LCI1, a Chlamydomonas reinhardtii plasma membrane protein, functions in active CO 2 uptake under low CO 2

Kono, Alfredo; Spalding, Martin H.

doi:10.1111/tpj.14761

Title: LCI1, a Chlamydomonas reinhardtii plasma membrane protein, functions in active CO ₂ uptake under low CO ₂

Journal Article · Mon Apr 27 00:00:00 EDT 2020 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.14761· OSTI ID:1616228

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Department of Genetics, Development, and Cell Biology Iowa State University Ames IA 50011 USA

Summary In response to high CO ₂ environmental variability, green algae, such as Chlamydomonas reinhardtii , have evolved multiple physiological states dictated by external CO ₂ concentration. Genetic and physiological studies demonstrated that at least three CO ₂ physiological states, a high CO ₂ (0.5–5% CO ₂ ), a low CO ₂ (0.03–0.4% CO ₂ ) and a very low CO ₂ (< 0.02% CO ₂ ) state, exist in Chlamydomonas . To acclimate in the low and very low CO ₂ states, Chlamydomonas induces a sophisticated strategy known as a CO ₂ ‐concentrating mechanism (CCM) that enables proliferation and survival in these unfavorable CO ₂ environments. Active uptake of C _i from the environment is a fundamental aspect in the Chlamydomonas CCM, and consists of CO ₂ and HCO ₃ ^– uptake systems that play distinct roles in low and very low CO ₂ acclimation states. LCI1, a putative plasma membrane C _i transporter, has been linked through conditional overexpression to active C _i uptake. However, both the role of LCI1 in various CO ₂ acclimation states and the species of C _i , HCO ₃ ^– or CO ₂ , that LCI1 transports remain obscure. Here we report the impact of an LCI1 loss‐of‐function mutant on growth and photosynthesis in different genetic backgrounds at multiple pH values. These studies show that LCI1 appears to be associated with active CO ₂ uptake in low CO ₂ , especially above air‐level CO ₂ , and that any LCI1 role in very low CO ₂ is minimal.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: DEFG02–12ER16335

OSTI ID:: 1616228

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Vol. 102 Journal Issue: 6; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 15 works

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References (32)

Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Gorman, D. S.; Levine, R. P. Proceedings of the National Academy of Sciences, Vol. 54, Issue 6 https://doi.org/10.1073/pnas.54.6.1665	journal	December 1965
LCIB in the Chlamydomonas CO2-concentrating mechanism Wang, Yingjun; Spalding, Martin H. Photosynthesis Research, Vol. 121, Issue 2-3 https://doi.org/10.1007/s11120-013-9956-5	journal	December 2013
Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO ₂ concentrations and CO ₂ /O ₂ ratios: CO ₂ regulates multiple acclimation states Vance, Peter; Spalding, Martin H. Canadian Journal of Botany, Vol. 83, Issue 7 https://doi.org/10.1139/b05-064	journal	July 2005
Structural insights into the LCIB protein family reveals a new group of β-carbonic anhydrases Jin, Shengyang; Sun, Jian; Wunder, Tobias Proceedings of the National Academy of Sciences, Vol. 113, Issue 51 https://doi.org/10.1073/pnas.1616294113	journal	December 2016
Light and Low-CO2-Dependent LCIB–LCIC Complex Localization in the Chloroplast Supports the Carbon-Concentrating Mechanism in Chlamydomonas reinhardtii Yamano, Takashi; Tsujikawa, Tomoki; Hatano, Kyoko Plant and Cell Physiology, Vol. 51, Issue 9 https://doi.org/10.1093/pcp/pcq105	journal	July 2010
Thylakoid Lumen Carbonic Anhydrase ( CAH3 ) Mutation Suppresses Air-Dier Phenotype of LCIB Mutant in Chlamydomonas reinhardtii Duanmu, Deqiang; Wang, Yingjun; Spalding, Martin H. Plant Physiology, Vol. 149, Issue 2 https://doi.org/10.1104/pp.108.132456	journal	December 2008
Knockdown of limiting-CO2-induced gene HLA3 decreases HCOFormula transport and photosynthetic Ci affinity in Chlamydomonas reinhardtii Duanmu, D.; Miller, A. R.; Horken, K. M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 14 https://doi.org/10.1073/pnas.0812885106	journal	March 2009
Portrait of a Species Pröschold, Thomas; Harris, Elizabeth H.; Coleman, Annette W. Genetics, Vol. 170, Issue 4 https://doi.org/10.1534/genetics.105.044503	journal	June 2005
The Chlamydomonas CO ₂ -concentrating mechanism and its potential for engineering photosynthesis in plants Mackinder, Luke C. M. New Phytologist, Vol. 217, Issue 1 https://doi.org/10.1111/nph.14749	journal	August 2017
Microalgal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters Spalding, M. H. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/erm128	journal	June 2007
Inheritance in the Green alga Chlamydomonas Reinhardi Sager, Ruth Genetics, Vol. 40, Issue 4 https://doi.org/10.1093/genetics/40.4.476	journal	July 1955
Thylakoid localized bestrophin-like proteins are essential for the CO ₂ concentrating mechanism of Chlamydomonas reinhardtii Mukherjee, Ananya; Lau, Chun Sing; Walker, Charlotte E. Proceedings of the National Academy of Sciences, Vol. 116, Issue 34 https://doi.org/10.1073/pnas.1909706116	journal	August 2019
An inorganic carbon transport system responsible for acclimation specific to air levels of CO2 in Chlamydomonas reinhardtii Wang, Y.; Spalding, M. H. Proceedings of the National Academy of Sciences, Vol. 103, Issue 26 https://doi.org/10.1073/pnas.0603402103	journal	June 2006
Active CO ₂ Transport by the Green Alga Chlamydomonas reinhardtii Sültemeyer, Dieter F.; Miller, Anthony G.; Espie, George S. Plant Physiology, Vol. 89, Issue 4 https://doi.org/10.1104/pp.89.4.1213	journal	April 1989
Post-translational processing of the highly processed, secreted periplasmic carbonic anhydrase of Chlamydomonas is largely conserved in transgenic tobacco Roberts, Cyril S.; Spalding, Martin H. Plant Molecular Biology, Vol. 29, Issue 2 https://doi.org/10.1007/BF00043654	journal	October 1995
Insertional Mutants of Chlamydomonas reinhardtii That Require Elevated CO ₂ for Survival Van, Kyujung; Wang, Yingjun; Nakamura, Yoshiko Plant Physiology, Vol. 127, Issue 2 https://doi.org/10.1104/pp.010333	journal	October 2001
Characterization of cooperative bicarbonate uptake into chloroplast stroma in the green alga Chlamydomonas reinhardtii Yamano, Takashi; Sato, Emi; Iguchi, Hiro Proceedings of the National Academy of Sciences, Vol. 112, Issue 23 https://doi.org/10.1073/pnas.1501659112	journal	May 2015
The evolution of inorganic carbon concentrating mechanisms in photosynthesis Raven, John A.; Cockell, Charles S.; De La Rocha, Christina L. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504 https://doi.org/10.1098/rstb.2008.0020	journal	May 2008
Reduced Inorganic Carbon Transport in a CO ₂ -Requiring Mutant of Chlamydomonas reinhardii Spalding, Martin H.; Spreitzer, Robert J.; Ogren, William L. Plant Physiology, Vol. 73, Issue 2 https://doi.org/10.1104/pp.73.2.273	journal	October 1983
The CO ₂ concentrating mechanism and photosynthetic carbon assimilation in limiting CO ₂ : how Chlamydomonas works against the gradient Wang, Yingjun; Stessman, Dan J.; Spalding, Martin H. The Plant Journal, Vol. 82, Issue 3 https://doi.org/10.1111/tpj.12829	journal	March 2015
Acclimation to Very Low CO ₂ : Contribution of Limiting CO ₂ Inducible Proteins, LCIB and LCIA, to Inorganic Carbon Uptake in Chlamydomonas reinhardtii Wang, Yingjun; Spalding, Martin H. Plant Physiology, Vol. 166, Issue 4 https://doi.org/10.1104/pp.114.248294	journal	October 2014
A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism Mackinder, Luke C. M.; Chen, Chris; Leib, Ryan D. Cell, Vol. 171, Issue 1 https://doi.org/10.1016/j.cell.2017.08.044	journal	September 2017
Chlamydomonas (Chlorophyceae) colony PCR Cao, Muqing; Fu, Yu; Guo, Yan Protoplasma, Vol. 235, Issue 1-4 https://doi.org/10.1007/s00709-009-0036-9	journal	February 2009
Isolation of cDNA clones of genes induced upon transfer of Chlamydomonas reinhardtii cells to low CO2 Burow, Mark D.; Chen, Zhi-Yuan; Mouton, Tricia M. Plant Molecular Biology, Vol. 31, Issue 2 https://doi.org/10.1007/BF00021807	journal	May 1996
An Indexed, Mapped Mutant Library Enables Reverse Genetics Studies of Biological Processes in Chlamydomonas reinhardtii Li, Xiaobo; Zhang, Ru; Patena, Weronika The Plant Cell, Vol. 28, Issue 2 https://doi.org/10.1105/tpc.15.00465	journal	January 2016
Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC6803 Shibata, Mari; Ohkawa, Hiroshi; Katoh, Hirokazu Functional Plant Biology, Vol. 29, Issue 3 https://doi.org/10.1071/PP01188	journal	January 2002
Active uptake of inorganic carbon by Chlamydomonas reinhardtii : evidence for simultaneous transport of HCO ₃ ⁻ and CO ₂ and characterization of active CO ₂ transport Sültemeyer, Dieter F.; Fock, Heinrich P.; Canvin, David T. Canadian Journal of Botany, Vol. 69, Issue 5 https://doi.org/10.1139/b91-128	journal	May 1991
A short history of RubisCO: the rise and fall (?) of Nature's predominant CO2 fixing enzyme Erb, Tobias J.; Zarzycki, Jan Current Opinion in Biotechnology, Vol. 49 https://doi.org/10.1016/j.copbio.2017.07.017	journal	February 2018
Expression of a Low CO ₂ –Inducible Protein, LCI1, Increases Inorganic Carbon Uptake in the Green Alga Chlamydomonas reinhardtii Ohnishi, Norikazu; Mukherjee, Bratati; Tsujikawa, Tomoki The Plant Cell, Vol. 22, Issue 9 https://doi.org/10.1105/tpc.109.071811	journal	September 2010
Expression activation and functional analysis of HLA3, a putative inorganic carbon transporter in Chlamydomonas reinhardtii Gao, Han; Wang, Yingjun; Fei, Xiaowen The Plant Journal, Vol. 82, Issue 1 https://doi.org/10.1111/tpj.12788	journal	March 2015
From molecular manipulation of domesticated Chlamydomonas reinhardtii to survival in nature Sasso, Severin; Stibor, Herwig; Mittag, Maria eLife, Vol. 7 https://doi.org/10.7554/eLife.39233	journal	November 2018
Acclimation of Chlamydomonas to changing carbon availability Spalding, Martin H.; Van, Kyujung; Wang, Yingjun Functional Plant Biology, Vol. 29, Issue 3 https://doi.org/10.1071/PP01182	journal	January 2002

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