Life cycles

LIFE CYCLE, SIGNIFICANCE, AND STRUCTURES OF ARBUSCULAR MYCORRHIZAE

A symbiotic association of a fungus and roots has been discovered in Monotropa hypopitys L. by Franciszek Kamienski (Kamienski 1881), a Polish mycologist. Later, Frank (1885) coined the term “mycorrhiza” to the association.

Professor Franciszek Kamienski

(1851-1912)

Arbuscular mycorrhizae form or are considered to form fungi of thirteen of the fourteen genera of the phylum Glomeromycota (Blaszkowski 2003; Schüßler at al. 2001). The fourteen genus of the phylum, Geosiphon contains only G. pyriformis, which produces endocytosymbioses with photoautotrophic prokaryotes (Schüßler 2002; Schüßler and Kluge 2001).

Arbuscular mycorrhizal fungi are obligate biotrophs feeding only on the products of photosynthesis of their alive plant hosts. Generally, the fungi are not specialized to their potential hosts, although some plant species more favour the development of these fungi than others (Blaszkowski 1993; Smith and Read 1997). The fungi belong to the most commonly occurring soil microorganisms of the world and are associated with at last 80% of plants of the Earth (Gianinazzi and Gianinazzi-Pearson 1986), including angiosperms, gymnosperms and pteridophytes having roots, as well as the gametophytes of some mosses, lycopods, and Psilotalus, which do not have true roots (Smith and Read 1997).

Literature data indicate that arbuscular mycorrhizal fungi increase the root absorptive area and hence the plant nutrition (Bieleski 1973), influence succession of plant communities (Janos 1980), their competitiveness (Allen and Allen 1984; Fitter 1977) and phenology (Allen and Allen 1986), equalize the level of nutrition of co-existing plants by formation of hyphal bridges transferring nutrients between them (Newman 1988), and improve soil structure through binding sand grains into aggregates by extraradical hyphae (Koske et al. 1975; Sutton and Sheppard 1976). Additionally, arbuscular mycorrhizal fungi increased the tolerance of plants to heavy metals (Dehn and Schüepp 1989; Griffioen and Ernst 1989), water stresses (Stahl and Smith 1984), as well as pathogenic fungi and nematodes (Schönbeck 1978). The requirement of arbuscular fungi for up to 20% of host photosynthate for establishment and maintenance is well accepted (Graham 2000; Jakobsen and Rosedahl 1990).

Arbuscular mycorrhizae consist of intra- and extraradical structures. The intraradical structures are arbuscules, vesicles, and intraradical hyphae. The extraradical structures are extraradical hyphae, spores, and auxiliary cells, the latter are formed only by members of the genera Gigaspora, Pacispora, and Scutellospora.

Haustorium-like arbuscules are the main sites of nutrient exchange between a plant host and a fungus (Gianinazzi et al. 1979). They are formed within the cells of the inner root cortex (Mosse 1973) and are indicators of active mycorrhizae.


In roots of Plantago lanceolata			In roots of Zea mays

Arbuscules differ in morphology, depending on the generic affiliation of the arbuscular fungal species (Morton 2000). Fungi of the genera Acaulospora, Archaeospora, Ambispora, Diversispora, Entrophospora, Glomus, Intraspora, Kuklospora, Pacispora, and Paraglomus produce arbuscules with cylindrical or slightly flared, narrow trunks, whose branches progressively taper in width towards tips. Arbuscules of members of the genera Gigaspora and Scutellospora generally have swollen trunks with branches tapering abruptly at tips. The characters of mycorrhizae of Otospora bareai, the only member of the genus Otospora, have not been recognized to date (Palenzuela et al. 2008).


In roots of P. lanceolata	In roots of Z. mays

Globose or ovoid, thin-walled vesicles are storage organs filled with lipids and glycolipids (Mosse 1981). They origin by an intercalary or terminal swelling of a mycorrhizal intraradical hypha of an arbuscular fungus. Vesicles may be inter- or intracellular and may be found in both the inner and the outer layers of the cortical parenchyma. In Glomus spp., vesicles generally are ellipsoid, whereas those of Acaulospora, Entrophospora, and Kuklospora highly vary in shape and frequently have knobs and concavities on their surface (Morton 2000). Not all Glomus spp. form vesicles (Morton and Redecker 2001). They are never produced by members of the genera Gigaspora and Scutellospora. Members of the genera Archaeospora, Intraspora, and Paraglomus rarely produce vesicles or do not form them at al.


