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 inThe Plant cell Vol. 15; no. 12; pp. 2805 - 2815
Main Authors Oikawa, Kazusato, Kasahara, Masahiro, Kiyosue, Tomohiro, Kagawa, Takatoshi, Suetsugu, Noriyuki, Takahashi, Fumio, Kanegae, Takeshi, Niwa, Yasuo, Kadota, Akeo, Wada, Masamitsu
Format Journal Article
LanguageEnglish
Published United States American Society of Plant Biologists 01.12.2003
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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.
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
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/14615600$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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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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.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/282804
PMID 14615600
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PublicationTitle The Plant cell
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– 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
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– 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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