Phosphate-(P)-solubilizing microorganisms (PSM) are important drivers of P cycling in natural and agro-ecosystems. Their use as plant inoculants to improve P acquisition of crops has been investigated for decades. However, limited reproducibility of the expected effects, particularly under field conditions, remains a major challenge. This study demonstrates that the form of nitrogen fertilization has a significant impact on the performance of various fungal and bacterial PSM inoculants in maize grown on neutral to alkaline soils with limited P availability. Under these conditions, a high soil pH-buffering capacity frequently limits the efficiency of nutrient mobilization, mediated by plant roots and microorganisms via rhizosphere acidification. In a soil pH range between 7.0 and 8.0, nitrate fertilization promoting rhizosphere alkalinisation further aggravates this problem. Accordingly, in greenhouse experiments, six strains of Pseudomonas, Bacillus, Paenibacillus, Streptomyces, and Penicillium with proven P-solubilizing potential, completely failed to promote P acquisition in maize grown on a calcareous Loess sub-soil pH 7.6 with nitrate fertilization and rock phosphate (Rock-P) as a sparingly soluble P source. However, after replacement of nitrate fertilization by ammonium, stabilized with the nitrification inhibitor 3,4-dimethylpyrazole-phosphate (DMPP), five out of seven investigated PSM inoculants (comprising 12 fungal and bacterial PSM strains) exerted beneficial effects on plant growth and reached up to 88% of the shoot biomass production of a control supplied with soluble triple-superphosphate (TSP). Stabilized ammonium combined with PSM-inoculants improved P acquisition (Trichoderma harzianum T22, Pseudomonas sp. DMSZ 13134), while other strains particularly stimulated root growth (T. harzianum OMG16, Bacillus amyloliquefaciens FZB42), which promoted the acquisition also of other mineral nutrients, such as N, K, and Mn. A similar effect was recorded under field conditions on an alkaline clay-loam soil pH 8.6. The combination of stabilized ammonium with a range of consortium products based on T. harzianum OMG16, B. amyloliquefaciens, micronutrients, and humic acids completely compensated the effect of a TSP fertilization on field establishment, nutrient acquisition, and yield formation in maize, while non-stabilized urea-di-ammonium phosphate fertilization was largely ineffective. These findings suggest that the efficiency of PSM-plant interactions can be influenced by the form of N fertilization, offering promising perspectives for synergistic effects with stabilized ammonium fertilizers.

The use of plant growth-promoting microorganisms (PGPMs) as bio-effectors (BEs) to improve the nutrient acquisition of crops has a long history. However, limited reproducibility of the expected effects still remains a major challenge for practical applications. Based on the hypothesis that the expression of PGPM effects depends on soil type and the properties of the applied fertilizers, in this study, the performance of selected microbial inoculants was investigated for two contrasting low-fertility soils supplied with different organic and inorganic fertilizers. Greenhouse experiments were conducted with tomato on an alkaline sandy loam of pH 7.8 and an acidic loamy sand of pH 5.6 with limited phosphate (P) availability. Municipal waste compost, with and without poultry manure (PM), rock phosphate (RP), stabilized ammonium, and mineral nitrogen, phosphorus and potassium (NPK) fertilization were tested as fertilizer variants. Selected strains of Bacillus amyloliquefaciens (Priest et al. 1987) Borriss et al. 2011 (FZB42) and Trichoderma harzianum Rifai (OMG16) with proven plant growth-promoting potential were used as inoculants. On both soils, P was identified as a major limiting nutrient. Microbial inoculation selectively increased the P utilization in the PM-compost variants by 116% and 56% on the alkaline and acidic soil, while RP utilization was increased by 24%. This was associated with significantly increased shoot biomass production by 37–42%. Plant growth promotion coincided with a corresponding stimulation of root growth, suggesting improved spatial acquisition of soluble soil P fractions, associated also with improved acquisition of nitrogen (N), potassium (K), magnesium (Mg), and calcium (Ca). There was no indication for mobilization of sparingly soluble Ca phosphates via rhizosphere acidification on the alkaline soil, and only mineral NPK fertilization reached a sufficient P status and maximum biomass production. However, on the moderately acidic soil, FZB42 significantly stimulated plant growth of the variants supplied with Ca–P in the form of RP + stabilized ammonium and PM compost, which was equivalent to NPK fertilization; however, the P nutritional status was sufficient only in the RP and NPK variants. The results suggest that successful application of microbial biofertilizers requires more targeted application strategies, considering the soil properties and compatible fertilizer combinations.

