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

Title: Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS

Abstract

Photosynthetic organisms use nonphotochemical quenching (NPQ) mechanisms to dissipate excess absorbed light energy and protect themselves from photooxidation. In the model green algaChlamydomonas reinhardtii, the capacity for rapidly reversible NPQ (qE) is induced by high light, blue light, and UV light via increased expression ofLHCSRandPSBSgenes that are necessary for qE. Here, we used a forward genetics approach to identify SPA1 and CUL4, components of a putative green algal E3 ubiquitin ligase complex, as critical factors in a signaling pathway that controls light-regulated expression of theLHCSRandPSBSgenes inC. reinhardtii. Thespa1andcul4mutants accumulate increased levels of LHCSR1 and PSBS proteins in high light, and unlike the wild type, they express LHCSR1 and exhibit qE capacity even when grown in low light. Thespa1-1mutation resulted in constitutively high expression ofLHCSRandPSBSRNAs in both low light and high light. The qE and gene expression phenotypes ofspa1-1are blocked by mutation of CrCO, a B-box Zn-finger transcription factor that is a homolog of CONSTANS, which controls flowering time in plants. CONSTANS-likecis-regulatory sequences were identified proximal to the qE genes, consistent with CrCO acting as a direct activator of qE gene expression. We conclude that SPA1 and CUL4 are components of a conserved E3 ubiquitin ligase that acts upstream of CrCO,more » whose regulatory function is wired differently inC. reinhardtiito control qE capacity viacis-regulatory CrCO-binding sites at key photoprotection genes.« less

Authors:
; ; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH)
OSTI Identifier:
1565995
Alternate Identifier(s):
OSTI ID: 1572044
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 35; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; light harvesting; light signaling; nonphotochemical quenching; photomorphogenesis; photosynthesis

Citation Formats

Gabilly, Stéphane T., Baker, Christopher R., Wakao, Setsuko, Crisanto, Thien, Guan, Katharine, Bi, Ke, Guiet, Elodie, Guadagno, Carmela R., and Niyogi, Krishna K. Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. United States: N. p., 2019. Web. doi:10.1073/pnas.1821689116.
Gabilly, Stéphane T., Baker, Christopher R., Wakao, Setsuko, Crisanto, Thien, Guan, Katharine, Bi, Ke, Guiet, Elodie, Guadagno, Carmela R., & Niyogi, Krishna K. Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS. United States. https://doi.org/10.1073/pnas.1821689116
Gabilly, Stéphane T., Baker, Christopher R., Wakao, Setsuko, Crisanto, Thien, Guan, Katharine, Bi, Ke, Guiet, Elodie, Guadagno, Carmela R., and Niyogi, Krishna K. Mon . "Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS". United States. https://doi.org/10.1073/pnas.1821689116.
@article{osti_1565995,
title = {Regulation of photoprotection gene expression in Chlamydomonas by a putative E3 ubiquitin ligase complex and a homolog of CONSTANS},
author = {Gabilly, Stéphane T. and Baker, Christopher R. and Wakao, Setsuko and Crisanto, Thien and Guan, Katharine and Bi, Ke and Guiet, Elodie and Guadagno, Carmela R. and Niyogi, Krishna K.},
abstractNote = {Photosynthetic organisms use nonphotochemical quenching (NPQ) mechanisms to dissipate excess absorbed light energy and protect themselves from photooxidation. In the model green algaChlamydomonas reinhardtii, the capacity for rapidly reversible NPQ (qE) is induced by high light, blue light, and UV light via increased expression ofLHCSRandPSBSgenes that are necessary for qE. Here, we used a forward genetics approach to identify SPA1 and CUL4, components of a putative green algal E3 ubiquitin ligase complex, as critical factors in a signaling pathway that controls light-regulated expression of theLHCSRandPSBSgenes inC. reinhardtii. Thespa1andcul4mutants accumulate increased levels of LHCSR1 and PSBS proteins in high light, and unlike the wild type, they express LHCSR1 and exhibit qE capacity even when grown in low light. Thespa1-1mutation resulted in constitutively high expression ofLHCSRandPSBSRNAs in both low light and high light. The qE and gene expression phenotypes ofspa1-1are blocked by mutation of CrCO, a B-box Zn-finger transcription factor that is a homolog of CONSTANS, which controls flowering time in plants. CONSTANS-likecis-regulatory sequences were identified proximal to the qE genes, consistent with CrCO acting as a direct activator of qE gene expression. We conclude that SPA1 and CUL4 are components of a conserved E3 ubiquitin ligase that acts upstream of CrCO, whose regulatory function is wired differently inC. reinhardtiito control qE capacity viacis-regulatory CrCO-binding sites at key photoprotection genes.},
doi = {10.1073/pnas.1821689116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 35,
volume = 116,
place = {United States},
year = {Mon Aug 12 00:00:00 EDT 2019},
month = {Mon Aug 12 00:00:00 EDT 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1821689116

