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Title: The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response

Abstract

In response to proteotoxic stress, chloroplasts communicate with the nuclear gene expression system through a chloroplast unfolded protein response (cpUPR). We isolated Chlamydomonas reinhardtii mutants that disrupt cpUPR signaling and identified a gene encoding a previously uncharacterized cytoplasmic protein kinase, termed Mars1—for mutant affected in chloroplast-to-nucleus retrograde signaling—as the first known component in cpUPR signal transmission. Lack of cpUPR induction in MARS1 mutant cells impaired their ability to cope with chloroplast stress, including exposure to excessive light. Conversely, transgenic activation of cpUPR signaling conferred an advantage to cells undergoing photooxidative stress. Our results indicate that the cpUPR mitigates chloroplast photodamage and that manipulation of this pathway is a potential avenue for engineering photosynthetic organisms with increased tolerance to chloroplast stress.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [1]
  1. Univ. of California, San Francisco, CA (United States). Howard Hughes Medical Inst., and Dept. of Biochemistry and Biophysics
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
  3. Princeton Univ. NJ (United States). Dept. of Molecular Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1572856
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Perlaza, Karina, Toutkoushian, Hannah, Boone, Morgane, Lam, Mable, Iwai, Masakazu, Jonikas, Martin C., Walter, Peter, and Ramundo, Silvia. The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response. United States: N. p., 2019. Web. doi:10.7554/eLife.49577.
Perlaza, Karina, Toutkoushian, Hannah, Boone, Morgane, Lam, Mable, Iwai, Masakazu, Jonikas, Martin C., Walter, Peter, & Ramundo, Silvia. The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response. United States. https://doi.org/10.7554/eLife.49577
Perlaza, Karina, Toutkoushian, Hannah, Boone, Morgane, Lam, Mable, Iwai, Masakazu, Jonikas, Martin C., Walter, Peter, and Ramundo, Silvia. Tue . "The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response". United States. https://doi.org/10.7554/eLife.49577. https://www.osti.gov/servlets/purl/1572856.
@article{osti_1572856,
title = {The Mars1 kinase confers photoprotection through signaling in the chloroplast unfolded protein response},
author = {Perlaza, Karina and Toutkoushian, Hannah and Boone, Morgane and Lam, Mable and Iwai, Masakazu and Jonikas, Martin C. and Walter, Peter and Ramundo, Silvia},
abstractNote = {In response to proteotoxic stress, chloroplasts communicate with the nuclear gene expression system through a chloroplast unfolded protein response (cpUPR). We isolated Chlamydomonas reinhardtii mutants that disrupt cpUPR signaling and identified a gene encoding a previously uncharacterized cytoplasmic protein kinase, termed Mars1—for mutant affected in chloroplast-to-nucleus retrograde signaling—as the first known component in cpUPR signal transmission. Lack of cpUPR induction in MARS1 mutant cells impaired their ability to cope with chloroplast stress, including exposure to excessive light. Conversely, transgenic activation of cpUPR signaling conferred an advantage to cells undergoing photooxidative stress. Our results indicate that the cpUPR mitigates chloroplast photodamage and that manipulation of this pathway is a potential avenue for engineering photosynthetic organisms with increased tolerance to chloroplast stress.},
doi = {10.7554/eLife.49577},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {Tue Oct 15 00:00:00 EDT 2019},
month = {Tue Oct 15 00:00:00 EDT 2019}
}

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Works referenced in this record:

An Engineered Streptomyces hygroscopicus aph 7″ Gene Mediates Dominant Resistance against Hygromycin B in Chlamydomonas reinhardtii
journal, December 2002


Photosystem II Subunit PsbS Is Involved in the Induction of LHCSR Protein-dependent Energy Dissipation in Chlamydomonas reinhardtii
journal, June 2016

  • Correa-Galvis, Viviana; Redekop, Petra; Guan, Katharine
  • Journal of Biological Chemistry, Vol. 291, Issue 33
  • DOI: 10.1074/jbc.M116.737312

ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999

  • Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
  • Protein Science, Vol. 8, Issue 5
  • DOI: 10.1110/ps.8.5.978

STAR: ultrafast universal RNA-seq aligner
journal, October 2012


Evidence for a Role of VIPP1 in the Structural Organization of the Photosynthetic Apparatus in Chlamydomonas
journal, February 2012

  • Nordhues, André; Schöttler, Mark Aurel; Unger, Ann-Katrin
  • The Plant Cell, Vol. 24, Issue 2
  • DOI: 10.1105/tpc.111.092692

Thiamine biosynthesis in algae is regulated by riboswitches
journal, December 2007

  • Croft, M. T.; Moulin, M.; Webb, M. E.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 52
  • DOI: 10.1073/pnas.0705786105

Isolation and Characterization of Chlamydomonas Autophagy-Related Mutants in Nutrient-Deficient Conditions
journal, October 2018

