Microbial Interactions in the Rhizosphere .1 Bacteria

The bacterial community in the rhizosphere promotes the production and germina-tion of spores and hyphal growth of arbuscular mycorrhizal (AM) fungi. In addigermina-tion to plant roots, spores (Bharadwaj et al. 2008; Cruz and Ishii 2012) and extraradical mycelium (Mansfeld-Giese et al. 2002) of AM fungi also associate predominantly with bacteria in the mycosphere. A bacterial community in the rhizosphere not only associates with the extraradical mycelium but also with spores of AM fungi. The association of bacteria with AM fungal spores is related to the size and surface roughness of the outer spore wall (Bharadwaj et al. 2008). Some bacterial taxa are exclusively restricted to a few mycorrhizal isolates, whereas others are extensively found in the mycosphere of several AM fungal taxa (Rillig et al. 2005). Bacterial association with AM fungal spores induces germination and establishment of mycorrhizal association under unfavorable conditions (Xavier and Germida 2003;

Hildebrandt et al. 2006). This is often due to the bacterial secretion of volatile com-pounds, rupturing of the spore wall, and nutrient acquisition (Ruiz-Lozano and Bonfante 2000). Studies on AM fungal interactions with rhizosphere bacteria sug-gests that it may be either positive (Abdel-Fattah and Mohamedin 2000) or negative (Amora-Lazcano et al. 1998). Though AM fungal processes are enhanced by bacte-ria, some studies showed prohibitory activity of bacteria on AM fungal growth (Azcón 1989). This might be due to specificity in bacterial species and AM fungi.

The AM fungi form a bridge between the root and soil (Bethlenfalvay and Schüepp 1994); in turn, the AM fungi affect the composition of bacterial communities in the rhizosphere (Linderman 1988; Paulitz and Lindennan 1991).

The fungi and bacteria in the rhizosphere are also involved in plant resistance to various types of stresses (Linderman 2000; Han and Lee 2005). The bacterial popu-lation in the rhizosphere mainly includes the beneficial associative N2-fixing bacte-ria (Subba Rao et al. 1985), PGPR (Meyer and Linderman 1986), and phosphate-solubilizing bacteria (PSB) (Toro et al. 1997; Bonfante and Anca 2005).

However, bacterial populations also vary under the influence of different plant and AM fungal species. The size and the composition of bacterial populations in the rhizosphere depend on the quantity of the root exudates (Azaizeh et al. 1995) and the competition for carbon source (Christensen and Jakobsen 1993). The carbon source is the major energy provider for various microbial communities, and its ben-eficial effect on plants has been well established. Mycorrhiza-associated bacteria also succeed to establish from AM fungal exudates (Toljander et al. 2007), which facilitate nutrition for both plant and fungal partners as well as protection from root pathogens (Larsen et al. 2015).

5.2.4.2 Fungi and Phytopathogens

In defense mechanism, mycorrhizal species directly or indirectly protect the host plant in the ecosystem. Such direct mechanisms include the production of physical structures (e.g., mantle by ectomycorrhizal fungi), secretion of toxic compounds against the pathogens, providing mechanical strength to the root system, and

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activating the host plant production of compounds like salicylic and jasmonic acids (Artursson et al. 2006; Finlay 2008). Indirect mechanisms include protection of the host plant by changing the microbial community, root exudates, and stimulation of suitable antagonistic microorganisms (Zarnea 1994; Zamfirache and Toma 2000;

Miransari 2011). For example, the architecture of AM fungi-colonized roots is greatly modified. The mycorrhizal roots are highly branched, short and thick with reduced specific root length, resulting in conditions that are unfavorable for patho-genic microorganisms (Berta et al. 1993).

Studies have shown that rhizosphere bacteria could suppress plant pathogens (Berg and Hallmann 2006; Shehata et al. 2016). The rhizosphere fluorescent Pseudomonas strains produce the antibiotic 2,4-diacetylphloroglucinol (DAPG) that protects the plants against Gaeumannomyces graminis var. tritici. The bacte-rium produced significantly large amounts of DAPG in the presence of soluble car-bon exuded by Rhizophagus intraradices and offered a sustainable strategy for plant protection (Siasou et al. 2009). The AM fungi and pathogen share common resources in the root system (Whipps 2004). But, competition in the endorhizosphere would arise when the carbon source from the host plant becomes scarce, resulting in the reduction in the colonization by AM fungi (Wehner et al. 2009). The intensity of the pathogenic effect on the host plant is reduced when multiple AM fungi species colo-nize the root system compared to colonization by an individual AM fungus (Jaiti et al. 2007). Bacteria associated with AM fungi enhance the plant resistance against pathogens through their antagonistic activity. For example, bacteria isolated from the spores of AM fungi inhibited the growth of Ganoderma boninense, which causes basal stem rot disease in oil palm (Elaeis guineensis) (Bakhtiar et al. 2010).

