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Soil phosphorus transformation and plant uptake driven by phosphate-solubilizing microorganisms

Fei Pang, Qing Li, Manoj Kumar Solanki and 3 more

Frontiers in Microbiology · 2024 · Review · CC BY

doi:10.3389/fmicb.2024.1383813

Abstract

Phosphorus (P) is an important nutrient for plants, and a lack of available P greatly limits plant growth and development. Phosphate-solubilizing microorganisms (PSMs) significantly enhance the ability of plants to absorb and utilize P, which is important for improving plant nutrient turnover and yield. This article summarizes and analyzes how PSMs promote the absorption and utilization of P nutrients by plants from four perspectives: the types and functions of PSMs, phosphate-solubilizing mechanisms, main functional genes, and the impact of complex inoculation of PSMs on plant P acquisition. This article reviews the physiological and molecular mechanisms of phosphorus solubilization and growth promotion by PSMs, with a focus on analyzing the impact of PSMs on soil microbial communities and its interaction with root exudates. In order to better understand the ability of PSMs and their role in soil P transformation and to provide prospects for research on PSMs promoting plant P absorption. PSMs mainly activate insoluble P through the secretion of organic acids, phosphatase production, and mycorrhizal symbiosis, mycorrhizal symbiosis indirectly activates P via carbon exchange. PSMs can secrete organic acids and produce phosphatase, which plays a crucial role in soil P cycling, and related genes are involved in regulating the P-solubilization ability. This article reviews the mechanisms by which microorganisms promote plant uptake of soil P, which is of great significance for a deeper understanding of PSM-mediated soil P cycling, plant P uptake and utilization, and for improving the efficiency of P utilization in agriculture.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 24, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

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. 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. 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. 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%. 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. Phosphate ore is a nonrenewable resource. Half of the world’s existing P reserves are predicted to be depleted within 50–100 years. 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. 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. 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. 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.

Types and functions 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. P-solubilizing bacteria included 34 genera, including Bacillus, Pseudomonas, Escherichia, and Burkholderia. Of these, Bacillus, Pseudomonas, and Acinetobacter have been studied extensively. P-solubilizing fungi include Arbuscularmy sp., Aspergillus, Penicillium, among which Aspergillus is the most reported, followed by Penicillium. 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. The main P-solubilizing actinomycetes are Streptomyces and Micromonospora. 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.

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. 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. PSMs can also secrete antibiotics, iron carriers, and lyases to protect plants from various soil-borne pathogens and promote plant growth. 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. 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. In addition, there are strains with different abiotic stress tolerance abilities, Such as Pseudomonas PGERs17, which is resistant to cold stress, Bacillus YMX5, which is resistant to high salt stress, and Streptomyces laurentii EU-LWT3-69, which is resistant to drought stress. This type of PSMs not only promotes plant P absorption but also helps plants grow in extreme environments.

The P removal mechanism of PSMs

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, while soluble P mainly exists as hydrogen phosphate and dihydrogen phosphate ions (HPO42− and H2PO4−). Organic P mainly includes P-containing organic compounds, such as orthophosphate monoesters, orthophosphate diesters, organic polyphosphates, and phosphonates. Organic acids and phosphatases produced by microorganisms are crucial for the cycling of inorganic and organic phosphorus in soil. 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:

Secretion of organic acids

Organic acids secreted by PSMs transform insoluble inorganic P into plant-usable P. Microorganisms produce organic acids in two ways: physiological secretion and decomposition of organic matter. The organic acids secreted by PSMs include gluconic, lactic, citric, and oxalic acids. Organic acids mainly dissolve insoluble inorganic P as follows: organic acid anions compete with phosphate ions for binding sites on soil particles, reducing soil adsorption of phosphate ions; complex metal ions such as iron, aluminum, and calcium in soil to release bound phosphate ions; and reduction of the pH of the medium promotes the dissolution of insoluble inorganic P. The organic acids secreted by PSMs not only enhance the solubility of insoluble P, such as apatite and calcium phosphate, but also chelate with cations such as Ca2+, Fe3+, Al3+, and Mg2+, and organic acid anions compete with inorganic P physically or electrostatically for the same adsorption sites in the soil, releasing phosphate ions and increasing the effective P content. The organic acids produced by microorganisms chelate with cations through hydroxyl and carboxyl groups, transforming phosphates into soluble forms and increasing the effective P content. Many bacteria secrete organic acids (carboxylic acids) that can increase the solubility of calcium phosphate. In addition, organic acids can promote the dissolution of insoluble inorganic phosphate compounds, such as tricalcium phosphate, dicalcium phosphate, hydroxyapatite, and phosphate rock, thereby improving the utilization rate of phosphate fertilizers. PSMs secrete various organic acids to convert insoluble inorganic phosphorus into soluble orthophosphates that are easily absorbed by plants. The types, contents, and phosphate solubility of organic acids produced by PSM vary, such as of Enterobacter sp. strain 15S, can produce organic acids such as citric, fumaric, ketoglutaric, malic, and oxalic acids. However, Trichoderma sp. produce different types of organic acids, including lactic acid, fuzzy acid, ascorbic acid, isocitric acid, malic acid, citric acid, and phytic acid.

Gluconic acid is considered a common and important organic acid, and is one of the many organic acids produced by microorganisms that have been extensively studied. Glucose can form gluconic acid through the synergistic effects of pyrroloquinoline quinine (PQQ) and glucose dehydrogenase (GDH), which dissolves insoluble phosphate. Pseudomonas produces gluconic acid to increase phosphate solubility, which has become an important technology for improving phosphate fertilizer management in modern agriculture. Inoculation of Pseudomonas fluorescens and Pseudomonas putida under soluble phosphate-restricted conditions can produce a large amount of gluconic acid, which promotes plant growth.

