soil influenced by only AM fungi is called mycosphere. In the mycorrhizosphere, AM fungi structures and various rhizobacteria (AM fungi-associated rhizobacteria or AMB, e.g.
The beneficial effects of AM fungi on the host plant physiology, in the decrease of intraradical and mycorrhizosphere population and in the decrease of disease symptoms of soilborne pathogens were reported in many biological systems, probably due to synergistic mechanisms [23, 24, 25]. The use of chemical pesticides are now avoided and not advocated in fields due to its risks to human health and the environment, and thus the implementation of sustainable agriculture has become essential in crop industry. The perception of the mechanisms involved in the AM fungi-mediated biocontrol will allow to maximize the performance of management of such sustainable agroecosystems and thus authorize the use of AM fungi and its benefits [26]. The main mechanisms involved in the biological control of diseases induced by soilborne phytopathogens start after root colonization with AM fungi especially due to its association with rhizobacteria which constitutes major element for this biocontrol.
2. Mechanisms of the AM fungi-mediated biocontrol
Reduction in the detrimental effects of soilborne pathogens after root colonization with AM fungi was described a long time ago [27, 28] and has been observed on various fungi, stramenopiles, nematodes and bacteria [12, 29]. Carlsen et al. [30] reported the total check of infectivity caused by
Further, higher concentrations of phenolic acids could be detectable in plants which are colonized with AM fungi species subjected for biocontrol activities. Accumulation of jasmonic acid involved in the rhizobacteria-mediated ISR in mycorrhizal roots could be related to the systemic pathogen biocontrol [38, 39]. Cordier et al. [40] identified local cell wall modifications (callose accumulation around arbuscule-containing cortical cells of tomato roots). The synthesis of constitutive and additional isoforms of defense-related enzymes (e.g. chininases, chitosanases, β-1,3-glucanases, peroxidases and SOD) has also been locally detected in mycorrhizal roots [41, 42, 43]. The level of production of these enzymes or flavonoids was reported to be unrelated to the capacity of biocontrol of the AM fungi species [30, 44]. The transcript profiling and real-time quantitative PCR used to explore the transcriptional changes triggered by AM fungus colonization revealed a complex pattern of local and systemic changes in gene expression in roots of
The most commonly documented response to AM fungi colonization is an increase in phosphorus nutrition to the host plants which subsequently imparts more dynamic and more resistant properties against pathogen invasion. However, AM fungi-mediated biocontrol is unrelated to the soil phosphorus (P) availability and to the phosphorus status in plant tissues, thus possibly more dependent on other mechanisms [46, 47, 48, 49].
Arbuscular mycorrhizal fungi normally compete for space and nutrients with soilborne pathogens within the zone of mycorrhizosphere and the host roots. Larsen and Bodker [50], using signature fatty acid profiles, demonstrated the decrease in biomass and energy reserves of both
The extraradical network formed by
In vitro results of impact studies of the exudates of extraradical AM fungi network or by the mycorrhizal roots on pathogens are in contradiction. Crude extracts from the extraradical network of
Another example can be seen in the exudates of tomato roots which are reported to double the microconidia germination of
From the above it is evident that none of the cited mechanisms is involved in the AM fungus-mediated biocontrol, but it has been shown to happen in every plant-fungi system. These mechanisms might act in synergistic way with each other, with one mechanism becoming preponderant depending on the environmental conditions and the plant cultivar-pathogen/AM fungus strain. However, the mechanism related to the capacity of interaction of AM fungi with other soil microorganisms can significantly be attributed as one of the main reasons involved in the control of soilborne diseases.
3. Interactions between AM-associated bacteria and AM fungus extraradical network
The bacterial communities associated with various AM fungal inoculum or spores have been reported to differ from one another based on their association as one found in mycorrhizal isolate and others largely encountered in the mycosphere [15]. The species assemblages of cultivable bacteria from surface-disinfected spores of
The roots colonized with
Arbuscular mycorrhizal fungi can stimulate the growth of rhizobacteria by providing nutritional resource through the release of exudates. Exudates collected from tomato roots which were colonized by
The reduction in exudation through defoliation of pea plants did not change the PCR-DGGE profile of rhizosphere bacteria, while missing and supplementary bands were observed from the rhizosphere of plants which were pre-colonized with
4. AM-associated bacteria and biocontrol activities
Most of AM-associated bacteria (AMB) described so far in detail showed antagonistic characteristics towards soilborne pathogens or behaved as mycorrhization helper [16]. Similar studies have been performed by various researchers in aiming to identify AMB with biocontrol activities. A bacterial strain of
Under compartmentalized growth system, Mansfeld-Giese et al. [78] identified
5. Unfavorable zone to pathogen development: the mycorrhizosphere
The mycorrhizosphere has been hypothesized to comprise of favorable surroundings for the growth and development of microorganisms which works antagonistic to soilborne pathogens proliferation. Undeniably, co-culture of the non-mycorrhizal species (e.g.
The mycorrhizosphere influenced by the rhizobacteria + AM fungus + root tripartite associations presents specific characteristics, in which individual factor influences the others’ growth and health. Remarkably in the presence of glycoproteins such as glomalin, AM fungi favor the formation of aggregates which provide stable microsites favorable to root and microbe establishment [84, 85]. The AM fungi extraradical network also constitutes specific microsites which favor the growth of some bacteria. Among different plant growth-promoting rhizobacteria, P-solubilizing and N-fixing bacteria has been reported for more efficient synergistic interaction with AM fungi. Increased P and N availability to the plants promotes its growth and probably favors its capacity to counteract pathogen impact [11, 86, 87, 88].
Plant growth-promoting rhizobacteria can also display biocontrol properties and impact pathogen proliferation through direct liberation of toxic compounds or by competing for space and nutrients, reduction of Fe and Mn availability, modification of the plant hormone balance and stimulation of plant defense mechanisms [89, 90]. A synergistic or additive impact by dual inoculation of AM fungi with rhizobacteria in controlling pathogens reflects the dependence of biocontrol properties on the combinations of bacterial and fungal species used, nutritional status in soil and probably other environmental conditions [87].
Reduction in gall formation and nematode multiplication (which are usually responsible for causing root rot in chick pea) was significantly reported in the tomato plants when its roots were inoculated together with
6. Conclusion
The competence of AM fungi to control disease symptoms and the intraradical and rhizosphere proliferation of soilborne pathogens is multifaceted and influenced by different mechanisms possibly acting in a synergetic way with each other. Among these mechanisms, the capacity of extraradical network of AM fungi to stimulate beneficial microorganisms is possibly a strongly responsible factor involved. Different bacteria with high capacities of antagonistic activities against several soilborne pathogens have been reported within AM fungal extraradical structures and in the mycorrhizosphere of several AM fungi species. The AM fungi-mediated biocontrol activities can not solely be due to the AM fungus function but also related strongly to the capacity of the AM fungi to constitute an environment which favors the establishment of rhizobacteria with potential biocontrol abilities.
Acknowledgments
PKS, and MS thank the SERB, Department of Science and Technology, Government of India, for awarding Fast Track Young Scientist and for the financial assistance.
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