Citation Metrics:
Cited by: 19 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

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


Cutadapt removes adapter sequences from high-throughput sequencing reads
journal, May 2011


Light-Activated Phytochrome A and B Interact with Members of the SPA Family to Promote Photomorphogenesis in Arabidopsis by Reorganizing the COP1/SPA Complex
journal, January 2015

  • Sheerin, David J.; Menon, Chiara; zur Oven-Krockhaus, Sven
  • The Plant Cell, Vol. 27, Issue 1
  • DOI: 10.1105/tpc.114.134775

Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
journal, August 1970


Regulation of Light Harvesting in the Green Alga Chlamydomonas reinhardtii : The C-Terminus of LHCSR Is the Knob of a Dimmer Switch
journal, November 2013

  • Liguori, Nicoletta; Roy, Laura M.; Opacic, Milena
  • Journal of the American Chemical Society, Vol. 135, Issue 49
  • DOI: 10.1021/ja4107463

A blue-light photoreceptor mediates the feedback regulation of photosynthesis
journal, September 2016

  • Petroutsos, Dimitris; Tokutsu, Ryutaro; Maruyama, Shinichiro
  • Nature, Vol. 537, Issue 7621
  • DOI: 10.1038/nature19358

Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light
journal, April 2011


The functional divergence between SPA1 and SPA2 in Arabidopsis photomorphogenesis maps primarily to the respective N-terminal kinase-like domain
journal, July 2016


Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids
journal, April 1984


An ancient light-harvesting protein is critical for the regulation of algal photosynthesis
journal, November 2009

  • Peers, Graham; Truong, Thuy B.; Ostendorf, Elisabeth
  • Nature, Vol. 462, Issue 7272
  • DOI: 10.1038/nature08587

Super deduper, fast PCR duplicate detection in fastq files
conference, January 2015

  • Petersen, Kristen R.; Streett, David A.; Gerritsen, Alida T.
  • Proceedings of the 6th ACM Conference on Bioinformatics, Computational Biology and Health Informatics - BCB '15
  • DOI: 10.1145/2808719.2811568

COP1-Mediated Ubiquitination of CONSTANS Is Implicated in Cryptochrome Regulation of Flowering in Arabidopsis
journal, February 2008


SPA proteins: SPAnning the gap between visible light and gene expression
journal, April 2016


Chlamydomonas CONSTANS and the Evolution of Plant Photoperiodic Signaling
journal, March 2009


Photoprotective Energy Dissipation Involves the Reorganization of Photosystem II Light-Harvesting Complexes in the Grana Membranes of Spinach Chloroplasts
journal, April 2011

  • Johnson, Matthew P.; Goral, Tomasz K.; Duffy, Christopher D. P.
  • The Plant Cell, Vol. 23, Issue 4
  • DOI: 10.1105/tpc.110.081646

The xanthophyll cycle affects reversible interactions between PsbS and light-harvesting complex II to control non-photochemical quenching
journal, January 2017


Conversion from CUL4-based COP1-SPA E3 apparatus to UVR8-COP1-SPA complexes underlies a distinct biochemical function of COP1 under UV-B
journal, September 2013

  • Huang, X.; Ouyang, X.; Yang, P.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
  • DOI: 10.1073/pnas.1316622110

Regulation of Light Harvesting in Green Plants
journal, June 1996

  • Horton, P.; Ruban, A. V.; Walters, R. G.
  • Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
  • DOI: 10.1146/annurev.arplant.47.1.655

CONSTANS Imparts DNA Sequence Specificity to the Histone Fold NF-YB/NF-YC Dimer
journal, May 2017

  • Gnesutta, Nerina; Kumimoto, Roderick W.; Swain, Swadhin
  • The Plant Cell, Vol. 29, Issue 6
  • DOI: 10.1105/tpc.16.00864

FLASH: fast length adjustment of short reads to improve genome assemblies
journal, September 2011


Primer3—new capabilities and interfaces
journal, June 2012

  • Untergasser, Andreas; Cutcutache, Ioana; Koressaar, Triinu
  • Nucleic Acids Research, Vol. 40, Issue 15
  • DOI: 10.1093/nar/gks596

