Organic acid-mediated phosphorus mobilization in black soils: differential effects of maize root exudates on alfisols and mollisols in Northeast China

Wenzhi Zhao; Yuan Zhang; Xu Xie; He Li; Jintao Zhang

doi:10.1371/journal.pone.0333230

Abstract

Soil phosphorus exists in various forms, but only minimal soluble phosphorus is bioavailable. While phosphate fertilizers address deficiency, low efficiency leads to insoluble phosphate accumulation, wasting resources. Enhancing phosphorus availability by converting non-available forms is a critical research priority. Under phosphorus-deficient conditions, plants enhance soil phosphorus availability by secreting organic acids. This study aims to explore phosphorus activation in Alfisol and Mollisol soils through maize root-secreted organic acids. Semi-hydroponic maize cultivation under low/medium/high phosphorus levels and sterilized soil (Alfisol/Mollisol) incubation with root-secreted organic acids (0.5–2%). Exudates analyzed via UHPLC-MS/MS; soil phosphorus dynamics monitored over 60 days. Under phosphorus limitation, maize root exudates showed marked increases in malic, citric, tartaric, and trans-aconitic acids. Soil incubation revealed peak phosphorus release during 0–20 d, with Alfisol exhibiting 95.8% (tartaric), 91.1% (citric), 81.8% (malic), and 67.7% (trans-aconitic) increases in available phosphorus, while Mollisol showed 94.0%, 119.6%, 83.1%, and 75.2% increments, respectively. Tartaric and citric acids outperformed others, boosting H₂O-P and NaHCO₃-P_i, whereas malic and trans-aconitic acids mainly elevated NaHCO₃-P_i. Fractionation analysis highlighted distinct mechanisms: citric acid primarily mobilizes HCl-P; malic acid mainly targets NaOH-P_i and HCl-P; tartaric acid mobilizes NaOH-P_o, HCl-P, and NaOH-P_i; while trans-aconitic acid influences NaOH-P_o, HCl-P, and Res-P. These findings demonstrate acid-specific phosphorus pool mobilization, identifying tartaric and citric acids as most effective, supporting optimized phosphorus management strategies in black soils.

Citation: Zhao W, Zhang Y, Xie X, Li H, Zhang J (2025) Organic acid-mediated phosphorus mobilization in black soils: differential effects of maize root exudates on alfisols and mollisols in Northeast China. PLoS One 20(9): e0333230. https://doi.org/10.1371/journal.pone.0333230

Editor: Paulo H. Pagliari, University of Minnesota, UNITED STATES OF AMERICA

Received: May 19, 2025; Accepted: September 11, 2025; Published: September 24, 2025

Copyright: © 2025 Zhao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This research was supported by Liaoning Provincial Science and Technology Plan Joint Program (Natural Science Foundation-General Program) (2024-MSLH-492) and the Project of China Geological Survey (grant number DD20242328).Wenzhi Zhao received the fund awards. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

1 Introduction

Phosphorus (P), a critical yet frequently limiting nutrient for plant productivity and ecosystem functioning in terrestrial environments, exhibits substantial variation in bioavailability due to its complex speciation in soils [1,2]. In northeast China’s black soil regions, while total phosphorus (TP) reserves are abundant, low bioavailability persists due to mineral adsorption, organic complexation, and land management practices [3]. Conventional phosphate fertilization, though widely adopted to address P deficiencies and enhance crop yields, suffers from limited efficiency as 70–90% of applied P becomes immobilized in insoluble calcium-, iron-, and aluminum-phosphate forms, exacerbating resource waste [4,5]. Furthermore, unutilized P migrates via leaching and runoff, posing risks of eutrophication in aquatic systems and groundwater contamination [6]. Given that phosphate rock, the primary source of P fertilizers, is a finite, non-renewable resource facing escalating extraction costs and diminishing reserves, innovative strategies to enhance soil P availability through speciation conversion are urgently required [7].

The challenge of phosphorus inefficiency is particularly acute in the globally vital black soil regions, such as Northeast China’s “breadbasket”. These deep, carbon-rich soils are among the world’s most productive but face significant degradation threats, including organic matter decline and nutrient imbalances, which exacerbate phosphorus fixation and reduce fertilizer efficacy [8,9]. Enhancing P bioavailability in these critical agroecosystems is thus not merely a local concern but a cornerstone of global food security, given their outsized contribution to staple grain production. Organic acid-mediated phosphorus mobilization, leveraging a naturally evolved plant strategy, represents a fundamentally sustainable pathway with global relevance [10–13]. By harnessing inherent root processes to unlock fixed soil P reserves, this approach reduces dependence on finite, geopolitically concentrated rock phosphate resources [14–17].

Critically, optimizing P bioavailability through organic acids in black soils offers significant co-benefits for climate change mitigation. By improving the efficiency of existing soil P reserves and reducing fertilizer demand, organic acid-mediated strategies can lower the carbon footprint of crop production in these regions [18]. Furthermore, reducing P runoff protects water quality and mitigates a potent secondary greenhouse gas (GHG) source: eutrophic aquatic systems. The vast scale of agriculture on the Northeast China black soil belt means that widespread adoption of such P-efficiency strategies could yield substantial regional GHG reductions [19,20]. For black soils specifically, minimizing tillage disturbance for fertilizer incorporation–often replaced by targeted organic acid approaches–also helps preserve soil organic carbon, further contributing to climate goals [21,22].

Under phosphorus deficiency, plants enhance rhizospheric phosphorus (P) availability through root-secreted organic acids, which mobilize fixed P via ligand exchange and competitive adsorption [23–29]. However, critical knowledge gaps persist. Existing studies predominantly quantify total P mobilization but lack resolution on how specific organic acids target distinct P fractions across divergent soil type [30–32]. Furthermore, the differential responsiveness of Alfisols and Mollisols to organic acid-mediated P activation remains poorly characterized, despite their contrasting mineralogy and organic matter content. Agronomically, while maize is a key crop in Northeast China, its root exudate profile under P limitation-and the subsequent impact on regional soils-has not been systematically linked to P fraction dynamics [33,34]. Consequently, current strategies for optimizing P bioavailability remain generic, with limited capacity to tailor interventions based on soil-specific P speciation or crop exudate signatures.

