CHLOROPLAST UNUSUAL POSITIONING1 Is Essential for Proper Chloroplast Positioning
The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photoreloca...
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Published in | The Plant cell Vol. 15; no. 12; pp. 2805 - 2815 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Society of Plant Biologists
01.12.2003
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Subjects | |
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Abstract | The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photorelocation movement, we isolated six mutant clones in which chloroplasts gathered at the bottom of the cells and did not distribute throughout cells. These mutants, termed chloroplast unusual positioning (chup), were shown to belong to a single genetic locus by complementation tests. Observation of the positioning of other organelles, such as mitochondria, peroxisomes, and nuclei, revealed that chloroplast positioning and movement are impaired specifically in this mutant, although peroxisomes are distributed along with chloroplasts. The CHUP1 gene encodes a novel protein containing multiple domains, including a coiled-coil domain, an actin binding domain, a Pro-rich region, and two Leu zipper domains. The N-terminal hydrophobic segment of CHUP1 was expressed transiently in leaf cells of Arabidopsis as a fusion protein with the green fluorescent protein. The fusion protein was targeted to envelope membranes of chloroplasts in mesophyll cells, suggesting that CHUP1 may localize in chloroplasts. A glutathione S-transferase fusion protein containing the actin binding domain of CHUP1 was found to bind F-actin in vitro. CHUP1 is a unique gene identified that encodes a protein required for organellar positioning and movement in plant cells. |
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AbstractList | The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photorelocation movement, we isolated six mutant clones in which chloroplasts gathered at the bottom of the cells and did not distribute throughout cells. These mutants, termed chloroplast unusual positioning (chup), were shown to belong to a single genetic locus by complementation tests. Observation of the positioning of other organelles, such as mitochondria, peroxisomes, and nuclei, revealed that chloroplast positioning and movement are impaired specifically in this mutant, although peroxisomes are distributed along with chloroplasts. The CHUP1 gene encodes a novel protein containing multiple domains, including a coiled-coil domain, an actin binding domain, a Pro-rich region, and two Leu zipper domains. The N-terminal hydrophobic segment of CHUP1 was expressed transiently in leaf cells of Arabidopsis as a fusion protein with the green fluorescent protein. The fusion protein was targeted to envelope membranes of chloroplasts in mesophyll cells, suggesting that CHUP1 may localize in chloroplasts. A glutathione S-transferase fusion protein containing the actin binding domain of CHUP1 was found to bind F-actin in vitro. CHUP1 is a unique gene identified that encodes a protein required for organellar positioning and movement in plant cells. The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photorelocation movement, we isolated six mutant clones in which chloroplasts gathered at the bottom of the cells and did not distribute throughout cells. These mutants, termed chloroplast unusual positioning (chup), were shown to belong to a single genetic locus by complementation tests. Observation of the positioning of other organelles, such as mitochondria, peroxisomes, and nuclei, revealed that chloroplast positioning and movement are impaired specifically in this mutant, although peroxisomes are distributed along with chloroplasts. The CHUP1 gene encodes a novel protein containing multiple domains, including a coiled-coil domain, an actin binding domain, a Pro-rich region, and two Leu zipper domains. The N-terminal hydrophobic segment of CHUP1 was expressed transiently in leaf cells of Arabidopsis as a fusion protein with the green fluorescent protein. The fusion protein was targeted to envelope membranes of chloroplasts in mesophyll cells, suggesting that CHUP1 may localize in chloroplasts. A glutathione S-transferase fusion protein containing the actin binding domain of CHUP1 was found to bind F-actin in vitro. CHUP1 is a unique gene identified that encodes a protein required for organellar positioning and movement in plant cells.The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photorelocation movement, we isolated six mutant clones in which chloroplasts gathered at the bottom