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pmid:33238539
Effects of Excess Manganese on the Xylem Sap Protein Profile of Tomato (Solanum lycopersicum) as Revealed by Shotgun Proteomic Analysis.
Laura Ceballos-Laita · Elain Gutierrez-Carbonell · Daisuke Takahashi · Andrew Lonsdale · Anunciación Abadía · Monika S Doblin · Antony Bacic · Matsuo Uemura · Javier Abadía · Ana Flor López-Millán
International journal of molecular sciences · 2020 doi:10.3390/ijms21228863
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Complete file
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Some metals are naturally toxic, whereas others such as manganese (Mn) are essential micro-nutrients for plant growth but can become toxic when in excess. Changes in the composition of the xylem sap, which is the main pathway for ion transport within the plant, is therefore vital to understanding the plant's response(s) to metal toxicity. In this study we have assessed the effects of exposure of tomato roots to excess Mn on the protein profile of the xylem sap, using a shotgun proteomics approach. Plants were grown in nutrient solution using 4.6 and 300 µM MnCl2 as control and excess Mn treatments, respectively. This approach yielded 668 proteins reliably identified and quantified. Excess Mn caused statistically significant (at p ≤ 0.05) and biologically relevant changes in relative abundance (≥2-fold increases or ≥50% decreases) in 322 proteins, with 82% of them predicted to be secretory using three different prediction tools, with more decreasing than increasing (181 and 82, respectively), suggesting that this metal stress causes an overall deactivation of metabolic pathways. Processes most affected by excess Mn were in the oxido-reductase, polysaccharide and protein metabolism classes. Excess Mn induced changes in hydrolases and peroxidases involved in cell wall degradation and lignin formation, respectively, consistent with the existence of alterations in the cell wall. Protein turnover was also affected, as indicated by the decrease in proteolytic enzymes and protein synthesis-related proteins. Excess Mn modified the redox environment of the xylem sap, with changes in the abundance of oxido-reductase and defense protein classes indicating a stress scenario. Finally, results indicate that excess Mn decreased the amounts of proteins associated with several signaling pathways, including fasciclin-like arabinogalactan-proteins and lipids, as well as proteases, which may be involved in the release of signaling peptides and protein maturation. The comparison of the proteins changing in abundance in xylem sap and roots indicate the existence of tissue-specific and systemic responses to excess Mn. Data are available via ProteomeXchange with identifier PXD021973.", "claims": [{"id": "claim-method", "statement": "Only changes with a p ≤ 0.05 (ANOVA) and a ratio (fold change) ≥2 or ≤0.5 were considered as statistically significant and biologically relevant, respectively.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:33238539", "locator": "sections[21] \"4.5. 