  • Kajikawa, Masataka; Yamauchi, Marika; Shinkawa, Haruka
  • Plant and Cell Physiology, Vol. 60, Issue 1
  • DOI: 10.1093/pcp/pcy193

A genome-wide algal mutant library and functional screen identifies genes required for eukaryotic photosynthesis
journal, March 2019


A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle
journal, May 2016

  • Mackinder, Luke C. M.; Meyer, Moritz T.; Mettler-Altmann, Tabea
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 21
  • DOI: 10.1073/pnas.1522866113

Cellular Fractionation of Chlamydomonas reinhardii with Emphasis on the Isolation of the Chloroplast
journal, June 1983

  • Klein, Uwe; Chen, Changguo; Gibbs, Martin
  • Plant Physiology, Vol. 72, Issue 2
  • DOI: 10.1104/pp.72.2.481

The mitochondrial UPR: mechanisms, physiological functions and implications in ageing
journal, November 2017

  • Shpilka, Tomer; Haynes, Cole M.
  • Nature Reviews Molecular Cell Biology, Vol. 19, Issue 2
  • DOI: 10.1038/nrm.2017.110

Downregulation of ClpR2 Leads to Reduced Accumulation of the ClpPRS Protease Complex and Defects in Chloroplast Biogenesis in Arabidopsis
journal, June 2006

  • Rudella, Andrea; Friso, Giulia; Alonso, Jose M.
  • The Plant Cell, Vol. 18, Issue 7
  • DOI: 10.1105/tpc.106.042861

The Central Role of a SNRK2 Kinase in Sulfur Deprivation Responses
journal, March 2008

  • Gonzalez-Ballester, David; Pollock, Steve V.; Pootakham, Wirulda
  • Plant Physiology, Vol. 147, Issue 1
  • DOI: 10.1104/pp.108.116137

Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA
journal, December 2003


Low Density Membranes Are Associated with RNA-binding Proteins and Thylakoids in the Chloroplast of Chlamydomonas reinhardtii
journal, January 1998

  • Zerges, William; Rochaix, Jean-David
  • The Journal of Cell Biology, Vol. 140, Issue 1
  • DOI: 10.1083/jcb.140.1.101

SIMcheck: a Toolbox for Successful Super-resolution Structured Illumination Microscopy
journal, November 2015

  • Ball, Graeme; Demmerle, Justin; Kaufmann, Rainer
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep15915

NIH Image to ImageJ: 25 years of image analysis
journal, June 2012

  • Schneider, Caroline A.; Rasband, Wayne S.; Eliceiri, Kevin W.
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2089

Light stress and photoprotection in Chlamydomonas reinhardtii
journal, March 2015

  • Erickson, Erika; Wakao, Setsuko; Niyogi, Krishna K.
  • The Plant Journal, Vol. 82, Issue 3
  • DOI: 10.1111/tpj.12825

Impaired PSII proteostasis triggers a UPR-like response in the var2 mutant of Arabidopsis
journal, April 2019

  • Dogra, Vivek; Duan, Jianli; Lee, Keun Pyo
  • Journal of Experimental Botany, Vol. 70, Issue 12
  • DOI: 10.1093/jxb/erz151

Interference with Clp protease impairs carotenoid accumulation during tomato fruit ripening
journal, January 2018

  • D’Andrea, Lucio; Simon-Moya, Miguel; Llorente, Briardo
  • Journal of Experimental Botany, Vol. 69, Issue 7
  • DOI: 10.1093/jxb/erx491

Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal
journal, June 2013

  • Yamano, Takashi; Iguchi, Hiro; Fukuzawa, Hideya
  • Journal of Bioscience and Bioengineering, Vol. 115, Issue 6
  • DOI: 10.1016/j.jbiosc.2012.12.020

Repression of Essential Chloroplast Genes Reveals New Signaling Pathways and Regulatory Feedback Loops in Chlamydomonas
journal, January 2013

  • Ramundo, Silvia; Rahire, Michèle; Schaad, Olivier
  • The Plant Cell, Vol. 25, Issue 1
  • DOI: 10.1105/tpc.112.103051

Genome-wide analysis on Chlamydomonas reinhardtii reveals the impact of hydrogen peroxide on protein stress responses and overlap with other stress transcriptomes
journal, December 2015

  • Blaby, Ian K.; Blaby-Haas, Crysten E.; Pérez-Pérez, María Esther
  • The Plant Journal, Vol. 84, Issue 5
  • DOI: 10.1111/tpj.13053

Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes
journal, July 2018

  • Iwai, Masakazu; Roth, Melissa S.; Niyogi, Krishna K.
  • The Plant Journal, Vol. 96, Issue 1
  • DOI: 10.1111/tpj.14021

The Intracellular Localization of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase in Chlamydomonas reinhardtii
journal, April 1998

  • Borkhsenious, Olga N.; Mason, Catherine B.; Moroney, James V.
  • Plant Physiology, Vol. 116, Issue 4
  • DOI: 10.1104/pp.116.4.1585

mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes
journal, March 2004


edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


A rapid procedure for selective enrichment of photosynthetic electron transport mutants.
journal, February 1977

