DOI: 10.1046/j.1365-313x.1993.t01-21-00999.x. The 20 kDa apoprotein of the CP24 complex of photosystem II: An alternative model to study import and intra‐organellar routing of nuclear‐encoded thylakoid proteins

The 20 kDa apoprotein of the CP24 complex of photosystem II: An alternative model to study import and intra‐organellar routing of nuclear‐encoded thylakoid proteins

10.1046/j.1365-313x.1993.t01-21-00999.x

Crossref journal-article

Wiley

The Plant Journal (311)

Abstract

SummaryThe 20 kDa polypeptide, the apoprotein of the chlorophyll a/b antenna complex CP24 associated with photosystem II, is a remote relative of light‐harvesting complex (LHC) apoproteins and thus a member of the extended cab gene family. LHC apoproteins are poly‐topic integral components of the thylakoid membrane with probably three transmembrane segments which originate in nuclear genes and are made in the cytosol as precursors. They possess exclusively stroma‐targeting transit peptides for import into the organelle and integrate into the thylakoid membrane via uncleaved hydrophobic domains of the mature protein. The CP24 apoprotein displays intriguing structural differences to LHC apoproteins with a potential impact on the routing and targeting processes during biogenesis. In particular, it lacks a pronounced second hydrophobic segment in the mature polypeptide chain found in LHCPs, and carries a transit peptide that is reminiscent of thylakoid‐targeting transit peptides. We have used in organello assays with isolated intact chloroplasts and the authentic precursor of the 20 kDa apoprotein from spinach, or appropriate chimaeric polypeptides consisting of a transit peptide and the mature part of various nuclear‐encoded thylakoid proteins of known location and targeting epitopes, in order to resolve the characteristics of its targeting properties, as well as to determine the contribution of the individual parts of the precursor molecule to its import and subsequent intra‐organellar routing. Our experiments demonstrate that the transit peptide of the CP24 apoprotein is required only for the import of the protein into the organelle. All subsequent steps, such as the integration of the protein into the thylakoid membrane, binding of chlorophyll, assembly into the CP24 complex and migration to the grana lamellae, still take place if the authentic transit peptide is replaced by a targeting signal of a nuclear‐encoded stromal protein.

Bibliography

Cai, D., Herrmann, R. G., & KlÃ¶sgen, R. B. (1993). The 20 kDa apoprotein of the CP24 complex of photosystem II: An alternative model to study import and intraâorganellar routing of nuclearâencoded thylakoid proteins. The Plant Journal, 3(3), 383â392. Portico.

Authors 3

Daguang Cai (first)
Reinhold G. Herrmann (additional)
Ralf Bernd Klösgen (additional)