Enzymatic hydrolysis

Organic P cannot be directly absorbed by plants but needs to be mineralized into inorganic P before it can be utilized by plants. Enzymatic hydrolysis is the main way to mineralize organic P under conditions of low available P content, PSMs can hydrolyze organic P through biological enzymes, such as phosphatase, phytase, and C-P lyase. Two hydrolytic enzymes, phytase and phosphatase, play important roles in PSM mineralization. Phytase is an extracellular enzyme involved in the mineralization process of soil P, and phytase produced by microorganisms can release orthophosphate from phytate organic compounds, converting P into a form that can be utilized by plants. Microbial phytase activity is closely related to its ability to dissolve phosphorus.

PSMs not only secrete phytase, but also produce phosphatase to mineralize organic P. Phosphatases are divided into acid phosphatase (ACP) and alkaline phosphatase (ALP), and their existence is greatly influenced by the acidity and alkalinity of the environment. ACP is more abundant in acidic soils, while ALP dominates in neutral and alkaline soils. The activity of ALP is inhibited by inorganic phosphates in the environment, while ACP activity is not inhibited by high levels of phosphates. In addition, temperature can affect phosphatase activity, and an increase in temperature can enhance the activity of phosphatases secreted by PSMs. Phosphatases are responsible for mineralizing approximately 90% of the organic P in soils, except phytates. Many microorganisms, including Aspergillus, Bacillus, and Pseudomonas, produce phosphatases. Purified ALP from Bacillus licheniformis MTCC 2312 has been added to sterilized soil, which improved the phosphate content in the roots and stems of maize.

The role of mycorrhizal symbiosis

Mycorrhizal fungi can form mutualistic symbioses with plant roots and help plants absorb mineral elements and water from the soil, while plants provide carbohydrates to the fungi. Arbuscular mycorrhizal fungi (AMF) can form mycorrhizal fungi in symbiosis with 70–80% of terrestrial plants, which is an effective way for plants to obtain P. The symbiotic interface between AMF and plants is an important site for material exchange between plants and fungi, which can increase the range of plant P absorption and the transport of P to root cells. Plants absorb P through a series of morphological changes to expand the surface area of the roots and improve the exchange interface between the roots and soil when subjected to low P stress. Examples of this include increasing the number and length of root hairs; increasing the root-to-shoot ratio; adjusting the angle of root growth; increasing the number of lateral roots, adventitious roots, and young roots; increasing root length, shallow roots; and increasing root length and density in the soil surface layer. Mycorrhizal plants can obtain P from the soil through the root pathway absorbed by root hairs and root epidermal cells, as well as the hyphal pathway absorbed by arbuscular mycorrhizal fungi, which synergistically promote nutrient absorption. In the hyphal pathway, arbuscular mycorrhizal fungi improve plant P nutrient status through the hyphae. Hyphae not only penetrate soil pores smaller than root hairs but also extend further from the root surface to obtain a larger range of P in the soil. While expanding the absorption range, AMF can stimulate the secretion of organic acids and ACP by host plant roots; their own mycelia can also secrete organic acids and ACP, reduce the pH of the surrounding soil, and convert insoluble phosphates into available P, which has the similar function as phosphate-solubilizing bacteria. Organic acids, carbohydrates, amino acids, plant hormones, and other substances have been found in the mycelial secretions of AMF (Rhizophagus clarius and Rhizophagus irregularis). Plants are likely to form mycorrhizal symbioses with mycorrhizal fungi to enhance their ability to obtain P under P-deficient conditions. The absorption of soil P through mycorrhizal fungi is an effective way for plants to supplement P (Figure 2).

Other functions

Compared with organic acids, the efficiency of inorganic acids (such as sulfuric acid and nitric acid) produced by PSMs in dissolving phosphates is lower. Nitrobacter and Thiobacillus spp. produce inorganic acids, such as nitric acid and sulfuric acid, to dissolve P and increase the available P content in the soil. PSMs also produce extracellular polysaccharides (EPS) that can form complexes with metal ions and enhance the solubilization of P. The combined action of EPS and organic acids can dissolve Ca3(PO4)2, which adds EPS to the culture medium and increases the solubilization of tricalcium phosphate by organic acids. Ammonium (NH4+) present in soil is absorbed by PSMs to synthesize amino acids. Proton efflux caused by ammonium ion assimilation is another P-solubilization mechanism in microorganisms. Bacillus marisflavi FA7 is accompanied by ammonium ion assimilation, which decreases the pH of the culture medium and dissolves insoluble phosphates. PSMs can also promote P absorption by increasing root weight, root length, projection area, surface area, tip, and branch number.

Main P cycling functional genes of PSMs

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. Research on the functional genes of PSMs has mainly focused on genes related to the microbial secretion of organic acids and phosphatase production.

Organic acid-related genes

Gluconic acid is the main organic acid secreted by PSMs. Genes related to gluconic acid synthesis are key for the regulation of P-solubilization ability. Gluconic acid is synthesized by the oxidation of glucose by GDH, which requires pyroquinoline quinone (PQQ) as a cofactor to participate in the reaction. PQQ synthesis involves six core genes (pqqA, pqqB, pqqC, pqqD, pqqE, and pqqF) associated with dehydrogenase activity and mineral phosphate dissolution in microorganisms. The pqqA gene plays an important role in PQQ biosynthesis and P solubilization. Mutations in pqqA in Rahnella aquatilis HX2H significantly reduce the gluconic acid content in the culture medium, leading to a significant decrease in the solubility of mineral phosphates. In addition, pqqE is highly conserved and crucial for the biosynthesis of PQQ. Pantoea sp. and Pseudomonas sp. carrying pqqE can solubilize P and increase crop yields. The expression level of the pqq gene in Serratia sp. S119 increases under P-deficient growth conditions, catalyzing the oxidation of glucose to gluconic acid and alleviating P deficiency.

