A Plant-Specific Protein Essential for Blue-Light-Induced Chloroplast Movements1

In Arabidopsis (Arabidopsis thaliana), light-dependent chloroplast movements are induced by blue light. When exposed to low fluence rates of light, chloroplasts accumulate in periclinal layers perpendicular to the direction of light, presumably to optimize light absorption by exposing more chloroplast area to the light. Under high light conditions, chloroplasts become positioned parallel to the incoming light in a response that can reduce exposure to light intensities that may damage the photosynthetic machinery. To identify components of the pathway downstream of the photoreceptors that mediate chloroplast movements (i.e. phototropins), we conducted a mutant screen that has led to the isolation of several Arabidopsis mutants displaying altered chloroplast movements. The plastid movement impaired1 (pmi1) mutant exhibits severely attenuated chloroplast movements under all tested fluence rates of light, suggesting that it is a necessary component for both the low- and high-light-dependant chloroplast movement responses. Analysis of pmi1 leaf cross sections revealed that regardless of the light condition, chloroplasts are more evenly distributed in leaf mesophyll cells than in the wild type. The pmi1-1 mutant was found to contain a single nonsense mutation within the open reading frame of At1g42550. This gene encodes a plant-specific protein of unknown function that appears to be conserved among angiosperms. Sequence analysis of the protein suggests that it may be involved in calcium-mediated signal transduction, possibly through protein–protein interactions.

[1]  T. Kagawa,et al.  Brief irradiation with red or blue light induces orientational movement of chloroplasts in dark-adapted prothallial cells of the fernAdiantum , 1994, Journal of Plant Research.

[2]  S. Takagi,et al.  Dynamic changes in the organization of microfilaments associated with the photocontrolled motility of chloroplasts in epidermal cells ofVattisneria , 1996, Protoplasma.

[3]  M. Wada,et al.  Photoinduction of formation of circular structures by microfilaments on chloroplasts during intracellular orientation in protonemal cells of the fernAdiantum capillus-veneris , 1992, Protoplasma.

[4]  N. Suetsugu,et al.  Plant organelle positioning. , 2004, Current opinion in plant biology.

[5]  Marie-France Carlier,et al.  Formin Is a Processive Motor that Requires Profilin to Accelerate Actin Assembly and Associated ATP Hydrolysis , 2004, Cell.

[6]  L. Godfrey,et al.  Changes in ion fluxes during phototropic bending of etiolated oat coleoptiles. , 2004, Annals of botany.

[7]  T. Kiyosue,et al.  Phototropins Mediate Blue and Red Light-Induced Chloroplast Movements in Physcomitrella patens1 , 2004, Plant Physiology.

[8]  S. Yoshida,et al.  Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. , 2004, Plant & cell physiology.

[9]  T. Pesacreta,et al.  A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone subunit TCP-1alpha in maize. , 2004, Cell motility and the cytoskeleton.

[10]  K. Okada,et al.  RPT2 Is a Signal Transducer Involved in Phototropic Response and Stomatal Opening by Association with Phototropin 1 in Arabidopsis thaliana , 2004, The Plant Cell Online.

[11]  M. Tlałka,et al.  Influence of calcium on blue-light-induced chloroplast movement in Lemna trisulca L. , 1993, Planta.

[12]  O. Björkman,et al.  Chloroplast movements in leaves: Influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation , 1992, Photosynthesis Research.

[13]  Kazuo Shibata,et al.  Light-induced chloroplast rearrangements and their action spectra as measured by absorption spectrophotometry , 1973, Planta.

[14]  T. Kanegae,et al.  CHLOROPLAST UNUSUAL POSITIONING1 Is Essential for Proper Chloroplast Positioning Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016428. , 2003, The Plant Cell Online.

[15]  J. Mullen,et al.  Phytochrome Modulation of Blue Light-Induced Chloroplast Movements in Arabidopsis1 , 2003, Plant Physiology.

[16]  K. Folta,et al.  Primary Inhibition of Hypocotyl Growth and Phototropism Depend Differently on Phototropin-Mediated Increases in Cytoplasmic Calcium Induced by Blue Light1 , 2003, Plant Physiology.

[17]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[18]  K. Okada,et al.  phot1 and phot2 mediate blue light-induced transient increases in cytosolic Ca2+ differently in Arabidopsis leaves , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  S. Goff,et al.  A network of rice genes associated with stress response and seed development , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Hedrich,et al.  Blue light activates calcium-permeable channels in Arabidopsis mesophyll cells via the phototropin signaling pathway , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Masahiro Kasahara,et al.  Chloroplast avoidance movement reduces photodamage in plants , 2002, Nature.

[22]  S. Shabala,et al.  Blue light-induced kinetics of H+ and Ca2+ fluxes in etiolated wild-type and phototropin-mutant Arabidopsis seedlings , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Jonathan D. G. Jones,et al.  Regulatory Role of SGT1 in Early R Gene-Mediated Plant Defenses , 2002, Science.

[24]  H. Anisman,et al.  Role of bombesin-related peptides in the mediation or integration of the stress response , 2002, Cellular and Molecular Life Sciences CMLS.

[25]  M. Wada,et al.  External Ca(2+) is essential for chloroplast movement induced by mechanical stimulation but not by light stimulation. , 2001, Plant physiology.

[26]  T. McNellis,et al.  A Humidity-Sensitive Arabidopsis Copine Mutant Exhibits Precocious Cell Death and Increased Disease Resistance , 2001, The Plant Cell Online.

[27]  Ping Wang,et al.  The tandem C2 domains of synaptotagmin contain redundant Ca2+ binding sites that cooperate to engage t-SNAREs and trigger exocytosis , 2001, The Journal of cell biology.