UV-B Perception and Acclimation in Chlamydomonas reinhardtii
journal, March 2016

  • Tilbrook, Kimberley; Dubois, Marine; Crocco, Carlos D.
  • The Plant Cell, Vol. 28, Issue 4
  • DOI: 10.1105/tpc.15.00287

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light.
journal, June 2016

  • Tibiletti, Tania; Auroy, Pascaline; Peltier, Gilles
  • Plant Physiology
  • DOI: 10.1104/pp.16.00572

PsbS interactions involved in the activation of energy dissipation in Arabidopsis
journal, February 2016

  • Correa-Galvis, Viviana; Poschmann, Gereon; Melzer, Michael
  • Nature Plants, Vol. 2, Issue 2
  • DOI: 10.1038/nplants.2015.225

Blue Light-Dependent Interaction of CRY2 with SPA1 Regulates COP1 activity and Floral Initiation in Arabidopsis
journal, May 2011


Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching
journal, March 2013

  • Wilk, L.; Grunwald, M.; Liao, P. -N.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
  • DOI: 10.1073/pnas.1205561110

Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response
journal, April 2008

  • Jang, Seonghoe; Marchal, Virginie; Panigrahi, Kishore C. S.
  • The EMBO Journal, Vol. 27, Issue 8
  • DOI: 10.1038/emboj.2008.68

The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
journal, October 2007

  • Merchant, S. S.; Prochnik, S. E.; Vallon, O.
  • Science, Vol. 318, Issue 5848, p. 245-250
  • DOI: 10.1126/science.1143609

The photomorphogenic repressors COP1 and DET1: 20 years later
journal, October 2012


Photoreceptor-dependent regulation of photoprotection
journal, June 2017


Algal photoprotection is regulated by the E3 ligase CUL4–DDB1DET1
journal, December 2018


MEME SUITE: tools for motif discovery and searching
journal, May 2009

  • Bailey, T. L.; Boden, M.; Buske, F. A.
  • Nucleic Acids Research, Vol. 37, Issue Web Server
  • DOI: 10.1093/nar/gkp335

A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts
journal, October 1979

  • Briantais, J. -M.; Vernotte, C.; Picaud, M.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 548, Issue 1
  • DOI: 10.1016/0005-2728(79)90193-2

The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling
journal, June 2017


Non-Photochemical Quenching. A Response to Excess Light Energy
journal, April 2001

  • Müller, Patricia; Li, Xiao-Ping; Niyogi, Krishna K.
  • Plant Physiology, Vol. 125, Issue 4
  • DOI: 10.1104/pp.125.4.1558

CONSTITUTIVELY PHOTOMORPHOGENIC1 Is Required for the UV-B Response in Arabidopsis
journal, July 2006

  • Oravecz, Attila; Baumann, Alexander; Máté, Zoltán
  • The Plant Cell, Vol. 18, Issue 8
  • DOI: 10.1105/tpc.105.040097

The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


A Flavin Binding Cryptochrome Photoreceptor Responds to Both Blue and Red Light in Chlamydomonas reinhardtii
journal, July 2012


UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii
journal, December 2016

  • Allorent, Guillaume; Lefebvre-Legendre, Linnka; Chappuis, Richard
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 51
  • DOI: 10.1073/pnas.1607695114

Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching
journal, August 1997

  • Niyogi, Krishna K.; Bjorkman, Olle; Grossman, Arthur R.
  • The Plant Cell, Vol. 9, Issue 8
  • DOI: 10.2307/3870388

Red-Light-Dependent Interaction of phyB with SPA1 Promotes COP1–SPA1 Dissociation and Photomorphogenic Development in Arabidopsis
journal, March 2015


Analysis of LhcSR3, a Protein Essential for Feedback De-Excitation in the Green Alga Chlamydomonas reinhardtii
journal, January 2011


A Plant Cryptochrome Controls Key Features of the Chlamydomonas Circadian Clock and Its Life Cycle
journal, March 2017

  • Müller, Nico; Wenzel, Sandra; Zou, Yong
  • Plant Physiology, Vol. 174, Issue 1
  • DOI: 10.1104/pp.17.00349

Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism
journal, April 2011

  • Lian, H. -L.; He, S. -B.; Zhang, Y. -C.
  • Genes & Development, Vol. 25, Issue 10
  • DOI: 10.1101/gad.2025111

Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
journal, June 2008


Photoreceptor-mediated regulation of the COP1/SPA E3 ubiquitin ligase
journal, October 2018