The membrane-bound quinoprotein glucose dehydrogenase (PQQGDH) is an important enzyme that regulates the synthesis of gluconic acid and dissolution of insoluble phosphate and is encoded by the gcd gene. The genes related to gluconic acid production include gabY and mps. Pseudomonas sp. MS16 was isolated from the rhizosphere soil of wheat and its P-solubilization activity was further validated through amplification, sequencing, and phylogenetic analysis of gcd gene. The abundances of gcd genes were significantly correlated with environmental factors such as dissolved oxygen, phosphorus hydrochloride, and dissolved total phosphorus. The gcd gene can serve as a genetic marker to evaluate the potential of microorganisms to dissolve inorganic phosphorus. Acinetobacter sp. MR5 and Pseudomonas sp. MR7 carrying the gcd gene have the effect of promoting plant P absorption and growth, and rice plants treated with bacteria exhibited an increase in P content and grain yield of approximately 67 and 55%, respectively, compared with control plants. However, the expression of gcd is inhibited by an increase in the soluble phosphate concentration.

Phosphatase genes

Phosphatases are important enzymes for mineralizing organic P and include ACP and ALP. ACP is mainly secreted by plants and fungi, whereas ALP is mainly produced by bacteria. ALP and gluconic acid are important factors that affect the availability of P in soil. Among the enzymes involved in organic P mineralization, bacterial ALP has been extensively studied in terms of its biosynthesis, genetic control, and catalytic properties. ALP is primarily encoded by PhoA, PhoD, and PhoX. PhoA hydrolyzes phosphate monoesters, whereas phoD and phoX decompose phosphate monoesters and phosphate diesters. Among the genes encoding ALP, phoD is a key gene in soil microorganisms. The abundance of phoD in soil correlated positively with ALP activity and the available P concentration. The phoD gene is used as a marker gene to estimate the abundance and community composition of organic P-mineralization microorganisms, thereby allowing investigation of the microbial regulatory mechanisms of phosphorus cycling. In addition to the ALP genes, the ACP genes mainly include phoC, whereas the phytase genes include phyA, appA, etc. The phoC gene is an important gene encoding acid phosphatase. In neutral or low-pH soils, the phoC gene is more dominant than the phoD gene. After genetic transformation of maize using the phytase gene (phyA2) of Aspergillus ficuum, the growth and ability to obtain P from phytates were significantly improved. In addition, a large number of studies have reported the isolation of various genes with P-solubilization ability from different species, such as mMDH from Penicillium oxalicum C2, vgb from Vitreoscilla hemoglobin, Eno from Burkholderia cenococcia 71-2, Zymomonas mobility (invB), and Saccharomyces cerevisiae (suc2).

The use of metagenomic methods to analyze soil microbial P-cycling functional genes lays a solid foundation for the study of P-cycling genes, which helps us explore the potential functions of PSMs from a more comprehensive perspective. The P-cycling functional genes are mainly divided into three categories and seven functional groups, including those involved in P activation (including phosphate ester mineralization and inorganic phosphate dissolution), P absorption (phosphate ester transport and inorganic phosphate transport), and regulation of P-deficiency-induced responses. With the development of omics technologies and improvement of functional gene reference databases, researchers will more comprehensively reveal the functions and molecular mechanisms of microorganisms involved in plant soil P cycling.

The effect of co-inoculation of PSMs on plant P acquisition

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. 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. 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. 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. 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. 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.

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. The mycelia of AMF can secrete compounds such as sugars, carboxylates, and amino acids, which can be utilized by phosphate-solubilizing bacteria. 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. 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. Bacteria colonize the surface of AMF mycelia to facilitate the acquisition of mycelial exudates. 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. 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. 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. Ectomycorrhizal fungi recruit specific bacterial colonies by providing carbon sources, such as trehalose, mannitol, and organic acids. These recruited bacteria can perform various ecological functions, such as promoting mycelial growth and assisting ectomycorrhizal fungi in absorbing nutrients. 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. 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.

Conclusion and perspective

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.

Author contributions

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.

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    Campos A. L. Fronza B. M. Rodrigues M. C. Souza Chiari M. D. E. Braga R. R. (2023 ). Influence of the calcium orthophosphate: glass ratio and calcium orthophosphate functionalization on the degree of conversion and mechanical properties of resin-based composites. J. Biomed. Mater. Res. B 111, 95–102. doi:, PMID:

    Not in our library10.1002/jbm.b.35136

  21. 21.

    Cartabia A. Tsiokanos E. Tsafantakis N. Lalaymia I. Termentzi A. Miguel M.. (2021 ). The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 modulates metabolites production of Anchusa officinalis L. under semi-hydroponic cultivation. Front. Plant Sci. 12:724352

    Not in our library10.3389/fpls.2021.724352

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    Castagno L. N. Sannazzaro A. I. Gonzalez M. E. Pieckenstain F. L. Estrella M. J. (2021 ). Phosphobacteria as key actors to overcome phosphorus deficiency in plants. Ann. Appl. Biol. 178, 256–267

    Not in our library10.1111/aab.12673

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    Chen A. Arai Y. (2023 ). A review of the reactivity of phosphatase controlled by clays and clay minerals: implications for understanding phosphorus mineralization in soils. Clay Clay Miner. 71, 119–142

    Not in our library10.1007/s42860-023-00243-7

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    Chen X. Jiang N. Condron L. M. Dunfield K. E. Chen Z. Wang J.. (2019 ). Soil alkaline phosphatase activity and bacterial phoD gene abundance and diversity under long-term nitrogen and manure inputs. Geoderma 349, 36–44