References 47 Referenced 36

{'key': 'e_1_2_1_2_1', 'first-page': '33', 'volume-title': 'Plant Membranes ‐ Structure, Assembly and Function', 'author': 'Andersson B.', 'year': '1988'} / Plant Membranes ‐ Structure, Assembly and Function by Andersson B. (1988)
{'key': 'e_1_2_1_3_1', 'first-page': '119', 'article-title': 'Towards epitope models for chloroplast transit sequences', 'volume': '2', 'author': 'Bartling D.', 'year': '1990', 'journal-title': 'Bot. Mag. Tokyo Special Issue'} / Bot. Mag. Tokyo Special Issue / Towards epitope models for chloroplast transit sequences by Bartling D. (1990)
10.1111/j.1751-1097.1990.tb08457.x
10.1002/j.1460-2075.1991.tb07825.x
10.1016/0005-2728(87)90162-9
10.1073/pnas.85.11.3797
10.1083/jcb.102.3.982
10.1007/BF00039485
10.1105/tpc.2.2.173
Clausmeyer S. Klösgen R.B.andHerrmann R.G.(1993)Protein import into chloroplasts: the hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. Manuscript submitted. (10.1016/S0021-9258(19)85183-9)
10.1016/S0021-9258(18)45935-2 / J. Biol. Chem. / Protein‐specific energy requirements for protein transport across or into thylakoid membranes by Cline K. (1992)
10.1002/j.1460-2075.1992.tb05030.x
10.1104/pp.80.2.429
10.1016/0014-5793(90)80614-O
10.1016/0968-0004(91)90072-4
10.1007/BF00027318
10.1105/tpc.2.5.479
10.1002/j.1460-2075.1989.tb08478.x
10.1111/j.1432-1033.1989.tb14679.x
10.1007/978-1-4615-3304-7_40
10.1016/0014-5793(87)80696-8
10.1007/BF02427758
10.1007/BF00019226
10.1002/j.1460-2075.1989.tb08477.x
10.1105/tpc.1.1.159
10.1038/307478a0
10.1038/350130a0
10.1016/0022-2836(82)90515-0
10.1111/j.1462-5822.2007.00901.x
10.1016/S0021-9258(18)68137-2 / J. Biol. Chem. / The chlorophyll a/b‐binding protein inserts into the thylakoids independent of its cognate transit peptide by Lamppa G.K. (1988)
10.1002/j.1460-2075.1985.tb03832.x
10.1016/S0021-9258(18)98879-4
10.1016/S0021-9258(17)44588-1 / J. Biol. Chem. / The amino acid sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts by Mullet J.E. (1983)
{'key': 'e_1_2_1_35_1', 'first-page': '701', 'volume-title': 'Progress in Photosynthesis Research', 'author': 'Murata N.', 'year': '1987'} / Progress in Photosynthesis Research by Murata N. (1987)
{'key': 'e_1_2_1_36_1', 'first-page': '194', 'volume-title': 'Methods in Plant Biochemistry, Volume 5, Amino Acids, Proteins, and Nucleic Acids', 'author': 'Peter G.F.', 'year': '1991'} / Methods in Plant Biochemistry, Volume 5, Amino Acids, Proteins, and Nucleic Acids by Peter G.F. (1991)
10.1007/BF00035679 / Photosynth. Res. / An amino‐proximal hydrophobic domain in the major light‐harvesting chlorophyll a/b‐protein is essential for membrane integration and protein stability by Reinero A. (1991)
10.1111/j.1432-1033.1984.tb08291.x
{'key': 'e_1_2_1_39_1', 'volume-title': 'Molecular Cloning. A Laboratory Manual', 'author': 'Sambrook J.', 'year': '1989'} / Molecular Cloning. A Laboratory Manual by Sambrook J. (1989)
10.1073/pnas.74.12.5463
10.1016/0003-2697(87)90587-2
10.1007/BF00017734
10.1007/BF00014912
10.1007/978-1-4684-8571-4_17
{'key': 'e_1_2_1_45_1', 'first-page': '253', 'volume-title': 'Current Research in Photosynthesis', 'author': 'Spangfort M.', 'year': '1990'} / Current Research in Photosynthesis by Spangfort M. (1990)
10.1016/S0021-9258(18)83490-1
{'key': 'e_1_2_1_47_1', 'first-page': '249', 'volume-title': 'Regulation of Chloroplast Differentiation', 'author': 'Thornber J.P.', 'year': '1986'} / Regulation of Chloroplast Differentiation by Thornber J.P. (1986)
10.1016/S0021-9258(18)68138-4 / J. Biol. Chem. / What is the role of the transit peptide in thylakoid integration of the light‐harvesting chlorophyll a/b protein by Viitanen P.V. (1988)

Dates

Type	When
Created	22 years, 5 months ago (March 12, 2003, 4:40 p.m.)
Deposited	1 year, 10 months ago (Oct. 24, 2023, 3:46 p.m.)
Indexed	1 month ago (Aug. 5, 2025, 8:10 a.m.)
Issued	32 years, 6 months ago (March 1, 1993)
Published	32 years, 6 months ago (March 1, 1993)
Published Online	16 years, 11 months ago (Sept. 24, 2008)
Published Print	32 years, 6 months ago (March 1, 1993)