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Data are means ± SE (n = 6 for collection parameters and n = 4 for micronutrient concentrations). Statistically significant differences were calculated with the Student’s t-test: * p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001).", "structure": {"pmcid": "PMC7700171", "section_index": 3, "section_title": "2.1. Xylem Sap Collection and Mineral Composition", "row_count": 9, "column_count": 3}, "table": {"label": "Table 1", "caption": "Exudation rates, protein yields, leaf transpiration rates and Mn, Fe, Zn and Cu concentrations in the xylem sap of Solanum lycopersicum plants grown in control and excess Mn conditions for 8 days. Data are means ± SE (n = 6 for collection parameters and n = 4 for micronutrient concentrations). Statistically significant differences were calculated with the Student’s t-test: * p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001).", "rows": [["Collection Parameters", "Control", "Excess Mn"], ["Exudation rate (mL g−1 DW h−1)", "0.56 ± 0.11", "0.52 ± 0.21"], ["Protein yield (ng protein µL−1 xylem)", "9.0 ± 3.4", "27.0 ± 12.5 *"], ["Leaf transpiration rate (mmol H2O m−2 s−1)", "10.9 ± 0.5", "5.2 ± 0.1 ***"], ["Micronutrient concentrations (µM)"], ["Mn", "6.5 ± 0.8", "385.7 ± 16.1 ***"], ["Fe", "47.8 ± 12.5", "15.7 ± 2.5 **"], ["Zn", "9.5 ± 1.3", "8.0 ± 0.9 *"], ["Cu", "3.6 ± 0.8", "3.1 ± 0.5"]], "row_count": 9, "column_count": 3, "numeric_cells": 17, "header_rows": 1, "locator": "section[3]/table-wrap[1]#ijms-21-08863-t001"}}, {"id": "asset:table:pmid:33238539:2", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:9e0eb0f6fdb84c87a0f562462b36c9d0be7a8ba76e26cecd967e9d8ac5d395b2", "bytes": 3571, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[4]/table-wrap[1]#ijms-21-08863-t002", "version": null, "note": "List of proteins contributing to component 1 in the PCA. Standardized component scores were obtained in the PCA analysis of the differential proteins (ANOVA, p ≤ 0.05). Accession and description correspond to identifier and name in the ITAG3.2 database, respectively. Fold-changes (Fold +Mn/Control) were calculated by dividing the mean of normalized abundances (obtained with Progenesis QI v.2.5.1) in plants affected by excess Mn by that of control plants. The single protein with an asterisk after the ITAG database identifier was not included in Table S3 because it was out of the biological threshold range.", "structure": {"pmcid": "PMC7700171", "section_index": 4, "section_title": "2.2. Proteins Detected, Class Annotation and PCA Analysis", "row_count": 37, "column_count": 5}, "table": {"label": "Table 2", "caption": "List of proteins contributing to component 1 in the PCA. Standardized component scores were obtained in the PCA analysis of the differential proteins (ANOVA, p ≤ 0.05). Accession and description correspond to identifier and name in the ITAG3.2 database, respectively. Fold-changes (Fold +Mn/Control) were calculated by dividing the mean of normalized abundances (obtained with Progenesis QI v.2.5.1) in plants affected by excess Mn by that of control plants. The single protein with an asterisk after the ITAG database identifier was not included in Table S3 because it was out of the biological threshold range.", "rows": [["Accession", "Comp. 1 Score", "Comp. 2 Score", "Description", "Fold +Mn/Control"], ["Polysaccharide metabolism (9 proteins)"], ["Solyc01g104950.3.1", "0.001", "0.013", "LEXYL2 (GH3)", "0.5"], ["Solyc12g056960.2.1", "−0.002", "−0.061", "glucan endo-1,3-β-d-glucosidase (GH17)", "4.0"], ["Solyc10g079860.2.1", "−0.008", "−0.034", "glucan