Phosphorus (P) is an essential nutrient for plant growth and development, playing an important role in the synthesis of DNA, cell membrane components (phospholipids), adenosine triphosphate (ATP), respiration, and photosynthesis (Kafle et al., 2019; Bai et al., 2020). P in soil includes two forms: organic and inorganic P. Although soil contains a large amount of phosphorus, it usually exists in a form that cannot be directly utilized by plants (Ikhajiagbe et al., 2020; Divjot et al., 2021). P combines with Ca, Fe, and Al metals to form minerals, and P is adsorbed by iron/aluminum (hydrogen) oxides, leading to P fixation in the soil (Ma J. et al., 2021; Zhou J. et al., 2021). The mobility of P is poor in soil, and plants cannot directly absorb and utilize P, leading to the widespread phenomenon of low P in ecosystems, which limits plant growth and yield. A large amount of P fertilizer is applied during production to meet the P demand of plants. Because of the adsorption and fixation effects of soil on P, the applied P fertilizer rapidly becomes fixed, resulting in a P fertilizer utilization efficiency of only 10–25% (Dejene et al., 2023; Dong et al., 2023). Moreover, fixed P in the soil can lead to non-point source pollution, resulting in large amounts of P fertilizer flowing into water bodies, in turn leading to groundwater eutrophication, which is not conducive to the sustainable development of the ecological environment (Lyu et al., 2023; Wang et al., 2023). Phosphate ore is a nonrenewable resource. Half of the world’s existing P reserves are predicted to be depleted within 50–100 years (Zhu et al., 2018). Therefore, improving the utilization efficiency of P in soil is crucial for promoting plant growth, reducing environmental pollution, and improving resource management.

Phosphate-solubilizing microorganisms (PSMs) can convert soil P into a form that plants can absorb and utilize, and the application of PSMs is currently an important measure for increasing the available P content in soil (Yadav et al., 2017; Yadav, 2020). Many types of microorganisms dissolve P, which plays an important role in P cycling processes such as organic P mineralization, insoluble inorganic P dissolution, and P absorption (Zhu et al., 2018; Wise et al., 2021). Inoculating PSMs is an environmentally friendly method to promote crop productivity and understanding the mechanism of P solubilization by PSMs is of great significance for plants to adapt to low P stress and improve P utilization efficiency (Billah et al., 2019). This article discusses the types and functions of PSMs, P-solubilization mechanisms, main functional genes, and the impact of composite inoculation of PSMs on plant P partitioning, emphasizing the role of PSMs in plant P acquisition and utilization, and—based on this—proposes issues and corresponding measures that need to be considered in future research and applications of PSMs.

PSMs are widely distributed in nature, and microorganisms with P-solubilizing functions include bacteria, fungi, actinomycetes, and cyanobacteria, among which P-solubilizing fungi account for 0.1–0.5% of PSMs, and P-solubilizing bacteria account for 1–50% of the total (Fatima et al., 2022). P-solubilizing bacteria included 34 genera, including Bacillus, Pseudomonas, Escherichia, and Burkholderia. Of these, Bacillus, Pseudomonas, and Acinetobacter have been studied extensively (Divjot et al., 2021; Timofeeva et al., 2022). P-solubilizing fungi include Arbuscularmy sp., Aspergillus, Penicillium, among which Aspergillus is the most reported, followed by Penicillium (Jiang et al., 2020; Divjot et al., 2021; Etesami et al., 2021). P-solubilizing fungi produce 10 times more organic acids than P-solubilizing bacteria and can increase the contact area with the soil through the mycelium, thereby increasing the application potential of P-solubilizing fungi (Jiang et al., 2020). The main P-solubilizing actinomycetes are Streptomyces and Micromonospora (Aallam et al., 2021; De Zutter et al., 2022). Microorganisms not only promote the conversion of difficult-to-utilize P to available P but also assist plants with absorbing P outside the rhizosphere, thus playing an important role in the process of plant P acquisition (Castagno et al., 2021).

PSMs not only have P-solubilizing effects but can also produce organic acids and iron carriers, regulate plant hormone levels, and fix nitrogen to promote the acquisition and growth of rice nutrients (Ribeiro et al., 2018; Unnikrishnan and Binitha, 2024). PSMs can secrete plant hormones such as auxins, cytokinins, and gibberellins, produce antifungal compounds and volatile bactericidal metabolites, and synthesize 1-aminocyclopropane-1-carboxylate (ACC) deaminase to improve phosphorus absorption and disease resistance, thereby increasing plant growth and yield (Hakim et al., 2021; Rawat et al., 2021). PSMs can also secrete antibiotics, iron carriers, and lyases to protect plants from various soil-borne pathogens and promote plant growth (Toscano-Verduzco et al., 2020; Kumawat et al., 2021). Moreover, inoculation with PSMs can significantly affect the diversity and abundance of soil microbial communities and enhance the interactions between microorganisms, ultimately resulting in improved organic matter degradation and soil nutrient quality (Zhang X. et al., 2021). PSMs also have different functions in different ecological environments and can enhance crop resistance to certain abiotic stresses, including cold, salt, heavy metals, and drought (Table 1). The P-solubilizing bacterium Bacillus atrophaeus GQJK17 S8 can tolerate 11% NaCl, which can improve the germination rate, seedling biomass, and growth vitality index of quinoa plants (Mahdi et al., 2021). In addition, there are strains with different abiotic stress tolerance abilities, Such as Pseudomonas PGERs17, which is resistant to cold stress (Rizvi et al., 2021), Bacillus YMX5, which is resistant to high salt stress (Jiang et al., 2020), and Streptomyces laurentii EU-LWT3-69, which is resistant to drought stress (Toscano-Verduzco et al., 2020). This type of PSMs not only promotes plant P absorption but also helps plants grow in extreme environments.

