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pmid:32257229

Al-induced proteomics changes in tomato plants over-expressing a glyoxalase I gene.

Xudong Sun · Hui Li · Santosh Thapa · Sasikiran Reddy Sangireddy · Xiaobo Pei · Wei Liu · Yuping Jiang · Shaolan Yang · Dafeng Hui · Sarabjit Bhatti · Suping Zhou · Yong Yang · Tara Fish · Theodore W Thannhauser

Horticulture research · 2020 doi:10.1038/s41438-020-0264-x

Paper

complete

Experiment

complete

Data

partial

Analysis

complete

Execution

absent

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Record details sci_version · id · kind · revision · content_hash · schema · created_at · updated_at · generator
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pmid:32257229
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science-record
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2026-11-01T15:40:59Z
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paper object · 10 fields
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title
Al-induced proteomics changes in tomato plants over-expressing a glyoxalase I gene.
doi
10.1038/s41438-020-0264-x
pmid
32257229
authors array · 14 items
[0]
Xudong Sun
[1]
Hui Li
[2]
Santosh Thapa
[3]
Sasikiran Reddy Sangireddy
[4]
Xiaobo Pei
[5]
Wei Liu
[6]
Yuping Jiang
[7]
Shaolan Yang
[8]
Dafeng Hui
[9]
Sarabjit Bhatti
[10]
Suping Zhou
[11]
Yong Yang
[12]
Tara Fish
[13]
Theodore W Thannhauser
journal
Horticulture research
year
2020
abstract
Glyoxalase I (Gly I) is the first enzyme in the glutathionine-dependent glyoxalase pathway for detoxification of methylglyoxal (MG) under stress conditions. Transgenic tomato 'Money Maker' plants overexpressing tomato SlGlyI gene (tomato unigene accession SGN-U582631/Solyc09g082120.3.1) were generated and homozygous lines were obtained after four generations of self-pollination. In this study, SlGlyI-overepxressing line (GlyI), wild type (WT, negative control) and plants transformed with empty vector (ECtr, positive control), were subjected to Al-treatment by growing in Magnavaca's nutrient solution (pH 4.5) supplemented with 20 µM Al3+ ion activity. After 30 days of treatments, the fresh and dry weight of shoots and roots of plants from Al-treated conditions decreased significantly compared to the non-treated conditions for all the three lines. When compared across the three lines, root fresh and dry weight of GlyI was significant higher than WT and ECtr, whereas there was no difference in shoot tissues. The basal 5 mm root-tips of GlyI plants expressed a significantly higher level of glyoxalase activity under both non-Al-treated and Al-treated conditions compared to the two control lines. Under Al-treated condition, there was a significant increase in MG content in ECtr and WT lines, but not in GlyI line. Quantitative proteomics analysis using tandem mass tags mass spectrometry identified 4080 quantifiable proteins and 201 Al-induced differentially expressed proteins (DEPs) in root-tip tissues from GlyI, and 4273 proteins and 230 DEPs from ECtr. The Al-down-regulated DEPs were classified into molecular pathways of gene transcription, RNA splicing and protein biosynthesis in both GlyI and ECtr lines. The Al-induced DEPs in GlyI associated with tolerance to Al3+ and MG toxicity are involved in callose degradation, cell wall components (xylan acetylation and pectin degradation), oxidative stress (antioxidants) and turnover of Al-damaged epidermal cells, repair of damaged DNA, epigenetics, gene transcription, and protein translation. A protein-protein association network was constructed to aid the selection of proteins in the same pathway but differentially regulated in GlyI or ECtr lines. Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title '25Dec2017_Suping_XSexp2_ITAG3.2' for SlGlyI-overexpressing tomato plants and PXD009848 under project title '25Dec2017_Suping_XSexp3_ITAG3.2' for positive control ECtr line transformed with empty vector.
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Aluminum and salt induced protein changes in tomato overexpressing a glyoxalase I gene
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Aluminum and salt induced protein changes in tomato plants transformed with bar gene
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The Al-induced differentially expressed proteins associated with degradation of methylglyoxal and Al toxicity in tomato plants overexpressing a SlGlyI gene