To bridge these gaps, this study integrates root exudation chemistry with soil P fractionation kinetics. Using semi-hydroponic maize cultivation and sterile soil incubation, we investigated: 1) genotype-specific organic acid secretion under P limitation; 2) differential activation pathways of four key organic acids (citric, malic, tartaric, trans-aconitic) on Alfisol versus Mollisol P pools; and 3) time-dependent redistribution of Hedley P fraction to establish acid- and soil-specific mobilization mechanisms.

2 Materials and methods

2.1 Experimental design I: Semi-hydroponic maize cultivation for root exudate collection

(1) Semi-hydroponic experiment of maize.

Following surface sterilization with 10% H₂O₂ for 10 minutes, maize seeds of three varieties (SY-1, ZD-958, XY-335) were thoroughly rinsed with distilled water, soaked in warm water for 10 hours, and germinated in a semi-hydroponic system under controlled humidity maintained by daily irrigation with distilled water. Upon emergence of the first leaf, seedlings were subjected to nutrient solutions with three phosphorus (P) levels: low (LP, 1 μM P), medium (MP, 100 μM P), and high (HP, 250 μM P), supplied via KH₂PO₄. Potassium concentrations between LP and MP treatments were balanced using KCl. Nutrient solutions (initial pH 6.0) were refreshed every 3 days, with pH readjusted to 6.0 using 1 M HCl or NaOH during each replacement to ensure consistent growth conditions.

(2) Collection and analysis of root-secreted organic acids.

Root exudates were collected from 18-day-old maize plants using a standardized protocol: Roots were gently rinsed 3–5 times with distilled water during morning hours (10:00 AM), then immersed in 0.5 mM CaCl₂ solution for 4 h under microbial inhibition with 0.01% thymol [35]. The collected solution underwent sequential filtration through qualitative filter paper (removing particulate residues) followed by a 0.22 μm nylon membrane. Processed exudates were immediately concentrated, flash-frozen at −80°C, and stored at −20°C until analysis. Organic acid profiles were quantitatively determined using ultra-high-performance liquid chromatography coupled with tandem mass spectrometry (UHPLC-MS/MS) with external calibration standards [36].

2.2 Experimental Design II: Sterile soil incubation for phosphorus activation

Soil incubation period and organic acid concentration selection were based on preliminary kinetic studies and established literature on organic acid-mediated P release in black soils. Previous research indicates that maximum P solubilization typically occurs within 2–4 weeks of organic acid application, followed by potential re-adsorption or stabilization. A 60-day incubation period was chosen to capture the complete dynamic trajectory of P release, stabilization, and potential decline, ensuring observation of both short-term solubilization peaks (expected within 0–20 d) and longer-term equilibrium states [37,38]. Similarly, the applied organic acid concentrations (0.5–2% w/w) were selected to reflect: 1) the range of physiologically relevant concentrations observed in maize rhizosphere microsites under P stress, where localized concentrations can significantly exceed bulk soil levels; and 2) concentrations demonstrated in prior incubation studies to effectively mobilize recalcitrant P pools in Alfisols and Mollisols without inducing excessive artificial acidification beyond field-relevant conditions [39].

Soil samples (0–20 cm depth) were collected from two long-term maize fields in Heilongjiang Province, China: brown soil (Alfisol) from Heihe field observation station (127°26′56″ E, 50°15′47″ N) and black soil (Mollisol) from Hulan field observation station (126°39′49″ E, 45°58′26″ N). Soils were air-dried, sterilized by gamma irradiation (25 kGy), and sieved through a 100-mesh stainless steel screen (0.15 mm). Triplicate 300 g aliquots were transferred to sterile 500 mL polypropylene bottles and incubated at 25°C with gravimetric moisture maintained at 0.3 g·g ⁻ ¹ (30% water-holding capacity). After a 7-day acclimation phase, soils underwent sterilization validation through microbial plate assays to confirm sterility. Heihe and Hulan field observation station permitted the work, field site access, and soil sampling in cultivated areas.

Root-secreted organic acids (0.5%, 1%, 1.5%, 2% w/w) were aseptically applied as phosphorus activators, with untreated controls (CK) receiving equivalent sterile water. Treatments were homogenized under laminar airflow to prevent contamination. Soil sampling was conducted at eight intervals (0, 5, 10, 20, 30, 40, 50, 60 days post-treatment), with triplicate samples immediately frozen at −80°C for subsequent physicochemical analyses.

2.3 Soil physicochemical characterization

Total phosphorus (TP) content was determined via inductively coupled plasma optical emission spectroscopy, while available phosphorus (AP) was extracted with NH₄Cl-HCl and measured by molybdenum-antimony anti-spectrophotometry. Phosphorus speciation analysis using the Hedley sequential fractionation method revealed distinct partitioning patterns between the Alfisol and Mollisol soils..All analytical determinations were performed in triplicate, with results expressed as mean ± standard error (SE). Key soil properties are summarized in Table 1. Both soil types exhibit acidic conditions (pH < 7), with AP representing 3.59% and 6.34% of TP in the Alfisol and Mollisol soils, respectively, highlighting limited phosphorus bioavailability in both pedological systems.

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Table 1. Basic characteristics of soils in the study area.

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Labile phosphorus pools, including H₂O-extractable inorganic P (H₂O-Pi: 0.91% vs. 1.56%) and NaHCO₃-extractable fractions (inorganic NaHCO₃-P_i: 2.15% vs. 3.78%; organic NaHCO₃-P_o: 7.09% vs. 10.43%), collectively constituted the bioavailable P reservoirs, with the Mollisol exhibiting higher labile P proportions. Moderately labile NaOH-extractable organic P (NaOH-P_o) dominated both soils, representing 39.19% (Alfisol) and 31.25% (Mollisol) of total P. Stable P fractions (HCl-P + Res-P) accounted for 18–20% of total P in both pedons, demonstrating comparable long-term P sequestration capacities despite divergent pedogenic processes.

