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Article

Comparative Metabolomics Reveals Phosphine-Induced Metabolic Disruptions in Planococcus citri (Risso)

by
Junbeom Lee
1,
Soo-Jung Suh
2,
Bong-Su Kim
2,* and
Dae-Weon Lee
3,*
1
Metabolomics Research Center for Functional Materials, Kyungsung University, Busan 48434, Republic of Korea
2
Plant Quarantine Technology Center, Animal and Plant Quarantine Agency, Gimcheon 39660, Republic of Korea
3
Department of SmartBio, Kyungsung University, Busan 48434, Republic of Korea
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2025, 26(16), 8020; https://doi.org/10.3390/ijms26168020
Submission received: 23 July 2025 / Revised: 14 August 2025 / Accepted: 18 August 2025 / Published: 19 August 2025
(This article belongs to the Section Molecular Endocrinology and Metabolism)
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Abstract

Phosphine (PH3) is a fumigant often used to control insect pests, but its metabolic effects on insect physiology remain unclear. In this study, a comparative metabolomics analysis was performed to elucidate the physiological metabolic pathways affected by PH3 exposure in Planococcus citri, and significant changes in the metabolic profiles induced by PH3 treatment were identified. Principal component analysis and correlation analysis revealed different metabolic changes, and a total of 45 metabolites were identified and mapped to metabolic pathways using the KEGG database. PH3 exposure inhibited energy metabolism by down-regulating riboflavin and flavin adenine dinucleotide, which are important cofactors in oxidative phosphorylation and reactive oxygen species generation. In addition, purine and pyrimidine metabolism, essential for nucleotide synthesis and cellular energy homeostasis, were also suppressed. Notably, lipid metabolism was significantly altered, and the juvenile hormone biosynthesis pathway was down-regulated. These results suggest that PH3 inhibits electron transport chain activity, induces oxidative stress, and disrupts lipid homeostasis. This study enhances our understanding of the potential biomarkers of PH3 exposure, the metabolic processes involved, and the resistance mechanisms that pests may develop in response to such exposure.

1. Introduction

Phosphine (PH3) is one of the most widely used fumigants for controlling pests in agriculture and plant quarantine. PH3 exhibits high efficacy in various insect pests and has excellent penetration due to its high vapor pressure; therefore, it is widely used for purposes such as durable commodities and facility fumigation [1,2,3]. In particular, it is known to have high efficacy in mealybugs, a major pest of imported fresh commodities, and it is expected to be promising as an alternative fumigant to replace methyl bromide, an ozone-depleting substance [4,5,6]. It is commonly commercialized in the form of metal phosphides like aluminum phosphide due to the high fire risk of pure phosphine [7]. In the case of such metal phosphides, ammonia gas is generated as a warning substance, but ammonia gas can cause damage to fruits or vegetables, making it difficult to use on fresh commodities [8]. Recently, a cylinderized product mixed with carbon dioxide has been commercialized, reducing the fire risk. This phosphine product can be applied to fresh commodities as it does not generate ammonia gas [9,10].
The citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), is found across Asia, the Americas, and Europe and is a plant quarantine pest [11]. Nymphs and female adults attach to the stems, branches, and leaves of host plants and suck the sap with their stingers, causing the leaves to wilt, become deformed, turn yellow, and fall early [12]. In addition, they secrete honeydew, which reduces the photosynthetic activity of the leaves, resulting in lower quality fruit, reducing plant vitality, and damaging the appearance of ornamental flowers [13,14,15]. Biological control can be applicable for this pest, including predators, parasites and entomopathogenic fungi [12,16]. Because citrus mealybugs secrete a wax that covers their entire body, agrochemicals that rely on contact toxicity have very little effect on them [17,18]. Therefore, insecticides with a diffusive mechanism are now being considered in toxicity studies, and fumigants have been suggested as an alternative. The effects and mechanism of action of PH3 are known in several pests, mainly insects with complete metamorphosis [19,20,21]. However, there are few studies on the metabolic mechanisms of citrus mealybugs, an incomplete metamorphosis insect, exposed to PH3 [22]. In this study, the effect of PH3 was analyzed based on comparative metabolomics to elucidate the physiological changes in P. citri. Additionally, functional relationships among metabolites induced by PH3 were demonstrated based on the metabolite–metabolite interaction network.

2. Results

2.1. Comparative Metabolic Profiling by PH3 Exposure

An in vivo assay was performed to investigate the concentration of PH3 required to kill P. citri (Table 1). The 10% and 50% lethal concentration–time (LCt) values of PH3, when administered over 2 h, were 0.161 and 0.216 mg·h/L for adult P. citri, respectively. To elucidate the metabolite changes in P. citri induced by PH3, comparative metabolomics analysis was conducted based on these LCts. When a PCA was performed with raw fold change (FC) data, the reliability of the metabolic analysis was ensured through the use of well-aligned clusters of metabolic data for each group (Figure 1). Significant differences in the positive- (ESI+) and negative-ion modes (ESI−) mass spectrometry were observed after PH3 exposure, suggesting that the metabolic physiology of P. citri was altered by PH3 (Figure 1A). In addition, correlation analysis revealed that there are the relationships between each of the experimental groups. The difference between the control group and LCt10 treatment group was clearly discernible (Figure 1B), whereas the correlation among PH3 concentrations was low. In the LCt50 treatment, a difference was observed more clearly in the ESI+ than in the ESI− (Figure 1B). These results suggest that the metabolome of P. citri is changed by PH3 exposure and that these altered metabolites can be utilized to determine PH3-treatment-specific indicators.
A total of 408 and 216 metabolites were extracted from PH3 exposure (both LCt10 and LCt50) in the ESI+ and ESI− of the mass spectrometry, respectively (Supplementary Data S1), and 90 of these compounds were filtered through annotation processing based on the metabolite database and KEGG ID assignments (Supplementary Data S2). Finally, 45 PH3 treatment-specific indicators matching the metabolic pathways of the reference insect, aphid Acyrthosiphon pisum, were obtained, along with the peak intensity and related metabolic pathways for each treatment group (Table 2). Among these, 10 and 35 indicators were found to be up- and down-regulated, respectively, suggesting that PH3-induced metabolic disruptions occurred in P. citri.