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Al-induced proteins associated with MG and Al toxicity
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Table 1
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The Al-induced differentially expressed proteins associated with degradation of methylglyoxal and Al toxicity in tomato plants overexpressing a SlGlyI gene
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[0] array · 3 items
[0]
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Fold (T/C)a
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[0]
GlyIb
[1]
ECtrc
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MG detoxification
[1]
Glyoxalase I (Solyc02g080630.3.1)
[2]
0.51*d
[3]
n/ie
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[0]
[1]
Glyoxalase I (Solyc12g007310.2.1)
[2]
0.36*d
[3]
0
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[0]
[1]
Glyoxalase I (Solyc07g040950.3.1)
[2]
−0.25
[3]
0.12
[5] array · 4 items
[0]
[1]
Glyoxalase I (Solyc06g007610.2.1)
[2]
−0.1*d
[3]
−0.06
[6] array · 4 items
[0]
[1]
Glyoxalase I (Solyc09g082120.3.1)f
[2]
0
[3]
−0.32
[7] array · 4 items
[0]
[1]
Glyoxalase II (Solyc06g053310.3.1)
[2]
0.41*d
[3]
0.04
[8] array · 4 items
[0]
[1]
Glyoxalase II (Solyc07g061960.3.1)
[2]
0.40*d
[3]
0.08
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[0]
Callose degredation
[1]
Beta-1 3-glucanases (Solyc01g008620.3.1;Solyc01g060020.3.1)
[2]
0.72–0.76*d
[3]
n/i
[10] array · 4 items
[0]
Cell wall matrix: Xylan
[1]
Acetyl xylan esterase A (Solyc04g078440.3.1)
[2]
−0.60*d
[3]
n/i
[11] array · 4 items
[0]
[1]
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[2]
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[3]
0.53*d
[12] array · 4 items
[0]
[1]
Caffeoyl-CoA O-methyltransferase (Solyc03g032220.3.1),O-methyltransferase 3 (Solyc10g008120.3.1)
[2]
0.74*d0.79*d
[3]
n/i
[13] array · 4 items
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[1]
Laccase-22 (Solyc08g079090.3.1)
[2]
−0.05
[3]
0.51*d
[14] array · 4 items
[0]
[1]
Polygalacturonases (Solyc05g005170,Solyc09g075460.3.1)Polygalacturonase inhibitor (Solyc09g014480)
[2]
n/i
[3]
0.51–0.59*d−0.67*d
[15] array · 4 items
[0]
[1]
Glutathione S-transferases (6 enzymes)
[2]
0.66 –1.18*d
[3]
0.67–0.69*d
[16] array · 4 items
[0]
Pectin
[1]
[2]
[3]
[17] array · 4 items
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Peroxidases (4 enzymes)
[2]
0.54–0.73*d
[3]
0.55–0.71*d
[18] array · 4 items
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Polyphenol oxidase (Solyc02g078650.3.1)
[2]
0.54*d
[3]
n/i
[19] array · 4 items
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[1]
Oxalate oxidase (Solyc03g123410.1.1)
[2]
0.48*d
[3]
n/i
[20] array · 4 items
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Vacolar sequestration
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Citrate binding protein (Solyc11g005480.2.1)
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0.78*d
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n/i
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section[18]/table-wrap[1]#Tab1
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Al-induced proteomics changes in tomato plants over-expressing a g
[1]
WT lines, but not in GlyI line. Quantitative proteomics analysis using tandem mass tags mass spectro
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ferentially regulated in GlyI or ECtr lines. Proteomics data are available via ProteomeXchange with
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all relevant TMT tags. The mass spectrometry proteomics data have been deposited in the ProteomeXcha
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Complete file
{"sci_version": "1.2", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:32257229", "kind": "science-record", "revision": 7, "content_hash": "sha256:528c132263f0853b31a8c97ecd4d5e720082de8e987eb3a00b32d326f140792f", "created_at": "2026-11-01T15:40:59Z", "updated_at": "2026-11-01T22:01:28Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Al-induced proteomics changes in tomato plants over-expressing a glyoxalase I gene.", "doi": "10.1038/s41438-020-0264-x", "pmid": "32257229", "authors": ["Xudong Sun", "Hui Li", "Santosh Thapa", "Sasikiran Reddy Sangireddy", "Xiaobo Pei", "Wei Liu", "Yuping Jiang", "Shaolan Yang", "Dafeng Hui", "Sarabjit Bhatti", "Suping Zhou", "Yong