Microbiome-based solutions are regarded key for sustainable agroecosystems. However, it is unclear how agricultural practices affect the rhizosphere microbiome, plant–microorganism interactions and crop performance under field conditions. Therefore, we installed root observation windows in a winter wheat field cultivated either under long-term mouldboard plough (MP) or cultivator tillage (CT). Each tillage practice was also compared at two nitrogen (N) fertilization intensities, intensive (recommended N-supply with pesticides/growth regulators) or extensive (reduced N-supply, no fungicides/growth regulators). Shoot biomass, root exudates and rhizosphere metabolites, physiological stress indicators, and gene expression were analyzed together with the rhizosphere microbiome (bacterial/archaeal 16S rRNA gene, fungal ITS amplicon, and shotgun metagenome sequencing) shortly before flowering. Compared to MP, the rhizosphere of CT winter wheat contained more primary and secondary metabolites, especially benzoxazinoid derivatives. Potential copiotrophic and plant-beneficial taxa (e.g. Bacillus, Devosia, and Trichoderma) as well as functional genes (e.g. siderophore production, trehalose synthase, and ACC deaminase) were enriched in the CT rhizosphere, suggesting that tillage affected belowground plant–microorganism interactions. In addition, physiological stress markers were suppressed in CT winter wheat compared to MP. In summary, tillage practice was a major driver of crop performance, root deposits, and rhizosphere microbiome interactions, while the N-fertilization intensity was also relevant, but less important.

The long-term effects of agricultural management such as different fertilization strategies on soil microbiota and soil suppressiveness against plant pathogens are crucial. Therefore, the suppressiveness of soils differing in fertilization history was assessed using two Rhizoctonia solani isolates and their respective host plants (lettuce, sugar beet) in pot experiments. Further, the effects of fertilization history and the pathogen R. solani AG1-IB on the bulk soil, root-associated soil and rhizosphere microbiota of lettuce were analyzed based on amplicon sequencing of the 16S rRNA gene and ITS2 region. Organic fertilization history supported the spread of the soil-borne pathogens compared to long-term mineral fertilization. The fertilization strategy affected bacterial and fungal community composition in the root-associated soil and rhizosphere, respectively, but only the fungal community shifted in response to the inoculated pathogen. The potential plant-beneficial genus Talaromyces was enriched in the rhizosphere by organic fertilization and presence of the pathogen. Moreover, increased expression levels of defense-related genes in shoots of lettuce were observed in the soil with organic fertilization history, both in the absence and presence of the pathogen. This may reflect the enrichment of potential plant-beneficial microorganisms in the rhizosphere, but also pathogen infestation. However, enhanced defense responses resulted in retarded plant growth in the presence of R. solani (plant growth/defense tradeoff).

Background: Plant beneficial microorganisms as inoculants can improve crop performance, but factors affecting their impact on plant performance under field conditions remain unclear, thereby limiting their use in farming. Here, we investigated how farming practices (e.g., tillage and N-fertilization intensity) and growing seasons influenced the impact of a beneficial microorganism consortium (BMc: Trichoderma, Bacillus, and Pseudomonas strains) in maize and affected the rhizosphere competence of each BMc strain. In addition, we tested whether the consortium affects the resident rhizosphere microbiome and crop performance. In two growing seasons (2020 and 2021), we assessed how BMc inoculation affects maize growth, nutritional status, gene expression, and rhizosphere microbiome under different farming practices at the flowering stage. Results: Inoculated strains successfully colonized the maize rhizosphere independently of farming practice. BMc inoculation improved plant growth and iron uptake in 2020, regardless of farming practice. These effects co-occurred with lower precipitation levels in 2020 compared to 2021. BMc inoculation reduced the expression of several stress-related genes in maize in 2020 under drought. An increased iron uptake by the BMc-inoculated plants was observed in 2020 and was associated with the upregulation of the gene ZmNAS3, which is linked to iron uptake. Therefore, BMc inoculation mitigated the drought impact on maize. The microbial rhizosphere communities were altered by BMc inoculation in both years, but patterns of responder taxa differed between seasons. Metagenome analysis revealed that more genes (e.g., genes encoding biosurfactants and siderophores) were enriched in the rhizosphere of BMc-inoculated plants in 2020 than in 2021. Moreover, we identified bacterial and fungal taxa positively associated with maize iron uptake. The relative abundance of these iron uptake-associated bacterial and fungal taxa significantly increased due to BMc inoculation in 2020, while they showed overall higher relative abundances in 2021, independently of BMc inoculation. We mapped the sequences of these iron-associated taxa to publicly available genomes and verified the occurrence of various plant beneficial traits in several mapped genomes. Conclusions: Overall, we show that the growing season determined the effect of BMc inoculation on maize plants by shaping microbiome composition and function in the maize rhizosphere more than farming practice. These findings highlight the importance of the complex interplay between microbial inoculants and the resident rhizosphere microorganisms under abiotic stress conditions.