Light and low-CO2-dependent LCIBLCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii

Takashi Yamano, Tomoki Tsujikawa, Kyoko Hatano, Shinichiro Ozawa, Yuichiro Takahashi, Hideya Fukuzawa

Research output: Contribution to journalArticle

68 Citations (Scopus)

Abstract

The carbon-concentrating mechanism (CCM) is essential to support photosynthesis under CO2-limiting conditions in aquatic photosynthetic organisms, including the green alga Chlamydomonas reinhardtii. The CCM is assumed to be comprised of inorganic carbon transport systems that, in conjunction with carbonic anhydrases, maintain high levels of CO2 around ribulose-1, 5-bisphosphate carboxylase/oxygenase in a specific compartment called the pyrenoid. A set of transcripts up-regulated during the induction of the CCM was identified previously and designated as low-CO 2 (LC)-inducible genes. Although the functional importance of one of these LC-inducible genes, LciB, has been shown recently, the biochemical properties and detailed subcellular localization of its product LCIB remain to be elucidated. Here, using yeast two-hybrid, immunoprecipitation and mass spectrometry analyses we provide evidence to demonstrate that LCIB interacts with the LCIB homologous protein LCIC in yeast and in vivo. We also show that LCIB and LCIC are co-localized in the vicinity of the pyrenoid under LC conditions in the light, forming a hexamer complex of approximately 350 kDa, as estimated by gel filtration chromatography. LCIB localization around the pyrenoid was dependent on light illumination and LC conditions during active operation of the CCM. In contrast, in the dark or under high-CO2 conditions when the CCM was inactive, LCIB immediately diffused away from the pyrenoid. Based on these observations, we discuss possible functions of the LCIBLCIC complex in the CCM.

Original languageEnglish
Pages (from-to)1453-1468
Number of pages16
JournalPlant and Cell Physiology
Volume51
Issue number9
DOIs
Publication statusPublished - Sep 2010

Fingerprint

Chlamydomonas reinhardtii
concentrating
Chloroplasts
Carbon
chloroplasts
Light
Carbon Monoxide
carbon
Yeasts
yeasts
Aquatic Organisms
Oxygenases
Chlorophyta
Carbonic Anhydrases
carbonate dehydratase
Photosynthesis
ribulose 1,5-diphosphate
autotrophs
oxygenases
Lighting

Keywords

  • Carbon-concentrating mechanism
  • Chlamydomonas reinhardtii
  • Chloroplast
  • LciB
  • Photosynthesis
  • Pyrenoid

ASJC Scopus subject areas

  • Plant Science
  • Physiology
  • Cell Biology
  • Medicine(all)

Cite this

Light and low-CO2-dependent LCIBLCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii. / Yamano, Takashi; Tsujikawa, Tomoki; Hatano, Kyoko; Ozawa, Shinichiro; Takahashi, Yuichiro; Fukuzawa, Hideya.

In: Plant and Cell Physiology, Vol. 51, No. 9, 09.2010, p. 1453-1468.

Research output: Contribution to journalArticle

@article{78b9446f3a584920be601ef1ee738a18,
title = "Light and low-CO2-dependent LCIBLCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii",
abstract = "The carbon-concentrating mechanism (CCM) is essential to support photosynthesis under CO2-limiting conditions in aquatic photosynthetic organisms, including the green alga Chlamydomonas reinhardtii. The CCM is assumed to be comprised of inorganic carbon transport systems that, in conjunction with carbonic anhydrases, maintain high levels of CO2 around ribulose-1, 5-bisphosphate carboxylase/oxygenase in a specific compartment called the pyrenoid. A set of transcripts up-regulated during the induction of the CCM was identified previously and designated as low-CO 2 (LC)-inducible genes. Although the functional importance of one of these LC-inducible genes, LciB, has been shown recently, the biochemical properties and detailed subcellular localization of its product LCIB remain to be elucidated. Here, using yeast two-hybrid, immunoprecipitation and mass spectrometry analyses we provide evidence to demonstrate that LCIB interacts with the LCIB homologous protein LCIC in yeast and in vivo. We also show that LCIB and LCIC are co-localized in the vicinity of the pyrenoid under LC conditions in the light, forming a hexamer complex of approximately 350 kDa, as estimated by gel filtration chromatography. LCIB localization around the pyrenoid was dependent on light illumination and LC conditions during active operation of the CCM. In contrast, in the dark or under high-CO2 conditions when the CCM was inactive, LCIB immediately diffused away from the pyrenoid. Based on these observations, we discuss possible functions of the LCIBLCIC complex in the CCM.",
keywords = "Carbon-concentrating mechanism, Chlamydomonas reinhardtii, Chloroplast, LciB, Photosynthesis, Pyrenoid",
author = "Takashi Yamano and Tomoki Tsujikawa and Kyoko Hatano and Shinichiro Ozawa and Yuichiro Takahashi and Hideya Fukuzawa",
year = "2010",
month = "9",
doi = "10.1093/pcp/pcq105",
language = "English",
volume = "51",
pages = "1453--1468",
journal = "Plant and Cell Physiology",
issn = "0032-0781",
publisher = "Oxford University Press",
number = "9",

