Endofungal bacteria as symbionts residing in the fungal mycelium and spores were first describes as Bacteria-Like Organisms (BLOs) in 1970 s (Mosse 1970). The bipartite relationship between fungi and terrestrial plants on the rhizosphere becomes complicated tripartite interaction as the discovery of endobacteria. In the last decade, research focussed on the endobacteria in arbuscular mycorrhizal fungi (Bonfante and Anca 2009; Naumann et al. 2010; Salvioli et al. 2015), in ectomycorrhizal basidiomycete fungus (Bertaux et al. 2005), and in rice pathogenic fungus Rhizopus microsporus (Partida-Martinez and Hartweck 2005; Moebius et al. 2014). We extended the former work to explore and establish a model tripartite symbiosis system among the Sebacinalean fungus Piriformospora indica, the Alphaproteobacterium Rhizobium radiobacter and a broad spectrum of plants. The free-living bacterial strain R. radiobacter F4 (RrF4) showed similar colonization pattern as its fungal host P. indica in plant roots. RrF4 cells heavily colonizedthe root maturation zone, embedded in dense polysaccharides biofilms and were interwoven in cellulose fiber-like structures on the root surface. Thereafter, RrF4 cells entered into inner tissue through lateral root emergence, root hair protrusion and cracks on the root, proliferated in the intercellular space in the rhizodermal and cortical layers into the central vascular system. Nevertheless, RrF4 only invaded and colonized the dead root cells instead of inducing plant host cell death. The systemic resistance mediated by RrF4 is based on the jasmonate-based ISR pathway, and defense gene expression resembles that observed with P. indica (Gleaser et al. 2015). The increased amount of endobacteria R. radiobacter in plant roots inoculated with P. indica, and the significantly reduced amount of endobateria in the sub-cultured P. indica that was isolated from plant roots indicate endobacteria R. radiobacter obtain more benefit from the tripartite relationship with both fungal and plant hosts than in the bipartite relation with only the fungus. It is an open question whether the endobacteria R. radiobacter released from P. indica into root tissue during the fungal colonization on plant. It was not successful to cure P. indica from the endobacteria through antibiotics treatment and single protoplast cultivation. However, we obtained a P. indica culture with reduced amount of endobacteria R. radiobacter, and partially cured P. indica showed low beneficial activity on plants. We presume the endobacteria R. radidobacter inside P. indica are at a stationary phase, which is the reason for the low number, small size and resistance to antibiotics in axenic culture. The endobacteria R. radiobacter resuscitate from stationary phase to growth phase when there is third partner plant supplying with enough nutrition and better propagation conditions, which results in the increased amount of endobacteria R. radiobacter when P. indica colonized on plant root. Taken together, this study underlines the crucial role of endofungal bacteria in the tripartite symbiosis. Further studies are needed to better understand the mechanism of R. radiobacter in the tripartite interaction, such as the regulation of mRNA on transcriptome level.
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