2.4 Statistical analysis

Statistical analyses were performed using SPSS 18.0 (IBM Corp., Armonk, NY, USA) and Canoco 4.5 (Microcomputer Power, Ithaca, NY, USA). Redundancy analysis (RDA), a constrained ordination method, was conducted to quantify multivariate relationships between P speciation (Hedley fractions) and environmental variables. RDA was selected over alternative multivariate methods due to its ability to explicitly model the relationship between response variables (P fractions) and explanatory environmental variables (soil physicochemical properties). As a constrained ordination technique, RDA directly tests hypotheses regarding the influence of predefined environmental factors on multivariate response data, aligning with our objective to quantify drivers of phosphorus fraction dynamics under organic acid treatments.

Prior to analysis, data validation procedures were implemented: 1) Potential outliers were identified via visual inspection of boxplots and scatterplots, with data points exceeding ±3 standard deviations from the mean flagged; 2) No outliers required exclusion as all values fell within biologically plausible ranges; 3) Multicollinearity among predictors was assessed via variance inflation factors (VIF), with all variables retaining VIF < 5, well below the critical threshold of 10.

3 Results

3.1 Changes of organic acids secreted by maize roots under phosphorus restriction

Under varying phosphorus regimes, three maize varieties (SY-1, ZD-958, XY-335) demonstrated genotype-specific organic acid secretion patterns in root exudates (Fig 1). Acetic, malic, tartaric, and trans-aconitic acids emerged as dominant components across all varieties, while succinic and lactic acids showed minimal secretion. Low phosphorus (LP, 1 μM P) treatment markedly stimulated citric and malic acid production in all genotypes, with SY-1 exhibiting superior adaptive responses through 34.1–63.4% higher secretion of these acids compared to ZD-958 and XY-335.

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Fig 1. Effects of varying phosphorus supplies on the rhizosphere organic acid concentrations of three maize varieties.

Different lowercase letters indicate significant differences among phosphorus treatments for the same organic acid; different uppercase letters indicate significant differences among maize varieties for the same organic acid.

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Distinct varietal responses emerged in tartaric and trans-aconitic acid dynamics under phosphorus limitation. SY-1 and ZD-958 showed progressive decreases in tartaric acid secretion under LP stress, contrasting with XY-335’s 16.1–47.9% increase. Conversely, trans-aconitic acid secretion exhibited inverse patterns: LP treatment enhanced its production in SY-1 and ZD-958 by 3.4–22.0%, while suppressing secretion in XY-335 by 11.2–13.3%. These differential regulatory mechanisms highlight genotype-dependent strategies for phosphorus acquisition, with SY-1 demonstrating particularly effective metabolic adjustments through coordinated upregulation of key organic acids under nutrient deprivation.

These genotype-specific exudation profiles have direct implications for maize breeding programs. SY-1’s superior capacity to upregulate citric and malic acid secretion under P limitation positions it as a prime candidate for developing P-efficient genotypes. Incorporating such root exudate traits into breeding schemes could reduce fertilizer dependency in black soil regions, aligning with sustainable intensification goals.

3.2 Influence of different treatment levels on soil AP

Soil activation experiments were conducted using four maize root-secreted organic acids–malic acid, citric acid, tartaric acid, and trans-aconitic acid–applied at five concentrations (0%, 0.5%, 1%, 1.5%, 2% w/w). Phosphorus fractionation dynamics were monitored over a 60-day incubation period, with temporal sampling at 5, 10, 20, 30, 40, 50, and 60 days post-application.

The activation of AP in both soils demonstrated concentration-dependent variations in response to organic acid applications, as illustrated in Fig 2. Higher organic acid concentrations (0.5–2%) consistently enhanced AP mobilization, with maximal activation observed at the 2% treatment level. After application, AP concentrations increased sharply during the first 10–15 days, followed by a gradual decline and stabilization. This biphasic response–rapid solubilization followed by stabilization–was consistent across all four organic acids, with activation magnitudes directly proportional to applied concentrations.

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Fig 2. Changes in the AP content at various time points in soils amended with organic acids over the 60 d incubation period.

Different lowercase letters indicate significant differences among incubation times for the same organic acid; different uppercase letters indicate significant differences among organic acids at the same incubation time. Panels: AP variation in organic acid-amended soils across 60 d. AP: available P.

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In Alfisol (Fig 2a, 2b), all organic acids significantly increased AP concentrations at equivalent application rates (0.5–2% w/w), with efficacy ranking: citric acid > malic acid > tartaric acid > trans-aconitic acid. Citric acid induced the strongest activation, elevating AP by 21.1–30.2% (0.5%), 31.0–49.5% (1%), 64.0–91.1% (1.5%), and 101.5–143.8% (2%). Malic acid showed moderate effects, ranging from minimal change up to 28.1% (0.5%) to 70.4–95.8% (2%), while tartaric and trans-aconitic acids had weaker initial responses at <1% concentration but still achieved 53.6–81.8% and 48.3–67.7% increases at 2%, respectively.

In Mollisol (Fig 2c, 2d), all acids enhanced AP across sequential incubation periods at identical concentrations. Citric acid generated the highest increments (7.4–26.3% to 91.6–119.6%), followed by malic acid (up to 17.2% initially, rising to 83.1%), tartaric acid (5.0–59.8% to 70.3–94.0%), and trans-aconitic acid (effects up to 11.0% initially, reaching 75.2%). Notably, malic acid outperformed citric acid at low concentrations (<0.5% w/w) during early incubation (≤20 days), but citric acid surpassed all others above 1% concentration, peaking at 119.6% elevation.

While the efficacy hierarchy remained consistent across both Alfisol and Mollisol, the magnitude of AP activation varied significantly. Citric acid induced substantially greater AP elevation in Alfisol than in Mollisol. Similarly, malic acid’s performance was more pronounced in Alfisol versus Mollisol. Trans-aconitic acid consistently exhibited the weakest effects in both soils, though its lowest concentration (0.5%) triggered near-neutral responses in Alfisol compared to slightly positive effects in Mollisol. The anomaly of malic acid surpassing citric acid at <0.5% w/w during early incubation was exclusive to Mollisol, highlighting soil-specific ligand interactions at trace concentrations.