}

TY - JOUR

T1 - Light and low-CO2-dependent LCIBLCIC complex localization in the chloroplast supports the carbon-concentrating mechanism in Chlamydomonas reinhardtii

AU - Yamano, Takashi

AU - Tsujikawa, Tomoki

AU - Hatano, Kyoko

AU - Ozawa, Shinichiro

AU - Takahashi, Yuichiro

AU - Fukuzawa, Hideya

PY - 2010/9

Y1 - 2010/9

N2 - The carbon-concentrating mechanism (CCM) is essential to support photosynthesis under CO2-limiting conditions in aquatic photosynthetic organisms, including the green alga Chlamydomonas reinhardtii. The CCM is assumed to be comprised of inorganic carbon transport systems that, in conjunction with carbonic anhydrases, maintain high levels of CO2 around ribulose-1, 5-bisphosphate carboxylase/oxygenase in a specific compartment called the pyrenoid. A set of transcripts up-regulated during the induction of the CCM was identified previously and designated as low-CO 2 (LC)-inducible genes. Although the functional importance of one of these LC-inducible genes, LciB, has been shown recently, the biochemical properties and detailed subcellular localization of its product LCIB remain to be elucidated. Here, using yeast two-hybrid, immunoprecipitation and mass spectrometry analyses we provide evidence to demonstrate that LCIB interacts with the LCIB homologous protein LCIC in yeast and in vivo. We also show that LCIB and LCIC are co-localized in the vicinity of the pyrenoid under LC conditions in the light, forming a hexamer complex of approximately 350 kDa, as estimated by gel filtration chromatography. LCIB localization around the pyrenoid was dependent on light illumination and LC conditions during active operation of the CCM. In contrast, in the dark or under high-CO2 conditions when the CCM was inactive, LCIB immediately diffused away from the pyrenoid. Based on these observations, we discuss possible functions of the LCIBLCIC complex in the CCM.

AB - The carbon-concentrating mechanism (CCM) is essential to support photosynthesis under CO2-limiting conditions in aquatic photosynthetic organisms, including the green alga Chlamydomonas reinhardtii. The CCM is assumed to be comprised of inorganic carbon transport systems that, in conjunction with carbonic anhydrases, maintain high levels of CO2 around ribulose-1, 5-bisphosphate carboxylase/oxygenase in a specific compartment called the pyrenoid. A set of transcripts up-regulated during the induction of the CCM was identified previously and designated as low-CO 2 (LC)-inducible genes. Although the functional importance of one of these LC-inducible genes, LciB, has been shown recently, the biochemical properties and detailed subcellular localization of its product LCIB remain to be elucidated. Here, using yeast two-hybrid, immunoprecipitation and mass spectrometry analyses we provide evidence to demonstrate that LCIB interacts with the LCIB homologous protein LCIC in yeast and in vivo. We also show that LCIB and LCIC are co-localized in the vicinity of the pyrenoid under LC conditions in the light, forming a hexamer complex of approximately 350 kDa, as estimated by gel filtration chromatography. LCIB localization around the pyrenoid was dependent on light illumination and LC conditions during active operation of the CCM. In contrast, in the dark or under high-CO2 conditions when the CCM was inactive, LCIB immediately diffused away from the pyrenoid. Based on these observations, we discuss possible functions of the LCIBLCIC complex in the CCM.

KW - Carbon-concentrating mechanism

KW - Chlamydomonas reinhardtii

KW - Chloroplast

KW - LciB

KW - Photosynthesis

KW - Pyrenoid

UR - http://www.scopus.com/inward/record.url?scp=77956892304&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77956892304&partnerID=8YFLogxK

U2 - 10.1093/pcp/pcq105

DO - 10.1093/pcp/pcq105

M3 - Article

C2 - 20660228

AN - SCOPUS:77956892304

VL - 51

SP - 1453

EP - 1468

JO - Plant and Cell Physiology

JF - Plant and Cell Physiology

SN - 0032-0781

IS - 9

ER -