2.2. Enrichment and Pathway Impact of Altered Metabolites

Metabolite set enrichment analysis (MSEA) identifies biologically meaningful patterns in metabolite concentration changes. Therefore, 45 treatment-specific indicators, categorized as up- or down-regulated by PH3 exposure, were classified into metabolite sets based on their chemical structures (Figure 2). Isoprenoids glycosphingolipids, which are involved in membrane structural integrity and cell signaling, were up-regulated, suggesting an adaptive response to PH3-induced stress (Figure 2A). In contrast, glycosylamines, glycerophosphoserines, and glycerophosphoethanolamines, key components of membrane phospholipids and glycan-related metabolism, were down-regulated, indicating energy conservation or metabolic suppression (Figure 2B). These results highlight that lipid remodeling is an important response to PH3 exposure in P. citri. Moreover, purine and pyrimidine derivatives, which are fundamental to nucleic acid biosynthesis and energy metabolism, also exhibited significant down-regulation under PH3-induced stress. Potential disruption of nucleotide biosynthesis and energy metabolism could result in impairment of DNA/RNA synthesis or repair mechanisms.
To investigate the importance of these 45 indicators within the overall metabolic network of P. citri, the metabolites changed by PH3 exposure were analyzed using their pathway impact scores from the KEGG database (Figure 3). The results revealed distinct pathway modulations between up-regulated (Figure 3A) and down-regulated (Figure 3B) metabolites. In the up-regulated pathways, sphingolipid metabolism was the most enriched in terms of both statistical significance and pathway impact. Since sphingolipids function to maintain membrane integrity under oxidative stress conditions, membrane remodeling and stress signaling may be enhanced [23]. In contrast, the down-regulated metabolite profiles showed significant inhibition across several biosynthetic and signaling pathways. Notably, riboflavin metabolism was most affected, suggesting a disruption of redox homeostasis in P. citri, considering the role of riboflavin-derived cofactors in mitochondrial and oxidative metabolism [24]. In addition, glycerophospholipid metabolism, pyrimidine metabolism, and sphingolipid metabolism were significantly affected, indicating widespread disruption of membrane lipid biosynthesis and nucleotide metabolism [25]. The down-regulation of folate biosynthesis, cysteine and methionine metabolism, and pentose-related metabolism suggests inhibition of cellular biosynthetic capacity and antioxidant defense mechanisms [26,27]. These results suggest that PH3 exposure in P. citri may act as an energy-conservation or damage-control mechanism by up-regulating stress-adaptive lipid pathways while down-regulating essential biosynthetic pathways.

2.3. Metabolite–Metabolite Interaction Network

Since the metabolite–metabolite network helps to reveal potential functional relationships between metabolites and identify key metabolites, the interaction network of PH3-induced metabolites was analyzed (Figure 4). The 10 up-regulated indicators were classified into three subnetworks—dihydroceramide, estrone sulfate, and triradylglycerols—as the central metabolites (Figure 4A and Supplementary Data S3). In addition, metabolic network analysis based on the 35 down-regulated indicators elucidated that metabolites related to purine metabolism (AMP and guanine), pyrimidine metabolism (UDP, cytidine, and deoxycytidine), and riboflavin metabolism (FAD and riboflavin) showed the closest interactions with other metabolites, suggesting that they function as key metabolites within the network (Figure 4B and Supplementary Data S4). These metabolic networks support the results obtained from the MSEA and pathway impact and suggest PH3 treatment-specific indicators can be used as potential biomarkers.

2.4. Lipid Metabolism Disorders by PH3 Stress

Pathway analyses revealed that metabolites involved in sphingolipids (SPs), glycerolipids (GLs) metabolism, and glycosylphosphatidylinositol (GPI) anchor biosynthesis were significantly affected by PH3 exposure (Figure 3). Therefore, the changes in lipid profiles induced by PH3 stress were investigated. Based on lipid DB annotations, 107 lipids were identified, and differential regulation was evaluated through multivariate statistical analysis (Table 3). PCA and correlation analysis showed that the clusters were well aligned across groups and clearly distinguished from the mock control (Supplementary Data S5). However, there was no significant difference between PH3 concentrations, as found in the untargeted metabolic analysis. Lipid types of SPs, GLs, and glycerophospholipids (GPs) were quantitatively changed, but fatty acids (FAs), polyketides (PKs), sterol lipids (STs), or prenols (PRs) were not observed. In addition, most lipids were down-regulated by PH3 exposure. These results suggest that lipid metabolism in P. citri is disrupted by exposure to PH3, regardless of concentration.