P in soil includes two forms: inorganic and organic P. Inorganic P usually exists as phosphates, divided into soluble and insoluble P. Insoluble P mainly includes phosphates such as aluminum phosphate, iron phosphate, magnesium phosphate, and calcium phosphate (Aliyat et al., 2022), while soluble P mainly exists as hydrogen phosphate and dihydrogen phosphate ions (HPO₄²⁻ and H₂PO₄⁻) (Hao et al., 2020; Divjot et al., 2021; Li et al., 2021). Organic P mainly includes P-containing organic compounds, such as orthophosphate monoesters, orthophosphate diesters, organic polyphosphates, and phosphonates (Li C. et al., 2019). Organic acids and phosphatases produced by microorganisms are crucial for the cycling of inorganic and organic phosphorus in soil (Rasul et al., 2021). Insoluble inorganic P is mainly dissolved by organic acids, and enzymatic hydrolysis is the main method used to dissolve the organic forms of P (Figure 1). The mechanisms of microbial P solubilization can be divided into the following types:

With the continuous development of molecular biology, researchers have explored the mechanism of P solubilization from a genetic perspective. The specific molecular genetic mechanisms underlying mineral phosphate dissolution have not been clearly elucidated to date (Timofeeva et al., 2022). Research on the functional genes of PSMs has mainly focused on genes related to the microbial secretion of organic acids and phosphatase production.

P-solubilizing bacteria and fungi on their own have a limited ability to mineralize organic P and solubilize inorganic P. Co-inoculation of plants with two or more strains promotes P absorption and plant growth (Table 2). The interaction between AMF and phosphate-solubilizing bacteria is more effective than inoculation alone for promoting P absorption and plant growth (El Maaloum et al., 2020; Wahid et al., 2020). The combination of bacteria and fungi has a synergistic effect, and mixed inoculation of AMF and P-solubilizing bacteria increases the root dry weight of plants by up to 58% compared with a single inoculation (Sharma et al., 2020). Mixed inoculation of AMF and PSMs not only improves soil fertility but also significantly increases crop yield. Inoculation with Azospirillum brasilense and Bacillus subtilis can improve the efficiency of P fertilizer utilization in sugarcane and positively affect the quality and yield of sugarcane crops (Rosa et al., 2020). Co-inoculation with Trichoderma viride, Humicola spp., Paecilomyces lilacinus, Gluconacetobater diazotropicus, Azospiriillum brasilense, and Bacillus subtilis can improve nutrient cycling and soil fertility, thereby promoting sugarcane root development (Tayade et al., 2019). Co-inoculation with phosphate-solubilizing bacteria and AMF significantly increases the soil enzyme activity and rhizosphere microbial count, and both synergistically promote nitrogen and P nutrient uptake (Varinderpal-Singh et al., 2020; Cozzolino et al., 2021). The composite inoculation of Bradyrhizobium japonicum 5038 and Paenibacillus mucilaginosus 3016 on soybeans resulted in a significant increase in the abundance of phosphorus cycle genes, as well as an increase in soil available phosphorus and phosphatase activity (Xing et al., 2022).

The interactions between microorganisms to form complexes help plants absorb P. Fructose secreted by AMF can stimulate the expression of PSMs phosphatase genes, promote phosphatase synthesis and secretion, and increase the mineralization of organic P (Zhang et al., 2018). The mycelia of AMF can secrete compounds such as sugars, carboxylates, and amino acids, which can be utilized by phosphate-solubilizing bacteria (Cartabia et al., 2021; Weng et al., 2022). The exudate of AM fungi can serve as a source of carbon for bacteria as well as a signal and effector molecule that stimulates bacterial growth and activity (Zhang et al., 2016; Zeng et al., 2018; Zhang et al., 2018). In addition, bacteria on the surface of the mycelium can move along the mycelium and migrate to nutrient patches to activate organic P, thereby improving the utilization efficiency of the P in the soil by plants (Jiang et al., 2021). Bacteria colonize the surface of AMF mycelia to facilitate the acquisition of mycelial exudates (Emmett et al., 2021). Cooperation between AMF and bacteria is a manifestation of the symbiotic relationship between AMF and plants.

