Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis
Abstract
Metallochaperones traffic copper (Cu+) from its point of entry at the plasma membrane to its destination. In plants, one destination is the chloroplast, which houses plastocyanin, a Cu-dependent electron transfer protein involved in photosynthesis. In this paper, we present a previously unidentified Cu+ chaperone that evolved early in the plant lineage by an alternative-splicing event of the pre-mRNA encoding the chloroplast P-type ATPase in Arabidopsis 1 (PAA1). In several land plants, recent duplication events created a separate chaperone-encoding gene coincident with loss of alternative splicing. The plant-specific Cu+ chaperone delivers Cu+ with specificity for PAA1, which is flipped in the envelope relative to prototypical bacterial ATPases, compatible with a role in Cu+ import into the stroma and consistent with the canonical catalytic mechanism of these enzymes. The ubiquity of the chaperone suggests conservation of this Cu+-delivery mechanism and provides a unique snapshot into the evolution of a Cu+ distribution pathway. Finally, we also provide evidence for an interaction between PAA2, the Cu+-ATPase in thylakoids, and the Cu+-chaperone for Cu/Zn superoxide dismutase (CCS), uncovering a Cu+ network that has evolved to fine-tune Cu+ distribution.
- Authors:
-
- Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry
- Worcester Polytechnic Inst., MA (United States). Dept. of Chemistry and Biochemistry
- Univ. of California, Los Angeles, CA (United States). Dept. of Chemistry and Biochemistry. Inst. of Genomics and Proteomics
- Publication Date:
- Research Org.:
- Univ. of California, Los Angeles, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States); National Science Foundation (NSF)
- Contributing Org.:
- Worcester Polytechnic Inst., MA (United States)
- OSTI Identifier:
- 1348351
- Grant/Contract Number:
- FC02-02ER63421; GM42143; MCB-0743901; GM100753
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Volume: 111; Journal Issue: 50; Journal ID: ISSN 0027-8424
- Publisher:
- National Academy of Sciences, Washington, DC (United States)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 60 APPLIED LIFE SCIENCES; Cu-transfer; inner envelope; metal transporter; Arabidopsis thaliana; Atx1
Citation Formats
Blaby-Haas, Crysten E., Padilla-Benavides, Teresita, Stübe, Roland, Argüello, José M., and Merchant, Sabeeha S. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. United States: N. p., 2014.
Web. doi:10.1073/pnas.1421545111.
Blaby-Haas, Crysten E., Padilla-Benavides, Teresita, Stübe, Roland, Argüello, José M., & Merchant, Sabeeha S. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis. United States. https://doi.org/10.1073/pnas.1421545111
Blaby-Haas, Crysten E., Padilla-Benavides, Teresita, Stübe, Roland, Argüello, José M., and Merchant, Sabeeha S. Tue .
"Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis". United States. https://doi.org/10.1073/pnas.1421545111. https://www.osti.gov/servlets/purl/1348351.
@article{osti_1348351,
title = {Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis},
author = {Blaby-Haas, Crysten E. and Padilla-Benavides, Teresita and Stübe, Roland and Argüello, José M. and Merchant, Sabeeha S.},
abstractNote = {Metallochaperones traffic copper (Cu+) from its point of entry at the plasma membrane to its destination. In plants, one destination is the chloroplast, which houses plastocyanin, a Cu-dependent electron transfer protein involved in photosynthesis. In this paper, we present a previously unidentified Cu+ chaperone that evolved early in the plant lineage by an alternative-splicing event of the pre-mRNA encoding the chloroplast P-type ATPase in Arabidopsis 1 (PAA1). In several land plants, recent duplication events created a separate chaperone-encoding gene coincident with loss of alternative splicing. The plant-specific Cu+ chaperone delivers Cu+ with specificity for PAA1, which is flipped in the envelope relative to prototypical bacterial ATPases, compatible with a role in Cu+ import into the stroma and consistent with the canonical catalytic mechanism of these enzymes. The ubiquity of the chaperone suggests conservation of this Cu+-delivery mechanism and provides a unique snapshot into the evolution of a Cu+ distribution pathway. Finally, we also provide evidence for an interaction between PAA2, the Cu+-ATPase in thylakoids, and the Cu+-chaperone for Cu/Zn superoxide dismutase (CCS), uncovering a Cu+ network that has evolved to fine-tune Cu+ distribution.},
doi = {10.1073/pnas.1421545111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 50,
volume = 111,
place = {United States},
year = {Tue Dec 02 00:00:00 EST 2014},
month = {Tue Dec 02 00:00:00 EST 2014}
}
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Works referenced in this record:
The transport mechanism of bacterial Cu+-ATPases: distinct efflux rates adapted to different function
journal, January 2011
- Raimunda, Daniel; González-Guerrero, Manuel; Leeber, Blaise W.