  • Schmidt, G. W.; Matlin, K. S.; Chua, N. H.
  • Proceedings of the National Academy of Sciences, Vol. 74, Issue 2
  • DOI: 10.1073/pnas.74.2.610

The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote
journal, April 2013

  • Liao, Yang; Smyth, Gordon K.; Shi, Wei
  • Nucleic Acids Research, Vol. 41, Issue 10
  • DOI: 10.1093/nar/gkt214

Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond
journal, April 2016


RNA-Seq Analysis of Sulfur-Deprived Chlamydomonas Cells Reveals Aspects of Acclimation Critical for Cell Survival
journal, June 2010

  • González-Ballester, David; Casero, David; Cokus, Shawn
  • The Plant Cell, Vol. 22, Issue 6
  • DOI: 10.1105/tpc.109.071167

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

  • Rütgers, Mark; Muranaka, Ligia Segatto; Mühlhaus, Timo
  • Plant Molecular Biology, Vol. 95, Issue 6
  • DOI: 10.1007/s11103-017-0672-y

Chloroplast Damage Induced by the Inhibition of Fatty Acid Synthesis Triggers Autophagy in Chlamydomonas
journal, September 2018

  • Heredia-Martínez, Luis Gonzaga; Andrés-Garrido, Ascensión; Martínez-Force, Enrique
  • Plant Physiology, Vol. 178, Issue 3
  • DOI: 10.1104/pp.18.00630

Loss of chloroplast ClpP elicits an autophagy-like response in Chlamydomonas
journal, July 2014

  • Ramundo, Silvia; Rochaix, Jean-David
  • Autophagy, Vol. 10, Issue 9
  • DOI: 10.4161/auto.29960

Chloroplast signaling within, between and beyond cells
journal, October 2015


Identification and functional study of the endoplasmic reticulum stress sensor IRE 1 in Chlamydomonas reinhardtii
journal, March 2018

  • Yamaoka, Yasuyo; Choi, Bae Young; Kim, Hanul
  • The Plant Journal, Vol. 94, Issue 1
  • DOI: 10.1111/tpj.13844

The plastid clpP1 protease gene is essential for plant development
journal, September 2003


Unraveling Vitamin B 12 -Responsive Gene Regulation in Algae
journal, March 2014

  • Helliwell, Katherine E.; Scaife, Mark A.; Sasso, Severin
  • Plant Physiology, Vol. 165, Issue 1
  • DOI: 10.1104/pp.113.234369

The Chlamydomonas chloroplast clpP gene contains translated large insertion sequences and is essential for cell growth
journal, January 1994

  • Huang, Changzhi; Wang, Shenglong; Chen, Ling
  • MGG Molecular & General Genetics, Vol. 244, Issue 2
  • DOI: 10.1007/BF00283516

The Unfolded Protein Response: From Stress Pathway to Homeostatic Regulation
journal, November 2011


Insights into the Survival of Chlamydomonas reinhardtii during Sulfur Starvation Based on Microarray Analysis of Gene Expression
journal, October 2004


An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii
journal, January 2016

  • Li, Xiaobo; Zhang, Ru; Patena, Weronika
  • The Plant Cell, Vol. 28, Issue 2
  • DOI: 10.1105/tpc.15.00465

Evidence for a Role of ClpP in the Degradation of the Chloroplast Cytochrome b 6 f Complex
journal, January 2000

  • Majeran, Wojciech; Wollman, Francis-Andre; Vallon, Olivier
  • The Plant Cell, Vol. 12, Issue 1
  • DOI: 10.2307/3871035

Mutants of Chlamydomonas with Aberrant Responses to Sulfur Deprivation
journal, January 1994

  • Davies, John P.; Yildiz, Fitnat; Grossman, Arthur R.
  • The Plant Cell, Vol. 6, Issue 1
  • DOI: 10.2307/3869674

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Identification and Regulation of Plasma Membrane Sulfate Transporters in Chlamydomonas
journal, May 2010

  • Pootakham, Wirulda; Gonzalez-Ballester, David; Grossman, Arthur R.
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.157875

Eleven Golden Rules of Quantitative RT-PCR
journal, July 2008

  • Udvardi, Michael K.; Czechowski, Tomasz; Scheible, Wolf-Rüdiger
  • The Plant Cell, Vol. 20, Issue 7
  • DOI: 10.1105/tpc.108.061143

Transcriptional profiling of two contrasting genotypes uncovers molecular mechanisms underlying salt tolerance in alfalfa
journal, March 2021


Mutants of Chlamydomonas with Aberrant Responses to Sulfur Deprivation.
journal, January 1994


Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis
journal, September 2020


A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle.
text, January 2016

  • Mackinder, Luke CM; Meyer, Moritz; Mettler-Altmann, Tabea
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.23023

Works referencing / citing this record:

How chloroplasts protect themselves from unfolded proteins
journal, October 2019