3. Discussion

Because metabolites immediately reflect physiological responses, metabolomics can effectively reveal changes in the metabolome induced by external stimuli. Although the insecticidal activity of PH3 in P. citri has been previously studied [30], the physiological metabolic pathways for PH3 treatment have not been elucidated. Therefore, metabolic changes induced by PH3 exposure in P. citri were investigated by comparative metabolomics, and the mechanism of action of PH3 was demonstrated. Most of the metabolites changed by PH3 affected P. citri metabolic pathways related to energy biosynthesis. Notably, its inhibitory effect on the FAD metabolite involved in the ETC cycle can be an important indicator of physiological changes. Additionally, altered levels of the cell membrane lipids glycerophospholipid and sphingolipid demonstrated various effects of PH3.
Topological analysis is based on the centrality measure of each metabolite in the metabolic network. Centrality is a comparative measure that indicates the relative position of a particular node to other nodes and is utilized to estimate the relative importance or role of a node in a network configuration [31]. In this study, the network highlights the importance of purine (AMP and guanine) and pyrimidine (cytidine, deoxycytidine, and UDP) metabolites in PH3 exposure in P. citri, and riboflavin and FAD showed high centrality (Figure 4).
Riboflavin (vitamin B2) is a precursor of flavin adenine mononucleotide (FMN) and flavin dinucleotide (FAD), which are involved in energy metabolism and redox reactions. FMN and FAD act as cofactors for various oxidoreductases and play key roles in glycolysis, the citric acid cycle (TCA cycle), the electron transport chain (ETC), detoxification, and neurotransmission [32]. In cellular respiration in insects, FMN and FAD play roles in accepting and transferring electrons from nicotinamide adenine dinucleotide (NADH) in complex I (NADH dehydrogenase) or producing FADH2 form in complex II of the ETC, thereby activating oxidative phosphorylation within the mitochondria and generating adenosine triphosphate (ATP) [33,34]. In addition, FMN and FAD are involved in antioxidant processes that can suppress reactive oxygen species (ROS). Insecticides cause oxidative stress in cells and generate ROS free radicals, and reduced glutathione (GSH) acts as a cofactor to scavenge toxic oxygen radicals [35]. During redox stress, GSH levels decrease, and oxidized glutathione disulfide (GSSG) levels increase by glutathione peroxidase, which functions to prevent lipid peroxidation. On the other hand, in the antioxidant process, FAD transfers hydrogen to activate glutathione reductase (GR), which converts GSSG into GSH [36]. The reduced GSH acts as an endogenous antioxidant within the cell, scavenging ROS. PH3 directly interferes with mitochondrial respiration, causing a deficiency in energy metabolism. Briefly, PH3 inhibits complex IV (cytochrome c oxidase) of the ETC, which is located in the mitochondrial inner membrane [37,38]. In this study, PH3 exposure inhibited riboflavin and FAD metabolites compared to control (Table 2). In previous studies, ethyl formate, a fumigant with similar functional properties to PH3, was shown to inhibit FMN, resulting in elevating GSSG [39]. These results support that riboflavin and FAD metabolites are down-regulated in P. citri by PH3 exposure. Considering the mechanism of action of PH3, the inactivation of the ETC, including FAD, may not only inhibit mitochondrial energy metabolism but also promote ROS, causing oxidative stress in P. citri.
Ascorbate (AsA) is a hydrophilic antioxidant that neutralizes ROS free radicals, serving as a primary line of defense against oxidative stress in a wide range of organisms, including insects [40,41]. The ascorbate/aldarate metabolic pathway encompasses AsA synthesis, degradation, and recycling, enabling electron transfer from reducing cofactors such as NADPH to remove ROS. This function establishes a direct connection with the GSH-dependent antioxidant detoxification system in insect cells [42,43,44,45]. Recent studies revealed that insecticide-induced ROS accumulation stimulates antioxidant cycles involving both AsA and GSH, with KEGG analysis revealing marked regulation of the ascorbate/aldarate pathway under such stress [46,47]. The AsA-GSH cycle is broadly recognized as a key mechanism for ROS scavenging under environmental challenges [48,49]. In the present study, PH3 exposure decreased β-D-glucuronoside, which may reflect either elevated ascorbate accumulation or reduced metabolic activity linked to energy depletion. The alteration in ascorbate/aldarate metabolism observed here suggest enhanced redox imbalance and oxidative stress responses in P. citri. Considering the pivotal role of ascorbate in insect antioxidant defense, these metabolic perturbations are likely to exacerbate PH3-induced toxicity by impairing detoxification capacity and disrupting redox homeostasis [38,40,50].
The major pathways related to energy metabolism include purine metabolism, which is associated with the production of ATP/GTP, key molecules that control intracellular energy homeostasis and nucleotide synthesis [51]. In addition, pyrimidine nucleotides provide the DNA and RNA compositions needed for cell growth and division [52]. In this study, PH3 exposure down-regulated purine (AMP, guanine, and guanosine 3’-phosphate) and pyrimidine (cytidine, deoxycytidine, and UDP) metabolites by 2-fold in P. citri (Table 2). These metabolites are involved in the de novo synthesis of purine and pyrimidine and the salvage pathway in insects. A recent study suggested that purine recycling deficiencies cause metabolic and neurobehavioral disturbances in Drosophila melanogaster [53].
Comparative proteomic studies on PH3 have revealed that cytochrome P450 metabolism-related molecules are significantly up-regulated in PH3-resistant insect groups [54,55]. In this study, cytochrome P450 metabolism and four metabolites were inhibited by PH3 exposure in P. citri (Table 2). These results support the reports that cytochrome P450-related detoxification processes are involved in the acquisition of PH3 resistance in insects [54,55].
Because PH3-specific metabolites could be utilized as biomarkers, metabolites and their pathways that are specific for PH3 exposure were additionally investigated. Interestingly, the metabolism associated with the biosynthesis of juvenile hormone (JH) was completely inhibited by PH3 exposure (Table 2 and Figure 3B). Generally, JH biosynthesis and insect metabolism show a positive correlation. In addition, the main JH structure of hemipteran insects is known as the juvenile hormone III skipped bisepoxide (JHSB3), which contains an epoxide ring attached to JH III [56]. The process by which JH III is converted to JHSB3 is not yet clear. In P. citri exposed to PH3, the production of JH III diol, degradative form of JH III, was completely inhibited, and JHSB3 was not found. This result suggests that JH III diol may be an intermediate in the process of JHSB3 production.
A recent study showed that PH3-resistant insects had higher levels of lipids (glycerolipids and phospholipids) than susceptible ones [57]. GLs function as a storage for energy shortage [58,59], and cell membrane phospholipids, mainly composed of phosphatidylethanolamine (PE) and GP class, act as a barrier separating the cell from the external environment [60]. Lipids serve as an energy source that enables insects to survive under phosphine-induced stress and provide a suitable environment to protect mitochondria from phosphine. In this study, PH3 exposure completely inhibited PE in the glycosylphosphatidylinositol (GPI) anchor biosynthetic pathway (Figure 3B). These results explain the reason most lipids were down-regulated or suppressed in P. citri. In addition, cell surface-associated lipids such as GPs and SPs were significantly down-regulated under PH3 stress (Table 3). SPs, as key components of lipid rafts, are involved in cell membrane receptor function and signal transduction, and exhibit strong affinity for the GPI anchors [61,62,63]. GPI-anchors are covalently linked to the carboxyl terminus of proteins and function to attach GPI proteins to the lipid bilayer [64,65]. Interestingly, diglycerides (DGs) were up-regulated, whereas triglycerides (TGs) were mostly suppressed (Table 3). This lipid regulation pattern is similar to that of Drosophila suzukii after PH3 treatment [66]. In insects, lipids are the major component of the fat body and are stored as TG, a form that can be used during long-term energy demands [58,67]. In contrast, diglycerides (DGs), the major lipid in insect hemolymph, are rapidly utilized during short-term energy demands such as flight [58,68]. Considering the mechanism of action of PH3 involving energy depletion in mitochondria, the increase in DG and decrease in TG in response to stress suggest that PH3 adversely affects the energy metabolic pathway in P. citri.