endo-1,3-β-d-glucosidase (GH17)", "51.6"], ["Solyc01g008620.3.1", "−0.024", "0.169", "glucan endo-1,3-β-glucosidase (GH17)", "233.6"], ["Solyc01g059965.1.1", "−0.492", "−2.371", "glucan endo-1,3- β-glucosidase (GH17)", "188.7"], ["Solyc02g086700.3.1", "−0.001", "−0.018", "glucan endo-1,3-β-glucosidase-like (GH17)", "48.8"], ["Solyc05g050130.3.1", "−0.001", "0.002", "acidic endochitinase (GH18)", "18.3"], ["Solyc10g055800.2.1", "−0.004", "−0.041", "endochitinase (GH19)", "51.1"], ["Solyc02g082920.3.1", "−0.001", "0.005", "chitinase (GH19)", "91.3"], ["Protein metabolism (5 proteins)"], ["Solyc04g078110.1.1", "0.002", "0.014", "serine protease SBT1 (MEROPS peptidase family S8)", "0.5"], ["Solyc06g074850.3.1", "0.001", "0.006", "carboxypeptidase (MEROPS peptidase family S10)", "0.3"], ["Solyc08g067100.2.1", "0.024", "0.047", "eukaryotic aspartyl protease family protein (MEROPS peptidase family A1)", "0.5"], ["Solyc08g079870.3.1", "−0.011", "0.072", "Subtilisin (MEROPS peptidase family S8)", "74.3"], ["Solyc08g079900.3.1", "−0.390", "3.028", "subtilisin-like protease (MEROPS peptidase family S8)", "57.1"], ["Oxido-reductases (5 proteins)"], ["Solyc06g076630.3.1", "0.007", "0.093", "peroxidase", "0.3"], ["Solyc12g094620.2.1", "0.015", "0.247", "catalase", "0.2"], ["Solyc01g105070.3.1", "−0.012", "−0.205", "LECEVI16G peroxidase precursor", "14.1"], ["Solyc06g005940.3.1", "−0.001", "−0.001", "protein disulfide-isomerase-like", "11.5"], ["Solyc09g009390.3.1", "−0.001", "−0.004", "monodehydroascorbate reductase", "2.2"], ["Defense (5 proteins)"], ["Solyc01g097240.3.1", "−0.003", "0.011", "pathogenesis-related protein PR-4", "153.6"], ["Solyc00g174340.2.1", "−0.001", "0.003", "pathogenesis-related protein PR-1", "27.2"], ["Solyc09g090980.3.1", "0.003", "−0.024", "major allergen Mal d 1", "25.7"], ["Solyc12g005720.1.1", "−0.001", "−0.012", "cysteine-rich receptor-like kinase protein", "9.8"], ["Solyc09g091000.3.1", "0.003", "−0.016", "major allergen d 1", "54.3"], ["Lipid metabolism (2 proteins)"], ["Solyc03g079880.3.1", "0.003", "0.043", "protease inhibitor/seed storage/lipid transfer family protein", "0.4"], ["Solyc08g067500.1.1", "0.002", "0.030", "non-specific lipid-transfer protein", "0.2"], ["Carbohydrate metabolism (1 protein)"], ["Solyc06g073190.3.1 *", "0.003", "0.66", "fructokinase-2", "0.7"], ["Miscellaneous (2 proteins)"], ["Solyc01g111170.3.1", "0.002", "0.032", "diageotropica/Peptidyl-prolyl cis-trans isomerase", "0.2"], ["Solyc08g074682.1.1", "0.001", "−0.015", "polyphenol oxidase precursor", "22.3"]], "row_count": 37, "column_count": 5, "numeric_cells": 140, "header_rows": 1, "locator": "section[4]/table-wrap[1]#ijms-21-08863-t002"}}, {"id": "asset:table:pmid:33238539:3", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:e44d25093fd6229fd9338481d218476cb061ad319f2896f0bc2ae2055757e423", "bytes": 6744, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[6]/table-wrap[1]#ijms-21-08863-t003", "version": null, "note": "Xylem sap proteins showing large changes in abundance (>25-fold increases or 90% decreases) among the total 263 secretory proteins affected by excess Mn (ANOVA, p ≤ 0.05 and fold-change ≥2 or ≤0.5). Accession ITAG3.2 and UniProt indicates the database entry. Abundance changes (change +Mn/Control) were calculated by dividing the mean of normalized abundances (obtained with