DOI: 10.1104/pp.112.210757. Time-Resolved Fluorescence Imaging Reveals Differential Interactions of<i>N</i>-Glycan Processing Enzymes across the Golgi Stack in Planta

Time-Resolved Fluorescence Imaging Reveals Differential Interactions ofN-Glycan Processing Enzymes across the Golgi Stack in Planta

10.1104/pp.112.210757

Crossref journal-article

Oxford University Press (OUP)

Plant Physiology (286)

Abstract

AbstractN-Glycan processing is one of the most important cellular protein modifications in plants and as such is essential for plant development and defense mechanisms. The accuracy of Golgi-located processing steps is governed by the strict intra-Golgi localization of sequentially acting glycosidases and glycosyltransferases. Their differential distribution goes hand in hand with the compartmentalization of the Golgi stack into cis-, medial-, and trans-cisternae, which separate early from late processing steps. The mechanisms that direct differential enzyme concentration are still unknown, but the formation of multienzyme complexes is considered a feasible Golgi protein localization strategy. In this study, we used two-photon excitation-Förster resonance energy transfer-fluorescence lifetime imaging microscopy to determine the interaction of N-glycan processing enzymes with differential intra-Golgi locations. Following the coexpression of fluorescent protein-tagged amino-terminal Golgi-targeting sequences (cytoplasmic-transmembrane-stem [CTS] region) of enzyme pairs in leaves of tobacco (Nicotiana spp.), we observed that all tested cis- and medial-Golgi enzymes, namely Arabidopsis (Arabidopsis thaliana) Golgi α-mannosidase I, Nicotiana tabacum β1,2-N-acetylglucosaminyltransferase I, Arabidopsis Golgi α-mannosidase II (GMII), and Arabidopsis β1,2-xylosyltransferase, form homodimers and heterodimers, whereas among the late-acting enzymes Arabidopsis β1,3-galactosyltransferase1 (GALT1), Arabidopsis α1,4-fucosyltransferase, and Rattus norvegicus α2,6-sialyltransferase (a nonplant Golgi marker), only GALT1 and medial-Golgi GMII were found to form a heterodimer. Furthermore, the efficiency of energy transfer indicating the formation of interactions decreased considerably in a cis-to-trans fashion. The comparative fluorescence lifetime imaging of several full-length cis- and medial-Golgi enzymes and their respective catalytic domain-deleted CTS clones further suggested that the formation of protein-protein interactions can occur through their amino-terminal CTS region.

Bibliography

Schoberer, J., Liebminger, E., Botchway, S. W., Strasser, R., & Hawes, C. (2013). Time-Resolved Fluorescence Imaging Reveals Differential Interactions ofN-Glycan Processing Enzymes across the Golgi Stack in Planta Â Â . Plant Physiology, 161(4), 1737â1754.

Authors 5

Jennifer Schoberer (first)
Eva Liebminger (additional)
Stanley W. Botchway (additional)
Richard Strasser (additional)
Chris Hawes (additional)