4. Materials and Methods

4.1. Insect Rearing

The citrus mealybugs, P. citri, used in this study were collected from nursery trees in greenhouses (Suwon, Republic of Korea) in 2022. They were mounted on microscope slides for identification. After verifying their identity, the individuals were continuously reared on potato tubers (Solanum tuberosum L.), which were provided twice a month, at 25°C with a 60% relative humidity and photoperiod of 16:8 h (light:dark) at the Plant Quarantine Technology Center, Animal and Plant Quarantine Agency (Gimcheon, Republic of Korea) [30].

4.2. Phosphine and Thermal Treatment

PH3 (Vivakill®, 2% PH3 + 98% CO2) was purchased from FarmHannong (Seoul, Republic of Korea). Adult mealybugs (a mixture of male and female adults) were placed on potato slices in separate 100 mm × 40 mm breeding dishes for each experimental treatment group (SPL, Pocheon, Republic of Korea). PH3 was administered for 2 h at 20°C in a 12 L desiccator (DWK Life Sciences, Mainz, Germany). The LCt values of fumigant on P. citri were calculated using a Probit analysis [69]. Adults from each group were transferred to glass vials and rapidly frozen in liquid nitrogen to prevent metabolic changes. All treatments and controls were performed in triplicate (n = 10).

4.3. Metabolite Extraction

Total metabolites were extracted from whole body of P. citri adults in triplicate (10 insects/replicate). Briefly, each sample was suspended in 1 mL of extraction solution (3:1:1, methanol/chloroform/water, v/v/v) and homogenized using a Beadbug microtube homogenizer (Benchmark Scientific Inc., Sayreville, NJ, USA) for 3 min. Samples were incubated at room temperature for 20 min and then centrifuged at 20,000× g and 4°C for 5 min. The supernatant was filtered through a 0.22 μm pore mesh (Ultrafree-MC, Millipore, Burlington, MA, USA) and immediately loaded into the liquid chromatograph triple-quadrupole time-of-flight mass spectrometry (LC-QTOF/MS; Agilent Technologies 1290 and 6545 System, Agilent Technologies, Santa Clara, CA, USA; Metabolomics Research Center for Functional Materials, Kyungsung University) for metabolomics. The metabolite recovery rate of the sample was investigated with internal standards (L-alanine, Sigma-Aldrich, Oakville, ON, Canada), and the extraction process demonstrated a recovery rate of 50% or greater [66].

4.4. Lipid Extraction

Total lipids were extracted from whole body of P. citri adults in triplicate (10 insects/replicate) using the modified Bligh and Dyer method, as described previously [70]. Briefly, each sample was suspended in 3 mL of solution (methanol/chloroform, 2:1, v/v) and homogenized using glass beads. Samples were incubated at room temperature for 20 min and centrifuged at 20,000× g for 5 min at 4°C. Supernatants were transferred to new tubes to remove tissue debris. One milliliter of chloroform and 1.8 mL of water were added to each sample, followed by vortexing for 1 min. The lower layer was separated by centrifugation at 2000× g for 10 min at 4°C, followed by transfer to a new tube and drying under pure N2 gas. Dried samples were then suspended in 200 μL of solution (methanol/chloroform, 1:1, v/v) and sonicated for 5 min. The resulting supernatants were filtered through 0.22 μm pore size filters (Millipore) and immediately loaded into the LC-QTOF/MS (Agilent Technologies) instrument for lipid analysis. The recovery rates of lipid standards (SPLASH® LIPIDOMIX® Mass Spec Standard, Avanti Research, London, UK) were used to confirm the efficiency of lipid extraction, and the extraction process demonstrated more than 50% recovery rates.

4.5. Metabolomics

Untargeted metabolomics was performed using an LC-QTOF/MS instrument (Agilent Technologies) with an electrospray ionization (ESI) source. Since metabolites have ionization preferences depending on their structure and properties, mass spectrometry was performed in both ESI+ and ESI−. For the metabolome analysis, 3 μL of each sample was injected into an InfinityLab Poroshell 120 HILIC-Z column (2.1 mm × 100 mm, 2.7 μm; Agilent Technologies), which was kept at 25°C in its ESI+ and 50°C in its ESI−. The binary mobile phase system utilized in its ESI+, i.e., phase A, was 10 mM of ammonium formate in water containing 0.1% formic acid, while phase B was 10 mM ammonium formate in 90% acetonitrile containing 0.1% formic acid. The mobile phase had a flow rate of 0.25 mL/min and was created under the following conditions: initiation at 2% A, followed by a linear gradient to 2% A over 3 min, 30% A at 11 min, 40% A at 12 min, 95% A at 16 min, 95% A at 18 min, 2% A at 19 min, 2% A at 20 min, and 2% B at 24 min. The binary mobile phase system utilized in ESI−, phase A, was 10 mM of ammonium acetate in water (pH 9.0), while phase B was 10 mM of ammonium acetate in 85% acetonitrile (pH 9.0). The mobile phase had a flow rate of 0.25 mL/min and was created under the following conditions: initiation at 4% A, followed by a linear gradient to 4% A over 2 min, then 12% A at 5.5 min, 12% A at 8.5 min, 14% A at 9 min, 14% A at 14 min, 18% A at 17 min, 35% A at 23 min, 35% A at 24 min, 4% A at 24.5 min, and 4% B at 29 min. The capillary voltage was set to 3.0 kV in the column’s ESI+ and 3.5 kV in its ESI−. Metabolites with a mass within the range of 50 to 1600 m/z were detected using a quadrupole time-of-flight instrument.

4.6. Data Processing and Statistical Analysis

To ensure that the parameters were applied to all samples consistently, the data were analyzed in one batch and normalized using the total ion intensity. All potential metabolites were extracted from the LC peaks of each sample and analyzed using Mass Hunter Qualitative software (Ver. 10.0, Agilent Technologies). These compounds were annotated using the METLIN metabolite database and then filtered, scaled, integrated, and statistically analyzed and visualized using Mass Profiler Professional software (Ver. 14.0; Agilent Technologies). Significant differences between experimental groups were confirmed through a principal component analysis (PCA) and Pearson correlation analysis. Differentially up- or down-regulated metabolites were compared to the mock control group and are defined as changes in entities with [raw fold change (FC)] values > 2 and a p < 0.05. Metabolite and lipid data were evaluated using MetaboAnalyst 6.0, https://www.metaboanalyst.ca (accessed on 20 July 2025), and related pathways were visualized using the Kyoto Encyclopedia of Genes and Genomes (KEGG) database.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijms26168020/s1.

