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Title: The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

Journal Article · · Plant Physiology (Bethesda)
 [1];  [1];  [1];  [2];  [3];  [2];  [4];  [1];  [4];  [5];  [1];  [2];  [6];  [1]
  1. Michigan State Univ., East Lansing, MI (United States)
  2. Washington State Univ., Pullman, WA (United States)
  3. Donald Danforth Plant Science Center, St. Louis, MO (United States); National Center of Biomedical Analysis, Beijing (China)
  4. New Mexico State Univ., Las Cruces, NM (United States)
  5. Cambridge Advanced Imaging Centre, Cambridge (United Kingdom)
  6. Donald Danforth Plant Science Center, St. Louis, MO (United States); Univ. of North Carolina, Chapel Hill, NC (United States)

The accumulation of carbon storage compounds by many unicellular algae after nutrient deprivation occurs despite declines in their photosynthetic apparatus. To understand the regulation and roles of photosynthesis during this potentially bioenergetically valuable process, we analyzed photosynthetic structure and function after nitrogen deprivation in the model alga Chlamydomonas reinhardtii. Transcriptomic, proteomic, metabolite, and lipid profiling and microscopic time course data were combined with multiple measures of photosynthetic function. Levels of transcripts and proteins of photosystems I and II and most antenna genes fell with differing trajectories; thylakoid membrane lipid levels decreased, while their proportions remained similar and thylakoid membrane organization appeared to be preserved. Cellular chlorophyll (Chl) content decreased more than 2-fold within 24 h, and we conclude from transcript protein and 13C labeling rates that Chl synthesis was down-regulated both pre- and posttranslationally and that Chl levels fell because of a rapid cessation in synthesis and dilution by cellular growth rather than because of degradation. Photosynthetically driven oxygen production and the efficiency of photosystem II as well as P700+ reduction and electrochromic shift kinetics all decreased over the time course, without evidence of substantial energy overflow. The results also indicate that linear electron flow fell approximately 15% more than cyclic flow over the first 24 h. Comparing Calvin-Benson cycle transcript and enzyme levels with changes in photosynthetic 13CO2 incorporation rates also pointed to a coordinated multilevel down-regulation of photosynthetic fluxes during starch synthesis before the induction of high triacylglycerol accumulation rates.

Research Organization:
Energy Frontier Research Centers (EFRC) (United States). Center for Advanced Biofuel Systems (CABS); Donald Danforth Plant Science Center, St. Louis, MO (United States); Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0001295; FG02-91ER20021
OSTI ID:
1459199
Alternate ID(s):
OSTI ID: 1602547
Journal Information:
Plant Physiology (Bethesda), Vol. 167, Issue 2; ISSN 0032-0889
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 81 works
Citation information provided by
Web of Science

References (107)