    Not in our library10.1016/j.geoderma.2019.04.039

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    Cheng Y. Narayanan M. Shi X. Chen X. Li Z. Ma Y. (2023 ). Phosphate-solubilizing bacteria: their agroecological function and optimistic application for enhancing agro-productivity. Sci. Total Environ. 901:166468. doi:, PMID:

    Not in our library10.1016/j.scitotenv.2023.166468

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    Cheng J. Zhuang W. Li N. Tang C. Ying H. (2017 ). Efficient biosynthesis of d-ribose using a novel co-feeding strategy in Bacillus subtilis without acid formation. Lett. Appl. Microbiol. 64, 73–78. doi:, PMID:

    Not in our library10.1111/lam.12685

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    Chiu C. H. Paszkowski U. (2019 ). Mechanisms and impact of symbiotic phosphate acquisition. Cold Spring Harb. Perspect. Biol. 11:a034603. doi:, PMID:

    Not in our library10.1101/cshperspect.a034603

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    Chu Q. Zhang L. Zhou J. Yuan L. Chen F. Zhang F.. (2020 ). Soil plant-available phosphorus levels and maize genotypes determine the phosphorus acquisition efficiency and contribution of mycorrhizal pathway. Plant Soil 449, 357–371

    Not in our library10.1007/s11104-020-04494-4

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    Cozzolino V. Monda H. Savy D. Di Meo V. Vinci G. Smalla K. (2021 ). Cooperation among phosphate-solubilizing bacteria, humic acids and arbuscular mycorrhizal fungi induces soil microbiome shifts and enhances plant nutrient uptake. Chem. Biol. Technol. Agric. 8:31

    Not in our library10.1186/s40538-021-00230-x

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    Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems · 2019
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    De Zutter N. Ameye M. Vermeir P. Verwaeren J. De Gelder L. Audenaert K. (2022 ). Innovative rhizosphere-based enrichment under P-limitation selects for bacterial isolates with high-performance P-solubilizing traits. Microbiol. Spectr. 10:e0205222

    Not in our library10.1128/spectrum.02052-22

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    Dejene M. Abera G. Desalegn T. (2023 ). The effect of phosphorus fertilizer sources and lime on acidic soil properties of mollic rhodic nitisol in Welmera District, Central Ethiopia. Appl. Environ. Soil Sci. 2023:7002816

    Not in our library10.1155/2023/7002816

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    Della Mónica I. F. Godeas A. M. Scervino J. M. (2020 ). In vivo modulation of arbuscular mycorrhizal symbiosis and soil quality by fungal P solubilizers. Microb. Ecol. 79, 21–29

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    Deveau A. Brulé C. Palin B. Champmartin D. Rubini P. Garbaye J.. (2010 ). Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8. Environ. Microbiol. Rep. 2, 560–568

    Not in our library10.1111/j.1758-2229.2010.00145.x

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    Dipta B. Bhardwaj S. Kaushal M. Kirti S. Sharma R. (2019 ). Obliteration of phosphorus deficiency in plants by microbial interceded approach. Symbiosis 78, 163–176

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    Divjot K. Rana K. L. Tanvir K. Yadav N. Yadav A. N. Kumar M.. (2021 ). Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and-mobilizing microbes: a review. Pedosphere 31, 43–75

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    Dong Z. Liu Y. Li M. Ci B. Lu X. Feng X.. (2023 ). Effect of different NPK fertilization timing sequences management on soil-petiole system nutrient uptake and fertilizer utilization efficiency of drip irrigation cotton. Sci. Rep. 13:14287. doi:, PMID:

    Not in our library10.1038/s41598-023-40620-9

  38. 38.

    Drozd M. Gangaiah D. Liu Z. Rajashekara G. (2011 ). Contribution of TAT system translocated PhoX to Campylobacter jejuni phosphate metabolism and resilience to environmental stresses. PLoS One 6:e26336. doi:, PMID:

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    Duan S. Declerck S. Feng G. Zhang L. (2023 ). Hyphosphere interactions between Rhizophagus irregularis and Rahnella aquatilis promote carbon–phosphorus exchange at the peri-arbuscular space in Medicago truncatula. Environ. Microbiol. 25, 867–879. doi:, PMID:

    Not in our library10.1111/1462-2920.16333

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    Dudeja S. S. Suneja-Madan P. Paul M. Maheswari R. Kothe E. (2021 ). Bacterial endophytes: molecular interactions with their hosts. J. Basic Microbiol. 61, 475–505. doi:, PMID:

    Not in our library10.1002/jobm.202000657

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    El Maaloum S. Elabed A. Alaoui-Talibi Z. E. Meddich A. Filali-Maltouf A. Douira A.. (2020 ). Effect of arbuscular mycorrhizal fungi and phosphate-solubilizing bacteria consortia associated with phospho-compost on phosphorus solubilization and growth of tomato seedlings (Solanum lycopersicum L.). Commun. Soil Sci. Plant Anal. 51, 622–634

    Not in our library10.1080/00103624.2020.1729376

  42. 42.
    Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi · 2021
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  43. 43.
    Contribution of Arbuscular Mycorrhizal Fungi, Phosphate–Solubilizing Bacteria, and Silicon to P Uptake by Plant · 2021
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    Fatima F. Ahmad M. Verma S. Pathak N. (2022 ). Relevance of phosphate solubilizing microbes in sustainable crop production: a review. Int. J. Environ. Sci. Technol. 19, 9283–9296