Progenesis QI v.2.5.1) in plants affected by excess Mn by that in control plants. Description includes the protein name according to the ITAG3.2 and UniProt databases. The column Category indicates the classification (CPS, UPS or sUPS), and the column Prediction tool indicates the algorithms providing true values (SignalP, TargetP, SecretomeP, LSP and SPL). Detailed information about functional classification, identification and quantification is given in Tables S3 and S4.", "structure": {"pmcid": "PMC7700171", "section_index": 6, "section_title": "2.4. Protein Species Decreasing in Abundance", "row_count": 61, "column_count": 7}, "table": {"label": "Table 3", "caption": "Xylem sap proteins showing large changes in abundance (>25-fold increases or 90% decreases) among the total 263 secretory proteins affected by excess Mn (ANOVA, p ≤ 0.05 and fold-change ≥2 or ≤0.5). Accession ITAG3.2 and UniProt indicates the database entry. Abundance changes (change +Mn/Control) were calculated by dividing the mean of normalized abundances (obtained with Progenesis QI v.2.5.1) in plants affected by excess Mn by that in control plants. Description includes the protein name according to the ITAG3.2 and UniProt databases. The column Category indicates the classification (CPS, UPS or sUPS), and the column Prediction tool indicates the algorithms providing true values (SignalP, TargetP, SecretomeP, LSP and SPL). Detailed information about functional classification, identification and quantification is given in Tables S3 and S4.", "rows": [["#", "AccessionITAG3.2", "AccessionUniProt", "Change+Mn/Control", "Description", "Category", "Prediction Tool"], ["Polysaccharide metabolism (13 proteins)"], ["1", "Solyc09g092170.2.1", "A0A3Q7IA20", "0.1", "β-galactosidase STBG2 (GH35)", "CPS", "TarP, SecP"], ["2", "Solyc07g062210.3.1", "A0A3Q7HE74", "0.1", "protein trichome birefringence-like 41", "CPS", "SigP, TarP, SecP"], ["3", "Solyc04g016470.3.1", "A0A3Q7GST1", "111.6", "glucan endo-1,3-β-D-glucosidase (GH17)", "CPS", "TarP, SecP"], ["4", "Solyc10g079860.2.1", "A0A3Q7IKF2", "51.6", "glucan endo-1,3-β-D-glucosidase (GH17)", "CPS", "SigP, TarP, SecP"], ["5", "Solyc01g008620.3.1", "A0A3Q7E938", "233.6", "glucan endo-1,3-β-glucosidase (GH17)", "CPS", "SigP, TarP, SecP"], ["6", "Solyc01g059965.1.1", "Q01413", "188.7", "glucan endo-1,3-β-glucosidase (GH17)", "CPS", "SigP, TarP, SecP"], ["7", "Solyc02g086700.3.1", "A0A3Q7FVX4", "48.8", "glucan endo-1,3-β-glucosidase-like (GH17)", "CPS", "TarP, SecP"], ["8", "Solyc07g005100.3.1", "A0A3Q7H377", "30.4", "Chitinase/lysozyme (GH18)", "CPS", "SigP, TarP, SecP"], ["9", "Solyc10g055800.2.1", "A0A3Q7IHS3", "51.1", "endochitinase (GH19)", "CPS", "SigP, TarP, SecP"], ["10", "Solyc10g055810.2.1", "Q05538", "80.9", "basic 30 kDa endochitinase (GH19)", "CPS", "SigP, TarP, SecP"], ["11", "Solyc02g082920.3.1", "Q05539", "91.3", "acidic extracellular 26 kD chitinase (GH19)", "CPS", "SigP, TarP, SecP"], ["12", "Solyc10g055820.2.1", "A0A3Q7IIQ3", "44.4", "endochitinase (GH19)", "CPS", "SigP, TarP, SecP"], ["13", "Solyc11g005480.2.1", "A0A3Q7IP30", "26.1", "citrate-binding protein-like", "CPS", "SigP, TarP, SecP"], ["Protein metabolism (12 proteins)"], ["14", "Solyc00g005000.3.1", "A0A494G8A2", "0.1", "eukaryotic aspartyl protease family protein", "CPS", "SigP, TarP, SecP"], ["15", "Solyc07g064590.3.1", "A0A3Q7HFD0", "0.1", "inducible