Nitrogen chlorosis in blue-green algae journal January 1969
Cyclic electron flow around photosystem I in unicellular green algae journal June 2010
ABA-Dependent and -Independent G-Protein Signaling in Arabidopsis Roots Revealed through an iTRAQ Proteomics Approach journal July 2011
A comprehensive review on biodiesel as an alternative energy resource and its characteristics journal May 2012
Regulating the proton budget of higher plant photosynthesis journal June 2005
Electrochromism: a useful probe to study algal photosynthesis journal July 2010
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo journal June 2008
Determining the limitations and regulation of photosynthetic energy transduction in leaves journal September 2007
Carbon Isotope Discrimination and the CO2 Accumulating Mechanism in Chlorella emersonii journal August 1982
Differential Effects of Nitrogen Limitation on Photosynthetic Efficiency of Photosystems I and II in Microalgae journal February 1996
Systems-Level Analysis of Nitrogen Starvation-Induced Modifications of Carbon Metabolism in a Chlamydomonas reinhardtii Starchless Mutant journal November 2013
Metabolite Profiling of Chlamydomonas reinhardtii under Nutrient Deprivation journal November 2005
The Occurrence of the psbS Gene Product in Chlamydomonas reinhardtii and in Other Photosynthetic Organisms and Its Correlation with Energy Quenching journal November 2008
An original adaptation of photosynthesis in the marine green alga Ostreococcus journal May 2008
Biodiesel from microalgae journal May 2007
Identification of Extracellular Carbonic Anhydrase of Chlamydomonas reinhardtii journal October 1984
Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii journal September 1989
Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii journal August 2001
Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas journal March 2003
Responses of Nannochloropsis oceanica IMET1 to Long-Term Nitrogen Starvation and Recovery journal May 2013
Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii journal May 2012
Metabolic Flux Analysis of the Mixotrophic Metabolisms in the Green Sulfur Bacterium Chlorobaculum tepidum journal October 2010
Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii journal August 2009
A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues journal May 1957
Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation journal June 2004
Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation journal November 1998
Diurnal Regulation of Photosynthetic Carbon Metabolism in C3 Plants journal June 1994
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence journal January 1989
The Path to Triacylglyceride Obesity in the sta6 Strain of Chlamydomonas reinhardtii journal February 2014
Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. journal December 1965
Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum: diel variations and effects of N depletion journal January 2002
Acclimation of Chlamydomonas reinhardtii to its Nutrient Environment journal October 2000
Next-generation sequencing-based transcriptomic and proteomic analysis of the common reed, Phragmites australis (Poaceae), reveals genes involved in invasiveness and rhizome specificity journal February 2012
PGRL1 Is the Elusive Ferredoxin-Plastoquinone Reductase in Photosynthetic Cyclic Electron Flow journal February 2013
Light-induced dissociation of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching journal May 2012
Characterization of microalgal lipid feedstock by direct-infusion FT-ICR mass spectrometry journal January 2013
Regulation of Light Harvesting in Green Plants (Indication by Nonphotochemical Quenching of Chlorophyll Fluorescence) journal October 1994
Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas journal December 2011
Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances journal May 2008
Molecular Remodeling of Photosystem II during State Transitions in Chlamydomonas reinhardtii journal August 2008
The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II journal January 2012
Omics in algae: Paving the way for a systems biological understanding of algal stress phenomena? journal May 2009
A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas journal December 2008
Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant journal June 2000
Interaction between Starch Breakdown, Acetate Assimilation, and Photosynthetic Cyclic Electron Flow in Chlamydomonas reinhardtii journal June 2012
Central Carbon Metabolism and Electron Transport in Chlamydomonas reinhardtii: Metabolic Constraints for Carbon Partitioning between Oil and Starch journal March 2013
Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of Δ ATPase pgr5 and Δ rbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii journal March 2014
Lipids in photosynthetic reaction centres: Structural roles and functional holes journal January 2007
Intracellular Carbon Partitioning in Chlamydomonas reinhardtii journal December 1987
New Fluorescence Parameters for the Determination of Q A Redox State and Excitation Energy Fluxes journal January 2004
System Response of Metabolic Networks in Chlamydomonas reinhardtii to Total Available Ammonium journal July 2012
Effects of phospholipase and lipase treatments on photosystem II core dimer from a thermophilic cyanobacterium journal July 2008
A Galactoglycerolipid Lipase Is Required for Triacylglycerol Accumulation and Survival Following Nitrogen Deprivation in Chlamydomonas reinhardtii journal November 2012
Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii journal May 2010
Lipid metabolism in microalgae distinguishes itself journal April 2013
An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I ( hcef ) Involving the NADPH Dehydrogenase Complex journal January 2010