In roots of Plantago lanceolata

Inter- and intra-cellular hyphae in roots also contain storage materials and take part in transportation of the substances absorbed by extraradical hyphae from the soil to arbuscules or directly to root cells of the host plant (Bieleski 1973). Intraradical hyphae may be straight or with H- or Y-shaped branches. They may also form coils, whose frequency of occurrence depends on their location in a root and the generic affiliation of the arbuscular fungal species (Morton 2000). Generally, coils more abundantly occur at entry points. Intraradical hyphae of Glomus spp. are infrequently coiled in the other regions of a mycorrhizal root. In contrast, coils produced by species of the other genera of arbuscular fungi usually are abundant and evenly distributed along mycorrhizal roots.

Arbuscular mycorrhizae also differ in the degree of evenness of distribution along roots and the intensity of staining. The distribution of mycorrhizal structures of members of the genera Ambispora, Archaeospora, Acaulospora, Diversispora, Entrophospora, Intraspora, Kuklospora, and Paraglomus is patchy, whereas that of mycorrhizae of the genera Gigaspora, Glomus, Pacispora, and Scutellospora usually is continuous. The intensity of staining of mycorrhizae of fungi of the genera Ambispora, Archaeospora, Diversispora, Intraspora, and Paraglomus is very faint to faint, those of Acaulospora, Entrophospora, and Kuklospora faint to moderate, those of Glomus dark, and those of Gigaspora, Pacispora, and Scutellospora very dark (Blaszkowski, pers. observ.; Morton and Redecker 2001; Sieverding and Oehl 2006).

Extraradical hyphae significantly increase the absorptive area of roots (Bieleski 1973), form hyphal bridges transferring nutrients between co-occurring plants (Newman 1988), and bind sand grains into aggregates (Koske and Polson 1984). They also are important fungal propagules colonizing plant roots (Jasper et al. 1989, 1991).

Auxiliary cells are swollen structures produced terminally by extraradical hyphae of only Gigaspora, Pacispora, and Scutellospora spp. The cells are spiny in Gigaspora spp., and those of species of the genera Pacispora and Scutellospora are smooth or knobby (Blaszkowski 2003; Morton 2002).

Spores are multinucleate single cells mainly produced blastically at the tip of sporogenous hyphae continuous with mycorrhizal extraradical hyphae. Sometimes, spores also occur inside roots (e. g., Koske 1985), on the soil surface (Berch and Fortin 1983), and on plants or their decaying fragments (Blaszkowski 1998). The number of spores produced depends on, e. g., the fungal species (Blaszkowski 1993), the plant species and its variety (Blaszkowski 1993; Hetrick and Bloom 1986), soil fertility and fertilizer application (Hayman 1970), host phenology (Giovannetti 1985), light intensity (Daft and El Giahmi 1978), and competitive abilities of co-occurring arbuscular fungal species (Gemma et al. 1989). The reproduction of arbuscular fungi is stated to be clonal (Morton 2000) and the role of spores is to sequester the genetic information of a given fungal species, disperse this information to new habitats, and initiate new individuals spatially separated from the parent organisms (Morton 1993). Although Tommerup and Sivasithamparam (1990) observed zygospore formation in Gigaspora decipiens Hall & Abbott, this type of spore origination was not confirmed in other studies. Because many components of the subcellular structure of spores are stable in different environmental conditions, they are the most important structures considered in classification of arbuscular fungi.

The patterns of spore development differ significantly in the genera of the phylum Glomeromycota recognized. They along with properties of mycorrhizae formed by members of the genera are characterized below.

• Development of spores and properties of mycorrhizae of fungi of the genus Acaulospora

• Development of spores and properties of mycorrhizae of fungi of the genus Archaeospora

• Development of spores and properties of mycorrhizae of fungi of the genus Ambispora

• Development of spores and properties of mycorrhizae of fungi of the genus Diversispora

• Development of spores and properties of mycorrhizae of fungi of the genus Entrophospora

• Development of spores and properties of mycorrhizae of fungi of the genus Gigaspora

• Development of spores and properties of mycorrhizae of fungi of the genus Glomus

• Development of spores and properties of mycorrhizae of fungi of the genus Intraspora

• Development of spores and properties of mycorrhizae of fungi of the genus Kuklospora

• Development of spores and properties of mycorrhizae of fungi of the genus Pacispora

• Development of spores and properties of mycorrhizae of fungi of the genus Paraglomus

• Development of spores and properties of mycorrhizae of fungi of the genus Scutellospora

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