5.2.4.3 Microfauna

The rhizosphere contains microfauna like nematodes, protozoa, and arthropods.

Most of these organisms are involved in the complex system of the food web that shares the plant resources (Pierret et al. 2007; Raaijmakers et al. 2009). Among these organisms, nematodes are free-living, eukaryotic invertebrates that feed on bacteria and fungi and some existing as plant parasites (Tiberius and Cătălin 2011).

Nematodes cause diseases in plants by entering the root and establishing a stable feeding location within the root system (Badri et al. 2009). The interactions between mycophagous nematodes and mycorrhizal fungi result in the reduction of the extraradical hyphal production that can indirectly affect plant growth and yield (Giannakis and Sanders 1990; Khan 1993). However, to reduce the negative effect of nematode infestation, plants generally adapt various strategies like the associa-tion with mycorrhizal fungi, increased nutrient uptake, and structural and physio-logical changes in the root system (Schouteden et al. 2015). Even though AM fungi induce tolerance against adverse effects on host plants, several factors like host plant and AM fungal and nematode species determine the nature of interactions between AM fungi and nematodes (Hol and Cook 2005). Recently, Banuelos et al.

(2014) found that roots of Impatiens balsamina inoculated with a consortium of AM fungi (11 species) reduced the root-knot disease caused by the nematode Meloidogyne incognita than the plant inoculated with Glomus coronatum alone.

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However, the concentrations of antioxidant in shoots and phenolic compounds in roots were higher for AM fungal consortium inoculated plants and showed defense activity against the root-knot nematodes (Banuelos et al. 2014).

In addition to fungi, bacteria are also involved in the control of plant parasitic nematodes in soil. The nematophagous bacteria are differentiated based on their mode of activity and mostly belong to the genera Bacillus, Pseudomonas, and Pasteuria (Li et al. 2015). These bacteria have been isolated from soil, host tissues, and nematodes (Kerry 2000; Meyer 2003). The nematophagous bacteria affect nem-atodes through various mechanisms like producing toxins and antibiotics/enzymes, competing for nutrients, and inducing systemic resistance in plants (Tian et al.

2007). Some of the major rhizobacteria like Azotobacter and Gluconacetobacter also affect the plant parasitic nematodes. The antagonistic effect of bacteria against nematodes in the soil is due to the secretion of volatile compounds like ammonia and fatty acids which inhibit the juveniles of nematodes (Bansal and Bajaj 2003). A study by Bansal et al. (2005) in cotton showed that the antagonistic effect of Gluconacetobacter diazotrophicus (=Acetobacter diazotrophicus) on the root-knot nematode, M. incognita, was through suppression of egg hatching.

Abundance of bacterial grazers like the nematodes and protozoa significantly alters the bacterial community composition and their activities in the rhizosphere (Bonkowski 2004). Such changes in bacterial activities and populations are shown to significantly affect plant growth (Kreuzer et al. 2006; Mao et al. 2007). In a boreal forest, ectomycorrhizal fungus was shown to affect bacterial community composition, subsequently altering food resources for protozoa (Timonen et al.

2004). Both ectomycorrhizal fungi and protozoa can complement each other in ren-dering benefit for plants. For example, Bonkowski et al. (2001) showed that the protozoa increased the N availability to Norway spruce (Picea abies) seedlings, whereas the ectomycorrhizal fungus Paxillus involutus increased the availability of P. The excretion of N after the consumption of bacterial biomass by protozoans increases the N availability for direct or mycorrhizal mediated uptake by plants (Bonkowski 2004). In a microcosm study, Koller et al. (2013) showed that protozoa mobilized N by stimulating microbial activity in degradation of organic matter. The N released was transferred to the roots of Plantago lanceolata via hyphae of R.

intraradices. Though different microorganisms in the rhizosphere complement each other from the plant’s perspective, a competition for plant carbohydrates does exist between these microorganisms. A substantial reduction in the numbers of protozoa has been reported by Rønn et al. (2002) in AM-colonized pea plants. The presence of protozoa also affects root architecture and biomass in rice plants (Herdler et al.

2008). The influence of AM fungi on changes in the microbial community of the rhizosphere tends to vary with the growth phase of the plant. For example, in pea plants the presence of the AM fungus R. intraradices decreased the number of pro-tozoa during late vegetative phase prior to flowering, but the negative effect on protozoa decreased during flowering and pod formation (Wamberg et al. 2003).

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