HILIC- and SCX-Based Quantitative Proteomics of Chlamydomonas reinhardtii during Nitrogen Starvation Induced Lipid and Carbohydrate Accumulation journal October 2012
Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability journal October 2013
Gametic differentiation in Chlamydomonas reinhardtii. I. Production of gametes and their fine structure journal November 1975
Transcriptional Regulation of the Stress-Responsive Light Harvesting Complex Genes in Chlamydomonas Reinhardtii journal May 2014
Elemental Economy book January 2012
TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation journal June 2012
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions journal October 2007
Changes in Transcript Abundance in Chlamydomonas reinhardtii following Nitrogen Deprivation Predict Diversion of Metabolism journal October 2010
The role of lipids in photosystem II journal January 2012
Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus journal December 2002
Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169 journal March 2012
Non-Photochemical Quenching. A Response to Excess Light Energy journal April 2001
PGR5 Is Involved in Cyclic Electron Flow around Photosystem I and Is Essential for Photoprotection in Arabidopsis journal August 2002
Quantitative analysis of 77K fluorescence emission spectra in Synechocystis sp. PCC 6714 and Chlamydomonas reinhardtii with variable PS I/PS II stoichiometries journal September 1997
A Heterocomplex of Iron Superoxide Dismutases Defends Chloroplast Nucleoids against Oxidative Stress and Is Essential for Chloroplast Development in Arabidopsis journal November 2008
Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: With focus on proteins involved in lipid metabolism journal September 2011
Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching journal August 1997
Driving on Biomass journal May 2009
An ancient light-harvesting protein is critical for the regulation of algal photosynthesis journal November 2009
Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. journal June 1991
PGRL1 Participates in Iron-induced Remodeling of the Photosynthetic Apparatus and in Energy Metabolism in Chlamydomonas reinhardtii journal September 2009
Environmental control of plant nuclear gene expression by chloroplast redox signals journal January 2012
Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii journal October 2011
Nitrogen-dependent regulation of photosynthetic gene expression journal April 1989
Consistent Sets of Spectrophotometric Chlorophyll Equations for Acetone, Methanol and Ethanol Solvents journal June 2006
Chlamydomonas , a model system for studying the assembly and dynamics of photosynthetic complexes journal August 2002
Carotenoid accumulation in orange-pigmented Capsicum annuum fruit, regulated at multiple levels journal September 2011
Environmental Control of Glycerolipid Metabolism in Microalgae: Commercial Implications and Future Research Directions journal September 1990
Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response journal September 2007
Nitrogen-Sparing Mechanisms in Chlamydomonas Affect the Transcriptome, the Proteome, and Photosynthetic Metabolism journal April 2014
A transient isotopic labeling methodology for 13C metabolic flux analysis of photoautotrophic microorganisms journal August 2007
PHYTOPLANKTON LIPIDS: INTERSPECIFIC DIFFERENCES AND EFFECTS OF NITRATE, SILICATE AND LIGHT-DARK CYCLES 1 journal December 1981
Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves journal January 2011
The Response of Nannochloropsis gaditana to Nitrogen Starvation Includes De Novo Biosynthesis of Triacylglycerols, a Decrease of Chloroplast Galactolipids, and Reorganization of the Photosynthetic Apparatus journal March 2013
Carotenoids in Algae: Distributions, Biosyntheses and Functions journal June 2011
Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii journal May 2013
A Forward Genetic Approach in Chlamydomonas reinhardtii as a Strategy for Exploring Starch Catabolism journal September 2013
Environmentally Modulated Phosphoproteome of Photosynthetic Membranes in the Green Alga Chlamydomonas reinhardtii journal May 2006
Remodeling of Membrane Lipids in Iron-starved Chlamydomonas journal August 2013
Periplasmic Carbonic Anhydrase Structural Gene ( Cah1 ) Mutant in Chlamydomonas reinhardtii journal July 1999
Comprehensive Comparison of iTRAQ and Label-free LC-Based Quantitative Proteomics Approaches Using Two Chlamydomonas reinhardtii Strains of Interest for Biofuels Engineering journal December 2011
Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture journal March 2011
Algal Lipid Bodies: Stress Induction, Purification, and Biochemical Characterization in Wild-Type and Starchless Chlamydomonas reinhardtii journal October 2009
An Outlook on Microalgal Biofuels journal August 2010
Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics journal January 2010
Increased Lipid Accumulation in the Chlamydomonas reinhardtii sta7-10 Starchless Isoamylase Mutant and Increased Carbohydrate Synthesis in Complemented Strains journal June 2010
The Regulation of Photosynthetic Electron Transport during Nutrient Deprivation in Chlamydomonas reinhardtii journal May 1998
Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum journal May 2013
Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation journal January 2013
Induction of tolerance to oxidative stress in the green alga, Chlamydomonas reinhardtii , by abscisic acid: ABA-induced tolerance to oxidative stress in Chlamydomonas reinhardtii journal March 2003
Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis journal November 2011

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