The observed concentration threshold for net P mobilization has practical significance for amendment formulations. Field applications should exceed this critical concentration to avoid unintended P immobilization, particularly in Alfisols where adsorption dominance was more pronounced. Precision delivery systems could optimize acid efficacy while minimizing application rates.

The cultivation trials revealed that elevated concentrations of organic acids (2% w/w) elicited the most pronounced modifications in phosphorus fractionation profiles across both soil types. Consequently, subsequent experiments were conducted using elevated concentrations of activators.

3.3 Differential responses of soil P Pools to high-dose organic acid amendments

The effects of citric acid, tartaric acid, malic acid and trans-aconitic acid at a concentration of 2% on soil P fractions in two types of soil were depicted in Fig 3.

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Fig 3. Average percentage of different P fractions at various time points in soils amended with organic acids (organic acids applied at 2% by weight in the incubated soil) over the 60 d incubation period for (a) Alfisol, (b) Mollisol.

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In the Alfisol soil (Fig 3a), sequential extraction analysis revealed that citric acid amendment significantly enhanced labile phosphorus fractions, with H₂O-P and NaHCO₃-P_i contents increasing to 2.28% and 4.87% respectively by Day 20, showing a marked elevation compared to the CK values (0.84% and 2.20%). Both fractions exhibited an initial increase from Day 0 to Day 20 followed by a gradual decline, yet maintained consistently higher concentrations than CK throughout the experiment. The organic phosphorus component NaHCO₃-P_o showed a transient increase during early incubation before decreasing to stabilization, while NaOH-P_o demonstrated a progressive reduction over time, suggesting stimulated mineralization processes [27]. The HCl-P fraction decreased continuously with prolonged incubation, contributing to the observed enhancement in labile P pools. Notably, the NaOH-P_i and residual-P fractions remained stable without significant variations during the 20-day experimental period.

Tartaric acid application induced comparable dynamics to citric acid treatment, with H₂O-P, NaHCO₃-P_i, and NaHCO₃-P_o exhibiting similar temporal patterns. The NaOH-P_i fraction showed a gradual decline throughout the incubation period, while NaOH-P_o and HCl-P concentrations displayed a distinct trajectory: an initial reduction, followed by partial recovery, and eventual stabilization at values below those observed in the CK soil. Notably, the Res-P pool remained stable without significant variations despite prolonged cultivation.

Malic acid treatment significantly enhanced the NaHCO₃-P_i fraction, peaking at 4.23%, while H₂O-P and NaHCO₃-P_o exhibited a transient increase followed by stabilization with prolonged incubation. Concurrently, NaOH-P_i and HCl-P displayed dynamic trends characterized by an initial decline, subsequent recovery, and eventual stabilization at levels below those in the CK soil. In contrast, NaOH-P_o and Res-P remained stable without significant variations throughout the experimental period, highlighting the selective mobilization of specific phosphorus pools under organic acid treatment.

Sequential extraction analysis revealed distinct phosphorus mobilization patterns under trans-aconitic acid treatment. The NaHCO₃-P_i fraction exhibited significant activation, peaking at 4.06%, while H₂O-P and NaHCO₃-P_o showed marginal increases (slightly above CK levels) with transient fluctuations before stabilization. The HCl-P fraction displayed a biphasic response–initial reduction followed by recovery and stabilization–though remaining below CK values. In contrast, NaOH-P_o exhibited a progressive decrease with prolonged incubation, while NaOH-P_i and Res-P remained stable without significant variations. These trends underscore the selective activation and redistribution of specific phosphorus pools induced by trans-aconitic acid.

In the Mollisol soil (Fig 3b), Sequential extraction analysis demonstrated pronounced phosphorus fraction redistribution in Mollisol under organic acid treatments. Citric acid significantly enhanced labile P pools, elevating H₂O-P and NaHCO₃-P_i concentrations, while NaHCO₃-P_o and NaOH-P_i exhibited an initial rise followed by stabilization at levels exceeding CK. Notably, HCl-P decreased substantially, reaching 11.55% by Day 20 compared to 18.65% in CK. Tartaric, malic, and trans-aconitic acids induced similar trends for H₂O-P, NaHCO₃-P_i, and NaHCO₃-P_o as citric acid, though with NaOH-P_i consistently lower than CK. Mechanistic divergence emerged in P activation pathways: citric, tartaric, and malic acids primarily mobilized labile P through HCl-P depletion, whereas trans-aconitic acid preferentially reduced NaOH-P_o (from 12.4% to 9.2% by Day 20) to enhance labile P pools. Residual phosphorus remained stable across treatments, confirming selective chemical mobilization of specific fractions.

Comparative analysis revealed differential phosphorus mobilization capacities among organic acids across contrasting soil matrices, with Mollisol exhibiting greater responsiveness than Alfisol in labile phosphorus pool redistribution. Citric acid and tartaric acid treatments demonstrated superior efficacy in activating labile P fractions relative to malic acid and trans-aconitic acid, aligning with their distinct chemical activation pathways. This hierarchy of organic acid performance underscores soil-specific interactions in phosphorus fraction dynamics, where Mollisol’s enhanced reactivity amplified treatment effects compared to Alfisol’s more conservative response.

4 Discussion

Redundancy analysis (RDA) revealed significant ordination patterns between soil P fractions and physicochemical properties under organic acid treatments (Fig 4).

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Fig 4. Results of RDA for P fractions and soil physicochemical properties in 2% level treatments.

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In citric acid-treated soils (Fig 4a), pH exhibited a significant negative correlation with H₂O-P, NaHCO₃-P_i, and AP, but a positive correlation with HCl-P. AP showed strong positive correlations with H₂O-P, NaHCO₃-P_i, NaHCO₃-P_o, and NaOH-P_i, and negative correlations with HCl-P, Res-P, and NaOH-P_o, indicating its primary derivation from labile and moderately labile P fractions (H₂O-P, NaHCO₃-P_i, NaHCO₃-P_o, NaOH-P_i). The significant negative correlation between HCl-P and AP, as well as with other labile P components, identifies HCl-P as the principal source of mobilized phosphorus. This aligns with observed HCl-P reduction and concurrent AP elevation. While citric acid-induced pH decline correlated strongly with HCl-P dissolution, sustained AP elevation post-pH recovery (Day > 20) suggests complementary activation mechanisms. Ligand exchange between carboxylic anions and HPO₄^2-/H₂PO₄^- likely contributed to P release beyond initial acidification effects, as evidenced by persistent AP levels exceeding controls despite pH stabilization.

