Endosphere-inhabiting mutualistic bacteria establish intimate relationships with their host plant and often provide services like plant growth-promotion (PGP) or disease protection. How plants select for these microbes and which mechanism of PGP are employed remain mostly elusive. I assessed the relevance of plant ethylene (ET) signaling in the recruitment of culturable mutualistic bacteria to the root endosphere of the wild tobacco species Nicotiana attenuata. Wild-type (WT) and transgenic lines either deficient in ET biosynthesis (ir-aco1) or ET perception (35S-etr1) grown in native soils were employed. The bacterial diversity of N. attenuata’s was strongly determined by the soil type and, to a lesser extent, by plant ET signaling. In terms of PGP, about 50% of the isolated strains conferred positive effects on seedling growth. A consecutive study analyzed the PGP effects conferred by the isolate, Bacillus sp. B55 (extracted from an ET-insensitive 35S-etr1 plant). Inoculation with B55 increased growth and fitness of WT and 35S-etr1 plants in vitro and in the field. Interestingly, 35S-etr1 plants realized greater benefits than WT and 35S-etr1 roots were higher colonized by B55 than WT roots. While searching for novel bacterial traits mediating the observed PGP effects, I could show that volatile organic compounds (VOCs) emitted by B55 promote seedling growth. A sulfur (S)-containing VOC, dimethyl disulfide (DMDS), which was released by B55 and conferred the observed PGP effects, was identified. Again, 35S-etr1 seedlings, which I found to be impaired in S-metabolism, realized a greater benefit of the exposure to B55’s VOCs and DMDS than WT plants. My findings allow for the conclusion that stressed plants can recruit “little helpers” to balance for their deficiencies. Furthermore, it becomes clear that benefits of mutualistic plant-microbe interactions may only become apparent under adverse conditions, like nutrient limitation or impairments in plant physiology.