Yang", "Tara Fish", "Theodore W Thannhauser"], "journal": "Horticulture research", "year": 2020, "abstract": "Glyoxalase I (Gly I) is the first enzyme in the glutathionine-dependent glyoxalase pathway for detoxification of methylglyoxal (MG) under stress conditions. Transgenic tomato 'Money Maker' plants overexpressing tomato SlGlyI gene (tomato unigene accession SGN-U582631/Solyc09g082120.3.1) were generated and homozygous lines were obtained after four generations of self-pollination. In this study, SlGlyI-overepxressing line (GlyI), wild type (WT, negative control) and plants transformed with empty vector (ECtr, positive control), were subjected to Al-treatment by growing in Magnavaca's nutrient solution (pH 4.5) supplemented with 20 µM Al3+ ion activity. After 30 days of treatments, the fresh and dry weight of shoots and roots of plants from Al-treated conditions decreased significantly compared to the non-treated conditions for all the three lines. When compared across the three lines, root fresh and dry weight of GlyI was significant higher than WT and ECtr, whereas there was no difference in shoot tissues. The basal 5 mm root-tips of GlyI plants expressed a significantly higher level of glyoxalase activity under both non-Al-treated and Al-treated conditions compared to the two control lines. Under Al-treated condition, there was a significant increase in MG content in ECtr and WT lines, but not in GlyI line. Quantitative proteomics analysis using tandem mass tags mass spectrometry identified 4080 quantifiable proteins and 201 Al-induced differentially expressed proteins (DEPs) in root-tip tissues from GlyI, and 4273 proteins and 230 DEPs from ECtr. The Al-down-regulated DEPs were classified into molecular pathways of gene transcription, RNA splicing and protein biosynthesis in both GlyI and ECtr lines. The Al-induced DEPs in GlyI associated with tolerance to Al3+ and MG toxicity are involved in callose degradation, cell wall components (xylan acetylation and pectin degradation), oxidative stress (antioxidants) and turnover of Al-damaged epidermal cells, repair of damaged DNA, epigenetics, gene transcription, and protein translation. A protein-protein association network was constructed to aid the selection of proteins in the same pathway but differentially regulated in GlyI or ECtr lines. Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title '25Dec2017_Suping_XSexp2_ITAG3.2' for SlGlyI-overexpressing tomato plants and PXD009848 under project title '25Dec2017_Suping_XSexp3_ITAG3.2' for positive control ECtr line transformed with empty vector.", "claims": [{"id": "claim-data-access", "statement": "Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title ‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:32257229", "locator": "sections[0] \"Abstract\" paragraph 1", "quote": "Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title ‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector."}], "state": "complete"}], "gaps": []}, "experiment": {"state": "complete", "objective": null, "steps": [{"id": "read_published_estimate", "order": 1, "name": "Read the published estimate from the source", "kind": "other", "state": "complete", "blocked_on": null, "description": "The claim, method and evidence span published with the source article.", "duration_hours": null, "parameters": {}, "inputs": ["source:pmid:32257229"], "outputs": ["the published estimate and its evidence"], "instruments": [], "reagents": []}, {"id": "obtain_source_data", "order": 2, "name": "Obtain the source data from the named repository", "kind": "data-preparation", "state": "complete", "blocked_on": null, "description": "The GEO series accession resolves and its sample accessions are listed. This lane did not download the dataset or read its licence.", "duration_hours": null, "parameters": {}, "inputs": ["data:geo:PXD009456"], "outputs": ["the source data with its repository provenance"], "instruments": [], "reagents": []}, {"id": "run_analysis", "order": 3, "name": "Run the published analysis", "kind": "analysis", "state": "complete", "blocked_on": null, "description": "Apply the paper's statistical method to the resolved series and compare the result with the published target.", "duration_hours": null, "parameters": {}, "inputs": ["data:geo:PXD009456"], "outputs": ["the replicated result and its