plastid-lipid associated protein", "UPS", "LSP, SecP"], ["16", "Solyc06g008170.3.1", "K4CUW3", "0.1", "50S ribosomal protein L14", "sUPS", "SecP"], ["17", "Solyc09g066430.3.1", "A0A3Q7J0J5", "0.1", "60S ribosomal protein L14", "sUPS", "SecP"], ["18", "Solyc08g079870.3.1", "-", "74.3", "subtilisin (MEROPS S8, clan SB)", "CPS", "SigP, TarP, SecP"], ["19", "Solyc08g079900.3.1", "-", "57.1", "subtilisin-like protease (MEROPS S8, clan SB)", "CPS", "SigP, TarP, SecP"], ["20", "Solyc06g008620.1.1", "A0A3Q7GN27", "31.7", "tolB protein-like protein (MEROPS S9)", "UPS", "SPL, SecP"], ["21", "Solyc01g087850.2.1", "O82777", "31.0", "serine protease SBT3 (MEROPS I13, clan IG)", "CPS", "SigP, TarP, SecP"], ["22", "Solyc03g020010.1.1", "O48625", "93.3", "Miraculin (MEROPS I13, clan IG)", "CPS", "SigP, TarP, SecP"], ["23", "Solyc03g019690.1.1", "A0A3Q7FGU5", "37.8", "kunitz-type protease inhibitor (MEROPS I13, clan IG)", "CPS", "SigP, TarP, SecP"], ["24", "Solyc03g098740.1.1", "A0A3Q7FNG4", "208.5", "kunitz trypsin inhibitor (MEROPS I3, clan IC)", "CPS", "SigP, TarP, SecP"], ["25", "Solyc08g080630.3.1", "A0A3Q7IQ00", "31.8", "ethylene-responsive proteinase inhibitor 1 (MEROPS I3, clan IC)", "CPS", "SigP, TarP, SecP"], ["Oxido-reductases (6 proteins)"], ["26", "Solyc06g005160.3.1", "Q3I5C4", "0.1", "Ascorbate peroxidase", "UPS", "LSP"], ["27", "Solyc04g074740.3.1", "A0A3Q7G526", "0.0", "blue copper protein-like", "CPS", "SigP, TarP, SecP"], ["28", "Solyc08g066740.3.1", "A0A3Q7HR33", "0.1", "early nodulin-like protein 1-like", "CPS", "SigP, TarP, SecP"], ["29", "Solyc08g028690.3.1", "A0A3Q7HMQ9", "0.0", "NAD(P)-binding Rossmann-fold superfamily protein", "UPS", "LSP, SPL, SecP"], ["30", "Solyc03g006700.3.1", "A0A3Q7FFR5", "28.7", "peroxidase (AtPrx52)", "CPS", "SigP, TarP, SecP"], ["31", "Solyc04g071890.3.1", "-", "71.6", "peroxidase", "CPS", "TarP, SecP"], ["Defense (5 proteins)"], ["32", "Solyc01g097240.3.1", "P32045", "153.6", "pathogenesis-related protein PR-4", "CPS", "SigP, TarP, SecP"], ["33", "Solyc00g174340.2.1", "A0A494GA45", "27.2", "pathogenesis-related protein 1", "CPS", "SigP, TarP, SecP"], ["34", "Solyc01g106620.2.1", "B2LW68", "61.8", "pathogenesis-related protein 1", "CPS", "SigP, TarP, SecP"], ["35", "Solyc07g005380.3.1", "A0A3Q7H2K6", "37.7", "pathogenesis-related PR-10-related/norcoclaurine synthase-like protein", "UPS", "SPL, SecP"], ["36", "Solyc09g090980.3.1", "-", "25.7", "major allergen Mal d 1", "UPS", "SPL"], ["Carbohydrate metabolism (4 proteins)"], ["37", "Solyc01g094200.3.1", "A0A3Q7EKQ6", "0.1", "malic enzyme", "UPS", "LSP, SecP"], ["38", "Solyc01g101040.3.1", "A0A3Q7EPC2", "0.1", "ATP-citrate synthase", "UPS", "LSP"], ["39", "Solyc01g058390.3.1", "A0A3Q7EEN4", "0.1", "galactokinase", "sUPS", "SecP"], ["40", "Solyc02g088690.3.1", "A0A3Q7F9B8", "0.1", "UDP-glucose 6-dehydrogenase family protein", "UPS", "LSP, SecP"], ["Signaling/regulation (5 proteins)"], ["41", "Solyc02g063090.3.1", "A0A3Q7FJZ3", "0.1", "T-complex protein 1 subunit zeta 1", "UPS", "LSP"], ["42", "Solyc05g056310.3.1", "A0A3Q7GLM4", "0.1", "T-complex protein 1 subunit gamma", "UPS", "LSP"], ["43", "Solyc01g086920.3.1", "A0A3Q7F2I5", "0.0", "leucine-rich repeat receptor-like protein kinase family", "CPS", "SigP, TarP, SecP"], ["44", "Solyc10g050110.1.1", "A0A3Q7IFT3", "0.1", "leucine-rich