Malic acid treatment (Fig 4b) induced concurrent reductions in NaOH-P_i and HCl-P across both soils, signifying decreased Fe/Al/Ca-associated inorganic phosphorus (P_i). Comparative analysis revealed lower phosphorus activation efficacy relative to citric acid. Significant negative correlations emerged between pH and H₂O-P, NaHCO₃-P_i, AP, and NaHCO₃-P_o, while pH showed a positive correlation with HCl-P. HCl-P exhibited strong negative correlations with AP and labile P fractions (H₂O-P, NaHCO₃-P_i, NaHCO₃-P_o), mirroring the mobilization patterns observed under citric acid treatment. These parallel correlation dynamics suggest shared activation mechanisms between the two organic acids, likely involving proton-mediated dissolution of mineral-bound P and ligand exchange processes.

Tartaric acid treatment (Fig 4c) demonstrated distinct phosphorus mobilization dynamics, with pH exhibiting significant negative correlations with H₂O-P, NaHCO₃-P_i, and AP, and positive correlations with NaOH-P_o and HCl-P. Strong negative correlations emerged between NaOH-P_i, NaOH-P_o, HCl-P, and labile P fractions (AP, NaHCO₃-P_i, H₂O-P, NaHCO₃-P_o), identifying these stable P pools as contributors to labile P mobilization. HCl-P displayed the strongest inverse relationship with AP, indicating its dominant role in P activation. Concurrently, the progressive decline in NaOH-P_o concentration (from 12.4% to 9.2% by Day 20) suggests partial mineralization of organically bound phosphorus facilitated by tartaric acid. These patterns highlight a dual activation mechanism combining mineral-bound P dissolution (HCl-P depletion) and organic P transformation (NaOH-P_o reduction), distinct from other organic acid treatments.

Trans-aconitic acid treatment (Fig 4d) revealed distinct phosphorus mobilization dynamics, with pH demonstrating significant negative correlations with H₂O-P, NaHCO₃-P_i, and AP, contrasting with positive associations observed for NaOH-P_o, HCl-P, and Res-P. Strong inverse relationships emerged between NaOH-P_o, HCl-P, Res-P, and labile P fractions (AP, H₂O-P, NaHCO₃-P_i, NaHCO₃-P_o), identifying these stable pools as contributors to phosphorus release. NaOH-P_o exhibited the most pronounced negative correlation with AP, indicating its predominant role as a mobilized phosphorus source. The progressive reduction in NaOH-P_o and HCl-P highlight the compound’s capacity to destabilize recalcitrant organic and mineral-bound phosphorus. These patterns suggest ligand-promoted dissolution of stable P pools, with minimal residual phosphorus variation (<2% change), underscoring the efficacy of trans-aconitic acid in redistributing phosphorus from stable to labile fractions through chemical interaction mechanisms.

In the two contrasting black soils investigated here, citric acid and malic acid emerged as the most effective organic acids for enhancing phosphorus availability, as evidenced by substantial increases in labile P fractions. Tartaric acid showed moderate efficacy in both soils, while trans-aconitic acid exhibited the weakest mobilization capacity in Alfisols. Crucially, the efficacy of these organic acids varied significantly between the Alfisol and Mollisol, with Mollisol demonstrating greater responsiveness in labile P redistribution. This indicates that while root-secreted organic acids can accelerate the transformation of recalcitrant P pools into bioavailable forms, their performance is highly soil-specific. Thus, although organic acids clearly enhance P availability by facilitating legacy P fraction transformation, their practical effectiveness depends critically on inherent soil properties, including mineralogy, organic matter content, pH buffering capacity, and initial P speciation distribution–factors that diverged markedly between the Alfisol and Mollisol studied.

While this study elucidates chemical mechanisms of phosphorus mobilization, several limitations warrant consideration. First, the use of sterilized soils excluded biotic interactions, potentially overestimating direct acid effects; therefore, field validation is required to quantify contributions from microbial P-solubilizing communities. Second, the 60-day incubation captured short-term solubilization dynamics but not long-term P re-fixation processes; studies exceeding 6 months are needed to evaluate the persistence of mobilized P.

5 Conclusion

The maize cultivation experiment identified significant accumulation of acetic acid, malic acid, tartaric acid, and trans-aconitic acid in root exudates, with phosphorus limitation inducing marked quantitative changes specifically in malic, citric, tartaric, and trans-aconitic acid levels.

Soil activation studies demonstrated that citric, malic, tartaric, and trans-aconitic acids differentially mobilized residual phosphorus across soil types, targeting distinct P fractions. Citric acid predominantly enhanced labile P by reducing HCl-P, while malic acid concurrently decreased NaOH-P_i and HCl-P to achieve similar effects. Tartaric acid exhibited broader activation capacity, reducing NaOH-P_o, HCl-P, and NaOH-P_i, whereas trans-aconitic acid uniquely mobilized Res-P in addition to NaOH-P_o and HCl-P. pH acidification and ligand exchange mechanisms drove P release in citric and malic acid treatments, while tartaric and trans-aconitic acids additionally promoted organophosphorus mineralization, evidenced by progressive NaOH-P_o reduction. These findings establish organic acid-specific pathways for phosphorus mobilization, with HCl-P depletion common to all treatments and NaOH-P_o/Res-P reduction distinguishing trans-aconitic acid’s activation profile.

Supporting information

S1 Fig. Semi hydroponic cultivation of maize seedlings.

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S2 Fig. Changes in the AP content at various time points in Alfisols amended with LMWOAs over the 60 d incubation period.

(LMWOAs applied at 1% by weight in the incubated soil). CK: CK treatment, MA: malic acid, CA: citric acid, TA: tartaric acid, TAa: trans-aconitic acid.

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S3 Fig. Changes in the AP content at various time points in Alfisols amended with LMWOAs over the 60 d incubation period.