References 62 Referenced 52

10.1242/jcs.03284 / J Cell Sci / Plant G protein heterotrimers require dual lipidation motifs of Galpha and Ggamma and do not dissociate upon activation by Adjobo-Hermans (2006)
10.1104/pp.107.103986 / Plant Physiol / In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using Forster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy by Aker (2007)
10.1073/pnas.1112816108 / Proc Natl Acad Sci USA / Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex by Atmodjo (2011)
10.1016/S0962-8924(98)01410-X / Trends Cell Biol / Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell by Bastiaens (1999)
10.1186/1746-4811-8-25 / Plant Methods / Screening for in planta protein-protein interactions combining bimolecular fluorescence complementation with flow cytometry by Berendzen (2012)
10.1073/pnas.0500012102 / Proc Natl Acad Sci USA / Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain by Bhat (2005)
10.1046/j.1365-313X.1998.00208.x / Plant J / Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network by Boevink (1998)
10.1105/tpc.001586 / Plant Cell / Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching by Brandizzi (2002)
10.1104/pp.112.199356 / Plant Physiol / Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes by Chou (2012)
10.1093/glycob/7.1.1-b / Glycobiology / Golgi localization of glycosyltransferases: more questions than answers by Colley (1997)
10.1016/j.febslet.2011.05.066 / FEBS Lett / Förster resonance energy transfer demonstrates a flavonoid metabolon in living plant cells that displays competitive interactions between enzymes by Crosby (2011)
10.1023/A:1016061815748 / Plant Mol Biol / The Golgi localization of Arabidopsis thaliana beta1,2-xylosyltransferase in plant cells is dependent on its cytoplasmic and transmembrane sequences by Dirnberger (2002)
10.1016/S0014-5793(99)00712-7 / FEBS Lett / The N-terminal 77 amino acids from tobacco N-acetylglucosaminyltransferase I are sufficient to retain a reporter protein in the Golgi apparatus of Nicotiana benthamiana cells by Essl (1999)
10.1074/jbc.M412396200 / J Biol Chem / Multiple signals are required for alpha2,6-sialyltransferase (ST6Gal I) oligomerization and Golgi localization by Fenteany (2005)
10.1007/s11064-012-0741-1 / Neurochem Res / Spatial organization and stoichiometry of N-terminal domain-mediated glycosyltransferase complexes in Golgi membranes determined by FRET microscopy by Ferrari (2012)
10.1083/jcb.129.6.1543 / J Cell Biol / Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy: a stereochemical model for tyrosine kinase receptor activation by Gadella (1995)
10.1073/pnas.98.4.1625 / Proc Natl Acad Sci USA / Physical and functional association of glycolipid N-acetyl-galactosaminyl and galactosyl transferases in the Golgi apparatus by Giraudo (2001)
10.1016/j.pbi.2004.01.015 / Curr Opin Plant Biol / Posttranslational modification of therapeutic proteins in plants by Gomord (2004)
10.1007/s00425-012-1592-3 / Planta / ARAD proteins associated with pectic arabinan biosynthesis form complexes when transiently overexpressed in planta by Harholt (2012)
10.1074/jbc.M111.277681 / J Biol Chem / Functional organization of Golgi N- and O-glycosylation pathways involves pH-dependent complex formation that is impaired in cancer cells by Hassinen (2011)
10.1074/jbc.M110.103184 / J Biol Chem / Golgi N-glycosyltransferases form both homo- and heterodimeric enzyme complexes in live cells by Hassinen (2010)
10.1007/s11103-012-9891-4 / Plant Mol Biol / Unraveling the function of Arabidopsis thaliana OS9 in the endoplasmic reticulum-associated degradation of glycoproteins by Hüttner (2012)
10.1016/j.jbiosc.2011.09.011 / J Biosci Bioeng / Arabidopsis β1,2-xylosyltransferase: substrate specificity and participation in the plant-specific N-glycosylation pathway by Kajiura (2012)
10.1073/pnas.0800237105 / Proc Natl Acad Sci USA / Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus by Kang (2008)
10.1105/tpc.013862 / Plant Cell / The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress by Koiwa (2003)
10.1117/1.1577574 / J Biomed Opt / Quantitative imaging of protein-protein interactions by multiphoton fluorescence lifetime imaging microscopy using a streak camera by Krishnan (2003)
10.1177/108705719900400610 / J Biomol Screen / High throughput screening with multiphoton excitation by Lakowicz (1999)
10.1023/A:1006012005654 / Plant Mol Biol / N-Glycoprotein biosynthesis in plants: recent developments and future trends by Lerouge (1998)
10.1105/tpc.109.072363 / Plant Cell / Class I α-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana by Liebminger (2009)
