Fungus-Bacterium Symbionts Promote Plant Health and Performance

Anton de Bary (1831Bary ( -1888) ) initially presented the term 'symbiosis ' in 1879 (8), which implies an intimate relationship between organisms of two or more species with a broad spectrum of beneficial, neutral, or harmful relationships.Microbial symbioses are ubiquitous in nature (53); from protists to humans, all plants and animals are inhabited by microbes that comprise the majority of global biodiversity (6).In the past two decades, an increasing number of studies have shown that many plant-associated fungi, including foliar ascomycetes (1), dark septate endophytes (DSEs) (18), arbuscular mycorrhizal fungi (AMF) (4, 47), ectomycorrhizal basidiomycetes (3,19), and sebacinalean endophytes (40), as well as a few phytopathogenic fungi (27, 31) and neutral fungi living in soil ecosystems (30,37,39,51), harbor phylogenetically diverse bacteria in both epihyphal and endohyphal forms.These bacteria are affiliated to Alpha-, Beta-, Gammaproteobacteria, Mollicutes, Bacillaceae, Chitinophaga, and others, and are known to alter host morphology, sporulation, metabolite production, and even other properties involved in interactions with plants (16,36,41,49).However, symbiotic partners are generally regarded as separate individuals, which has limited the comprehensive assessment of the interaction mechanisms within these holobiont systems (6, 52).To date, the best-studied fungus-bacterium symbiont system is the phytopathogenic fungus Rhizopus microsporus and its endosymbiotic bacterium Burkholderia rhizoxinica (31), in which the host is associated with early diverging lineages of terrestrial fungi within Mucoromycotina (5,42).An interesting multilateral microbial interaction involving B. rhizoxinica was shown to cause rice seedling blight (30).R. microsporus was considered to be the causative agent of rice seedling blight and the antimitotic agent, rhizoxin, was used to bind β-tubulin in plant tissues as a virulence factor (38, 45).However, it became evident that this virulence factor was produced not by R. microsporus itself, but by the endosymbiotic bacterium B. rhizoxinica (32,33).Furthermore, the sporeformatting capacity of R. microsporus was completely dependent on the presence of B. rhizoxinica, which increased the fitness of both partners for the survival and dispersion of their population (34).This mutually beneficial relationship between a bacterium and fungus has also been reported between the phytopathogenic bacterium Ralstonia solanacearum, which contributes to chlamydospore formation in 34 species of fungi across three diverse taxa (Ascomycetes, Basidiomycetes, and Zygomycetes) (43).In this case, R. solanacearum produces the secondary metabolite 'ralsolamycin' using a non-ribosomal peptide synthetase-polyketide synthase hybrid, which contributes to