comparison"], "instruments": [], "reagents": []}], "materials": [], "instruments": [], "reagents": [], "conditions": {}, "gaps": []}, "data": {"state": "partial", "assets": [{"id": "source:pmid:32257229", "role": "manuscript", "format": "xml", "media_type": "application/xml", "uri": "https://doi.org/10.1038/s41438-020-0264-x", "sha256": 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‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector.", "structure": {"repository": "GEO", "access_route": "GEO accession URL", "access_statement_verbatim": "Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title ‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector.", "access_statement_kind": "data_availability_statement", "sample_accessions": [], "sample_count": null, "group_sizes": null, "group_sizes_basis": null, "platform": null, "taxon": null, "title": "Aluminum and salt induced protein changes in tomato overexpressing a glyoxalase I gene", "resolution_checked_at": "2026-10-31T18:35:55Z", "resolution_check": 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‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector.", "access_statement_kind": "data_availability_statement", "sample_accessions": [], "sample_count": null, "group_sizes": null, "group_sizes_basis": null, "platform": null, "taxon": null, "title": "Aluminum and salt induced protein changes  in tomato plants transformed with bar gene", "resolution_checked_at": "2026-10-31T18:35:55Z", "resolution_check": "identifier_resolution_only_no_download_no_licence_read", "downloaded": false, "licence_read": false}}, {"id": "asset:table:pmid:32257229:1", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:c9efdd1405e90949cd7bf767870278dee01b1db47212d9224ef21f2ee1e0902f", "bytes": 1779, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[18]/table-wrap[1]#Tab1", "version": null, "note": "The Al-induced differentially expressed proteins associated with degradation of methylglyoxal and Al toxicity in tomato plants overexpressing a SlGlyI gene", "structure": {"pmcid": "PMC7109090", "section_index": 18, "section_title": "Al-induced proteins associated with MG and Al toxicity", "row_count": 21, "column_count": 4}, "table": {"label": "Table 1", "caption": "The Al-induced differentially expressed proteins associated with degradation of methylglyoxal and Al toxicity in tomato plants overexpressing a SlGlyI gene", "rows": [["Biological function", "Protein description", "Fold (T/C)a"], ["GlyIb", "ECtrc"], ["MG detoxification", "Glyoxalase I (Solyc02g080630.3.1)", "0.51*d", "n/ie"], ["", "Glyoxalase I (Solyc12g007310.2.1)", "0.36*d", "0"], ["", "Glyoxalase I (Solyc07g040950.3.1)", "−0.25", "0.12"], ["", "Glyoxalase I (Solyc06g007610.2.1)", "−0.1*d", "−0.06"], ["", "Glyoxalase I (Solyc09g082120.3.1)f", "0", "−0.32"], ["", "Glyoxalase II (Solyc06g053310.3.1)", "0.41*d", "0.04"], ["", "Glyoxalase II (Solyc07g061960.3.1)", "0.40*d", "0.08"], ["Callose degredation", "Beta-1 3-glucanases (Solyc01g008620.3.1;Solyc01g060020.3.1)", "0.72–0.76*d", "n/i"], ["Cell wall matrix: Xylan", "Acetyl xylan esterase A (Solyc04g078440.3.1)", "−0.60*d", "n/i"], ["", "Xylanase inhibitor (Solyc01g080010.2.1)", "n/i", "0.53*d"], ["", "Caffeoyl-CoA O-methyltransferase (Solyc03g032220.3.1),O-methyltransferase 3 (Solyc10g008120.3.1)", "0.74*d0.79*d", "n/i"], ["Lignin", "Laccase-22 (Solyc08g079090.3.1)", "−0.05", "0.51*d"], ["", "Polygalacturonases (Solyc05g005170,Solyc09g075460.3.1)Polygalacturonase inhibitor (Solyc09g014480)", "n/i", "0.51–0.59*d−0.67*d"], ["", "Glutathione S-transferases (6 enzymes)", "0.66 –1.18*d", "0.67–0.69*d"], ["Pectin", "", "", ""], ["H2O2 metabolism", "Peroxidases (4 enzymes)", "0.54–0.73*d", "0.55–0.71*d"], ["", "Polyphenol oxidase (Solyc02g078650.3.1)", "0.54*d", "n/i"], ["", "Oxalate oxidase (Solyc03g123410.1.1)", "0.48*d", "n/i"], ["Vacolar sequestration", "Citrate binding protein (Solyc11g005480.2.1)", "0.78*d", "n/i"]], "row_count": 21, "column_count": 4, "numeric_cells": 45, "header_rows": 2, "locator": "section[18]/table-wrap[1]#Tab1"}}], "gaps": ["asset:data:geo:PXD009456 not downloaded", "asset:data:geo:PXD009456 licence not read", "asset:data:geo:PXD009848 not downloaded", "asset:data:geo:PXD009848 licence not read"]}, "analysis": {"state": "complete", "methods": [{"id": "method-1", "family": "group_comparison", "specific": "anova", "label": "Group comparison", "dsl_operations": ["group_summary", "welch_t", "bootstrap_mean_difference", "group_comparison_anova"], "missing_operations": [], "expressible": true, "parameters": {}, "data_shapes": ["two_or_more_groups_continuous"], "evidence": {"score": 0.8, "band": "high", "quote": "ANOVA"}}, {"id": "method-2", "family": "network_analysis", "specific": "ppi_network", "label": "Network / pathway analysis", 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The physical bench the paper used is not, so a physical validation cannot be run here."