10.1105/tpc.110.078154 / Plant Cell / Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants by Liu (2010)
10.1074/jbc.271.13.7758 / J Biol Chem / A disulfide-bonded dimer of the Golgi beta-galactoside alpha2,6-sialyltransferase is catalytically inactive yet still retains the ability to bind galactose by Ma (1996)
10.1016/0962-8924(91)90001-P / Trends Cell Biol / Golgi retention signals: do membranes hold the key? by Machamer (1991)
10.1073/pnas.97.2.668 / Proc Natl Acad Sci USA / The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate by McCormick (2000)
10.1104/pp.121.4.1127 / Plant Physiol / Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system by Nebenführ (1999)
10.1002/j.1460-2075.1994.tb06294.x / EMBO J / Kin recognition between medial Golgi enzymes in HeLa cells by Nilsson (1994)
10.1242/jcs.109.7.1975 / J Cell Sci / The role of the membrane-spanning domain and stalk region of N-acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells by Nilsson (1996)
10.1016/0014-5793(93)80906-B / FEBS Lett / Kin recognition: a model for the retention of Golgi enzymes by Nilsson (1993)
10.1016/S0300-9084(01)01312-8 / Biochimie / Trafficking and localisation of resident Golgi glycosylation enzymes by Opat (2001)
10.1111/j.1600-0854.2009.00930.x / Traffic / Fluorescence lifetime imaging of interactions between Golgi tethering factors and small GTPases in plants by Osterrieder (2009)
10.1046/j.0960-7412.2002.01604.x / Plant J / Structural requirements for Arabidopsis beta1,2-xylosyltransferase activity and targeting to the Golgi by Pagny (2003)
10.1016/S0960-9822(99)80117-1 / Curr Biol / Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy by Pepperkok (1999)
10.1073/pnas.241175798 / Proc Natl Acad Sci USA / Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo by Pinhal (2001)
10.1074/jbc.M103664200 / J Biol Chem / Location and mechanism of alpha 2,6-sialyltransferase dimer formation: role of cysteine residues in enzyme dimerization, localization, activity, and processing by Qian (2001)
10.1007/s11103-005-4618-4 / Plant Mol Biol / Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein by Renna (2005)
10.1002/jcp.21744 / J Cell Physiol / Elevated Golgi pH impairs terminal N-glycosylation by inducing mislocalization of Golgi glycosyltransferases by Rivinoja (2009)
10.1111/j.1462-5822.2010.01472.x / Cell Microbiol / ER quality control of immune receptors and regulators in plants by Saijo (2010)
10.1105/tpc.105.036400 / Plant Cell / Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway by Saint-Jore-Dupas (2006)
10.1139/o86-026 / Biochem Cell Biol / Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides by Schachter (1986)
10.1111/j.1600-0854.2010.01106.x / Traffic / Sequential depletion and acquisition of proteins during Golgi stack disassembly and reformation by Schoberer (2010)
10.1093/mp/ssq082 / Mol Plant / Sub-compartmental organization of Golgi-resident N-glycan processing enzymes in plants by Schoberer (2011)
10.1111/j.1600-0854.2008.00841.x / Traffic / Arginine/lysine residues in the cytoplasmic tail promote ER export of plant glycosylation enzymes by Schoberer (2009)
10.1105/tpc.110.074385 / Plant Cell / Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties by Sparkes (2010)
10.1038/nprot.2006.286 / Nat Protoc / Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants by Sparkes (2006)
10.1074/jbc.M208023200 / J Biol Chem / The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis by Stolz (2002)
10.1105/tpc.107.052985 / Plant Cell / A unique β1,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana by Strasser (2007)
10.1016/S0014-5793(00)01443-5 / FEBS Lett / Molecular cloning and functional expression of β1, 2-xylosyltransferase cDNA from Arabidopsis thaliana by Strasser (2000)
10.1111/j.1365-313X.2005.02648.x / Plant J / Molecular cloning and characterization of Arabidopsis thaliana Golgi α-mannosidase II, a key enzyme in the formation of complex N-glycans in plants by Strasser (2006)
10.1186/1471-2121-6-22 / BMC Cell Biol / The use of time-resolved fluorescence imaging in the study of protein kinase C localisation in cells by Stubbs (2005)
10.1038/nprot.2011.364 / Nat Protoc / Investigating protein-protein interactions in living cells using fluorescence lifetime imaging microscopy by Sun (2011)
10.1016/j.bpj.2010.06.004 / Biophys J / Three-color spectral FRET microscopy localizes three interacting proteins in living cells by Sun (2010)
10.1007/s00232-004-0656-5 / J Membr Biol / Organization of Golgi glycosyltransferases in membranes: complexity via complexes by Young (2004)
10.1104/pp.110.159749 / Plant Physiol / A glucurono(arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively by Zeng (2010)

