DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii

Journal Article · · Communications Biology
 [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [4];  [5];  [2];  [3];  [6];  [2];  [2]; ORCiD logo [2];  [7];  [2];  [2];  [5];  [6]; ORCiD logo [2]; ORCiD logo [4];  [4] more »; ORCiD logo [2] « less
  1. Donald Danforth Plant Science Center, St. Louis, MO (United States); Donald Danforth Plant Science Center
  2. Donald Danforth Plant Science Center, St. Louis, MO (United States)
  3. Washington University in Saint Louis, MO (United States); Donald Danforth Plant Science Center, St. Louis, MO (United States)
  4. TU Kaiserslautern (Germany)
  5. The Rockefeller University, New York, NY (United States)
  6. University of Missouri-Columbia, MO (United States)
  7. Donald Danforth Plant Science Center, St. Louis, MO (United States); Washington University in Saint Louis, MO (United States)

Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique responses to 24-hour moderate (35°C) and acute (40°C) high temperatures and subsequent recovery at 25°C. We identified previously overlooked unique elements in response to moderate high temperature. Heat at 35°C transiently arrested the cell cycle followed by partial synchronization, up-regulated transcripts/proteins involved in gluconeogenesis/glyoxylate-cycle for carbon uptake and promoted growth. But 40°C disrupted cell division and growth. Both high temperatures induced photoprotection, while 40°C distorted thylakoid/pyrenoid ultrastructure, affected the carbon concentrating mechanism, and decreased photosynthetic efficiency. We demonstrated increased transcript/protein correlation during both heat treatments and hypothesize reduced post-transcriptional regulation during heat may help efficiently coordinate thermotolerance mechanisms. During recovery after both heat treatments, especially 40°C, transcripts/proteins related to DNA synthesis increased while those involved in photosynthetic light reactions decreased. We propose down-regulating photosynthetic light reactions during DNA replication benefits cell cycle resumption by reducing ROS production. Our results provide potential targets to increase thermotolerance in algae and crops.

Research Organization:
Donald Danforth Plant Science Center, St. Louis, MO (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0020400; AC02-05CH11231
OSTI ID:
2318486
Journal Information:
Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 5; ISSN 2399-3642
Publisher:
Springer NatureCopyright Statement
Country of Publication:
United States
Language:
English

References (127)