repeat receptor-like protein kinase family", "CPS", "SigP, TarP, SecP"], ["45", "Solyc08g082820.3.1", "A0A3Q7HX02", "31.3", "tomato BiP (binding protein)/grp78 (HSP70)", "CPS", "SigP, TarP, SecP"], ["Lipid metabolism (1 protein)"], ["46", "Solyc01g107990.3.1", "A0A3Q7FCU3", "0.1", "PI-PLC X domain-containing protein", "CPS", "SigP, TarP, SecP"], ["Miscellaneous (4 proteins)"], ["47", "Solyc03g115630.3.1", "A0A3Q7FR13", "0.1", "carbamoyl-phosphate synthase", "UPS", "LSP, SPL, SecP"], ["48", "Solyc06g005360.3.1", "A0A3Q7GNQ9", "0.1", "actin-depolymerizing factor family protein", "sUPS", "SecP"], ["49", "Solyc07g064160.3.1", "A0A3Q7HFB9", "0.1", "thiamine thiazole synthase", "sUP", "SecP"], ["50", "Solyc10g049970.2.1", "A0A3Q7IFZ6", "24.9", "kynurenine formamidase", "CPS", "SigP, TarP, SecP"], ["Unknown function (1 protein)"], ["51", "Solyc06g035920.3.1", "A0A3Q7GU06", "0.1", "remorin", "sUPS", "SecP"]], "row_count": 61, "column_count": 7, "numeric_cells": 213, "header_rows": 1, "locator": "section[6]/table-wrap[1]#ijms-21-08863-t003"}}, {"id": "asset:table:pmid:33238539:4", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:5404389272315c674074ac505549da21eb2d2b2aa09a5de68f96016c0aa860b2", "bytes": 4038, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[8]/table-wrap[1]#ijms-21-08863-t004", "version": null, "note": "Comparison of the changes in the xylem and root protein profiles. List of proteins showing statistically significant (ANOVA, p ≤ 0.05) and biologically relevant (fold ≥ 2 or ≤ 0.5) changes in abundance in both root and xylem sap proteomes when tomato plants grown in excess Mn were compared to controls. The column Category indicates the classification (CPS, UPS or sUPS), and the column Prediction tool indicates the algorithms providing true values (SignalP, TargetP, SecretomeP, LSP and SPL). Proteins changing in abundance in roots as a result of excess Mn were described in [42].", "structure": {"pmcid": "PMC7700171", "section_index": 8, "section_title": "2.6. Comparison of Changes Observed in the Xylem and Root Protein Profiles in Response to Excess Mn", "row_count": 35, "column_count": 7}, "table": {"label": "Table 4", "caption": "Comparison of the changes in the xylem and root protein profiles. List of proteins showing statistically significant (ANOVA, p ≤ 0.05) and biologically relevant (fold ≥ 2 or ≤ 0.5) changes in abundance in both root and xylem sap proteomes when tomato plants grown in excess Mn were compared to controls. The column Category indicates the classification (CPS, UPS or sUPS), and the column Prediction tool indicates the algorithms providing true values (SignalP, TargetP, SecretomeP, LSP and SPL). Proteins changing in abundance in roots as a result of excess Mn were described in [42].", "rows": [["", "", "", "Xylem sap", "Root"], ["", "Category", "Prediction Tool", "Fold +Mn/Control", "Fold +Mn/Control"], ["Proteins decreasing in both proteomes (16 proteins)"], ["Polysaccharide metabolism", "Solyc01g104950.3.1", "β -D-xylosidase 2 precursor (LEXYL2)", "CPS", "SigP, TarP, SecP", "0.5", "0.4"], ["Solyc05g012070.3.1", "UDP-glucose:protein transglucosylase-like protein", "UPS", "SPL", "0.2", "0.5"], ["Protein metabolism", "Solyc02g068740.3.1", "glycine cleavage system H family protein (MEROPS peptidase family C1)", "CPS", "SecP", "0.3", "0.5"], ["Solyc12g008630.2.1", "mitochondrial-processing