- BioMetals, Vol. 24, Issue 3
Copper Delivery by the Copper Chaperone for Chloroplast and Cytosolic Copper/Zinc-Superoxide Dismutases: Regulation and Unexpected Phenotypes in an Arabidopsis Mutant
journal, November 2009
- Cohu, Christopher M.; Abdel-Ghany, Salah E.; Gogolin Reynolds, Kathryn A.
- Molecular Plant, Vol. 2, Issue 6
Cellular distribution of copper to superoxide dismutase involves scaffolding by membranes
journal, December 2013
- Pope, C. R.; De Feo, C. J.; Unger, V. M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 51
The Oligomeric Stromal Proteome of Arabidopsis thaliana Chloroplasts
journal, October 2005
- Peltier, Jean-Benoit; Cai, Yang; Sun, Qi
- Molecular & Cellular Proteomics, Vol. 5, Issue 1
A copper-transporting P-type ATPase found in the thylakoid membrane of the cyanobacterium Synechococcus species PCC7942
journal, July 1994
- Kanamaru, Kengo; Kashiwagi, Seiji; Mizuno, Takeshi
- Molecular Microbiology, Vol. 13, Issue 2
The structure and function of heavy metal transport P1B-ATPases
journal, January 2007
- Argüello, José M.; Eren, Elif; González-Guerrero, Manuel
- BioMetals, Vol. 20, Issue 3-4
Mechanisms of copper homeostasis in bacteria
journal, January 2013
- Argüello, José M.; Raimunda, Daniel; Padilla-Benavides, Teresita
- Frontiers in Cellular and Infection Microbiology, Vol. 3
Copper-transporting P-type ATPases use a unique ion-release pathway
journal, December 2013
- Andersson, Magnus; Mattle, Daniel; Sitsel, Oleg
- Nature Structural & Molecular Biology, Vol. 21, Issue 1
Membrane topology of the Rickettsia prowazekii ATP/ADP translocase revealed by novel dual pho-lac reporters 1 1Edited by G. von Heijne
journal, January 1999
- Alexeyev, Mikhail F.; Winkler, Herbert H.
- Journal of Molecular Biology, Vol. 285, Issue 4
The Mechanism of Cu + Transport ATPases : INTERACTION WITH CU
journal, November 2012
- Padilla-Benavides, Teresita; McCann, Courtney J.; Argüello, José M.
- Journal of Biological Chemistry, Vol. 288, Issue 1
AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7
journal, March 2005
- Abdel-Ghany, Salah E.; Burkhead, Jason L.; Gogolin, Kathryn A.
- FEBS Letters, Vol. 579, Issue 11
Using Sequence Similarity Networks for Visualization of Relationships Across Diverse Protein Superfamilies
journal, February 2009
- Atkinson, Holly J.; Morris, John H.; Ferrin, Thomas E.
- PLoS ONE, Vol. 4, Issue 2
On Allosteric Modulation of P-Type Cu+-ATPases
journal, July 2013
- Mattle, Daniel; Sitsel, Oleg; Autzen, Henriette E.
- Journal of Molecular Biology, Vol. 425, Issue 13
CDD: a Conserved Domain Database for the functional annotation of proteins
journal, November 2010
- Marchler-Bauer, A.; Lu, S.; Anderson, J. B.