Dates

Type	When
Created	12 years, 6 months ago (Feb. 11, 2013, 9:57 p.m.)
Deposited	3 years, 6 months ago (Feb. 8, 2022, 7:31 a.m.)
Indexed	1 month ago (July 26, 2025, 4:47 a.m.)
Issued	12 years, 6 months ago (Feb. 11, 2013)
Published	12 years, 6 months ago (Feb. 11, 2013)
Published Online	12 years, 6 months ago (Feb. 11, 2013)
Published Print	12 years, 4 months ago (April 2, 2013)

Funders 0

None

BibTeX

@article{Schoberer_2013, title={Time-Resolved Fluorescence Imaging Reveals Differential Interactions ofN-Glycan Processing Enzymes across the Golgi Stack in Planta }, volume={161}, ISSN={1532-2548}, url={http://dx.doi.org/10.1104/pp.112.210757}, DOI={10.1104/pp.112.210757}, number={4}, journal={Plant Physiology}, publisher={Oxford University Press (OUP)}, author={Schoberer, Jennifer and Liebminger, Eva and Botchway, Stanley W. and Strasser, Richard and Hawes, Chris}, year={2013}, month=feb, pages={1737–1754} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        26
      ]
    ],
    "date-time": "2025-07-26T08:47:08Z",
    "timestamp": 1753519628231
  },
  "reference-count": 62,
  "publisher": "Oxford University Press (OUP)",
  "issue": "4",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2021,
            1,
            25
          ]
        ],
        "date-time": "2021-01-25T00:00:00Z",
        "timestamp": 1611532800000
      },
      "content-version": "vor",
      "delay-in-days": 2905,
      "URL": "https://creativecommons.org/licenses/by/4.0/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2013,
        4,
        2
      ]
    ]
  },
  "abstract": "<jats:title>Abstract</jats:title><jats:p>N-Glycan processing is one of the most important cellular protein modifications in plants and as such is essential for plant development and defense mechanisms. The accuracy of Golgi-located processing steps is governed by the strict intra-Golgi localization of sequentially acting glycosidases and glycosyltransferases. Their differential distribution goes hand in hand with the compartmentalization of the Golgi stack into cis-, medial-, and trans-cisternae, which separate early from late processing steps. The mechanisms that direct differential enzyme concentration are still unknown, but the formation of multienzyme complexes is considered a feasible Golgi protein localization strategy. In this study, we used two-photon excitation-F\u00f6rster resonance energy transfer-fluorescence lifetime imaging microscopy to determine the interaction of N-glycan processing enzymes with differential intra-Golgi locations. Following the coexpression of fluorescent protein-tagged amino-terminal Golgi-targeting sequences (cytoplasmic-transmembrane-stem [CTS] region) of enzyme pairs in leaves of tobacco (Nicotiana spp.), we observed that all tested cis- and medial-Golgi enzymes, namely Arabidopsis (Arabidopsis thaliana) Golgi \u03b1-mannosidase I, Nicotiana tabacum \u03b21,2-N-acetylglucosaminyltransferase I, Arabidopsis Golgi \u03b1-mannosidase II (GMII), and Arabidopsis \u03b21,2-xylosyltransferase, form homodimers and heterodimers, whereas among the late-acting enzymes Arabidopsis \u03b21,3-galactosyltransferase1 (GALT1), Arabidopsis \u03b11,4-fucosyltransferase, and Rattus norvegicus \u03b12,6-sialyltransferase (a nonplant Golgi marker), only GALT1 and medial-Golgi GMII were found to form a heterodimer. Furthermore, the efficiency of energy transfer indicating the formation of interactions decreased considerably in a cis-to-trans fashion. The comparative fluorescence lifetime imaging of several full-length cis- and medial-Golgi enzymes and their respective catalytic domain-deleted CTS clones further suggested that the formation of protein-protein interactions can occur through their amino-terminal CTS region.</jats:p>",
  "DOI": "10.1104/pp.112.210757",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2013,
        2,
        12
      ]
    ],
    "date-time": "2013-02-12T02:57:52Z",
    "timestamp": 1360637872000
  },
  "page": "1737-1754",
  "source": "Crossref",
  "is-referenced-by-count": 52,
  "title": "Time-Resolved Fluorescence Imaging Reveals Differential Interactions of<i>N</i>-Glycan Processing Enzymes across the Golgi Stack in Planta \u00a0 \u00a0",
  "prefix": "10.1093",
  "volume": "161",
  "author": [
    {
      "given": "Jennifer",
      "family": "Schoberer",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Muthgasse 18, 1190 Vienna, Austria (J.S., E.L., R.S.)"
        },
        {
          "name": "Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Headington, Oxford OX3 0BP, United Kingdom (J.S., C.H.); and"
        }
      ]
    },
    {
      "given": "Eva",
      "family": "Liebminger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Muthgasse 18, 1190 Vienna, Austria (J.S., E.L., R.S.)"
        }
      ]
    },
    {
      "given": "Stanley W.",
      "family": "Botchway",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Research Complex at Harwell, Central Laser Facility, Science and Technology Facilities Council, Rutherford Appleton Laboratory, Harwell-Oxford, Didcot OX11 0QX, United Kingdom (S.W.B.)"
        }
      ]
    },
    {
      "given": "Richard",
      "family": "Strasser",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Muthgasse 18, 1190 Vienna, Austria (J.S., E.L., R.S.)"
        }
      ]
    },
    {
      "given": "Chris",
      "family": "Hawes",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Headington, Oxford OX3 0BP, United Kingdom (J.S., C.H.); and"
        }
      ]
    }
  ],
  "member": "286",
  "published-online": {
    "date-parts": [
      [
        2013,
        2,
        11
      ]
    ]
  },
  "reference": [
    {
      "key": "2021041916144317900_b1",
      "doi-asserted-by": "crossref",
      "first-page": "5087",
      "DOI": "10.1242/jcs.03284",
      "article-title": "Plant G protein heterotrimers require dual lipidation motifs of Galpha and Ggamma and do not dissociate upon activation",
      "volume": "119",
      "author": "Adjobo-Hermans",