of the cells and did not distribute throughout cells. These mutants, termed chloroplast unusual positioning (chup), were shown to belong to a single genetic locus by complementation tests. Observation of the positioning of other organelles, such as mitochondria, peroxisomes, and nuclei, revealed that chloroplast positioning and movement are impaired specifically in this mutant, although peroxisomes are distributed along with chloroplasts. The CHUP1 gene encodes a novel protein containing multiple domains, including a coiled-coil domain, an actin binding domain, a Pro-rich region, and two Leu zipper domains. The N-terminal hydrophobic segment of CHUP1 was expressed transiently in leaf cells of Arabidopsis as a fusion protein with the green fluorescent protein. The fusion protein was targeted to envelope membranes of chloroplasts in mesophyll cells, suggesting that CHUP1 may localize in chloroplasts. A glutathione S-transferase fusion protein containing the actin binding domain of CHUP1 was found to bind F-actin in vitro. CHUP1 is a unique gene identified that encodes a protein required for organellar positioning and movement in plant cells. The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize photosynthetic activity in response to ambient light conditions. Through screening of mutants of Arabidopsis defective in chloroplast photorelocation movement, we isolated six mutant clones in which chloroplasts gathered at the bottom of the cells and did not distribute throughout cells. These mutants, termed chloroplast unusual positioning ( chup ), were shown to belong to a single genetic locus by complementation tests. Observation of the positioning of other organelles, such as mitochondria, peroxisomes, and nuclei, revealed that chloroplast positioning and movement are impaired specifically in this mutant, although peroxisomes are distributed along with chloroplasts. The CHUP1 gene encodes a novel protein containing multiple domains, including a coiled-coil domain, an actin binding domain, a Pro-rich region, and two Leu zipper domains. The N-terminal hydrophobic segment of CHUP1 was expressed transiently in leaf cells of Arabidopsis as a fusion protein with the green fluorescent protein. The fusion protein was targeted to envelope membranes of chloroplasts in mesophyll cells, suggesting that CHUP1 may localize in chloroplasts. A glutathione S -transferase fusion protein containing the actin binding domain of CHUP1 was found to bind F-actin in vitro. CHUP1 is a unique gene identified that encodes a protein required for organellar positioning and movement in plant cells. |
Author | Kasahara, Masahiro Kiyosue, Tomohiro Kagawa, Takatoshi Oikawa, Kazusato Suetsugu, Noriyuki Takahashi, Fumio Niwa, Yasuo Wada, Masamitsu Kanegae, Takeshi Kadota, Akeo |
AuthorAffiliation | c Solution Oriented Research for Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan b National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan a Department of Biology, Faculty of Science, Graduate School of Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan d Laboratory of Plant Cell Technology, Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, Yada, Shizuoka 422-8526, Japan |
AuthorAffiliation_xml | – name: b National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan – name: c Solution Oriented Research for Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan – name: d Laboratory of Plant Cell Technology, Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, Yada, Shizuoka 422-8526, Japan – name: a Department of Biology, Faculty of Science, Graduate School of Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan |
Author_xml | – sequence: 1 givenname: Kazusato surname: Oikawa fullname: Oikawa, Kazusato – sequence: 2 givenname: Masahiro surname: Kasahara fullname: Kasahara, Masahiro – sequence: 3 givenname: Tomohiro surname: Kiyosue fullname: Kiyosue, Tomohiro – sequence: 4 givenname: Takatoshi surname: Kagawa fullname: Kagawa, Takatoshi – sequence: 5 givenname: Noriyuki surname: Suetsugu fullname: Suetsugu, Noriyuki – sequence: 6 givenname: Fumio surname: Takahashi fullname: Takahashi, Fumio – sequence: 7 givenname: Takeshi surname: Kanegae fullname: Kanegae, Takeshi – sequence: 8 givenname: Yasuo surname: Niwa fullname: Niwa, Yasuo – sequence: 9 givenname: Akeo surname: Kadota fullname: Kadota, Akeo – sequence: 10 givenname: Masamitsu surname: Wada fullname: Wada, Masamitsu |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/14615600$$D View this record in MEDLINE/PubMed |