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    Fernandes G. C. Rosa P. A. L. Jalal A. Oliveira C. E. S. Galindo F. S. Viana R. S.. (2023 ). Technological quality of sugarcane inoculated with plant-growth-promoting bacteria and residual effect of phosphorus rates. Plan. Theory 12:2699. doi:, PMID:

    Not in our library10.3390/plants12142699

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    Ferrol N. Azcón-Aguilar C. Pérez-Tienda J. (2019 ). Arbuscular mycorrhizas as key players in sustainable plant phosphorus acquisition: an overview on the mechanisms involved. Plant Sci. 280, 441–447. doi:, PMID:

    Not in our library10.1016/j.plantsci.2018.11.011

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    Fraser T. Lynch D. H. Entz M. H. Dunfield K. E. (2015 ). Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma 257–258, 115–122

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    Fraser T. D. Lynch D. H. Gaiero J. Khosla K. Dunfield K. E. (2017 ). Quantification of bacterial non-specific acid (phoC) and alkaline (phoD) phosphatase genes in bulk and rhizosphere soil from organically managed soybean fields. Appl. Soil Ecol. 111, 48–56

    Not in our library10.1016/j.apsoil.2016.11.013

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    Galindo F. S. Pagliari P. H. Fernandes G. C. Rodrigues W. L. Boleta E. H. M. Jalal A.. (2022 ). Improving sustainable field-grown wheat production with Azospirillum brasilense under tropical conditions: a potential tool for improving nitrogen management. Front. Environ. Sci. 10:821628

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  50. 50.

    Genre A. Lanfranco L. Perotto S. Bonfante P. (2020 ). Unique and common traits in mycorrhizal symbioses. Nat. Rev. Microbiol. 18, 649–660. doi:, PMID:

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    Gregory P. J. (2022 ). Russell review: are plant roots only “in” soil or are they “of” it? Roots, soil formation and function. Eur. J. Soil Sci. 73:e13219

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    Hakim S. Naqqash T. Nawaz M. S. Laraib I. Siddique M. J. Zia R.. (2021 ). Rhizosphere engineering with plant growth-promoting microorganisms for agriculture and ecological sustainability. Front. Sustain. Food Syst. 5:617157

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    Hammelehle A. Oberson A. Lüscher A. Mäder P. Mayer J. (2018 ). Above-and belowground nitrogen distribution of a red clover-perennial ryegrass sward along a soil nutrient availability gradient established by organic and conventional cropping systems. Plant Soil 425, 507–525

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    Hao J. Knoll A. H. Huang F. Schieber J. Hazen R. M. Daniel I. (2020 ). Cycling phosphorus on the Archean earth: part II. Phosphorus limitation on primary production in Archean ecosystems. Geochim. Cosmochim. Acta 280, 360–377

    Not in our library10.1016/j.gca.2020.04.005

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    Haq I. U. Dini-Andreote F. Van Elsas J. D. (2017 ). Transcriptional responses of the bacterium Burkholderia terrae BS001 to the fungal host Lyophyllum sp. strain Karsten under soil-mimicking conditions. Microb. Ecol. 73, 236–252. doi:, PMID:

    Not in our library10.1007/s00248-016-0885-7

  56. 56.

    Hessen D. O. Hafslund O. T. Andersen T. Broch C. Shala N. K. Wojewodzic M. W. (2017 ). Changes in stoichiometry, cellular RNA, and alkaline phosphatase activity of Chlamydomonas in response to temperature and nutrients. Front. Microbiol. 8:18

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    Hu M. Penuelas J. Sardans J. Tong C. Chang C. T. Cao W. (2020 ). Dynamics of phosphorus speciation and the phoD phosphatase gene community in the rhizosphere and bulk soil along an estuarine freshwater-oligohaline gradient. Geoderma 365:114236

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    Huang B. Yan D. Ouyang C. Zhang D. Zhu J. Liu J.. (2020 ). Chloropicrin fumigation alters the soil phosphorus and the composition of the encoding alkaline phosphatase PhoD gene microbial community. Sci. Total Environ. 711:135080. doi:, PMID:

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    Major phosphorus in soils is unavailable, yet critical for plant development · 2020
    Not checked
  60. 60.

    Jaiswal S. K. Mohammed M. Ibny F. Y. Dakora F. D. (2021 ). Rhizobia as a source of plant growth-promoting molecules: potential applications and possible operational mechanisms. Front. Sustain. Food Syst. 4:619676

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    Jayakumar N. Paulraj P. Sajeesh P. Sajna K. Zinneera A. (2019 ). Application of native phosphate solubilizing bacteria for the use of cheap organic and inorganic phosphate source in agricultural practise of Capsicum annum (chili)-a pilot scale field study. Mater. Today: Proc. 16, 1630–1639

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    Jha V. Dafale N. A. Purohit H. J. (2019 ). Regulatory rewiring through global gene regulations by PhoB and alarmone (p) ppGpp under various stress conditions. Microbiol. Res. 227:126309. doi:, PMID:

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    Jha Y. Mohamed H. I. (2023 ). Inoculation with Lysinibacillus fusiformis strain YJ4 and Lysinibacillus sphaericus strain YJ5 alleviates the effects of cold stress in maize plants. Gesunde Pflanzen 75, 77–95

    Not in our library10.1007/s10343-022-00666-7

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    Jiang S. Lu H. Liu J. Lin Y. Dai M. Yan C. (2018 ). Influence of seasonal variation and anthropogenic activity on phosphorus cycling and retention in mangrove sediments: a case study in China. Estuar. Coast. Shelf Sci. 202, 134–144

    Not in our library10.1016/j.ecss.2017.12.011

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    Jiang Y. Tian J. Ge F. (2020 ). New insight into carboxylic acid metabolisms and pH regulations during insoluble phosphate solubilisation process by Penicillium oxalicum PSF-4. Curr. Microbiol. 77, 4095–4103. doi:, PMID:

    Not in our library10.1007/s00284-020-02238-2

  66. 66.