Funders 0

None

BibTeX

@article{Cai_1993, title={The 20 kDa apoprotein of the CP24 complex of photosystem II: An alternative model to study import and intra‐organellar routing of nuclear‐encoded thylakoid proteins}, volume={3}, ISSN={1365-313X}, url={http://dx.doi.org/10.1046/j.1365-313x.1993.t01-21-00999.x}, DOI={10.1046/j.1365-313x.1993.t01-21-00999.x}, number={3}, journal={The Plant Journal}, publisher={Wiley}, author={Cai, Daguang and Herrmann, Reinhold G. and Klösgen, Ralf Bernd}, year={1993}, month=mar, pages={383–392} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        5
      ]
    ],
    "date-time": "2025-08-05T12:10:26Z",
    "timestamp": 1754395826285
  },
  "reference-count": 47,
  "publisher": "Wiley",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2008,
            9,
            24
          ]
        ],
        "date-time": "2008-09-24T00:00:00Z",
        "timestamp": 1222214400000
      },
      "content-version": "vor",
      "delay-in-days": 5686,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [
      "onlinelibrary.wiley.com"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        3
      ]
    ]
  },
  "abstract": "<jats:title>Summary</jats:title><jats:p>The 20 kDa polypeptide, the apoprotein of the chlorophyll <jats:italic>a/b</jats:italic> antenna complex CP24 associated with photosystem II, is a remote relative of light\u2010harvesting complex (LHC) apoproteins and thus a member of the extended cab gene family. LHC apoproteins are poly\u2010topic integral components of the thylakoid membrane with probably three transmembrane segments which originate in nuclear genes and are made in the cytosol as precursors. They possess exclusively stroma\u2010targeting transit peptides for import into the organelle and integrate into the thylakoid membrane via uncleaved hydrophobic domains of the mature protein. The CP24 apoprotein displays intriguing structural differences to LHC apoproteins with a potential impact on the routing and targeting processes during biogenesis. In particular, it lacks a pronounced second hydrophobic segment in the mature polypeptide chain found in LHCPs, and carries a transit peptide that is reminiscent of thylakoid\u2010targeting transit peptides. We have used in <jats:italic>organello</jats:italic> assays with isolated intact chloroplasts and the authentic precursor of the 20 kDa apoprotein from spinach, or appropriate chimaeric polypeptides consisting of a transit peptide and the mature part of various nuclear\u2010encoded thylakoid proteins of known location and targeting epitopes, in order to resolve the characteristics of its targeting properties, as well as to determine the contribution of the individual parts of the precursor molecule to its import and subsequent intra\u2010organellar routing. Our experiments demonstrate that the transit peptide of the CP24 apoprotein is required only for the import of the protein into the organelle. All subsequent steps, such as the integration of the protein into the thylakoid membrane, binding of chlorophyll, assembly into the CP24 complex and migration to the grana lamellae, still take place if the authentic transit peptide is replaced by a targeting signal of a nuclear\u2010encoded stromal protein.</jats:p>",
  "DOI": "10.1046/j.1365-313x.1993.t01-21-00999.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2003,
        3,
        12
      ]
    ],
    "date-time": "2003-03-12T21:40:26Z",
    "timestamp": 1047505226000
  },
  "page": "383-392",
  "update-policy": "http://dx.doi.org/10.1002/crossmark_policy",
  "source": "Crossref",
  "is-referenced-by-count": 36,
  "title": "The 20 kDa apoprotein of the CP24 complex of photosystem II: An alternative model to study import and intra\u2010organellar routing of nuclear\u2010encoded thylakoid proteins",
  "prefix": "10.1111",
  "volume": "3",
  "author": [
    {
      "given": "Daguang",
      "family": "Cai",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Reinhold G.",
      "family": "Herrmann",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Ralf Bernd",
      "family": "Kl\u00f6sgen",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2008,
        9,
        24
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_1",
      "first-page": "33",
      "volume-title": "Plant Membranes \u2010 Structure, Assembly and Function",
      "author": "Andersson B.",
      "year": "1988"
    },
    {
      "key": "e_1_2_1_3_1",
      "first-page": "119",
      "article-title": "Towards epitope models for chloroplast transit sequences",
      "volume": "2",
      "author": "Bartling D.",
      "year": "1990",
      "journal-title": "Bot. Mag. Tokyo Special Issue"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1751-1097.1990.tb08457.x"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1991.tb07825.x"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0005-2728(87)90162-9"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.85.11.3797"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.102.3.982"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00039485"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1105/tpc.2.2.173"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Clausmeyer S. Kl\u00f6sgen R.B.andHerrmann R.G.(1993)Protein import into chloroplasts: the hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. Manuscript submitted.",
      "DOI": "10.1016/S0021-9258(19)85183-9"
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "crossref",
      "first-page": "2688",
      "DOI": "10.1016/S0021-9258(18)45935-2",
      "article-title": "Protein\u2010specific energy requirements for protein transport across or into thylakoid membranes",