      "year": "2006",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2021041916144317900_b2",
      "doi-asserted-by": "crossref",
      "first-page": "339",
      "DOI": "10.1104/pp.107.103986",
      "article-title": "In vivo hexamerization and characterization of the Arabidopsis AAA ATPase CDC48A complex using Forster resonance energy transfer-fluorescence lifetime imaging microscopy and fluorescence correlation spectroscopy",
      "volume": "145",
      "author": "Aker",
      "year": "2007",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021041916144317900_b3",
      "doi-asserted-by": "crossref",
      "first-page": "20225",
      "DOI": "10.1073/pnas.1112816108",
      "article-title": "Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex",
      "volume": "108",
      "author": "Atmodjo",
      "year": "2011",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b4",
      "doi-asserted-by": "crossref",
      "first-page": "48",
      "DOI": "10.1016/S0962-8924(98)01410-X",
      "article-title": "Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell",
      "volume": "9",
      "author": "Bastiaens",
      "year": "1999",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2021041916144317900_b5",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1186/1746-4811-8-25",
      "article-title": "Screening for in planta protein-protein interactions combining bimolecular fluorescence complementation with flow cytometry",
      "volume": "8",
      "author": "Berendzen",
      "year": "2012",
      "journal-title": "Plant Methods"
    },
    {
      "key": "2021041916144317900_b6",
      "doi-asserted-by": "crossref",
      "first-page": "3135",
      "DOI": "10.1073/pnas.0500012102",
      "article-title": "Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain",
      "volume": "102",
      "author": "Bhat",
      "year": "2005",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b7",
      "doi-asserted-by": "crossref",
      "first-page": "441",
      "DOI": "10.1046/j.1365-313X.1998.00208.x",
      "article-title": "Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network",
      "volume": "15",
      "author": "Boevink",
      "year": "1998",
      "journal-title": "Plant J"
    },
    {
      "key": "2021041916144317900_b8",
      "doi-asserted-by": "crossref",
      "first-page": "1293",
      "DOI": "10.1105/tpc.001586",
      "article-title": "Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching",
      "volume": "14",
      "author": "Brandizzi",
      "year": "2002",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b9",
      "doi-asserted-by": "crossref",
      "first-page": "1355",
      "DOI": "10.1104/pp.112.199356",
      "article-title": "Xyloglucan xylosyltransferases XXT1, XXT2, and XXT5 and the glucan synthase CSLC4 form Golgi-localized multiprotein complexes",
      "volume": "159",
      "author": "Chou",
      "year": "2012",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021041916144317900_b10",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1093/glycob/7.1.1-b",
      "article-title": "Golgi localization of glycosyltransferases: more questions than answers",
      "volume": "7",
      "author": "Colley",
      "year": "1997",
      "journal-title": "Glycobiology"
    },
    {
      "key": "2021041916144317900_b11",
      "doi-asserted-by": "crossref",
      "first-page": "2193",
      "DOI": "10.1016/j.febslet.2011.05.066",
      "article-title": "F\u00f6rster resonance energy transfer demonstrates a flavonoid metabolon in living plant cells that displays competitive interactions between enzymes",
      "volume": "585",
      "author": "Crosby",
      "year": "2011",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2021041916144317900_b12",
      "doi-asserted-by": "crossref",
      "first-page": "273",
      "DOI": "10.1023/A:1016061815748",
      "article-title": "The Golgi localization of Arabidopsis thaliana beta1,2-xylosyltransferase in plant cells is dependent on its cytoplasmic and transmembrane sequences",
      "volume": "50",
      "author": "Dirnberger",
      "year": "2002",
      "journal-title": "Plant Mol Biol"
    },
    {
      "key": "2021041916144317900_b13",
      "doi-asserted-by": "crossref",
      "first-page": "169",
      "DOI": "10.1016/S0014-5793(99)00712-7",
      "article-title": "The N-terminal 77 amino acids from tobacco N-acetylglucosaminyltransferase I are sufficient to retain a reporter protein in the Golgi apparatus of Nicotiana benthamiana cells",
      "volume": "453",
      "author": "Essl",
      "year": "1999",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2021041916144317900_b14",
      "doi-asserted-by": "crossref",
      "first-page": "5423",
      "DOI": "10.1074/jbc.M412396200",
      "article-title": "Multiple signals are required for alpha2,6-sialyltransferase (ST6Gal I) oligomerization and Golgi localization",
      "volume": "280",
      "author": "Fenteany",
      "year": "2005",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b15",
      "doi-asserted-by": "crossref",
      "first-page": "1325",
      "DOI": "10.1007/s11064-012-0741-1",
      "article-title": "Spatial organization and stoichiometry of N-terminal domain-mediated glycosyltransferase complexes in Golgi membranes determined by FRET microscopy",
      "volume": "37",
      "author": "Ferrari",
      "year": "2012",
      "journal-title": "Neurochem Res"
    },
    {
      "key": "2021041916144317900_b16",
      "doi-asserted-by": "crossref",
      "first-page": "1543",
      "DOI": "10.1083/jcb.129.6.1543",
      "article-title": "Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy: a stereochemical model for tyrosine kinase receptor activation",
      "volume": "129",
      "author": "Gadella",
      "year": "1995",
      "journal-title": "J Cell Biol"
    },
    {
      "key": "2021041916144317900_b17",
      "doi-asserted-by": "crossref",
      "first-page": "1625",
      "DOI": "10.1073/pnas.98.4.1625",