    Jiang F. Zhang L. Zhou J. George T. S. Feng G. (2021 ). Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 230, 304–315. doi:, PMID:

    Not in our library10.1111/nph.17081

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    Jiao P. Yuan W.-Y. Zhao H.-D. Qu J. Wang P.-W. Guan S.-Y.. (2021 ). Construction of a new plant expression vector and the development of maize germplasm expressing the Aspergillus ficuum phytase gene PhyA2. Genet. Resour. Crop. Evol. 68, 1103–1115

    Not in our library10.1007/s10722-020-01052-w

  68. 68.

    Jin T. Ren J. Li Y. Bai B. Liu R. Wang Y. (2022 ). Plant growth-promoting effect and genomic analysis of the P. putida LWPZF isolated from C. japonicum rhizosphere. AMB Express 12:101. doi:, PMID:

    Not in our library10.1186/s13568-022-01445-3

  69. 69.

    Joshi S. Gangola S. Jaggi V. Sahgal M. (2023 ). Functional characterization and molecular fingerprinting of potential phosphate solubilizing bacterial candidates from Shisham rhizosphere. Sci. Rep. 13:7003. doi:, PMID:

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    Kafle A. Cope K. R. Raths R. Krishna Yakha J. Subramanian S. Bücking H.. (2019 ). Harnessing soil microbes to improve plant phosphate efficiency in cropping systems. Agronomy 9:127

    Not in our library10.3390/agronomy9030127

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    Kageyama H. Tripathi K. Rai A. K. Cha-Um S. Waditee-Sirisattha R. Takabe T. (2011 ). An alkaline phosphatase/phosphodiesterase, PhoD, induced by salt stress and secreted out of the cells of Aphanothece halophytica, a halotolerant cyanobacterium. Appl. Environ. Microbiol. 77, 5178–5183. doi:, PMID:

    Not in our library10.1128/aem.00667-11

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    Kalayu G. (2019 ). Phosphate solubilizing microorganisms: promising approach as biofertilizers. Int. J. Agron. 2019:4917256

    Not in our library10.1155/2019/4917256

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    Kang S.-M. Khan M.-A. Hamayun M. Kim L.-R. Kwon E.-H. Kang Y.-S.. (2021 ). Phosphate-solubilizing Enterobacter ludwigii AFFR02 and Bacillus megaterium Mj1212 rescues alfalfa’s growth under post-drought stress. Agriculture 11:485

    Not in our library10.3390/agriculture11060485

  74. 74.
    Purification and immobilization of engineered glucose dehydrogenase: a new approach to producing gluconic acid from breadwaste · 2020
    Not checked
  75. 75.

    Karimzadeh J. Alikhani H. A. Etesami H. Pourbabaei A. A. (2021 ). Improved phosphorus uptake by wheat plant (Triticum aestivum L.) with rhizosphere fluorescent pseudomonads strains under water-deficit stress. J. Plant Growth Regul. 40, 162–178

    Not in our library10.1007/s00344-020-10087-3

  76. 76.

    Kaur P. Chatli A. S. (2019 ). P Solubilisers for sustainance of agriculture-a review. Ind. J. Pure App. Biosci. 7, 375–392

    Not in our library10.18782/2320-7051.7852

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    Organic Acid Profiles of Phosphate Solubilizing Bacterial Strains in the Presence of Different Insoluble Phosphatic Sources Under In vitro Buffered Conditions · 2021
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  78. 78.

    Kour D. Rana K. L. Kaur T. Sheikh I. Yadav A. N. Kumar V.. (2020 ). Microbe-mediated alleviation of drought stress and acquisition of phosphorus in great millet (Sorghum bicolour L.) by drought-adaptive and phosphorus-solubilizing microbes. Biocatal. Agric. Biotechnol. 23:101501

    Not in our library10.1016/j.bcab.2020.101501

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    Kour D. Yadav A. N. (2023 ). Alleviation of cold stress in wheat with psychrotrophic phosphorus solubilizing Acinetobacter rhizosphaerae EU-KL44. Braz. J. Microbiol. 54, 371–383. doi:, PMID:

    Not in our library10.1007/s42770-023-00913-7

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    Kumar C. Wagh J. Archana G. Naresh Kumar G. (2016 ). Sucrose dependent mineral phosphate solubilization in Enterobacter asburiae PSI3 by heterologous overexpression of periplasmic invertases. World J. Microbiol. Biotechnol. 32:194. doi:, PMID:

    Not in our library10.1007/s11274-016-2153-x

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    Kumawat K. C. Sharma P. Nagpal S. Gupta R. Sirari A. Nair R. M.. (2021 ). Dual microbial inoculation, a game changer?—bacterial biostimulants with multifunctional growth promoting traits to mitigate salinity stress in spring mungbean. Front. Microbiol. 11:600576. doi:, PMID:

    Not in our library10.3389/fmicb.2020.600576

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    Li L. Jiao Z. Hale L. Wu W. Guo Y. (2014 ). Disruption of gene pqq A or pqq B reduces plant growth promotion activity and biocontrol of crown gall disease by Rahnella aquatilis HX2. PLoS One 9:e115010. doi:, PMID:

    Not in our library10.1371/journal.pone.0115010

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    Li C. Li Q. Wang Z. Ji G. Zhao H. Gao F.. (2019 ). Environmental fungi and bacteria facilitate lecithin decomposition and the transformation of phosphorus to apatite. Sci. Rep. 9:15291. doi:, PMID:

    Not in our library10.1038/s41598-019-51804-7

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    Li H. Song C. Yang L. Qin H. Cao X. Zhou Y. (2021 ). Nutrients regeneration pathway, release potential, transformation pattern and algal utilization strategies jointly drove cyanobacterial growth and their succession. J. Environ. Sci. 103, 255–267. doi:, PMID:

    Not in our library10.1016/j.jes.2020.11.010

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    Li X. Sun P. Zhang Y. Jin C. Guan C. (2020 ). A novel PGPR strain Kocuria rhizophila Y1 enhances salt stress tolerance in maize by regulating phytohormone levels, nutrient acquisition, redox potential, ion homeostasis, photosynthetic capacity and stress-responsive genes expression. Environ. Exp. Bot. 174:104023

    Not in our library10.1016/j.envexpbot.2020.104023

  86. 86.

