Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect
ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Figure 1Loading Img

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
  • 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
  • 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
  • Lujia Yu
    Lujia Yu
    Department of Chemical and Biological Engineering, The Hong Kong University of Science and Technology, Hong Kong SAR, China
    More by Lujia Yu
  • 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
    More by Shengwang Du
  • 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]
    More by Weichuan Yu
  • , 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.
    More by Ning Li
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

    Article Views

    1663

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (8)»

    Abstract

    Abstract Image

    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.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    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)

    Terms & Conditions

    Electronic Supporting Information files are available without a subscription to ACS Web Editions. The American Chemical Society holds a copyright ownership interest in any copyrightable Supporting Information. Files available from the ACS website may be downloaded for personal use only. Users are not otherwise permitted to reproduce, republish, redistribute, or sell any Supporting Information from the ACS website, either in whole or in part, in either machine-readable form or any other form without permission from the American Chemical Society. For permission to reproduce, republish and redistribute this material, requesters must process their own requests via the RightsLink permission system. Information about how to use the RightsLink permission system can be found at http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 16 publications.

    1. Nan Yang, Jia Ren, Shuaijian Dai, Kai Wang, Manhin Leung, Yinglin Lu, Yuxing An, Al Burlingame, Shouling Xu, Zhiyong Wang, Weichuan Yu, Ning Li. The Quantitative Biotinylproteomics Studies Reveal a WInd-Related Kinase 1 (Raf-Like Kinase 36) Functioning as an Early Signaling Component in Wind-Induced Thigmomorphogenesis and Gravitropism. Molecular & Cellular Proteomics 2024, 23 (3) , 100738. https://doi.org/10.1016/j.mcpro.2024.100738
    2. Cheng-Yen Chen, Poonguzhali Selvaraj, Naweed I. Naqvi. Functional analysis of auxin derived from a symbiotic mycobiont. Frontiers in Plant Science 2023, 14 https://doi.org/10.3389/fpls.2023.1216680
    3. Shuaijian Dai, Shichang Liu, Chen Zhou, Fengchao Yu, Guang Zhu, Wenhao Zhang, Haiteng Deng, Al Burlingame, Weichuan Yu, Tingliang Wang, Ning Li. Capturing the hierarchically assorted modules of protein–protein interactions in the organized nucleome. Molecular Plant 2023, 16 (5) , 930-961. https://doi.org/10.1016/j.molp.2023.03.013
    4. Mingya Zhang, Quan Liu, Yuqi Huang, Le Wang, Minjia Tan, Jun-Yu Xu. Comparative proteomic and phosphoproteomic analysis of Mycobacteria treated with flavonoid quercetin and non-flavonoid caffeic acid. International Journal of Mass Spectrometry 2022, 482 , 116934. https://doi.org/10.1016/j.ijms.2022.116934
    5. Shijuan Yan, Ruchika Bhawal, Zhibin Yin, Theodore W. Thannhauser, Sheng Zhang. Recent advances in proteomics and metabolomics in plants. Molecular Horticulture 2022, 2 (1) https://doi.org/10.1186/s43897-022-00038-9
    6. Pin‐Lian Jiang, Cong Wang, Anne Diehl, Rosa Viner, Chris Etienne, Premchendar Nandhikonda, Leigh Foster, Ryan D. Bomgarden, Fan Liu. A Membrane‐Permeable and Immobilized Metal Affinity Chromatography (IMAC) Enrichable Cross‐Linking Reagent to Advance In Vivo Cross‐Linking Mass Spectrometry. Angewandte Chemie 2022, 134 (12) https://doi.org/10.1002/ange.202113937
    7. Pin‐Lian Jiang, Cong Wang, Anne Diehl, Rosa Viner, Chris Etienne, Premchendar Nandhikonda, Leigh Foster, Ryan D. Bomgarden, Fan Liu. A Membrane‐Permeable and Immobilized Metal Affinity Chromatography (IMAC) Enrichable Cross‐Linking Reagent to Advance In Vivo Cross‐Linking Mass Spectrometry. Angewandte Chemie International Edition 2022, 61 (12) https://doi.org/10.1002/anie.202113937
    8. Sadegh Balotf, Richard Wilson, Robert S. Tegg, David S. Nichols, Calum R. Wilson. Shotgun Proteomics as a Powerful Tool for the Study of the Proteomes of Plants, Their Pathogens, and Plant–Pathogen Interactions. Proteomes 2022, 10 (1) , 5. https://doi.org/10.3390/proteomes10010005
    9. Chen Zhou, Weichuan Yu. Cross-Linking Mass Spectrometry Data Analysis. 2022, 339-370. https://doi.org/10.1007/978-3-662-65902-1_17
    10. Tianhu Sun, Xuesong Zhou, Sombir Rao, Jiping Liu, Li Li. Protein–protein interaction techniques to investigate post-translational regulation of carotenogenesis. 2022, 301-325. https://doi.org/10.1016/bs.mie.2022.02.001
    11. Xiaolu Wang, Shengxuan Jin, Xu Chang, Guanrong Li, Ling Zhang, Shumei Jin. Two interaction proteins between AtPHB6 and AtSOT12 regulate plant salt resistance through ROS signaling. Plant Physiology and Biochemistry 2021, 169 , 70-80. https://doi.org/10.1016/j.plaphy.2021.11.001
    12. Gad Armony, Albert J.R. Heck, Wei Wu. Extracellular crosslinking mass spectrometry reveals HLA class I – HLA class II interactions on the cell surface. Molecular Immunology 2021, 136 , 16-25. https://doi.org/10.1016/j.molimm.2021.05.010
    13. Atieh Moradi, Shuaijian Dai, Emily Oi Ying Wong, Guang Zhu, Fengchao Yu, Hon-Ming Lam, Zhiyong Wang, Al Burlingame, Chengtao Lin, Alireza Afsharifar, Weichuan Yu, Tingliang Wang, Ning Li. Isotopically Dimethyl Labeling-Based Quantitative Proteomic Analysis of Phosphoproteomes of Soybean Cultivars. Biomolecules 2021, 11 (8) , 1218. https://doi.org/10.3390/biom11081218
    14. Devang Mehta, Johanna Krahmer, R. Glen Uhrig. Closing the protein gap in plant chronobiology. The Plant Journal 2021, 106 (6) , 1509-1522. https://doi.org/10.1111/tpj.15254
    15. , , Amanda L. Smythers, Leslie M. Hicks. Mapping the plant proteome: tools for surveying coordinating pathways. Emerging Topics in Life Sciences 2021, 5 (2) , 203-220. https://doi.org/10.1042/ETLS20200270
    16. Ruihua Huang, Chengwei Yang, Shengchun Zhang. The Arabidopsis PHB3 is a pleiotropic regulator for plant development. Plant Signaling & Behavior 2019, 14 (11) , 1656036. https://doi.org/10.1080/15592324.2019.1656036