Author Contributions

Conceptualization, J.L., S.-J.S., B.-S.K. and D.-W.L.; software, J.L., S.-J.S., B.-S.K. and D.-W.L.; validation, J.L., S.-J.S., B.-S.K. and D.-W.L.; investigation, J.L., S.-J.S., B.-S.K. and D.-W.L.; data curation, J.L., S.-J.S., B.-S.K. and D.-W.L.; writing—original draft preparation, J.L., S.-J.S., B.-S.K. and D.-W.L.; writing—review and editing, J.L., S.-J.S., B.-S.K. and D.-W.L.; project administration, B.-S.K. and D.-W.L.; funding acquisition, J.L., S.-J.S., B.-S.K. and D.-W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the APQA research fund [I-1543086-2024-26-01]. This research was funded by the Korea Basic Science Institute (National Research Facilities and Equipment Center) and supported by the Ministry of Education [grant No. 2019R1A6C1010044]. This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education [grant no. RS-2023-00245952].

Data Availability Statement

All data generated or analyzed during this study are included in this published article [and its Supplementary Materials Files].

Conflicts of Interest

The authors declare no conflicts of interest.

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Ijms 26 08020 g001
Figure 1. Comparative analysis of metabolic change patterns induced by PH3 stress: (A) PCA and (B) correlation plots of experimental groups with altered metabolites as detected in (i) ESI+ and (ii) ESI−. Each colored dot indicates n = 3 repetitions. The variance percentage includes the z-axis values. Colors visually represent the strength and direction of the relationships among variables.
Figure 1. Comparative analysis of metabolic change patterns induced by PH3 stress: (A) PCA and (B) correlation plots of experimental groups with altered metabolites as detected in (i) ESI+ and (ii) ESI−. Each colored dot indicates n = 3 repetitions. The variance percentage includes the z-axis values. Colors visually represent the strength and direction of the relationships among variables.
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Ijms 26 08020 g002
Figure 2. Metabolite set enrichment analysis of altered metabolites. The (A) up- and (B) down-regulated metabolites were classified into 1250 subchemical metabolite sets based on their chemical structures. The colors of the bar graph describe the p-values, with red and orange representing high and low values, respectively.
Figure 2. Metabolite set enrichment analysis of altered metabolites. The (A) up- and (B) down-regulated metabolites were classified into 1250 subchemical metabolite sets based on their chemical structures. The colors of the bar graph describe the p-values, with red and orange representing high and low values, respectively.
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Ijms 26 08020 g003
Figure 3. Pathway analysis and impact scores of altered metabolites. The metabolic pathways of metabolites (A) up- and (B) down-regulated by PH3 exposure. Pathway analyses were performed using aphid information (Acyrthosiphon pisum, Hemiptera) from the Kyoto Encyclopedia of Genes and Genomes database. The pathway impact was calculated based on the sum of the importance measures of the matched metabolites normalized by the importance of all metabolites in each pathway [28].
Figure 3. Pathway analysis and impact scores of altered metabolites. The metabolic pathways of metabolites (A) up- and (B) down-regulated by PH3 exposure. Pathway analyses were performed using aphid information (Acyrthosiphon pisum, Hemiptera) from the Kyoto Encyclopedia of Genes and Genomes database. The pathway impact was calculated based on the sum of the importance measures of the matched metabolites normalized by the importance of all metabolites in each pathway [28].
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Ijms 26 08020 g004
Figure 4. Metabolite–metabolite interaction network for differentially accumulated PH3-specific metabolites. The network interaction of metabolites (A) up- regulated (subnetwork 1: nodes—11, edges—11, and seeds—2; subnetwork 2: nodes—8, edges—7, and seeds—1; subnetwork 3: nodes—7, edges—6, and seeds—1) and (B) down-regulated (nodes—411, edges—737, and seeds—12) by PH3 exposure. The metabolic networks are represented as compound networks with metabolites as nodes (circles) and reactions as edges (lines). Nodes indicate correlated metabolites in the network, and lines represent biological relationships between two metabolites. The color of the nodes indicates the betweenness centrality value (metabolites with high betweenness centrality are shown in red, followed by pink and blue), and the size of the nodes represents the degree value (the number of links the node has with other nodes) [29].
Figure 4. Metabolite–metabolite interaction network for differentially accumulated PH3-specific metabolites. The network interaction of metabolites (A) up- regulated (subnetwork 1: nodes—11, edges—11, and seeds—2; subnetwork 2: nodes—8, edges—7, and seeds—1; subnetwork 3: nodes—7, edges—6, and seeds—1) and (B) down-regulated (nodes—411, edges—737, and seeds—12) by PH3 exposure. The metabolic networks are represented as compound networks with metabolites as nodes (circles) and reactions as edges (lines). Nodes indicate correlated metabolites in the network, and lines represent biological relationships between two metabolites. The color of the nodes indicates the betweenness centrality value (metabolites with high betweenness centrality are shown in red, followed by pink and blue), and the size of the nodes represents the degree value (the number of links the node has with other nodes) [29].
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Table 1. Lethal concentration–time of PH3 for adult P. citri (treatment conditions: 2 h treatment at 20 °C in a 12 L desiccator).
Table 1. Lethal concentration–time of PH3 for adult P. citri (treatment conditions: 2 h treatment at 20 °C in a 12 L desiccator).
StageNumber TreatedLCt10
(95% CI)		LCt50
(95% CI)		Slope ± SEdfχ2
Adult4500.161
(0.137–0.174)		0.216
(0.205–0.232)		5.17 ± 1.931317.03
Table 2. Metabolites found to be differentially expressed under PH3-stress (N.D. means not detected).
Table 2. Metabolites found to be differentially expressed under PH3-stress (N.D. means not detected).
KEGG IDCompoundFold Change (vs. [Mock])Related Pathway
[LCt10][LCt50]
C00422TG(12:0/12:0/12:0)8.7655.578api00561Glycerolipid metabolism
C02960Cer(d18:1/18:0)12.796 3.470api00600Sphingolipid metabolism
C00319Sphingosine1.709 N.D.api00600Sphingolipid metabolism
C06126Galabiosylceramide (d18:1/22:0)339,388 N.D.api00600Sphingolipid metabolism
C12126Dihydroceramide7,290,115 N.D.api00600Sphingolipid metabolism
C039975-Hydroxymethyldeoxycytidylate213,974 N.D.api00240Pyrimidine metabolism
C02538Estrone 3-sulfate56,747 N.D.api01100Metabolic pathways
