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Development of in Planta Chemical Cross-Linking-Based Quantitative Interactomics in Arabidopsis

  • Shichang Liu
    Shichang Liu
    Division of Life Science, Energy Institute, Institute for the Environment, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    More by Shichang Liu
    Orcidhttp://orcid.org/0000-0002-0251-5898
  • , 
  • Fengchao Yu
    Fengchao Yu
    Division of Biomedical Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    Department of Electronic and Computer Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    More by Fengchao Yu
    Orcidhttp://orcid.org/0000-0002-7695-3698
  • , 
  • Qin Hu
    Qin Hu
    Division of Life Science, Energy Institute, Institute for the Environment, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    More by Qin Hu
  • , 
  • Tingliang Wang
    Tingliang Wang
    Tsinghua-Peking Joint Center for Life Sciences, Center for Structural Biology, School of Life Sciences and School of Medicine, Tsinghua University, Beijing 100084, China
    More by Tingliang Wang
  • , 
  • Lujia Yu
    Lujia Yu
    Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
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  • , 
  • Shengwang Du
    Shengwang Du
    Department of Physics, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
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  • , 
  • Weichuan Yu*
    Weichuan Yu
    Division of Biomedical Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    Department of Electronic and Computer Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    *W.Y.: E-mail: [email protected]
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  • , and 
  • Ning Li*
    Ning Li
    Division of Life Science, Energy Institute, Institute for the Environment, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    Division of Biomedical Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    The Hong Kong University of Science and Technology, Shenzhen Research Institute, Shenzhen Guangdong 518057, China
    *N.L.: E-mail: [email protected]. Tel: +852-23587335.
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Cite this: J. Proteome Res. 2018, 17, 9, 3195–3213
Publication Date (Web):August 7, 2018
https://doi.org/10.1021/acs.jproteome.8b00320
Copyright © 2018 American Chemical Society
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    Abstract

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    An in planta chemical cross-linking-based quantitative interactomics (IPQCX–MS) workflow has been developed to investigate in vivo protein–protein interactions and alteration in protein structures in a model organism, Arabidopsis thaliana. A chemical cross-linker, azide-tag-modified disuccinimidyl pimelate (AMDSP), was directly applied onto Arabidopsis tissues. Peptides produced from protein fractions of CsCl density gradient centrifugation were dimethyl-labeled, from which the AMDSP cross-linked peptides were fractionated on chromatography, enriched, and analyzed by mass spectrometry. ECL2 and SQUA-D software were used to identify and quantitate these cross-linked peptides, respectively. These computer programs integrate peptide identification with quantitation and statistical evaluation. This workflow eventually identified 354 unique cross-linked peptides, including 61 and 293 inter- and intraprotein cross-linked peptides, respectively, demonstrating that it is able to in vivo identify hundreds of cross-linked peptides at an organismal level by overcoming the difficulties caused by multiple cellular structures and complex secondary metabolites of plants. Coimmunoprecipitation and super-resolution microscopy studies have confirmed the PHB3–PHB6 protein interaction found by IPQCX–MS. The quantitative interactomics also found hormone-induced structural changes of SBPase and other proteins. This mass-spectrometry-based interactomics will be useful in the study of in vivo protein–protein interaction networks in agricultural crops and plant–microbe interactions.

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jproteome.8b00320.

    • Figure S1. MS spectrum of cross-linker AMDPS. Figure S2. MS spectrum of disulfide-linked biotin and alkyne (DLBA). Figure S3. MS2 spectra of intermediate products (1), (2), (3), and the final product of cross-linked synthetic peptides EAKELIEGLPR and KELDDLR shown in Figure 1C. Figure S4. Two Venn diagrams of identified PSMs from pLink, Kojak, and ECL2. Figure S5. Verification of phb3 T-DNA insertion line (SALK_020707) and phb6 T-DNA insertion line (CS858159) using PCR. Figure S6. Workflow of wet lab. Figure S7. Comparison of the results of Gene Ontology (GO) analysis between the cross-linked proteins and the leaf proteome of Arabidopsis. Figure S8. Ethylene production rate of 38 day old Arabidopsis and ethylene effects on the phenotypes of 38 day old wild-type Arabidopsis Col-0 and mutant ein3/eil1. Figure S9. Validation of anti-PHB6 and PHB3 antibodies on 21 day old Col-0, phb3, phb6, and ein3/eil1. Figure S10. Calibration of the volumes of preserum used as negative control for coimmunoprecipitation. Figure S11. Titration and mutant experiments using anti-PHB3 antibody. Figure S12. Titration and mutant experiments using anti-PHB6 antibody. Figure S13. Super-resolution imaging of PHB3 and PHB6. Figure S14. Super-resolution imaging of PHB3 and PIP2a. Figure S15. Super-resolution imaging of PHB6 and PIP2a. Figure S16. Comparison of rosette diameters between Col-0 and phb6 mutants. (PDF)

    • Table S1a. Published software used to identify the cross-linked peptides that were generated by MS-noncleavable cross-linkers. Table S1b. Published software used to identify cross-linked peptides that were generated by MS-cleavable cross-linkers. (XLSX)

    • Table S2a. All PSMs of AMDSP monolinked peptides with FDR ≤ 0.01. Table S2b. Table containing all unique AMDSP monolinked peptides from Table S2a. Table S2c. Cellular components analysis of AMDSP monolinked proteins. (XLSX)

    • Table S3a. All PSMs of cross-linked peptides with FDR ≤ 0.05. Table S3b. All unique cross-linked peptides from Table S3a. Table S3c. All PSMs of cross-linked peptides with FDR ≤ 0.01. (XLSX)

    • Table S4. Quantification results. (XLSX)

    • Table S5. Biological processes and cellular components enrichment analysis of cross-linked proteins using AMDSP, DSBSO, or PIR containing cross-linker-based cross-linking, respectively. (XLSX)

    • Table S6a. Non-cross-linked (linear) peptides whose proteins have been used to quantify the cross-linked peptides in Table S4. Table S6b. Comparison of ethylene-regulated fold change of non-cross-linked (linear) peptide and cross-linked peptide from the same protein. (XLSX)

    • Supplemental File. Parameter files, log files, and results from pLink, Kojak, and ECL2, respectively.(ZIP)

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