A Eukaryotic Factor Required for Accumulation of the Chloroplast NAD(P)H Dehydrogenase Complex in Arabidopsis1

The NAD(P)H dehydrogenase (NDH) complex in chloroplasts mediates photosystem I cyclic and chlororespiratory electron transport. Eleven chloroplast genes and three nuclear genes have been identified as encoding Ndh subunits, but the entire subunit composition is still unknown. An Arabidopsis (Arabidopsis thaliana) chlororespiratory reduction (crr3) mutant was isolated based on its lack of transient increase in chlorophyll fluorescence after actinic light illumination; this was due to a specific defect in accumulation of the NDH complex. The CRR3 gene (At2g01590) encodes a novel protein containing a putative plastid-targeting signal and a transmembrane domain. Consistent with the gene structure, CRR3 localized to the membrane fraction of chloroplasts. In addition to the essential function of CRR3 in stabilizing the NDH complex, the NDH complex is also required for the accumulation of CRR3. These results suggest that CRR3 interacts with the NDH complex in the thylakoid membrane. In contrast to other subunits in the chloroplast NDH complex, CRR3 is not conserved in cyanobacteria from which the chloroplast NDH complex is believed to have originated. We propose that CRR3 is a subunit of the NDH complex, which is specific to the chloroplast.

[1]  F. Ausubel,et al.  A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. , 1993, The Plant journal : for cell and molecular biology.

[2]  G. Peltier,et al.  Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. , 2000, Plant physiology.

[3]  T. Ogawa,et al.  Expression and Functional Roles of the Two Distinct NDH-1 Complexes and the Carbon Acquisition Complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803 , 2004, The Plant Cell Online.

[4]  Yasuyuki Yamada,et al.  Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  K. Asada,et al.  Thylakoid Membrane-Bound, NADPH-Specific Pyridine Nucleotide Dehydrogenase Complex Mediates Cyclic Electron Transport in the Cyanobacterium Synechocystis sp. PCC 6803 , 1995 .

[6]  Physiological function of a respiratory complex. NAD(P)H dehydrogenase in chloroplasts : Dissection by chloroplast reverse genetics , 2000 .

[7]  H. Koop,et al.  Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation , 1998, Molecular and General Genetics MGG.

[8]  K. Asada,et al.  Isolation of a novel NAD(P)H-quinone oxidoreductase from the cyanobacterium Synechocystis PCC6803. , 1998, Plant & cell physiology.

[9]  J. Meurer,et al.  PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis , 2002, Cell.

[10]  T. Shikanai,et al.  Identification of a novel protein, CRR7, required for the stabilization of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[11]  T. Ogawa,et al.  Expression and Functional Roles of the Two Distinct NDH-1 Complexes and the Carbon Acquisition Complex NdhD 3 / NdhF 3 / CupA / Sll 1735 in Synechocystis sp PCC 6803 , 2004 .

[12]  Frédérique Bitton,et al.  Genome-Wide Analysis of Arabidopsis Pentatricopeptide Repeat Proteins Reveals Their Essential Role in Organelle Biogenesis , 2004, The Plant Cell Online.

[13]  P. Nixon,et al.  The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves , 1998, FEBS letters.

[14]  J. Zapata,et al.  Chlororespiration and Poising of Cyclic Electron Transport , 2000, The Journal of Biological Chemistry.

[15]  T. Ogawa,et al.  Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M Complexes of Synechocystis sp. PCC 6803* , 2005, Journal of Biological Chemistry.

[16]  H. Fukuzawa,et al.  Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[17]  J. Barber,et al.  Evolution of oxygenic photosynthesis: genome-wide analysis of the OEC extrinsic proteins. , 2004, Trends in plant science.

[18]  M. Sugiura,et al.  Evolution and mechanism of translation in chloroplasts. , 1998, Annual review of genetics.

[19]  Gilles Peltier,et al.  A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[20]  M. Hippler,et al.  Subunit Composition of NDH-1 Complexes of Synechocystis sp. PCC 6803 , 2004, Journal of Biological Chemistry.

[21]  S. Munné-Bosch,et al.  Enhanced ferredoxin-dependent cyclic electron flow around photosystem I and α-tocopherol quinone accumulation in water-stressed ndhB-inactivated tobacco mutants , 2005, Planta.

[22]  Tsuyoshi Endo,et al.  Cyclic electron flow around photosystem I is essential for photosynthesis , 2004, Nature.

[23]  T. Ogawa,et al.  Two Types of Functionally Distinct NAD(P)H Dehydrogenases inSynechocystis sp. Strain PCC6803* , 2000, The Journal of Biological Chemistry.

[24]  P. Nixon,et al.  Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes , 1998, The EMBO journal.

[25]  M. Rahire,et al.  The chloroplast ycf7 (petL) open reading frame of Chlamydomonas reinhardtii encodes a small functionally important subunit of the cytochrome b6f complex. , 1996, The EMBO journal.

[26]  K. Niyogi,et al.  Is PsbS the site of non-photochemical quenching in photosynthesis? , 2004, Journal of experimental botany.

[27]  Teruo Ogawa,et al.  Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. , 2005, The Biochemical journal.

[28]  F. Wollman,et al.  The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1 , 1999, Biochimica et biophysica acta.

[29]  T. Shikanai,et al.  Chloroplastic NAD(P)H Dehydrogenase in Tobacco Leaves Functions in Alleviation of Oxidative Damage Caused by Temperature Stress1[OA] , 2006, Plant Physiology.

[30]  M. Rahire,et al.  The chloroplast ycf 7 ( petL ) open reading frame of Chiamydomonas reinhardtii encodes a small functionally important subunit of the cytochrome b 6 f complex , 2022 .

[31]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[32]  T. Shikanai,et al.  A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts , 2005, Nature.

[33]  K. Shinozaki,et al.  Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: Determination of the splice sites in ndhA and ndhB pre-mRNAs , 1987, Molecular and General Genetics MGG.

[34]  T. Shikanai,et al.  CHLORORESPIRATORY REDUCTION 6 Is a Novel Factor Required for Accumulation of the Chloroplast NAD(P)H Dehydrogenase Complex in Arabidopsis1 , 2006, Plant Physiology.

[35]  J. Garin,et al.  New Subunits NDH-M, -N, and -O, Encoded by Nuclear Genes, Are Essential for Plastid Ndh Complex Functioning in Higher Plantsw⃞ , 2005, The Plant Cell Online.

[36]  O. Vallon,et al.  Synthesis, assembly and degradation of thylakoid membrane proteins. , 2000, Biochimie.

[37]  F. Sato,et al.  The role of chloroplastic NAD(P)H dehydrogenase in photoprotection , 1999, FEBS letters.