C0550222R-hydroxycholesterolN.D.129,099api01100Metabolic pathways
C08972Quillaic acidN.D.242,641api01100Metabolic pathways
C11472D-glycero-D-manno-heptose 1,7-bisphosphateN.D.115,917api01250Biosynthesis of nucleotide sugars
C00350PE(17:2(9Z,12Z)/20:1(11Z))−3.167 −1.173api00563GPI-anchor biosynthesis
api00564Glycerophospholipid metabolism
C00319D-erythro-sphingosine C-17−2.251−1.868api00600Sphingolipid metabolism
C00836C17 sphinganine−2.648−2.127api00600Sphingolipid metabolism
C03033Epinephrine glucuronide−3.985 −1.869api00040Pentose and glucuronate interconversions
api00053Ascorbate and aldarate metabolism
C00255Riboflavin (vitamin B2)−3.677−1.833api00740Riboflavin metabolism
api02010ABC transporters
C00242Guanine−3.125−1.762api00230Purine metabolism
C00881Deoxycytidine−8.308−2.426api00240Pyrimidine metabolism
api02010ABC transporters
C165822-Hydroxyfelbamate−3.179−1.727api00982Drug metabolism: cytochrome P450
C14876S-(2-Hydroxyethyl)-N-acetyl-L-cysteine−6.718−2.825api00980Metabolism of xenobiotics by cytochrome P450
C00475Cytidine−7.167−2.400api00240Pyrimidine metabolism
api02010ABC transporters
C06193Guanosine 3’-phosphate−3.831−2.315api00230Purine metabolism
C00331Indolepyruvate−3.874−1.644api00380Tryptophan metabolism
C022375-Oxo-D-proline−4.788−2.178api01100Metabolic pathways
C00020Adenosine 5’-monophosphate (AMP)−3.620−1.854api00230Purine metabolism
C02989L-Methionine S-oxide−5.030−2.178api00270Cysteine and methionine metabolism
C06156D-Glucosamine 1-phosphate−4.036−1.826api01250Biosynthesis of nucleotide sugars
C00015Uridine diphosphate (UDP)−2.803−1.853api00240Pyrimidine metabolism
C00570CDP-ethanolamine−3.028−1.651api00564Glycerophospholipid metabolism
C10556Deoxypodophyllotoxin−10.196−2.280api01100Metabolic pathways
C02737PS(18:0/0:0)−4.339−3.272api00564Glycerophospholipid metabolism
C06542Ajmaline−6.059−1.892api01100Metabolic pathways
C195644-(Nitrosoamino)-1-(3-pyridinyl)-1-butanone−2.978−1.793api00980Metabolism of xenobiotics by cytochrome P450
C11680CathenamineN.D.N.D.api01100Metabolic pathways
C00422TG(16:1(9Z)/14:0/16:1(9Z))[iso3]N.D.N.D.api00561Glycerolipid metabolism
C16692MannopineN.D.N.D.api02010ABC transporters
C011523-Methyl-L-histidineN.D.N.D.api00340Histidine metabolism
C16505(10S)-Juvenile hormone III diolN.D.N.D.api00981Insect hormone biosynthesis
C048747,8-DihydroneopterinN.D.N.D.api00790Folate biosynthesis
C19606NNAL-N-glucuronideN.D.N.D.api00980Metabolism of xenobiotics by cytochrome P450
C00350PE(12:0/19:1(9Z))N.D.−1.260api00563GPI-anchor biosynthesis
api00564Glycerophospholipid metabolism
C00350PE(19:1(9Z)/0:0)N.D.1.079 api00563GPI-anchor biosynthesis
api00564Glycerophospholipid metabolism
C163655-Acetylamino-6-formylamino-3-methyluracilN.D.−1.010api00232Caffeine metabolism
C00016Flavin adenine dinucleotide (FAD)N.D.−1.875api00740Riboflavin metabolism
api04977Vitamin digestion and absorption
C001705’-Deoxy-5’-(methylthio)adenosine−4.264N.D.api00270Cysteine and methionine metabolism
Table 3. Lipidomic profiling altered by PH3 exposure.
Table 3. Lipidomic profiling altered by PH3 exposure.
Log2 Fold Change
(vs. [Mock])		LMP IDCategoryMain ClassCompound
[LCt10][LCt50]
−16.17−16.17LMSP02010018Sphingolipids [SP]Ceramides [SP02]Cer(d18:0/13:0)
−1.03−0.87LMSP02020015Sphingolipids [SP]Ceramides [SP02]Cer(d18:0/18:1(9Z))
−22.06−0.38LMSP02010004Sphingolipids [SP]Ceramides [SP02]Cer(d18:1/16:0)
−18.80−0.54LMSP02010006Sphingolipids [SP]Ceramides [SP02]Cer(d18:1/18:0)
−1.20−1.06LMSP02010003Sphingolipids [SP]Ceramides [SP02]Cer(d18:1/18:1(9Z))
0.0015.00LMSP02010007Sphingolipids [SP]Ceramides [SP02]Cer(d18:1/20:0)
−1.36−1.48LMSP02010008Sphingolipids [SP]Ceramides [SP02]Cer(d18:1/22:0)
−1.16−1.11LMSP02010026Sphingolipids [SP]Ceramides [SP02]Cer(d18:2/20:0)
−1.39−1.04LMSP02010027Sphingolipids [SP]Ceramides [SP02]Cer(d18:2/20:1)
−17.13−17.13LMSP02050007Sphingolipids [SP]Ceramides [SP02]CerP(d18:1/24:1(15Z))
2.292.10LMSP0501AA31Sphingolipids [SP]Neutral glycosphingolipids [SP05]GlcCer(d16:1/23:0)
1.761.73LMSP0501AA32Sphingolipids [SP]Neutral glycosphingolipids [SP05]GlcCer(d18:1/23:0)
1.971.50LMSP0501AA10Sphingolipids [SP]Neutral glycosphingolipids [SP05]GlcCer(d18:1/26:1(17Z))
1.170.77LMGL02010095Glycerolipids [GL]Diradylglycerols [GL02]DG(16:1(9Z)/21:0/0:0)[iso2]
18.2918.12LMGL02010034Glycerolipids [GL]Diradylglycerols [GL02]DG(17:0/18:2(9Z,12Z)/0:0)[iso2]
1.250.87LMGL02010068Glycerolipids [GL]Diradylglycerols [GL02]DG(17:0/20:2(11Z,14Z)/0:0)[iso2]
1.461.22LMGL02010088Glycerolipids [GL]Diradylglycerols [GL02]DG(18:3(9Z,12Z,15Z)/19:0/0:0)[iso2]
1.160.23LMGL02010190Glycerolipids [GL]Diradylglycerols [GL02]DG(19:0/22:0/0:0)[iso2]
0.0019.84LMGL02010250Glycerolipids [GL]Diradylglycerols [GL02]DG(19:0/22:6(4Z,7Z,10Z,13Z,16Z,19Z)/0:0)[iso2]
16.2816.15LMGL02010296Glycerolipids [GL]Diradylglycerols [GL02]DG(22:3(10Z,13Z,16Z)/22:5(7Z,10Z,13Z,16Z,19Z)/0:0)[iso2]
−18.49−18.49LMGL03010017Glycerolipids [GL]Triradylglycerols [GL03]TG(16:0/16:0/16:1(9Z))[iso3]
−0.70−1.06LMGL03010970Glycerolipids [GL]Triradylglycerols [GL03]TG(16:0/20:2(11Z,14Z)/22:1(13Z))[iso6]
−15.83−15.83LMGL03010303Glycerolipids [GL]Triradylglycerols [GL03]TG(16:1(9Z)/18:2(9Z,12Z)/20:1(11Z))[iso6]
−16.51−16.51LMGL03010948Glycerolipids [GL]Triradylglycerols [GL03]TG(16:1(9Z)/20:4(5Z,8Z,11Z,14Z)/20:5(5Z,8Z,11Z,14Z,17Z))[iso6]
−16.53−16.53LMGL03010177Glycerolipids [GL]Triradylglycerols [GL03]TG(17:0/17:1(9Z)/20:0)[iso6]
2.872.20LMGL03010554Glycerolipids [GL]Triradylglycerols [GL03]TG(17:0/18:3(9Z,12Z,15Z)/20:4(5Z,8Z,11Z,14Z))[iso6]
15.0214.48LMGL03010196Glycerolipids [GL]Triradylglycerols [GL03]TG(17:2(9Z,12Z)/17:2(9Z,12Z)/18:3(9Z,12Z,15Z))[iso3]
2.031.42LMGL03011824Glycerolipids [GL]Triradylglycerols [GL03]TG(17:2(9Z,12Z)/20:5(5Z,8Z,11Z,14Z,17Z)/22:5(7Z,10Z,13Z,16Z,19Z))[iso6]
1.762.06LMGL03010748Glycerolipids [GL]Triradylglycerols [GL03]TG(18:1(9Z)/18:1(9Z)/20:5(5Z,8Z,11Z,14Z,17Z))[iso3]
17.2117.33LMGL03011321Glycerolipids [GL]Triradylglycerols [GL03]TG(18:1(9Z)/20:4(5Z,8Z,11Z,14Z)/20:5(5Z,8Z,11Z,14Z,17Z))[iso6]
−18.36−18.36LMGL03011398Glycerolipids [GL]Triradylglycerols [GL03]TG(18:2(9Z,12Z)/20:4(5Z,8Z,11Z,14Z)/20:5(5Z,8Z,11Z,14Z,17Z))[iso6]
2.051.56LMGL03011018Glycerolipids [GL]Triradylglycerols [GL03]TG(18:3(9Z,12Z,15Z)/19:0/20:4(5Z,8Z,11Z,14Z))[iso6]
−14.22−14.22LMGL03012401Glycerolipids [GL]Triradylglycerols [GL03]TG(18:3(9Z,12Z,15Z)/22:4(7Z,10Z,13Z,16Z)/22:6(4Z,7Z,10Z,13Z,16Z,19Z))[iso6]
−18.42−18.42LMGL03011840Glycerolipids [GL]Triradylglycerols [GL03]TG(20:4(5Z,8Z,11Z,14Z)/20:4(5Z,8Z,11Z,14Z)/20:4(5Z,8Z,11Z,14Z))
−17.36−17.36LMGP02010101Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(10:0/10:0)
16.4315.77LMGP02010232Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(11:0/14:0)[U]
−22.56−22.56LMGP02010230Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(11:0/16:0)[U]
−21.89−21.89LMGP02010371Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(12:0/19:1(9Z))
