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Interactions between plant growth-promoting rhizobacteria (PGPRs) and the symbiotic plant growth-promoting fungus Piriformospora indica were demonstrated by adopting several working models. Different rhizobacteria either inhibit, promote, or have no influence on stimulatory effect of P. indica in gnotobiotic barley plants. In particular, it was demonstrated that, e.g., Pseudomonas fluorescens WS5 and Burkholderia cepacia LA3 inhibited the growth and development of P. indica including complete blockage of sporulation (chlamydospores). The interaction with Ps. fluorescens turned out to be “fungistatic” as well as “fungicidal” in nature. TEM study showed the degradation of cell walls. Gas chromatography/mass spectrometry ion fragmentation pattern suggests that one of the interactive compounds is pyoverdine—a potent siderophore. On the other hand, the severe inhibition of the P. indica by the excreted metabolites of B. cepacia was described at the metabolome level applying high accurate mass spectrometer measurements. It was observed that several pathways were deactivated in the fungus, but a few of them, like ubiquinone biosynthesis, limonene, and pinene degradation, were activated since increased number of metabolites was annotated. Saponin, a biosurfactant, also inhibited the fungus but did not affect the ubiquinone biosynthesis and the limonene–pinene degradation. The study clearly demonstrated that there is intense interaction at metabolome level between rhizobacteria, P. indica, and plant components. A balance maintained due to stimulation and inhibition of the fungus by different rhizobacteria appears to be one of the major factors responsible for fungal diversity, abundance, and function in the rhizosphere. The study opens new vistas to understand delicate balance among mycorrhizospheric organisms that largely allow diverse microbes to coexist and share common resources.

In a previous study aimed at identifying regulators of Nicotiana attenuata responses against chewing insects, a 26-nucleotide tag matching the HSPRO (ORTHOLOG OF SUGAR BEET Hs1pro - 1) gene was found to be strongly induced after simulated herbivory (Gilardoni et al., 2010). Here we characterized the function of HSPRO during biotic interactions in transgenic N. attenuata plants silenced in its expression (ir-hspro). In wild-type plants, HSPRO expression was not only induced during simulated herbivory but also when leaves were inoculated with Pseudomonas syringae pv tomato DC3000 and roots with the growth-promoting fungus Piriformospora indica. Reduced HSPRO expression did not affect the regulation of direct defenses against Manduca sexta herbivory or P. syringae pv tomato DC3000 infection rates. However, reduced HSPRO expression positively influenced early seedling growth during interaction with P. indica; fungus-colonized ir-hspro seedlings increased their fresh biomass by 30% compared with the wild type. Grafting experiments demonstrated that reduced HSPRO expression in roots was sufficient to induce differential growth promotion in both roots and shoots. This effect was accompanied by changes in the expression of 417 genes in colonized roots, most of which were metabolic genes. The lack of major differences in the metabolic profiles of ir-hspro and wild-type colonized roots (as analyzed by liquid chromatography time-of-flight mass spectrometry) suggested that accelerated metabolic rates were involved. We conclude that HSPRO participates in a whole-plant change in growth physiology when seedlings interact with P. indica.