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Copyright | Copyright 2003 American Society of Plant Biologists Copyright American Society of Plant Physiologists Dec 2003 Copyright © 2003, American Society of Plant Biologists 2003 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 ObjectType-Feature-2 Current address: Gene Research Center, Kagawa University, Miki-cho Kita-gun, Kagawa 761-0795, Japan. To whom correspondence should be addressed. E-mail wada-masamitsu@c.metro-u.ac.jp; fax 81-426-77-2559 Current address: Gene Research Center, Tokyo University of Agriculture and Technology, Saiwai-cho, Fuchu, Tokyo 183-8509, Japan. Current address: Institute of Applied Biochemistry, University of Tsukuba, Ten-noudai, Tsukuba 305-8572, Japan. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016428. |
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PublicationTitle | The Plant cell |
PublicationTitleAlternate | Plant Cell |
PublicationYear | 2003 |
Publisher | American Society of Plant Biologists |
Publisher_xml | – name: American Society of Plant Biologists |
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References_xml | – reference: 11251116 - Science. 2001 Mar 16;291(5511):2138-41 – reference: 11146297 - Trends Cell Biol. 2001 Jan;11(1):38-46 – reference: 12490952 - Nature. 2002 Dec 19-26;420(6917):829-32 – reference: 11148129 - J Cell Sci. 2001 Jan;114(Pt 2):269-79 – reference: 11540330 - Planta. 1997 Sep;203(Suppl 1):S63-8 – reference: 10406127 - Plant J. 1999 May;18(4):455-63 – reference: 10506746 - Cell Motil Cytoskeleton. 1999 Oct;44(2):110-8 – reference: 8805250 - Curr Biol. 1996 Mar 1;6(3):325-30 – reference: 11886885 - J Exp Bot. 2002 Apr;53(369):659-67 – reference: 9881160 - Plant J. 1998 Nov;16(3):393-401 – reference: 9051728 - Protein Eng. 1997 Jan;10(1):1-6 – reference: 11309623 - Nature. 2001 Apr 19;410(6831):952-4 – reference: 11595795 - Plant Cell. 2001 Oct;13(10):2175-90 – reference: 7108955 - J Mol Biol. 1982 May 5;157(1):105-32 – reference: 10213778 - Plant Cell. 1999 Apr;11(4):557-70 – reference: 11917088 - Plant Cell Physiol. 2002 Mar;43(3):331-41 – reference: 7667278 - Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8259-63 – reference: 11371609 - Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6969-74 – reference: 9750355 - Plant J. 1998 Aug;15(3):441-7 – reference: 10930466 - Mol Biol Cell. 2000 Aug;11(8):2733-41 – reference: 10482658 - Plant Physiol. 1999 Sep;121(1):37-44 – reference: 8953775 - Plant Cell. 1996 Nov;8(11):2117-26 – reference: 11891258 - Plant Physiol. 2002 Mar;128(3):1031-45 – reference: 11978863 - Plant Cell Physiol. 2002 Apr;43(4):367-71 – reference: 11978866 - Plant Cell Physiol. 2002 Apr;43(4):384-92 |
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Snippet | The intracellular distribution of organelles is a crucial aspect of effective cell function. Chloroplasts change their intracellular positions to optimize... |
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SubjectTerms | actin Actins Amino Acid Sequence amino acid sequences Arabidopsis Arabidopsis - cytology Arabidopsis - genetics Arabidopsis - physiology Arabidopsis Proteins Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana binding capacity binding proteins Cell Nucleus Cell Nucleus - physiology Cell Polarity Cell Polarity - physiology chemistry Chloroplast Proteins Chloroplasts Chloroplasts - physiology CHUP1 gene Cloning, Molecular complementary DNA cytology Cytoskeleton Cytoskeleton - genetics Cytoskeleton - physiology DNA, Complementary DNA, Complementary - chemistry DNA, Complementary - genetics gene expression Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Genetic Complementation Test genetics Green Fluorescent Proteins Hydrophobic and Hydrophilic Interactions Leaves Leucine Zippers Leucine Zippers - genetics light intensity Luminescent Proteins Luminescent Proteins - genetics Luminescent Proteins - metabolism Mesophyll cells metabolism Microfilament Proteins Microfilament Proteins - chemistry Microfilament Proteins - genetics Microfilament Proteins - metabolism Microfilaments Microscopy, Confocal Mitochondria Mitochondria - physiology Molecular Sequence Data Mutants Mutation nucleotide sequences Organelles Peroxisomes Peroxisomes - physiology physiology Plant cells Plant Leaves Plant Leaves - genetics Plant Leaves - physiology plant proteins Plants Protein Structure, Secondary Proteins Recombinant Fusion Proteins Recombinant Fusion Proteins - genetics Recombinant Fusion Proteins - metabolism Sequence Analysis, DNA Sequence Homology, Amino Acid spatial distribution structural genes |
Title | CHLOROPLAST UNUSUAL POSITIONING1 Is Essential for Proper Chloroplast Positioning |
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