    Li Y. Zhang J. Gong Z. Xu W. Mou Z. (2019 ). Gcd gene diversity of quinoprotein glucose dehydrogenase in the sediment of Sancha lake and its response to the environment. Int. J. Environ. Res. Public Health 16:1

    Not in our library10.3390/ijerph16010001

  87. 87.
    Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining · 2020
    No notice
  88. 88.

    Liu J. Cade-Menun B. J. Yang J. Hu Y. Liu C. W. Tremblay J.. (2018 ). Long-term land use affects phosphorus speciation and the composition of phosphorus cycling genes in agricultural soils. Front. Microbiol. 9:1643. doi:, PMID:

    Not in our library10.3389/fmicb.2018.01643

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    Liu X. Han R. Cao Y. Turner B. L. Ma L. Q. (2022 ). Enhancing phytate availability in soils and phytate-P acquisition by plants: a review. Environ. Sci. Technol. 56, 9196–9219. doi:, PMID:

    Not in our library10.1021/acs.est.2c00099

  90. 90.

    Liu X. Jiang X. He X. Zhao W. Cao Y. Guo T.. (2019 ). Phosphate-solubilizing Pseudomonas sp. strain P34-L promotes wheat growth by colonizing the wheat rhizosphere and improving the wheat root system and soil phosphorus nutritional status. J. Plant Growth Regul. 38, 1314–1324

    Not in our library10.1007/s00344-019-09935-8

  91. 91.

    Liu J. Liu X. Zhang Q. Li S. Sun Y. Lu W.. (2020 ). Response of alfalfa growth to arbuscular mycorrhizal fungi and phosphate-solubilizing bacteria under different phosphorus application levels. AMB Express 10:200. doi:, PMID:

    Not in our library10.1186/s13568-020-01137-w

  92. 92.

    Liu C. Mou L. Yi J. Wang J. Liu A. Yu J. (2019 ). The eno gene of Burkholderia cenocepacia strain 71-2 is involved in phosphate solubilization. Curr. Microbiol. 76, 495–502. doi:, PMID:

    Not in our library10.1007/s00284-019-01642-7

  93. 93.

    Liu F. Qian J. Zhu Y. Wang P. Hu J. Lu B.. (2024 ). Phosphate solubilizing microorganisms increase soil phosphorus availability: a review. Geomicrobiol J. 41, 1–16

    Not in our library10.1080/01490451.2023.2272620

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    Lo S.-C. Tsai S.-Y. Chang W.-H. Wu I.-C. Sou N.-L. Hung S.-H. W.. (2023 ). Characterization of the pyrroloquinoline quinone producing Rhodopseudomonas palustris as a plant growth-promoting bacterium under photoautotrophic and photoheterotrophic culture conditions. Int. J. Mol. Sci. 24:14080. doi:, PMID:

    Not in our library10.3390/ijms241814080

  95. 95.

    Lü J. Gao X. Dong Z. An L. (2012 ). Expression of mitochondrial malate dehydrogenase in Escherichia coli improves phosphate solubilization. Ann. Microbiol. 62, 607–614

    Not in our library10.1007/s13213-011-0297-3

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    Ludueña L. M. Anzuay M. S. Magallanes-Noguera C. Tonelli M. L. Ibañez F. J. Angelini J. G.. (2017 ). Effects of P limitation and molecules from peanut root exudates on pqqE gene expression and pqq promoter activity in the phosphate-solubilizing strain Serratia sp. S119. Res. Microbiol. 168, 710–721. doi:, PMID:

    Not in our library10.1016/j.resmic.2017.07.001

  97. 97.

    Luthfiana N. Inamura N. Tantriani S. Sato T. Saito K. Oikawa A.. (2021 ). Metabolite profiling of the hyphal exudates of Rhizophagus clarus and Rhizophagus irregularis under phosphorus deficiency. Mycorrhiza 31, 403–412. doi:, PMID:

    Not in our library10.1007/s00572-020-01016-z

  98. 98.

    Lynch J. P. (2019 ). Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol. 223, 548–564. doi:, PMID:

    Not in our library10.1111/nph.15738

  99. 99.

    Lyu J. Huang Y. Nie Q. Lu C. Zhang Y. Fu X.. (2023 ). Spatiotemporal variations and risk characteristics of potential non-point source pollution driven by LUCC in the loess plateau region, China. Front. Ecol. Evol. 11:1253328

    Not in our library10.3389/fevo.2023.1253328

  100. 100.

    Ma X. Li X. Ludewig U. (2021 ). Arbuscular mycorrhizal colonization outcompetes root hairs in maize under low phosphorus availability. Ann. Bot. 127, 155–166. doi:, PMID:

    Not in our library10.1093/aob/mcaa159

  101. 101.