−21.95−21.95LMGP02010397Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(13:0/20:2(11Z,14Z))
−22.61−22.61LMGP02010062Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(14:0/15:0)[U]
0.0021.68LMGP02010419Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(14:0/22:1(11Z))
−16.58−16.58LMGP02010430Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(14:1(9Z)/17:1(9Z))
22.520.00LMGP02010441Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(14:1(9Z)/20:1(11Z))
0.58−20.36LMGP02010456Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(15:0/17:1(9Z))
−23.50−23.50LMGP02010458Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(15:0/18:1(9Z))
−23.79−23.79LMGP02010041Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(16:0/18:3(9Z,12Z,15Z))
−25.08−25.08LMGP02010509Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(16:0/19:1(9Z))
−21.21−21.21LMGP02010356Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(16:1(5Z)/16:1(5Z))
−26.03−26.03LMGP02010528Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(16:1(9Z)/19:1(9Z))
22.3422.19LMGP02010531Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(16:1(9Z)/20:2(11Z,14Z))
−21.36−21.36LMGP02010251Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(17:0/14:0)[U]
0.0023.89LMGP02010580Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(17:1(9Z)/20:1(11Z))
−16.42−16.42LMGP02010630Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(18:0/19:0)
−22.82−22.82LMGP02011202Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(18:0/20:3(8Z,11Z,14Z))
−16.27−16.27LMGP20020004Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(18:0/22:6(4Z,7Z,10Z,12E,16Z,19Z)(14OH))
0.0019.69LMGP02010768Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(18:4(6Z,9Z,12Z,15Z)/22:6(4Z,7Z,10Z,13Z,16Z,19Z))
−19.63−19.63LMGP02010779Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(19:0/18:4(6Z,9Z,12Z,15Z))
−19.78−19.78LMGP02010816Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(19:1(9Z)/20:4(5Z,8Z,11Z,14Z))
−28.16−28.16LMGP02010851Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(20:1(11Z)/17:2(9Z,12Z))
−20.02−20.02LMGP02010906Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(20:3(8Z,11Z,14Z)/15:0)
−18.03−18.03LMGP02010955Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(20:4(5Z,8Z,11Z,14Z)/20:5(5Z,8Z,11Z,14Z,17Z))
−16.70−16.70LMGP02011167Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(21:0/18:0)
15.7115.54LMGP02050025Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(22:0/0:0)
−16.39−0.16LMGP02010292Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(22:0/24:1(15Z))
−18.97−18.97LMGP02011083Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(22:2(13Z,16Z)/18:1(9Z))
19.910.00LMGP02020034Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(O-16:0/21:0)
20.1519.95LMGP02020048Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(O-18:0/18:2(9Z,12Z))
−17.57−17.57LMGP02020070Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE(O-20:0/17:2(9Z,12Z))
−22.94−22.94LMGP02010347Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE-NMe(16:0/16:0)[U]
−24.09−24.09LMGP02010326Glycerophospholipids [GP]Glycerophosphoethanolamines [GP02]PE-NMe2(18:1(9Z)/18:1(9Z))
15.7715.40LMGP03050009Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(14:0/0:0)
18.9418.83LMGP03010921Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(14:0/22:0)
−24.05−24.05LMGP03010135Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(14:1(9Z)/22:1(11Z))
−21.60−21.60LMGP03010238Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(17:0/19:1(9Z))
15.2015.06LMGP03050003Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(18:0/0:0)[U]
1.000.79LMGP03010961Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(18:0/20:1(11Z))
−17.84−17.84LMGP03010960Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(18:0/20:2(11Z,14Z))
16.4716.26LMGP03050011Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(18:2(9Z,12Z)/0:0)
−18.20−18.20LMGP03010458Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(19:0/16:1(9Z))
18.980.00LMGP03010868Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(19:0/19:0)
18.0517.70LMGP03010536Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(20:1(11Z)/17:0)
−19.650.30LMGP03010537Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(20:1(11Z)/17:1(9Z))
18.3918.34LMGP03010614Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(20:3(8Z,11Z,14Z)/21:0)
−22.02−22.02LMGP03010733Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(22:1(11Z)/17:0)
1.110.79LMGP03010768Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(22:2(13Z,16Z)/18:1(9Z))
−15.14−15.14LMGP03010840Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(22:6(4Z,7Z,10Z,13Z,16Z,19Z)/20:5(5Z,8Z,11Z,14Z,17Z))
−14.47−14.47LMGP03030030Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(P-18:0/14:0)
−15.69−15.69LMGP03030053Glycerophospholipids [GP]Glycerophosphoserines [GP03]PS(P-18:0/22:1(11Z))
−18.04−0.57LMGP04010123Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(14:1(9Z)/18:3(9Z,12Z,15Z))
1.290.85LMGP04010256Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(17:1(9Z)/17:0)
0.0015.39LMGP04010004Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(21:0/22:6(4Z,7Z,10Z,13Z,16Z,19Z))
−15.58−15.58LMGP04020088Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(O-16:0/22:6(4Z,7Z,10Z,13Z,16Z,19Z))
−15.83−15.83LMGP04020037Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(O-18:0/21:0)
−20.74−20.74LMGP04060001Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(O-20:0/0:0)
16.6415.98LMGP04020065Glycerophospholipids [GP]Glycerophosphoglycerols [GP04]PG(O-20:0/21:0)
−18.54−18.54LMGP06010167Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(16:0/22:1(11Z))
−17.98−17.98LMGP06010168Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(16:0/22:2(13Z,16Z))
0.0022.05LMGP06010185Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(16:1(9Z)/20:1(11Z))
0.39−22.33LMGP06010283Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(18:0/18:3(6Z,9Z,12Z))
−21.93−21.93LMGP06010428Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(19:0/17:1(9Z))
−18.01−18.01LMGP06010611Glycerophospholipids [GP]Glycerophosphoinositols [GP06]PI(20:4(5Z,8Z,11Z,14Z)/21:0)
−15.77−15.77LMGP10010921Glycerophospholipids [GP]Glycerophosphates [GP10]PA(14:1(9Z)/14:1(9Z))
−16.64−16.64LMGP10050024Glycerophospholipids [GP]Glycerophosphates [GP10]PA(18:4(6Z,9Z,12Z,15Z)/0:0)
−17.232.22LMGP10010853Glycerophospholipids [GP]Glycerophosphates [GP10]PA(21:0/13:0)
16.0515.57LMGP10010004Glycerophospholipids [GP]Glycerophosphates [GP10]PA(21:0/22:6(4Z,7Z,10Z,13Z,16Z,19Z))
−17.53−17.53LMGP10020015Glycerophospholipids [GP]Glycerophosphates [GP10]PA(O-16:0/21:0)
−15.26−15.26LMGP10020043Glycerophospholipids [GP]Glycerophosphates [GP10]PA(O-20:0/13:0)
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MDPI and ACS Style