Mapping RNA‐seq Reads with STAR journal September 2015
Characterization of the GPR1/FUN34/YaaH protein family in the green microalga Chlamydomonas suggests their role as intracellular membrane acetate channels journal June 2019
Automatic clustering of orthologs and in-paralogs from pairwise species comparisons journal December 2001
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method journal December 2001
Control of lhc gene transcription by the circadian clock in Chlamydomonas reinhardtii journal October 1994
A Chlamydomonas gene encodes a G protein ? subunit-like polypeptide journal May 1990
Mechanisms of heat shock response in mammals journal April 2013
An inducible artificial microRNA system for Chlamydomonas reinhardtii confirms a key role for heat shock factor 1 in regulating thermotolerance journal May 2010
Chlamydomonas reinhardtii: duration of its cell cycle and phases at growth rates affected by temperature journal May 2011
Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress journal November 2011
CRISPR based targeted genome editing of Chlamydomonas reinhardtii using programmed Cas9-gRNA ribonucleoprotein journal October 2020
Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K journal March 2018
Substrates of the chloroplast small heat shock proteins 22E/F point to thermolability as a regulative switch for heat acclimation in Chlamydomonas reinhardtii journal November 2017
Photosynthetic electron transport and proton flux under moderate heat stress journal April 2009
Cyclic electron flow around photosystem I in unicellular green algae journal June 2010
Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability journal October 2013
The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron journal February 2019
Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods journal March 1979
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy journal August 1989
The Spectral Determination of Chlorophylls a and b, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution journal September 1994
Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions journal January 2010
Physiology of PSI cyclic electron transport in higher plants journal March 2011
Loss of CpSRP54 function leads to a truncated light-harvesting antenna size in Chlamydomonas reinhardtii journal January 2017
Yield response to heat stress as affected by nitrogen availability in maize journal November 2015
Microalgae for biodiesel production and other applications: A review journal January 2010
How do plants feel the heat? journal March 2012
Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions journal July 2004
Birth of a Photosynthetic Chassis: A MoClo Toolkit Enabling Synthetic Biology in the Microalga Chlamydomonas reinhardtii journal August 2018
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
Chlamydomonas reinhardtii thermal tolerance enhancement mediated by a mutualistic interaction with vitamin B12-producing bacteria journal March 2013
Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis journal April 2010
MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification journal November 2008
Redesigning the QA binding site of Photosystem II allows reduction of exogenous quinones journal May 2017
Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop journal March 2018
Antenna arrangement and energy transfer pathways of a green algal photosystem-I–LHCI supercomplex journal March 2019
The structural basis of Rubisco phase separation in the pyrenoid journal November 2020
A genome-wide algal mutant library and functional screen identifies genes required for eukaryotic photosynthesis journal March 2019
Nitrogen supply influences photosynthesis establishment along the sugarcane leaf journal February 2018
Genome-wide identification and characterization of CKIN/SnRK gene family in Chlamydomonas reinhardtii journal January 2019
Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii journal August 2019
Abscisic acid induced a negative geotropic response in dark-incubated Chlamydomonas reinhardtii journal August 2019
High light and temperature reduce photosynthetic efficiency through different mechanisms in the C4 model Setaria viridis journal September 2021
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
Information-theoretic analysis of phenotype changes in early stages of carcinogenesis journal May 2010
A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle journal May 2016
Temperature increase reduces global yields of major crops in four independent estimates journal August 2017
Genome-wide RNA structurome reprogramming by acute heat shock globally regulates mRNA abundance journal November 2018
Structure of a PSI–LHCI–cyt b 6 f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions journal September 2018
Multiomics resolution of molecular events during a day in the life of Chlamydomonas journal January 2019
A Rubisco-binding protein is required for normal pyrenoid number and starch sheath morphology in Chlamydomonas reinhardtii journal August 2019
Interaction between Starch Breakdown, Acetate Assimilation, and Photosynthetic Cyclic Electron Flow in Chlamydomonas reinhardtii journal June 2012
Quantitative Shotgun Proteomics Using a Uniform 15 N-Labeled Standard to Monitor Proteome Dynamics in Time Course Experiments Reveals New Insights into the Heat Stress Response of Chlamydomonas reinhardtii journal May 2011
Accurate Proteome-wide Label-free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ journal June 2014
THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY journal April 1963
Fast unfolding of communities in large networks journal October 2008
Impact of heat stress on crop yield—on the importance of considering canopy temperature journal April 2014
Dual effect of heat shock on DNA replication and genome integrity journal September 2012
STAR: ultrafast universal RNA-seq aligner journal October 2012
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Inheritance in the Green alga Chlamydomonas Reinhardi journal July 1955
Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity journal January 2020
Plasticity in light reactions of photosynthesis for energy production and photoprotection journal November 2004
Circadian regulation of chloroplastic f and m thioredoxins through control of the CCA1 transcription factor journal December 2010
Increasing cyclic electron flow is related to Na + sequestration into vacuoles for salt tolerance in soybean journal August 2015
The algal pyrenoid: key unanswered questions journal May 2017
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository journal January 2002
Phytozome: a comparative platform for green plant genomics journal November 2011
The PRIDE database and related tools and resources in 2019: improving support for quantification data journal November 2018
Oxidative damage diminishes mitochondrial DNA polymerase replication fidelity journal December 2019