(LMWOAs applied at 1.5% by weight in the incubated soil). CK: CK treatment, MA: malic acid, CA: citric acid, TA: tartaric acid, TAa: trans-aconitic acid.

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S4 Fig. Changes in the AP content at various time points in Mollisols amended with LMWOAs over the 60 d incubation period.

(LMWOAs applied at 1% by weight in the incubated soil). CK: CK treatment, MA: malic acid, CA: citric acid, TA: tartaric acid, TAa: trans-aconitic acid.

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S5 Fig. Changes in the AP content at various time points in Mollisols amended with LMWOAs over the 60 d incubation period.

(LMWOAs applied at 1.5% by weight in the incubated soil). CK: CK treatment, MA: malic acid, CA: citric acid, TA: tartaric acid, TAa: trans-aconitic acid.

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S1 Table. Operating parameters of LC-MSMS.

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S2 Table. Physical and chemical characteristics at various time points in the soils amended with malic acid (malic acid applied at 2% by weight in the incubated soil).

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S3 Table. Physical and chemical characteristics at various time points in the soils amended with tartaric acid (tartaric acid applied at 2% by weight in the incubated soil).

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S4 Table. Physical and chemical characteristics at various time points in the soils amended with citric acid (citric acid applied at 2% by weight in the incubated soil).

https://doi.org/10.1371/journal.pone.0333230.s009

(DOC)

S5 Table. Physical and chemical characteristics at various time points in the soils amended with trans-aconitonic acid (trans-aconitonic acid applied at 2% by weight in the incubated soil).

https://doi.org/10.1371/journal.pone.0333230.s010

(DOC)

Acknowledgments

We thank He Li and Tian He for their support during our field and laboratory work. The authors also express their gratitude to the reviewers and editors for their insightful comments and recommendations.

References

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- View Article
- Google Scholar
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- PubMed/NCBI
- Google Scholar
24. S.ALansari A, M.Yassin M, W.Seheib M. Role of organic acids on phosphorus fractions in silty clay loam soil. Qadisiyah J Agri Sci. 2018;8(2):12–21.
- View Article
- Google Scholar
25. Wang Y, Whalen JK, Chen X, Cao Y, Huang B, Lu C, et al. Mechanisms for altering phosphorus sorption characteristics induced by low-molecular-weight organic acids. Can J Soil Sci. 2016;96(3):289–98.
- View Article
- Google Scholar
26. Wang Y, Gao M, Wang Z, Huang T, Li H. How Organic acids affect plant nitrogen and phosphorus uptake under different fertilization treatments. J Soil Sci Plant Nutr. 2023;23(4):6048–58.
- View Article
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27. Zhu H, Bing H, Wu Y. Citric acid promotes the mobilization of phosphorus under the lower concentration of low molecular weight organic acids in acidic forest soil. Adsorp Sci Tech. 2022;2022.
- View Article
- Google Scholar
28. Jalali M, Jalali M. Effect of low-molecular-weight organic acids on the release of phosphorus from amended calcareous soils: experimental and modeling. J Soil Sci Plant Nutr. 2022;22(4):4179–93.
- View Article
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29. Wang Y, Chen X, Lu C, Huang B, Shi Y. Different mechanisms of organic and inorganic phosphorus release from Mollisols induced by low molecular weight organic acids. Can J Soil Sci. 2017.
- View Article
- Google Scholar
30. Yang X, Chen X, Guo E, Yang X. Path analysis of phosphorus activation capacity as induced by low-molecular-weight organic acids in a black soil of Northeast China. J Soils Sediments. 2018;19(2):840–7.
- View Article
- Google Scholar
31. Shahane AA, Shivay YS, Prasanna R. Enhancing phosphorus and iron nutrition of wheat through crop establishment techniques and microbial inoculations in conjunction with fertilization. Soil Sci Plant Nutr. 2020;66(5):763–71.
- View Article
- Google Scholar
32. Bai Z, Li H, Yang X, Zhou B, Shi X, Wang B, et al. The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types. Plant Soil. 2013;372(1–2):27–37.
- View Article
- Google Scholar
33. Spohn M, Kuzyakov Y. Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem. 2013;61:69–75.
- View Article
- Google Scholar
34. Richardson AE, Hocking PJ, Simpson RJ, George TS. Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci. 2009;60(2):124.
- View Article
- Google Scholar
35. Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M, Borriss R, von Wirén N. Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Z Pflanzenernähr Bodenk. 2010;174(1):3–11.
- View Article
- Google Scholar
36. Liu Y, Mi G, Chen F, Zhang J, Zhang F. Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci. 2004;167(2):217–23.
- View Article
- Google Scholar
37. Ström L, Owen AG, Godbold DL, Jones DL. Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Bio Biochem. 2002;34(5):703–10.
- View Article
- Google Scholar
38. Gerke J. The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. A critical review. J Plant Nutr Soil Sci. 2015;178(3):351–64.
- View Article
- Google Scholar
39. Dakora FD, Phillips DA. Root exudates as mediators of mineral acquisition in low-nutrient environments. In: Food security in nutrient-stressed environments: exploiting plants’ genetic capabilities. Springer Netherlands; 2002. 201–13. doi: https://doi.org/10.1007/978-94-017-1570-6_23

[ref1] 1. De Andrade SAL, Borghi AA, De Oliveira VH, Gouveia L de M, Martins API, Mazzafera P. Phosphorus shortage induces an increase in root exudation in fifteen eucalypts species. Agronomy. 2022;12(9):2041.
View Article
Google Scholar

[2] View Article

[3] Google Scholar

[ref2] 2. Abolfazli F, Forghani A, Norouzi M. Effects of phosphorus and organic fertilizers on phosphorus fractions in submerged soil. J Soil Sci Plant Nutr. 2012;12(2):349–62.
View Article
Google Scholar

[5] View Article

[6] Google Scholar

[ref3] 3. Yang X, Kong Y, Guo E, Chen X, Li L. Organic acid regulation of inorganic phosphorus release from Mollisols with different organic matter contents. Soil Use Manag. 2021;38(1):576–83.
View Article
Google Scholar