}, "data": {"tier": "R1", "reachable": true, "accessions": ["PXD009456", "PXD009848"], "resolved_accessions": ["PXD009456", "PXD009848"], "statements": ["Proteomics data are available via ProteomeXchange with identifiers PXD009456 under project title ‘25Dec2017_Suping_XSexp2_ITAG3.2’ for SlGlyI-overexpressing tomato plants and PXD009848 under project title ‘25Dec2017_Suping_XSexp3_ITAG3.2’ for positive control ECtr line transformed with empty vector."], "basis": "The paper names PXD009456, PXD009848 in ProteomeXchange Consortium via the PRIDE partner repository and the accession resolves in the repository. No dataset was downloaded and no licence was read."}}, "can_run": {"dsl_operations": ["group_summary", "welch_t", "bootstrap_mean_difference", "group_comparison_anova"], "assets": ["source:pmid:32257229", "data:geo:PXD009456", "asset:table:pmid:32257229:1"], "steps": ["run_analysis"]}, "must_build": {"dsl_operations": [], "converters": [], "readers": [], "capabilities": [], "data_gaps": ["data:geo:PXD009456"]}, "gaps": []}, "review": {"state": "partial", "machine_critique": {"kind": "extraction_review", "reader": {"model": "MiniMax-M3.1-Flash", "provider": "minimax", "provider_family": "minimax", "read_at": "2026-10-31T18:59:39Z", "independence": "single_reader"}, "evidence_check": {"method": null, "availability": "verbatim"}, "calls": 3, "usage": {"prompt_tokens": 41085, "completion_tokens": 1661, "cached_tokens": 792}}, "human_critique": null, "stages": [{"id": "extraction", "state": "complete", "reader": "MiniMax-M3.1-Flash", "provider": "minimax"}], "gaps": ["review.independent_reader", "review.machine_critique", "review.human_critique"]}, "execution": {"state": "absent", "status": "not_run", "mode": null, "runs": [], "gaps": ["execution.not_run"]}, "provenance": {"entities": [{"id": "pmid:32257229", "type": "paper", "label": "pmid:32257229"}, {"id": "source:pmid:32257229", "type": "manuscript", "label": "PMID 32257229 full text"}, {"id": "data:geo:PXD009456", "type": "dataset", "label": "GEO PXD009456"}], "activities": [{"id": "activity-reading-sci-2026-11-01", "type": "classification", "used": [{"id": "pmid:32257229", "type": "paper", "label": "pmid:32257229"}, {"id": "source:pmid:32257229", "type": "manuscript", "label": "PMID 32257229 full text"}, {"id": "data:geo:PXD009456", "type": "dataset", "label": "GEO PXD009456"}], "agent": "agent:corpus-assay-engine"}, {"id": "activity-read-32257229", "type": "extraction", "used": ["source:pmid:32257229"], "agent": "agent:minimax-reader"}, {"id": "activity-resolve-PXD009456", "type": "accession_resolution", "used": ["data:geo:PXD009456"], "agent": "agent:corpus-assay-engine"}], "agents": [{"id": "agent:corpus-assay-engine", "type": "software", "label": "Corpus assay engine"}, {"id": "agent:minimax-reader", "type": "software", "label": "MiniMax literature reader"}], "source_run_id": "reading-sci-2026-11-01", "dsl_catalogue_fingerprint": "343fb30756ba6ec3", "capability_table_fingerprint": "2cb3e42f047d2ecf", "snapshot_id": "ba34b49490d9bfaf"}, "lineage": {"parent_id": "pmid:32257229", "parent_hash": "sha256:5369bdb641ee90835067f4320d685802bac728ad66e61616da7a562b8b5bf6c5", "fork_of": null, "generation": 6}, "gaps": ["asset:data:geo:PXD009456 licence not read", "asset:data:geo:PXD009456 not downloaded", "asset:data:geo:PXD009848 licence not read", "asset:data:geo:PXD009848 not downloaded", "execution.not_run", "review.human_critique", "review.independent_reader", "review.machine_critique"], "assays": [{"role": "data_generation", "definition_id": "mass_spectrometry", "definition_version": "99e1195c7d6f", "definition_digest": null, "required_operations": [], "support_state": "partial", "source_hashes": {"assay_lexicon": "99e1195c7d6f"}, "confidence": 0.99, "evidence": ["Al-induced proteomics changes in tomato plants over-expressing a g", "WT lines, but not in GlyI line. 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