      "article-title": "Physical and functional association of glycolipid N-acetyl-galactosaminyl and galactosyl transferases in the Golgi apparatus",
      "volume": "98",
      "author": "Giraudo",
      "year": "2001",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b18",
      "doi-asserted-by": "crossref",
      "first-page": "171",
      "DOI": "10.1016/j.pbi.2004.01.015",
      "article-title": "Posttranslational modification of therapeutic proteins in plants",
      "volume": "7",
      "author": "Gomord",
      "year": "2004",
      "journal-title": "Curr Opin Plant Biol"
    },
    {
      "key": "2021041916144317900_b19",
      "doi-asserted-by": "crossref",
      "first-page": "115",
      "DOI": "10.1007/s00425-012-1592-3",
      "article-title": "ARAD proteins associated with pectic arabinan biosynthesis form complexes when transiently overexpressed in planta",
      "volume": "236",
      "author": "Harholt",
      "year": "2012",
      "journal-title": "Planta"
    },
    {
      "key": "2021041916144317900_b20",
      "doi-asserted-by": "crossref",
      "first-page": "38329",
      "DOI": "10.1074/jbc.M111.277681",
      "article-title": "Functional organization of Golgi N- and O-glycosylation pathways involves pH-dependent complex formation that is impaired in cancer cells",
      "volume": "286",
      "author": "Hassinen",
      "year": "2011",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b21",
      "doi-asserted-by": "crossref",
      "first-page": "17771",
      "DOI": "10.1074/jbc.M110.103184",
      "article-title": "Golgi N-glycosyltransferases form both homo- and heterodimeric enzyme complexes in live cells",
      "volume": "285",
      "author": "Hassinen",
      "year": "2010",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b22",
      "doi-asserted-by": "crossref",
      "first-page": "21",
      "DOI": "10.1007/s11103-012-9891-4",
      "article-title": "Unraveling the function of Arabidopsis thaliana OS9 in the endoplasmic reticulum-associated degradation of glycoproteins",
      "volume": "79",
      "author": "H\u00fcttner",
      "year": "2012",
      "journal-title": "Plant Mol Biol"
    },
    {
      "key": "2021041916144317900_b23",
      "doi-asserted-by": "crossref",
      "first-page": "48",
      "DOI": "10.1016/j.jbiosc.2011.09.011",
      "article-title": "Arabidopsis \u03b21,2-xylosyltransferase: substrate specificity and participation in the plant-specific N-glycosylation pathway",
      "volume": "113",
      "author": "Kajiura",
      "year": "2012",
      "journal-title": "J Biosci Bioeng"
    },
    {
      "key": "2021041916144317900_b24",
      "doi-asserted-by": "crossref",
      "first-page": "5933",
      "DOI": "10.1073/pnas.0800237105",
      "article-title": "Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus",
      "volume": "105",
      "author": "Kang",
      "year": "2008",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b25",
      "doi-asserted-by": "crossref",
      "first-page": "2273",
      "DOI": "10.1105/tpc.013862",
      "article-title": "The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress",
      "volume": "15",
      "author": "Koiwa",
      "year": "2003",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b26",
      "doi-asserted-by": "crossref",
      "first-page": "362",
      "DOI": "10.1117/1.1577574",
      "article-title": "Quantitative imaging of protein-protein interactions by multiphoton fluorescence lifetime imaging microscopy using a streak camera",
      "volume": "8",
      "author": "Krishnan",
      "year": "2003",
      "journal-title": "J Biomed Opt"
    },
    {
      "key": "2021041916144317900_b27",
      "doi-asserted-by": "crossref",
      "first-page": "355",
      "DOI": "10.1177/108705719900400610",
      "article-title": "High throughput screening with multiphoton excitation",
      "volume": "4",
      "author": "Lakowicz",
      "year": "1999",
      "journal-title": "J Biomol Screen"
    },
    {
      "key": "2021041916144317900_b28",
      "doi-asserted-by": "crossref",
      "first-page": "31",
      "DOI": "10.1023/A:1006012005654",
      "article-title": "N-Glycoprotein biosynthesis in plants: recent developments and future trends",
      "volume": "38",
      "author": "Lerouge",
      "year": "1998",
      "journal-title": "Plant Mol Biol"
    },
    {
      "key": "2021041916144317900_b29",
      "doi-asserted-by": "crossref",
      "first-page": "3850",
      "DOI": "10.1105/tpc.109.072363",
      "article-title": "Class I \u03b1-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana",
      "volume": "21",
      "author": "Liebminger",
      "year": "2009",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b30",
      "doi-asserted-by": "crossref",
      "first-page": "2930",
      "DOI": "10.1105/tpc.110.078154",
      "article-title": "Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants",
      "volume": "22",
      "author": "Liu",
      "year": "2010",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b31",
      "doi-asserted-by": "crossref",
      "first-page": "7758",
      "DOI": "10.1074/jbc.271.13.7758",
      "article-title": "A disulfide-bonded dimer of the Golgi beta-galactoside alpha2,6-sialyltransferase is catalytically inactive yet still retains the ability to bind galactose",
      "volume": "271",
      "author": "Ma",
      "year": "1996",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b32",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1016/0962-8924(91)90001-P",
      "article-title": "Golgi retention signals: do membranes hold the key?",
      "volume": "1",
      "author": "Machamer",
      "year": "1991",
      "journal-title": "Trends Cell Biol"
    },
    {
      "key": "2021041916144317900_b33",
      "doi-asserted-by": "crossref",
      "first-page": "668",
      "DOI": "10.1073/pnas.97.2.668",
      "article-title": "The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate",
      "volume": "97",
      "author": "McCormick",