[8] View Article

[9] Google Scholar

[ref4] 4. Balemi T, Negisho K. Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nutr. 2012;(ahead):0–0.
View Article
Google Scholar

[11] View Article

[12] Google Scholar

[ref5] 5. Chen X, Yan X, Wang M, Cai Y, Weng X, Su D, et al. Long-term excessive phosphorus fertilization alters soil phosphorus fractions in the acidic soil of pomelo orchards. Soil Tillage Res. 2022;215:105214.
View Article
Google Scholar

[14] View Article

[15] Google Scholar

[ref6] 6. Ahmed W, Jing H, Kaillou L, Qaswar M, Khan MN, Jin C, et al. Changes in phosphorus fractions associated with soil chemical properties under long-term organic and inorganic fertilization in paddy soils of southern China. PLoS One. 2019;14(5):e0216881. pmid:31075143
View Article
PubMed/NCBI
Google Scholar

[17] View Article

[18] PubMed/NCBI

[19] Google Scholar

[ref7] 7. Peñuelas J, Sardans J. The global nitrogen-phosphorus imbalance. Science. 2022;375(6578):266–7. pmid:35050668
View Article
PubMed/NCBI
Google Scholar

[21] View Article

[22] PubMed/NCBI

[23] Google Scholar

[ref8] 8. Wang H, Yang S, Wang Y, Gu Z, Xiong S, Huang X, et al. Rates and causes of black soil erosion in Northeast China. Catena. 2022;214:106250.
View Article
Google Scholar

[25] View Article

[26] Google Scholar

[ref9] 9. Yang XM, Zhang XP, Deng W, Fang HJ. Black soil degradation by rainfall erosion in Jilin, China. Land Degrad Dev. 2003;14(4):409–20.
View Article
Google Scholar

[28] View Article

[29] Google Scholar

[ref10] 10. Shen Q, Wen Z, Dong Y, Li H, Miao Y, Shen J. The responses of root morphology and phosphorus-mobilizing exudations in wheat to increasing shoot phosphorus concentration. AoB Plants. 2018;10(5):ply054. pmid:30338049
View Article
PubMed/NCBI
Google Scholar

[31] View Article

[32] PubMed/NCBI

[33] Google Scholar

[ref11] 11. Li X, Quan X, Mang M, Neumann G, Melchinger A, Ludewig U. Flint maize root mycorrhization and organic acid exudates under phosphorus deficiency: trends in breeding lines and doubled haploid lines from landraces. J Plant Nutr Soil Sci. 2021;184(3):346–59.
View Article
Google Scholar

[35] View Article

[36] Google Scholar

[ref12] 12. Edayilam N, Montgomery D, Ferguson B, Maroli AS, Martinez N, Powell BA, et al. Phosphorus stress-induced changes in plant root exudation could potentially facilitate uranium mobilization from stable mineral forms. Environ Sci Technol. 2018;52(14):7652–62. pmid:29722538
View Article
PubMed/NCBI
Google Scholar

[38] View Article

[39] PubMed/NCBI

[40] Google Scholar

[ref13] 13. Duan X, Zhao Y, Zhang J. Characteristics of the root exudate release system of typical plants in plateau lakeside wetland under phosphorus stress conditions. Open Chem. 2020;18(1):808–21.
View Article
Google Scholar

[42] View Article

[43] Google Scholar

[ref14] 14. Zhu H, Bing H, Wu Y, Sun H, Zhou J. Low molecular weight organic acids regulate soil phosphorus availability in the soils of subalpine forests, eastern Tibetan Plateau. CATENA. 2021;203:105328.
View Article
Google Scholar

[45] View Article

[46] Google Scholar

[ref15] 15. Zhao Y, Zhang M, Liu Z, Yang F. Migration and transformation of soil phosphorus by organic acids: a global meta-analysis. J Soils Sediments. 2023;24(2):589–602.
View Article
Google Scholar

[48] View Article

[49] Google Scholar

[ref16] 16. Barrow NJ, Debnath A, Sen A. Mechanisms by which citric acid increases phosphate availability. Plant Soil. 2017;423(1–2):193–204.
View Article
Google Scholar

[51] View Article

[52] Google Scholar

[ref17] 17. Cordell D, Drangert J-O, White S. The story of phosphorus: global food security and food for thought. Global Environ Change. 2009;19(2):292–305.
View Article
Google Scholar

[54] View Article

[55] Google Scholar

[ref18] 18. Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y. Managing nitrogen for sustainable development. Nature. 2015;528(7580):51–9. pmid:26595273
View Article
PubMed/NCBI
Google Scholar

[57] View Article

[58] PubMed/NCBI

[59] Google Scholar

[ref19] 19. Cao Y, Wang X, Bai Z, Chadwick D, Misselbrook T, G. Sommer S, et al. Mitigation of ammonia, nitrous oxide and methane emissions during solid waste composting with different additives: a meta-analysis. Journal of Cleaner Production. 2019;235:626–35.
View Article
Google Scholar

[61] View Article

[62] Google Scholar

[ref20] 20. Beaulieu JJ, DelSontro T, Downing JA. Eutrophication will increase methane emissions from lakes and impoundments during the 21st century. Nat Commun. 2019;10(1):1375. pmid:30914638
View Article
PubMed/NCBI
Google Scholar

[64] View Article

[65] PubMed/NCBI

[66] Google Scholar

[ref21] 21. Liu X, Herbert SJ, Hashemi AM, Zhang X, Ding G. Effects of agricultural management on soil organic matter and carbon transformation - a review. Plant Soil Environ. 2006;52(12):531–43.
View Article
Google Scholar

[68] View Article

[69] Google Scholar

[ref22] 22. Zhang Y, Li X, Gregorich EG, McLaughlin NB, Zhang X, Guo Y, et al. No-tillage with continuous maize cropping enhances soil aggregation and organic carbon storage in Northeast China. Geoderma. 2018;330:204–11.
View Article
Google Scholar

[71] View Article

[72] Google Scholar

[ref23] 23. Zhu J, Li M, Whelan M. Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Sci Total Environ. 2018;612:522–37. pmid:28865270
View Article
PubMed/NCBI
Google Scholar