Single-cell RNA sequencing of batch Chlamydomonas cultures reveals heterogeneity in their diurnal cycle phase journal February 2021
Real-time monitoring of subcellular H2O2 distribution in Chlamydomonas reinhardtii journal July 2021
Genome-Based Examination of Chlorophyll and Carotenoid Biosynthesis in Chlamydomonas reinhardtii journal April 2005
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
The Antarctic Psychrophile Chlamydomonas sp. UWO 241 Preferentially Phosphorylates a Photosystem I-Cytochrome b 6 / f Supercomplex journal July 2015
Heat Induction of Cyclic Electron Flow around Photosystem I in the Symbiotic Dinoflagellate Symbiodinium journal March 2016
The Type II NADPH Dehydrogenase Facilitates Cyclic Electron Flow, Energy-Dependent Quenching, and Chlororespiratory Metabolism during Acclimation of Chlamydomonas reinhardtii to Nitrogen Deprivation journal February 2016
Dynamic Thylakoid Stacking Is Regulated by LHCII Phosphorylation but Not Its interaction with PSI journal June 2019
Jasmonic Acid Is Required for Plant Acclimation to a Combination of High Light and Heat Stress journal October 2019
Chlamydomonas sp. UWO 241 Exhibits High Cyclic Electron Flow and Rewired Metabolism under High Salinity journal March 2020
Different Signaling and Cell Death Roles of Heterotrimeric G Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone journal February 2005
The Heat Shock Response in Moss Plants Is Regulated by Specific Calcium-Permeable Channels in the Plasma Membrane journal September 2009
Transcription Factor–Dependent Chromatin Remodeling at Heat Shock and Copper-Responsive Promoters in Chlamydomonas reinhardtii journal June 2011
High-Throughput Genotyping of Green Algal Mutants Reveals Random Distribution of Mutagenic Insertion Sites and Endonucleolytic Cleavage of Transforming DNA journal April 2014
A Microbial Avenue to Cell Cycle Control in the Plant Superkingdom journal October 2014
Reliable Gene Expression Analysis by Reverse Transcription-Quantitative PCR: Reporting and Minimizing the Uncertainty in Data Accuracy journal October 2014
Systems-Wide Analysis of Acclimation Responses to Long-Term Heat Stress and Recovery in the Photosynthetic Model OrganismChlamydomonas reinhardtii    journal November 2014
An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii journal January 2016
The Transcription Factor bZIP60 Links the Unfolded Protein Response to the Heat Stress Response in Maize journal August 2020
Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene journal March 2005
Determining the limitations and regulation of photosynthetic energy transduction in leaves journal September 2007
Early events in signalling high‐temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production journal November 2008
Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves journal November 2009
Heat shock‐induced biphasic Ca2+ signature and OsCaM1‐1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.) journal April 2012
Heat shock factor 1 is a key regulator of the stress response in Chlamydomonas journal August 2007
SYNCHRONOUS GROWTH OF CHLAMYDOMONAS REINHARDTII (CHLOROPHYCEAE): A REVIEW OF OPTIMAL CONDITIONS1 journal June 1979
High Temperature Effects on Electron and Proton Circuits of Photosynthesis journal July 2010
Lipidomic and transcriptomic analyses of Chlamydomonas reinhardtii under heat stress unveil a direct route for the conversion of membrane lipids into storage lipids : Lipid remodelling under heat stress in journal January 2016
Not changes in membrane fluidity but proteotoxic stress triggers heat shock protein expression in Chlamydomonas reinhardtii journal September 2017
Lack of isocitrate lyase in Chlamydomonas leads to changes in carbon metabolism and in the response to oxidative stress under mixotrophic growth journal January 2014
The Chlamydomonas cell cycle journal March 2015
Molecular techniques to interrogate and edit the Chlamydomonas nuclear genome journal March 2015
The Chlamydomonas heat stress response journal March 2015
CO 2 ‐fixing liquid droplets: Towards a dissection of the microalgal pyrenoid journal May 2019
Assembly of the algal CO 2 -fixing organelle, the pyrenoid, is guided by a Rubisco-binding motif journal November 2020
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions journal October 2007
Climate Trends and Global Crop Production Since 1980 journal May 2011
Central Carbon Metabolism and Electron Transport in Chlamydomonas reinhardtii: Metabolic Constraints for Carbon Partitioning between Oil and Starch journal March 2013
Reactive Oxygen Species in Plant Signaling journal April 2018
Physiological Functions of Cyclic Electron Transport Around Photosystem I in Sustaining Photosynthesis and Plant Growth journal April 2016
Prospects for Engineering Biophysical CO 2 Concentrating Mechanisms into Land Plants to Enhance Yields journal April 2020
Constructing gene co-expression networks and predicting functions of unknown genes by random matrix theory journal January 2007
WGCNA: an R package for weighted correlation network analysis journal December 2008
Effects of high temperature on photosynthesis and related gene expression in poplar journal April 2014
Eigengene networks for studying the relationships between co-expression modules journal November 2007
Differential expression analysis for sequence count data journal October 2010
Abscisic Acid Negatively Modulates Heat Tolerance in Rolled Leaf Rice by Increasing Leaf Temperature and Regulating Energy Homeostasis journal March 2020
ForceAtlas2, a Continuous Graph Layout Algorithm for Handy Network Visualization Designed for the Gephi Software journal June 2014
Portrait of a Species journal June 2005
Heat‐Induced Leaf Senescence Associated with Chlorophyll Metabolism in Bentgrass Lines Differing in Heat Tolerance journal July 2017
Production of Reactive Oxygen Species by Photosystem II as a Response to Light and Temperature Stress journal December 2016
Applications of Multi-Omics Technologies for Crop Improvement journal September 2021
Reactive Oxygen Species and Antioxidant Defense in Plants under Abiotic Stress: Revisiting the Crucial Role of a Universal Defense Regulator journal July 2020
Starch Production in Chlamydomonas reinhardtii through Supraoptimal Temperature in a Pilot-Scale Photobioreactor journal May 2021
TMEA: A Thermodynamically Motivated Framework for Functional Characterization of Biological Responses to System Acclimation journal September 2020
Metabolic Reprogramming in Chloroplasts under Heat Stress in Plants journal March 2018
Comparative Phenotyping of Two Commonly Used Chlamydomonas reinhardtii Background Strains: CC-1690 (21gr) and CC-5325 (The CLiP Mutant Library Background) journal February 2022
Carotenoid deficiency triggers autophagy in the model green alga Chlamydomonas reinhardtii journal March 2012