      "year": "2000",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b34",
      "doi-asserted-by": "crossref",
      "first-page": "1127",
      "DOI": "10.1104/pp.121.4.1127",
      "article-title": "Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system",
      "volume": "121",
      "author": "Nebenf\u00fchr",
      "year": "1999",
      "journal-title": "Plant Physiol"
    },
    {
      "key": "2021041916144317900_b35",
      "doi-asserted-by": "crossref",
      "first-page": "562",
      "DOI": "10.1002/j.1460-2075.1994.tb06294.x",
      "article-title": "Kin recognition between medial Golgi enzymes in HeLa cells",
      "volume": "13",
      "author": "Nilsson",
      "year": "1994",
      "journal-title": "EMBO J"
    },
    {
      "key": "2021041916144317900_b36",
      "doi-asserted-by": "crossref",
      "first-page": "1975",
      "DOI": "10.1242/jcs.109.7.1975",
      "article-title": "The role of the membrane-spanning domain and stalk region of N-acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells",
      "volume": "109",
      "author": "Nilsson",
      "year": "1996",
      "journal-title": "J Cell Sci"
    },
    {
      "key": "2021041916144317900_b37",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/0014-5793(93)80906-B",
      "article-title": "Kin recognition: a model for the retention of Golgi enzymes",
      "volume": "330",
      "author": "Nilsson",
      "year": "1993",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2021041916144317900_b38",
      "doi-asserted-by": "crossref",
      "first-page": "763",
      "DOI": "10.1016/S0300-9084(01)01312-8",
      "article-title": "Trafficking and localisation of resident Golgi glycosylation enzymes",
      "volume": "83",
      "author": "Opat",
      "year": "2001",
      "journal-title": "Biochimie"
    },
    {
      "key": "2021041916144317900_b39",
      "doi-asserted-by": "crossref",
      "first-page": "1034",
      "DOI": "10.1111/j.1600-0854.2009.00930.x",
      "article-title": "Fluorescence lifetime imaging of interactions between Golgi tethering factors and small GTPases in plants",
      "volume": "10",
      "author": "Osterrieder",
      "year": "2009",
      "journal-title": "Traffic"
    },
    {
      "key": "2021041916144317900_b40",
      "doi-asserted-by": "crossref",
      "first-page": "189",
      "DOI": "10.1046/j.0960-7412.2002.01604.x",
      "article-title": "Structural requirements for Arabidopsis beta1,2-xylosyltransferase activity and targeting to the Golgi",
      "volume": "33",
      "author": "Pagny",
      "year": "2003",
      "journal-title": "Plant J"
    },
    {
      "key": "2021041916144317900_b41",
      "doi-asserted-by": "crossref",
      "first-page": "269",
      "DOI": "10.1016/S0960-9822(99)80117-1",
      "article-title": "Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy",
      "volume": "9",
      "author": "Pepperkok",
      "year": "1999",
      "journal-title": "Curr Biol"
    },
    {
      "key": "2021041916144317900_b42",
      "doi-asserted-by": "crossref",
      "first-page": "12984",
      "DOI": "10.1073/pnas.241175798",
      "article-title": "Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo",
      "volume": "98",
      "author": "Pinhal",
      "year": "2001",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2021041916144317900_b43",
      "doi-asserted-by": "crossref",
      "first-page": "28641",
      "DOI": "10.1074/jbc.M103664200",
      "article-title": "Location and mechanism of alpha 2,6-sialyltransferase dimer formation: role of cysteine residues in enzyme dimerization, localization, activity, and processing",
      "volume": "276",
      "author": "Qian",
      "year": "2001",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b44",
      "doi-asserted-by": "crossref",
      "first-page": "109",
      "DOI": "10.1007/s11103-005-4618-4",
      "article-title": "Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein",
      "volume": "58",
      "author": "Renna",
      "year": "2005",
      "journal-title": "Plant Mol Biol"
    },
    {
      "key": "2021041916144317900_b45",
      "doi-asserted-by": "crossref",
      "first-page": "144",
      "DOI": "10.1002/jcp.21744",
      "article-title": "Elevated Golgi pH impairs terminal N-glycosylation by inducing mislocalization of Golgi glycosyltransferases",
      "volume": "220",
      "author": "Rivinoja",
      "year": "2009",
      "journal-title": "J Cell Physiol"
    },
    {
      "key": "2021041916144317900_b46",
      "doi-asserted-by": "crossref",
      "first-page": "716",
      "DOI": "10.1111/j.1462-5822.2010.01472.x",
      "article-title": "ER quality control of immune receptors and regulators in plants",
      "volume": "12",
      "author": "Saijo",
      "year": "2010",
      "journal-title": "Cell Microbiol"
    },
    {
      "key": "2021041916144317900_b47",
      "doi-asserted-by": "crossref",
      "first-page": "3182",
      "DOI": "10.1105/tpc.105.036400",
      "article-title": "Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway",
      "volume": "18",
      "author": "Saint-Jore-Dupas",
      "year": "2006",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b48",
      "doi-asserted-by": "crossref",
      "first-page": "163",
      "DOI": "10.1139/o86-026",
      "article-title": "Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides",
      "volume": "64",
      "author": "Schachter",
      "year": "1986",
      "journal-title": "Biochem Cell Biol"
    },
    {
      "key": "2021041916144317900_b49",
      "doi-asserted-by": "crossref",
      "first-page": "1429",
      "DOI": "10.1111/j.1600-0854.2010.01106.x",
      "article-title": "Sequential depletion and acquisition of proteins during Golgi stack disassembly and reformation",
      "volume": "11",
      "author": "Schoberer",
      "year": "2010",
      "journal-title": "Traffic"
    },
    {
      "key": "2021041916144317900_b50",
      "doi-asserted-by": "crossref",
      "first-page": "220",
      "DOI": "10.1093/mp/ssq082",