[74] View Article

[75] PubMed/NCBI

[76] Google Scholar

[ref24] 24. S.ALansari A, M.Yassin M, W.Seheib M. Role of organic acids on phosphorus fractions in silty clay loam soil. Qadisiyah J Agri Sci. 2018;8(2):12–21.
View Article
Google Scholar

[78] View Article

[79] Google Scholar

[ref25] 25. Wang Y, Whalen JK, Chen X, Cao Y, Huang B, Lu C, et al. Mechanisms for altering phosphorus sorption characteristics induced by low-molecular-weight organic acids. Can J Soil Sci. 2016;96(3):289–98.
View Article
Google Scholar

[81] View Article

[82] Google Scholar

[ref26] 26. Wang Y, Gao M, Wang Z, Huang T, Li H. How Organic acids affect plant nitrogen and phosphorus uptake under different fertilization treatments. J Soil Sci Plant Nutr. 2023;23(4):6048–58.
View Article
Google Scholar

[84] View Article

[85] Google Scholar

[ref27] 27. Zhu H, Bing H, Wu Y. Citric acid promotes the mobilization of phosphorus under the lower concentration of low molecular weight organic acids in acidic forest soil. Adsorp Sci Tech. 2022;2022.
View Article
Google Scholar

[87] View Article

[88] Google Scholar

[ref28] 28. Jalali M, Jalali M. Effect of low-molecular-weight organic acids on the release of phosphorus from amended calcareous soils: experimental and modeling. J Soil Sci Plant Nutr. 2022;22(4):4179–93.
View Article
Google Scholar

[90] View Article

[91] Google Scholar

[ref29] 29. Wang Y, Chen X, Lu C, Huang B, Shi Y. Different mechanisms of organic and inorganic phosphorus release from Mollisols induced by low molecular weight organic acids. Can J Soil Sci. 2017.
View Article
Google Scholar

[93] View Article

[94] Google Scholar

[ref30] 30. Yang X, Chen X, Guo E, Yang X. Path analysis of phosphorus activation capacity as induced by low-molecular-weight organic acids in a black soil of Northeast China. J Soils Sediments. 2018;19(2):840–7.
View Article
Google Scholar

[96] View Article

[97] Google Scholar

[ref31] 31. Shahane AA, Shivay YS, Prasanna R. Enhancing phosphorus and iron nutrition of wheat through crop establishment techniques and microbial inoculations in conjunction with fertilization. Soil Sci Plant Nutr. 2020;66(5):763–71.
View Article
Google Scholar

[99] View Article

[100] Google Scholar

[ref32] 32. Bai Z, Li H, Yang X, Zhou B, Shi X, Wang B, et al. The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types. Plant Soil. 2013;372(1–2):27–37.
View Article
Google Scholar

[102] View Article

[103] Google Scholar

[ref33] 33. Spohn M, Kuzyakov Y. Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem. 2013;61:69–75.
View Article
Google Scholar

[105] View Article

[106] Google Scholar

[ref34] 34. Richardson AE, Hocking PJ, Simpson RJ, George TS. Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci. 2009;60(2):124.
View Article
Google Scholar

[108] View Article

[109] Google Scholar

[ref35] 35. Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei M, Borriss R, von Wirén N. Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Z Pflanzenernähr Bodenk. 2010;174(1):3–11.
View Article
Google Scholar

[111] View Article

[112] Google Scholar

[ref36] 36. Liu Y, Mi G, Chen F, Zhang J, Zhang F. Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci. 2004;167(2):217–23.
View Article
Google Scholar

[114] View Article

[115] Google Scholar

[ref37] 37. Ström L, Owen AG, Godbold DL, Jones DL. Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Bio Biochem. 2002;34(5):703–10.
View Article
Google Scholar

[117] View Article

[118] Google Scholar

[ref38] 38. Gerke J. The acquisition of phosphate by higher plants: effect of carboxylate release by the roots. A critical review. J Plant Nutr Soil Sci. 2015;178(3):351–64.
View Article
Google Scholar

[120] View Article

[121] Google Scholar

[ref39] 39. Dakora FD, Phillips DA. Root exudates as mediators of mineral acquisition in low-nutrient environments. In: Food security in nutrient-stressed environments: exploiting plants’ genetic capabilities. Springer Netherlands; 2002. 201–13. doi: https://doi.org/10.1007/978-94-017-1570-6_23

Figures

Abstract

1 Introduction

2 Materials and methods

2.1 Experimental design I: Semi-hydroponic maize cultivation for root exudate collection

(1) Semi-hydroponic experiment of maize.

(2) Collection and analysis of root-secreted organic acids.

2.2 Experimental Design II: Sterile soil incubation for phosphorus activation

2.3 Soil physicochemical characterization

2.4 Statistical analysis

3 Results

3.1 Changes of organic acids secreted by maize roots under phosphorus restriction

3.2 Influence of different treatment levels on soil AP

3.3 Differential responses of soil P Pools to high-dose organic acid amendments

4 Discussion

5 Conclusion

Supporting information

S1 Fig. Semi hydroponic cultivation of maize seedlings.

S2 Fig. Changes in the AP content at various time points in Alfisols amended with LMWOAs over the 60 d incubation period.

S3 Fig. Changes in the AP content at various time points in Alfisols amended with LMWOAs over the 60 d incubation period.

S4 Fig. Changes in the AP content at various time points in Mollisols amended with LMWOAs over the 60 d incubation period.

S5 Fig. Changes in the AP content at various time points in Mollisols amended with LMWOAs over the 60 d incubation period.

S1 Table. Operating parameters of LC-MSMS.

S2 Table. Physical and chemical characteristics at various time points in the soils amended with malic acid (malic acid applied at 2% by weight in the incubated soil).

S3 Table. Physical and chemical characteristics at various time points in the soils amended with tartaric acid (tartaric acid applied at 2% by weight in the incubated soil).

S4 Table. Physical and chemical characteristics at various time points in the soils amended with citric acid (citric acid applied at 2% by weight in the incubated soil).

S5 Table. Physical and chemical characteristics at various time points in the soils amended with trans-aconitonic acid (trans-aconitonic acid applied at 2% by weight in the incubated soil).

Acknowledgments

References