    Ma J. Ma Y. Wei R. Chen Y. Weng L. Ouyang X.. (2021 ). Phosphorus transport in different soil types and the contribution of control factors to phosphorus retardation. Chemosphere 276:130012. doi:, PMID:

    Not in our library10.1016/j.chemosphere.2021.130012

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    Mahdi I. Fahsi N. Hafidi M. Benjelloun S. Allaoui A. Biskri L. (2021 ). Rhizospheric phosphate solubilizing Bacillus atrophaeus GQJK17 S8 increases quinoa seedling, withstands heavy metals, and mitigates salt stress. Sustain. For. 13:3307

    Not in our library10.3390/su13063307

  103. 103.

    Mei Y. Zhang M. Cao G. Zhu J. Zhang A. Bai H.. (2024 ). Endofungal bacteria and ectomycorrhizal fungi synergistically promote the absorption of organic phosphorus in Pinus massoniana. Plant Cell Environ. 47, 600–610. doi:, PMID:

    Not in our library10.1111/pce.14742

  104. 104.

    Mendoza-Arroyo G. E. Chan-Bacab M. J. Aguila-Ramírez R. N. Ortega-Morales B. O. Canché Solís R. E. Chab-Ruiz A. O.. (2020 ). Inorganic phosphate solubilization by a novel isolated bacterial strain Enterobacter sp. ITCB-09 and its application potential as biofertilizer. Agriculture 10:383

    Not in our library10.3390/agriculture10090383

  105. 105.

    Murgese P. Santamaria P. Leoni B. Crecchio C. (2020 ). Ameliorative effects of PGPB on yield, physiological parameters, and nutrient transporter genes expression in barattiere (Cucumis melo L.). J. Soil Sci. Plant Nutr. 20, 784–793

    Not in our library10.1007/s42729-019-00165-1

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    Nacoon S. Seemakram W. Ekprasert J. Jogloy S. Kuyper T. W. Mongkolthanaruk W.. (2022 ). Promoting growth and production of sunchoke (Helianthus tuberosus) by co-inoculation with phosphate solubilizing bacteria and arbuscular mycorrhizal fungi under drought. Front. Plant Sci. 13:1022319. doi:, PMID:

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    Ortega-Torres A. E. Rico-García E. Guzmán-Cruz R. Torres-Pacheco I. Tovar-Pérez E. G. Guevara-González R. G. (2021 ). Addition of phosphatases and phytases to mature compost to increase available phosphorus: a short study. Agronomy 11:2555

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    Rasul M. Yasmin S. Yahya M. Breitkreuz C. Tarkka M. Reitz T. (2021 ). The wheat growth-promoting traits of Ochrobactrum and Pantoea species, responsible for solubilization of different P sources, are ensured by genes encoding enzymes of multiple P-releasing pathways. Microbiol. Res. 246:126703. doi:, PMID:

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    Ribeiro V. P. Marriel I. E. Sousa S. M. D. Lana U. G. D. P. Mattos B. B. Oliveira C. A.. (2018 ). Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz. J. Microbiol. 49, 40–46. doi:, PMID:

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    Sharma S. Compant S. Ballhausen M.-B. Ruppel S. Franken P. (2020 ). The interaction between Rhizoglomus irregulare and hyphae attached phosphate solubilizing bacteria increases plant biomass of Solanum lycopersicum. Microbiol. Res. 240:126556. doi:, PMID:

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    Xing Y. Wang F. Yu S. Zhu Y. Ying Y. Shi W. (2023 ). Enhancing Phyllostachys edulis seedling growth in phosphorus-deficient soil: complementing the role of phosphate-solubilizing microorganisms with arbuscular mycorrhizal fungi. Plant Soil, 1–18

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    Xu L. Cao H. Li C. Wang C. He N. Hu S.. (2022 ). The importance of rare versus abundant phoD-harboring subcommunities in driving soil alkaline phosphatase activity and available P content in Chinese steppe ecosystems. Soil Biol. Biochem. 164:108491

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    Yadav K. Kumar C. Archana G. Kumar G. N. (2014 ). Artificial citrate operon and Vitreoscilla hemoglobin gene enhanced mineral phosphate solubilizing ability of Enterobacter hormaechei DHRSS. Appl. Microbiol. Biotechnol. 98, 8327–8336. doi:, PMID:

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    Yarzábal L. A. Monserrate L. Buela L. Chica E. (2018 ). Antarctic Pseudomonas spp. promote wheat germination and growth at low temperatures. Polar Biol. 41, 2343–2354

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    Yuan H. Cai Y. Wang H. Liu E. Li Q. Zeng Q. (2023 ). How phoD-harboring functional microbial populations trigger the release risk of phosphorus in water sediment system of Shijiuhu Lake, China after experiencing the transseasonal shift. Water Res. 240:120107. doi:, PMID:

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    Zaborowska M. Wyszkowska J. Kucharski J. (2020 ). Soil enzyme response to bisphenol F contamination in the soil bioaugmented using bacterial and mould fungal consortium. Environ. Monit. Assess. 192:20

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    Zeng Q. Wu X. Wen X. (2016 ). Effects of soluble phosphate on phosphate-solubilizing characteristics and expression of gcd gene in Pseudomonas frederiksbergensis JW-SD2. Curr. Microbiol. 72, 198–206. doi:, PMID:

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    Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium · 2018
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    Zhang J. Wang P. Tao Z. Tian H. Guo T. (2022 ). Phosphate-solubilizing bacteria abate cadmium absorption and restore the rhizospheric bacterial community composition of grafted watermelon plants. J. Hazard. Mater. 438:129563

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    Zolfaghari R. Rezaei K. Fayyaz P. Naghiha R. Namvar Z. (2021 ). The effect of indigenous phosphate-solubilizing bacteria on Quercus brantii seedlings under water stress. J. Sustain. For. 40, 733–747

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