Cyanobacterial-Plant Symbioses
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Cyanobacterial-Plant Symbioses DAVID G. ADAMS, BIRGITTA BERGMAN, S.A. NIERZWICKI-BAUER, A.N. RAI AND ARTHUR SCHÜßLER
Introduction Cyanobacteria are unique in the wide range of symbiotic associations they form with eukaryotic hosts including plants, fungi, sponges and protists (for reviews, see Adams [2000], Rai et al. [2000], Rai et al. [2002b], and Bergman et al. [2003]). Cyanobacteria are photoautotrophs, and in many cases facultative heterotrophs and nitrogen fixers, and can provide nonphotosynthetic hosts with both nitrogen and carbon. Even if the benefit to the host is clear, that to the cyanobacteria is less obvious. They often receive carbon from photosynthetic hosts, but they are capable of carbon fixation themselves. Perhaps a more likely advantage is protection from predation and from environmental extremes, such as high light intensity and desiccation, in the enclosed environment provided by the host. The cyanobacterial symbionts of plants all possess at least two essential characteristics—the ability to differentiate heterocysts, which are specialized nitrogen-fixing cells (for a review, see Adams and Duggan, 1999), and hormogonia, which are short, gliding filaments that lack heterocysts and provide a means of dispersal (Campbell and Meeks, 1989; Meeks, 1990; Meeks, 1998; Johansson and Bergman, 1994; Bergman et al., 1996). The hormogonia serve as the infective agents in most plant symbioses; some plants enhance their chances of infection by producing chemical signals that stimulate hormogonia formation and also chemoattractants that direct hormogonia into the plant tissue. Cyanobacteria are not restricted to the roots of plants but can infect thalli, stems and leaves. The major hosts are bryophytes (see the section Cyanobacteria in Symbiosis with Hornworts and Liverworts in this Chapter), the angiosperm Gunnera (see the section Interactions in the Nostoc-Gunnera Symbiosis in this Chapter), the aquatic fern Azolla (see the section The AzollaAnabaena Symbiosis in this Chapter), fungi (forming lichens; see the section Cyanolichens in this Chapter), the fungus Geosiphon (see the section The Geosiphon Pyriformis—Nostoc
Endocyanosis and its Relationship to the Arbuscular Mycorrhiza (AM) in this Chapter), and cycads (for a review of cycad symbioses, see Costa and Lindblad, 2002).
SECTION I: Cyanobacteria in Symbiosis with Hornworts and Liverworts Bryophyte Symbioses The division Bryophyta consists of the Hepaticae (liverworts), the Anthocerotae (hornworts), and the Musci (mosses), all of which are small, nonvascular terrestrial plants, some of which form epiphytic or endophytic associations with cyanobacteria, primarily of the genus Nostoc. Only the liverwort and hornwort associations will be dealt with here, but the cyanobacteria-moss associations have been well reviewed recently (Solheim and Zielke, 2002). In their natural habitat the liverworts and hornworts grow as a prostrate gametophyte thallus a few centimeters in length, attached to the substratum
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