Lee, J.; Suh, S.-J.; Kim, B.-S.; Lee, D.-W. Comparative Metabolomics Reveals Phosphine-Induced Metabolic Disruptions in Planococcus citri (Risso). Int. J. Mol. Sci. 2025, 26, 8020. https://doi.org/10.3390/ijms26168020

AMA Style

Lee J, Suh S-J, Kim B-S, Lee D-W. Comparative Metabolomics Reveals Phosphine-Induced Metabolic Disruptions in Planococcus citri (Risso). International Journal of Molecular Sciences. 2025; 26(16):8020. https://doi.org/10.3390/ijms26168020

Chicago/Turabian Style

Lee, Junbeom, Soo-Jung Suh, Bong-Su Kim, and Dae-Weon Lee. 2025. "Comparative Metabolomics Reveals Phosphine-Induced Metabolic Disruptions in Planococcus citri (Risso)" International Journal of Molecular Sciences 26, no. 16: 8020. https://doi.org/10.3390/ijms26168020

APA Style

Lee, J., Suh, S.-J., Kim, B.-S., & Lee, D.-W. (2025). Comparative Metabolomics Reveals Phosphine-Induced Metabolic Disruptions in Planococcus citri (Risso). International Journal of Molecular Sciences, 26(16), 8020. https://doi.org/10.3390/ijms26168020

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