The symbiotic relationship between AMF and terrestrial plants is one of the most representative examples of microbial–plant cooperation (Brundrett and Tedersoo, 2018). The interaction between AMF and phosphate-solubilizing bacteria can affect the P exchange between plants and mycorrhizal fungi because the interaction between AMF and phosphate-solubilizing bacteria increases the secretion of phosphatase and gluconic acid, promoting the absorption and transport of P by extraradicular hyphae. P is transferred to plant roots by AMF, and plants, in turn, provide carbon sources to AMF, improving C-P exchange between plants and AMF (Duan et al., 2023). Under natural conditions, close cooperation between microorganisms is scientifically more effective for completing ecological functions than the independent actions of a single microorganism. Suillus grevillea synergistically mineralizes phytic acid by recruiting Cedecea lapeti and stimulates the upregulation of its own P-solubilization-related gene expression and growth of Cedecea lapeti, thereby promoting plant uptake of organic P (Mei et al., 2024). Ectomycorrhizal fungi recruit specific bacterial colonies by providing carbon sources, such as trehalose, mannitol, and organic acids (Deveau et al., 2010; Haq et al., 2017). These recruited bacteria can perform various ecological functions, such as promoting mycelial growth and assisting ectomycorrhizal fungi in absorbing nutrients (Tarkka et al., 2018; Pent et al., 2020). The co-inoculation of phosphate-solubilizing bacteria and fungi has shown good results in promoting plant growth, nutrient absorption, mycorrhizal symbiosis, and microbial biomass. In addition, the co-inoculation of PSMs with other functional microorganisms can achieve various goals to promote plant growth. For example, the co-inoculation of PSMs with nitrogen-fixing bacteria can increase the utilization of phosphorus and the fixation of nitrogen in the atmosphere, thereby improving soil fertility and crop yield, and promoting the development of sustainable agriculture (Zveushe et al., 2023). The co-inoculation of PSMs with biocontrol bacteria not only improves plant absorption of phosphorus, but also significantly reduces the incidence and severity of diseases, which is more effective than the single inoculation of PSMs (Nepomuceno et al., 2019).

The low available P content in the soil and the low efficiency of P fertilizer utilization limit plant growth and yield. PSMs increase the soil available P content, improve the P fertilizer utilization efficiency, and promote plant growth. Therefore, the use of biological pathways to improve the utilization efficiency of P in soil has attracted the attention of scientists in various countries. Domestic and foreign scholars have identified many microorganisms with P-solubilization abilities through screening and conducted research on them. However, owing to factors such as the microbial P-solubilization ability, the colonization ability in the plant rhizosphere, and stability, relatively few strains have been applied in production practices to date. Many studies have focused on the effects of PSMs on plant growth under conventional cultivation conditions; however, little attention has been paid to their effects on plant growth under abiotic stress conditions. With the continuous development of molecular technologies and genomics, related P-solubilizing genes are constantly being explored; however, gene research mainly focuses on functional verification, and the interaction mechanism between P-solubilizing genes is still unclear. AMF and phosphate-solubilizing bacteria originate from different sources, and combining the two is not a natural correlation and may result in an unstable synergistic effect. The mechanism by which compound inoculation with PSMs causes microbial community changes in plant roots is not yet fully understood. Unlike the extensive research on the interactions between microorganisms and plant roots, there is currently limited research on the impact of microbial interactions on plant P-uptake efficiency.

Regarding the research direction of inoculating PSMs to improve the utilization efficiency of plant P, the current focus is to (1) expand the application scope of PSMs, combine functional research such as nitrogen fixation and soil remediation, and increase the application of composite microbial fertilizers to better serve agricultural development. (2) Continuously explore P-solubilization-related genes using a combination of genomics, proteomics, and metabolomics to further explain the mechanisms of soil P dissolution. Single-cell Raman D₂O technology and high-throughput P-cycling functional gene chips can determine the corresponding functional genes, groups, and activities of PSMs, thereby improving our understanding of the types and functions of PSMs. (3) Strengthening research on microbial interactions and mixed inoculation, which combines AMF with naturally related bacteria, may provide advantages over artificially combined microorganisms. Moreover, by using molecular biology techniques and isotope labeling methods to explore microbial interactions at a deeper level, the optimal effect of microbial interactions in the soil can be achieved, thereby playing an important role in improving soil fertility. (4) Further research is being conducted on the effects of specific chemical substances related to different stages of microbial interactions through a combination of transcriptomics and metabolomics. (5) More attention should be paid to the isolation of indigenous microorganisms, screening for higher-quality and multifunctional PSMs, enhancing plant uptake of soil P, and enhancing their resistance to different stress conditions, which is of great significance for promoting plant growth.

FP: Writing – original draft, Writing – review & editing. QL: Writing – original draft. MS: Conceptualization, Writing – original draft. ZW: Conceptualization, Funding acquisition, Writing – review & editing. Y-XX: Conceptualization, Writing – review & editing. D-FD: Funding acquisition, Supervision, Writing – review & editing.