      "article-title": "Sub-compartmental organization of Golgi-resident N-glycan processing enzymes in plants",
      "volume": "4",
      "author": "Schoberer",
      "year": "2011",
      "journal-title": "Mol Plant"
    },
    {
      "key": "2021041916144317900_b51",
      "doi-asserted-by": "crossref",
      "first-page": "101",
      "DOI": "10.1111/j.1600-0854.2008.00841.x",
      "article-title": "Arginine/lysine residues in the cytoplasmic tail promote ER export of plant glycosylation enzymes",
      "volume": "10",
      "author": "Schoberer",
      "year": "2009",
      "journal-title": "Traffic"
    },
    {
      "key": "2021041916144317900_b52",
      "doi-asserted-by": "crossref",
      "first-page": "1333",
      "DOI": "10.1105/tpc.110.074385",
      "article-title": "Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties",
      "volume": "22",
      "author": "Sparkes",
      "year": "2010",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b53",
      "doi-asserted-by": "crossref",
      "first-page": "2019",
      "DOI": "10.1038/nprot.2006.286",
      "article-title": "Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants",
      "volume": "1",
      "author": "Sparkes",
      "year": "2006",
      "journal-title": "Nat Protoc"
    },
    {
      "key": "2021041916144317900_b54",
      "doi-asserted-by": "crossref",
      "first-page": "44801",
      "DOI": "10.1074/jbc.M208023200",
      "article-title": "The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis",
      "volume": "277",
      "author": "Stolz",
      "year": "2002",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2021041916144317900_b55",
      "doi-asserted-by": "crossref",
      "first-page": "2278",
      "DOI": "10.1105/tpc.107.052985",
      "article-title": "A unique \u03b21,3-galactosyltransferase is indispensable for the biosynthesis of N-glycans containing Lewis a structures in Arabidopsis thaliana",
      "volume": "19",
      "author": "Strasser",
      "year": "2007",
      "journal-title": "Plant Cell"
    },
    {
      "key": "2021041916144317900_b56",
      "doi-asserted-by": "crossref",
      "first-page": "105",
      "DOI": "10.1016/S0014-5793(00)01443-5",
      "article-title": "Molecular cloning and functional expression of \u03b21, 2-xylosyltransferase cDNA from Arabidopsis thaliana",
      "volume": "472",
      "author": "Strasser",
      "year": "2000",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2021041916144317900_b57",
      "doi-asserted-by": "crossref",
      "first-page": "789",
      "DOI": "10.1111/j.1365-313X.2005.02648.x",
      "article-title": "Molecular cloning and characterization of Arabidopsis thaliana Golgi \u03b1-mannosidase II, a key enzyme in the formation of complex N-glycans in plants",
      "volume": "45",
      "author": "Strasser",
      "year": "2006",
      "journal-title": "Plant J"
    },
    {
      "key": "2021041916144317900_b58",
      "doi-asserted-by": "crossref",
      "first-page": "22",
      "DOI": "10.1186/1471-2121-6-22",
      "article-title": "The use of time-resolved fluorescence imaging in the study of protein kinase C localisation in cells",
      "volume": "6",
      "author": "Stubbs",
      "year": "2005",
      "journal-title": "BMC Cell Biol"
    },
    {
      "key": "2021041916144317900_b59",
      "doi-asserted-by": "crossref",
      "first-page": "1324",
      "DOI": "10.1038/nprot.2011.364",
      "article-title": "Investigating protein-protein interactions in living cells using fluorescence lifetime imaging microscopy",
      "volume": "6",
      "author": "Sun",
      "year": "2011",
      "journal-title": "Nat Protoc"
    },
    {
      "key": "2021041916144317900_b60",
      "doi-asserted-by": "crossref",
      "first-page": "1274",
      "DOI": "10.1016/j.bpj.2010.06.004",
      "article-title": "Three-color spectral FRET microscopy localizes three interacting proteins in living cells",
      "volume": "99",
      "author": "Sun",
      "year": "2010",
      "journal-title": "Biophys J"
    },
    {
      "key": "2021041916144317900_b61",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1007/s00232-004-0656-5",
      "article-title": "Organization of Golgi glycosyltransferases in membranes: complexity via complexes",
      "volume": "198",
      "author": "Young",
      "year": "2004",
      "journal-title": "J Membr Biol"
    },
    {
      "key": "2021041916144317900_b62",
      "doi-asserted-by": "crossref",
      "first-page": "78",
      "DOI": "10.1104/pp.110.159749",
      "article-title": "A glucurono(arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively",
      "volume": "154",
      "author": "Zeng",
      "year": "2010",
      "journal-title": "Plant Physiol"
    }
  ],
  "container-title": "Plant Physiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://academic.oup.com/plphys/article-pdf/161/4/1737/37167918/plphys_v161_4_1737.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "http://academic.oup.com/plphys/article-pdf/161/4/1737/37167918/plphys_v161_4_1737.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        2,
        8
      ]
    ],
    "date-time": "2022-02-08T12:31:55Z",
    "timestamp": 1644323515000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://academic.oup.com/plphys/article/161/4/1737/6110966"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2013,
        2,
        11
      ]
    ]
  },
  "references-count": 62,
  "journal-issue": {
    "issue": "4",
    "published-online": {
      "date-parts": [
        [
          2013,
          2,
          11
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2013,
          4,
          2
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1104/pp.112.210757",
  "relation": {},
  "ISSN": [
    "1532-2548"
  ],
  "subject": [],
  "published-other": {
    "date-parts": [
      [
        2013,
        4,
        1
      ]
    ]
  },
  "published": {
    "date-parts": [
      [
        2013,
        2,
        11
      ]
    ]
  }
}