- Nucleic Acids Research, Vol. 39, Issue Database
Characterization of a Thermophilic P-type Ag + /Cu + -ATPase from the Extremophile Archaeoglobus fulgidus
journal, December 2001
- Mandal, Atin K.; Cheung, Win D.; Argüello, José M.
- Journal of Biological Chemistry, Vol. 277, Issue 9
Ancestral polyploidy in seed plants and angiosperms
journal, April 2011
- Jiao, Yuannian; Wickett, Norman J.; Ayyampalayam, Saravanaraj
- Nature, Vol. 473, Issue 7345
Phytozome: a comparative platform for green plant genomics
journal, November 2011
- Goodstein, David M.; Shu, Shengqiang; Howson, Russell
- Nucleic Acids Research, Vol. 40, Issue D1
Snow ball earth and the split of Streptophyta and Chlorophyta
journal, April 2013
- Becker, Burkhard
- Trends in Plant Science, Vol. 18, Issue 4
Independent Evolution of Heavy Metal-Associated Domains in Copper Chaperones and Copper-Transporting ATPases
journal, December 2001
- Jordan, I. King; Natale, Darren A.; Koonin, Eugene V.
- Journal of Molecular Evolution, Vol. 53, Issue 6
Biochemistry of Na,K-ATPase
journal, June 2002
- Kaplan, Jack H.
- Annual Review of Biochemistry, Vol. 71, Issue 1
Copper Metallochaperones
journal, June 2010
- Robinson, Nigel J.; Winge, Dennis R.
- Annual Review of Biochemistry, Vol. 79, Issue 1
A folded protein can be transported across the chloroplast envelope and thylakoid membranes.
journal, May 1997
- Clark, S. A.; Theg, S. M.
- Molecular Biology of the Cell, Vol. 8, Issue 5
Structure of the Two Transmembrane Cu + Transport Sites of the Cu + -ATPases
journal, September 2008
- González-Guerrero, Manuel; Eren, Elif; Rawat, Swati
- Journal of Biological Chemistry, Vol. 283, Issue 44
Evolutionary convergence of alternative splicing in ion channels
journal, April 2004
- Copley, Richard R.
- Trends in Genetics, Vol. 20, Issue 4
Crystal structure of a copper-transporting PIB-type ATPase
journal, June 2011
- Gourdon, Pontus; Liu, Xiang-Yu; Skjørringe, Tina
- Nature, Vol. 475, Issue 7354
Cellular copper distribution: a mechanistic systems biology approach
journal, March 2010
- Banci, Lucia; Bertini, Ivano; Cantini, Francesca
- Cellular and Molecular Life Sciences, Vol. 67, Issue 15
Metallochaperone-like genes in Arabidopsis thaliana
journal, January 2010
- Tehseen, Muhammad; Cairns, Narelle; Sherson, Sarah
- Metallomics, Vol. 2, Issue 8
The most C-terminal tri-glycine segment within the polyglycine stretch of the pea Toc75 transit peptide plays a critical role for targeting the protein to the chloroplast outer envelope membrane
journal, April 2006
- Baldwin, Amy J.; Inoue, Kentaro
- FEBS Journal, Vol. 273, Issue 7
Confidence Limits on Phylogenies: An Approach Using the Bootstrap
journal, July 1985
- Felsenstein, Joseph
- Evolution, Vol. 39, Issue 4, p. 783-791
Biochemical characterization and intracellular localization of the Menkes disease protein
journal, November 1996
- Yamaguchi, Y.; Heiny, M. E.; Suzuki, M.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 24
Distinct functional roles of homologous Cu+ efflux ATPases in Pseudomonas aeruginosa: Role of Cu+ transport ATPases in Pseudomonas aeruginosa
journal, October 2010
- González-Guerrero, Manuel; Raimunda, Daniel; Cheng, Xin
- Molecular Microbiology, Vol. 78, Issue 5
Two P-Type ATPases Are Required for Copper Delivery in Arabidopsis thaliana Chloroplasts
journal, March 2005
- Abdel-Ghany, Salah E.; Müller-Moulé, Patricia; Niyogi, Krishna K.