[28]  Masahiro Kasahara,et al.  Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. Ecker,et al.  Phototropin-related NPL1 controls chloroplast relocation induced by blue light , 2001, Nature.

[30]  S. Ishiguro,et al.  Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. , 2001, Science.

[31]  M. Wada,et al.  Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor. , 2001, Journal of cell science.

[32]  C. Staiger SIGNALING TO THE ACTIN CYTOSKELETON IN PLANTS. , 2000, Annual review of plant physiology and plant molecular biology.

[33]  Yoshikatsu Sato,et al.  Intracellular chloroplast photorelocation in the moss Physcomitrella patens is mediated by phytochrome as well as by a blue-light receptor , 2000, Planta.

[34]  T. Wada,et al.  RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis , 2000, Plant Cell.

[35]  T. Kagawa,et al.  Blue light-induced chloroplast relocation in Arabidopsis thaliana as analyzed by microbeam irradiation. , 2000, Plant & cell physiology.

[36]  Fricker,et al.  The role of calcium in blue-light-dependent chloroplast movement in lemna trisulca L , 1999, The Plant journal : for cell and molecular biology.

[37]  E. Liscum,et al.  Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. , 1999, Science.

[38]  J. Augustynowicz Chloroplast movements in fern leaves: correlation of movement dynamics and environmental flexibility of the species , 1999 .

[39]  R. Meagher,et al.  Actin-organelle interaction: association with chloroplast in arabidopsis leaf mesophyll cells. , 1999, Cell motility and the cytoskeleton.

[40]  M. Yamaguchi,et al.  Role of regucalcin as an activator of Ca2+‐ATPase activity in rat liver microsomes , 1999, Journal of cellular biochemistry.

[41]  R. Tsien,et al.  Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. , 1999, The Plant journal : for cell and molecular biology.

[42]  Thomas C. Vogelmann,et al.  Chloroplast movement in Alocasia macrorrhiza , 1999 .

[43]  S. Pentyala,et al.  Selective interaction of the C2 domains of phospholipase C-β1 and -β2 with activated Gαq subunits: An alternative function for C2-signaling modules , 1999 .

[44]  S. Elledge,et al.  SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. , 1999, Molecular cell.

[45]  K. Niyogi,et al.  PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches. , 1999, Annual review of plant physiology and plant molecular biology.

[46]  M. I. D. Michelis,et al.  N-ETHYLMALEIMIDE MODIFIES THE CONFORMATION OF THE PLASMA MEMBRANE H+-ATPASE, STRENGTHENING THE INHIBITORY ACTION OF THE C-TERMINAL DOMAIN , 1999 .

[47]  T. Kinoshita,et al.  Involvement of intracellular Ca2+ in blue light-dependent proton pumping in guard cell protoplasts from Vicia faba , 1999 .

[48]  Kagawa,et al.  Chloroplast-avoidance response induced by high-fluence blue light in prothallial cells of the fern adiantum capillus-veneris as analyzed by microbeam irradiation , 1999, Plant physiology.

[49]  S. Pentyala,et al.  Selective interaction of the C 2 domains of phospholipase Cb 1 and-b 2 with activated G a q subunits : An alternative function for C 2-signaling modules , 1999 .

[50]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[51]  N. Chua,et al.  A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. , 1998, The Plant journal : for cell and molecular biology.

[52]  R. Golsteyn,et al.  The role of actin binding proteins in epithelial morphogenesis: models based upon Listeria movement. , 1997, Biophysical chemistry.

[53]  H. Gabryś,et al.  Light-induced chloroplast movements in Lemna trisulca. Identification of the motile system , 1996 .

[54]  S. Rhee,et al.  The Role of Carboxyl-terminal Basic Amino Acids in Gqα-dependent Activation, Particulate Association, and Nuclear Localization of Phospholipase C-β1* , 1996, The Journal of Biological Chemistry.

[55]  H. Gabryś,et al.  Chloroplast Distribution in Arabidopsis thaliana (L.) Depends on Light Conditions during Growth , 1996, Plant physiology.

[56]  B. Gibson,et al.  There Are Three Distinct Forms of Bombesin , 1996, The Journal of Biological Chemistry.

[57]  G. Hayman,et al.  ATPase Activity and Molecular Chaperone Function of the Stress70 Proteins , 1996, Plant physiology.

[58]  P. Quail,et al.  Phytochrome A Regulates Red-Light Induction of Phototropic Enhancement in Arabidopsis , 1996, Plant physiology.

[59]  J. Wolenski Regulation of calmodulin-binding myosins. , 1995, Trends in cell biology.

[60]  P. Cossart,et al.  Actin-based movement of Listeria monocytogenes: actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface , 1995, The Journal of cell biology.

[61]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[62]  D. Purich,et al.  Arrest of Listeria movement in host cells by a bacterial ActA analogue: implications for actin-based motility. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[63]  T. Shimmen,et al.  Physiological and Biochemical Aspects of Cytoplasmic Streaming , 1994 .

[64]  J. Ecker,et al.  Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. , 1994, Genomics.

[65]  A. Trewavas,et al.  Imaging calcium dynamics in living plant cells and tissues , 1993 .

[66]  A. Aderem,et al.  Signal transduction and the actin cytoskeleton: the roles of MARCKS and profilin. , 1992, Trends in biochemical sciences.

[67]  C. Lloyd,et al.  Association of Phosphatidylinositol 4-Kinase with the Plant Cytoskeleton. , 1992, The Plant cell.

[68]  I. Ferguson,et al.  Release of Ca2+ from plant hypocotyl microsomes by inositol-1,4,5-trisphosphate. , 1985, Biochemical and biophysical research communications.

[69]  N. Boardman Comparative photosynthesis of sun and shade plants. , 1977 .