peptidase subunit α-like (MEROPS peptidase family M16)", "UPS", "LSP, SecP", "0.4", "0.3"], ["Solyc02g081700.1.1", "proteasome subunit α type (MEROPS peptidase family T1A)", "UPS", "LSP, SecP", "0.5", "0.4"], ["Solyc06g073310.3.1", "60S ribosomal protein l9", "sUPS", "SecP", "0.5", "0.5"], ["Oxido-reductases", "Solyc06g005160.3.1", "ascorbate peroxidase", "UPS", "LSP", "0.1", "0.2"], ["Solyc01g107590.3.1", "cinnamyl alcohol dehydrogenase", "UPS", "LSP", "0.2", "0.3"], ["Amino acid metabolism", "Solyc02g080810.3.1", "aminomethyltransferase", "UPS", "LSP, SecP", "0.4", "0.5"], ["Solyc01g080280.3.1 *", "glutamine synthetase", "lnS", "LSP", "0.4", "0.5"], ["Carbohydrate metabolism", "Solyc08g080140.3.1", "3,5-epimerase/4-reductase", "sUPS", "SecP", "0.3", "0.2"], ["Signaling/regulation", "Solyc06g065520.3.1", "T-complex protein 1 subunit eta", "UPS", "LSP", "0.3", "0.2"], ["Miscellaneous", "Solyc02g087300.1.1", "transducin/WD40 repeat-like superfamily protein", "UPS", "SPL, SecP", "0.4", "0.5"], ["Solyc01g006280.3.1", "formate-tetrahydrofolate ligase", "UPS", "LSP, SPL", "0.4", "0.3"], ["Solyc01g109660.2.1", "meloidogyne-induced giant cell protein DB275 (glycine-rich RNA-binding protein)", "lnS", "None", "0.3", "0.5"], ["Solyc12g098150.2.1", "Aldo/keto reductase", "lnS", "None", "0.2", "0.5"], ["Proteins increasing in both proteomes (12 proteins)"], ["Polysaccharide metabolism", "Solyc01g059965.1.1", "β-1,3-glucanase (GH17)", "CPS", "SigP, TarP, SecP", "188.7", "8.3"], ["Solyc07g005100.3.1", "chitinase/lysozyme (GH18)", "CPS", "SigP, TarP, SecP", "30.4", "3.4"], ["Solyc10g055800.2.1", "chitinase (GH19)", "CPS", "SigP, TarP, SecP", "51.1", "3.6"], ["Solyc10g055810.2.1", "chitinase Z15140 (GH19)", "CPS", "SigP, TarP, SecP", "80.9", "4.9"], ["Solyc10g055820.2.1", "chitinase (GH19)", "CPS", "SigP, TarP, SecP", "44.4", "9.5"], ["Protein metabolism", "Solyc03g019690.1.1", "Kunitz-type protease inhibitor (MEROPS I3, clan IC)", "CPS", "SigP, TarP, SecP", "37.8", "105.3"], ["Oxido-reductases", "Solyc03g006700.3.1", "peroxidase", "CPS", "SigP, TarP, SecP", "28.7", "8.4"], ["Defense", "Solyc01g097240.3.1", "pathogenesis-related protein PR-4", "CPS", "SigP, TarP, SecP", "153.6", "12.2"], ["Solyc01g106620.2.1", "pathogenesis-related protein 1", "CPS", "SigP, TarP, SecP", "61.8", "4.3"], ["Solyc09g091000.3.1", "Major allergen d 1", "lnS", "None", "54.3", "10.5"], ["Miscellaneous", "Solyc10g049970.2.1", "kynurenine formamidase", "CPS", "SigP, TarP, SecP", "24.9", "32.6"], ["Solyc09g090430.3.1", "cyanate hydratase", "lnS", "None", "3.4", "2.4"], ["Proteins with opposite responses in root and xylem sap proteomes (2 proteins)"], ["Lipid metabolism", "Solyc12g017460.1.1", "GDSL esterase/lipase At1g28590-like", "CPS", "SigP, TarP, SecP", "13.5", "0.5"], ["Signaling/regulation", "Solyc01g106210.3.1", "heat shock protein 70", "UPS", "LSP", "3.4", "0.4"]], "row_count": 35, "column_count": 7, "numeric_cells": 110, "header_rows": 2, "locator": "section[8]/table-wrap[1]#ijms-21-08863-t004"}}], "gaps": ["asset:data:geo:PXD021973 not downloaded", "asset:data:geo:PXD021973 licence not read"]}, "analysis": {"state": "complete", "methods": [{"id": "method-1", "family": "group_comparison", "specific": "anova", "label": "Group comparison", "dsl_operations": 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