      "volume": "267",
      "author": "Cline K.",
      "year": "1992",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1992.tb05030.x"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1104/pp.80.2.429"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(90)80614-O"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0968-0004(91)90072-4"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00027318"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1105/tpc.2.5.479"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1989.tb08478.x"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1989.tb14679.x"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-1-4615-3304-7_40"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0014-5793(87)80696-8"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF02427758"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00019226"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1989.tb08477.x"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1105/tpc.1.1.159"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/307478a0"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/350130a0"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(82)90515-0"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1462-5822.2007.00901.x"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "14996",
      "DOI": "10.1016/S0021-9258(18)68137-2",
      "article-title": "The chlorophyll a/b\u2010binding protein inserts into the thylakoids independent of its cognate transit peptide",
      "volume": "263",
      "author": "Lamppa G.K.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1985.tb03832.x"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)98879-4"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "9941",
      "DOI": "10.1016/S0021-9258(17)44588-1",
      "article-title": "The amino acid sequence of the polypeptide segment which regulates membrane adhesion (grana stacking) in chloroplasts",
      "volume": "258",
      "author": "Mullet J.E.",
      "year": "1983",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "e_1_2_1_35_1",
      "first-page": "701",
      "volume-title": "Progress in Photosynthesis Research",
      "author": "Murata N.",
      "year": "1987"
    },
    {
      "key": "e_1_2_1_36_1",
      "first-page": "194",
      "volume-title": "Methods in Plant Biochemistry, Volume 5, Amino Acids, Proteins, and Nucleic Acids",
      "author": "Peter G.F.",
      "year": "1991"
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1007/BF00035679",
      "article-title": "An amino\u2010proximal hydrophobic domain in the major light\u2010harvesting chlorophyll a/b\u2010protein is essential for membrane integration and protein stability",
      "volume": "30",
      "author": "Reinero A.",
      "year": "1991",
      "journal-title": "Photosynth. Res."
    },
    {
      "key": "e_1_2_1_38_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1432-1033.1984.tb08291.x"
    },
    {
      "key": "e_1_2_1_39_1",
      "volume-title": "Molecular Cloning. A Laboratory Manual",
      "author": "Sambrook J.",
      "year": "1989"
    },
    {
      "key": "e_1_2_1_40_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.74.12.5463"
    },
    {
      "key": "e_1_2_1_41_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0003-2697(87)90587-2"
    },
    {
      "key": "e_1_2_1_42_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00017734"
    },
    {
      "key": "e_1_2_1_43_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00014912"
    },
    {
      "key": "e_1_2_1_44_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/978-1-4684-8571-4_17"
    },
    {
      "key": "e_1_2_1_45_1",
      "first-page": "253",
      "volume-title": "Current Research in Photosynthesis",
      "author": "Spangfort M.",
      "year": "1990"
    },
    {
      "key": "e_1_2_1_46_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)83490-1"
    },
    {
      "key": "e_1_2_1_47_1",
      "first-page": "249",
      "volume-title": "Regulation of Chloroplast Differentiation",
      "author": "Thornber J.P.",
      "year": "1986"
    },
    {
      "key": "e_1_2_1_48_1",
      "doi-asserted-by": "crossref",
      "first-page": "15000",
      "DOI": "10.1016/S0021-9258(18)68138-4",
      "article-title": "What is the role of the transit peptide in thylakoid integration of the light\u2010harvesting chlorophyll a/b protein",
      "volume": "263",
      "author": "Viitanen P.V.",
      "year": "1988",
      "journal-title": "J. Biol. Chem."
    }
  ],
  "container-title": "The Plant Journal",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1046%2Fj.1365-313X.1993.t01-21-00999.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313X.1993.t01-21-00999.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        24
      ]
    ],
    "date-time": "2023-10-24T19:46:32Z",
    "timestamp": 1698176792000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1046/j.1365-313X.1993.t01-21-00999.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        3
      ]
    ]
  },
  "references-count": 47,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1993,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1046/j.1365-313X.1993.t01-21-00999.x"
  ],
  "URL": "http://dx.doi.org/10.1046/j.1365-313X.1993.t01-21-00999.x",
  "relation": {},
  "ISSN": [
    "0960-7412",
    "1365-313X"
  ],
  "subject": [],
  "container-title-short": "The Plant Journal",
  "published": {
    "date-parts": [
      [
        1993,
        3
      ]
    ]
  },
  "assertion": [
    {
      "value": "2008-09-24",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}