- The Plant Cell, Vol. 17, Issue 4
Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics
journal, May 2004
- Paterson, A. H.; Bowers, J. E.; Chapman, B. A.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 26
Interaction of the copper chaperone HAH1 with the Wilson disease protein is essential for copper homeostasis
journal, November 1999
- Hamza, I.; Schaefer, M.; Klomp, L. W. J.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 23
Protein production by auto-induction in high-density shaking cultures
journal, May 2005
- Studier, F. William
- Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
journal, May 1976
- Bradford, Marion M.
- Analytical Biochemistry, Vol. 72, Issue 1-2
An improved assay for nanomole amounts of inorganic phosphate
journal, November 1979
- Lanzetta, Peter A.; Alvarez, Lawrence J.; Reinach, Peter S.
- Analytical Biochemistry, Vol. 100, Issue 1
Affinity gradients drive copper to cellular destinations
journal, May 2010
- Banci, Lucia; Bertini, Ivano; Ciofi-Baffoni, Simone
- Nature, Vol. 465, Issue 7298
PAA1, a P-Type ATPase of Arabidopsis, Functions in Copper Transport in Chloroplasts
journal, May 2003
- Shikanai, Toshiharu; Müller-Moulé, Patricia; Munekage, Yuri
- The Plant Cell, Vol. 15, Issue 6
Chapter 18 Characterization and Isolation of the Chloroplast Protein Import Machinery
book, January 1995
- Waegemann, Karin; Soll, Jürgen
- Methods in Cell Biology
The ins and outs of algal metal transport
journal, September 2012
- Blaby-Haas, Crysten E.; Merchant, Sabeeha S.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 9
The Copper Chaperone for Superoxide Dismutase
journal, September 1997
- Culotta, Valeria Cizewski; Klomp, Leo W. J.; Strain, Jeffrey
- Journal of Biological Chemistry, Vol. 272, Issue 38
Tic20 forms a channel independent of Tic110 in chloroplasts
journal, January 2011
- Kovács-Bogdán, Erika; Benz, J. Philipp; Soll, Jürgen
- BMC Plant Biology, Vol. 11, Issue 1
High Cu(I) and low proton affinities of the CXXC motif of Bacillus subtilis CopZ
journal, July 2008
- Zhou, Liang; Singleton, Chloe; Le Brun, Nick E.
- Biochemical Journal, Vol. 413, Issue 3
Structural Biology of Copper Trafficking
journal, October 2009
- Boal, Amie K.; Rosenzweig, Amy C.
- Chemical Reviews, Vol. 109, Issue 10
Mechanism of Cu+-transporting ATPases: Soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites
journal, April 2008
- Gonzalez-Guerrero, M.; Arguello, J. M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 16
Characterization of COX17 , a Yeast Gene Involved in Copper Metabolism and Assembly of Cytochrome Oxidase
journal, June 1996
- Glerum, D. Moira; Shtanko, Andrey; Tzagoloff, Alexander
- Journal of Biological Chemistry, Vol. 271, Issue 24
Stress induced and nuclear localized HIPP26 from Arabidopsis thaliana interacts via its heavy metal associated domain with the drought stress related zinc finger transcription factor ATHB29
journal, October 2008
- Barth, Olaf; Vogt, Sebastian; Uhlemann, Ria
- Plant Molecular Biology, Vol. 69, Issue 1-2
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013
- Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
- Molecular Biology and Evolution, Vol. 30, Issue 12
The localization of Tic20 proteins in Arabidopsis thaliana is not restricted to the inner envelope membrane of chloroplasts
journal, August 2011
- Machettira, Anu B.; Gross, Lucia E.; Sommer, Maik S.
- Plant Molecular Biology, Vol. 77, Issue 4-5
A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis: EZ Arabidopsis protein extraction
journal, October 1999
- Martínez-García, Jaime F.; Monte, Elena; Quail, Peter H.
- The Plant Journal, Vol. 20, Issue 2
Caloramator viterbensis sp. nov., a novel thermophilic, glycerol-fermenting bacterium isolated from a hot spring in Italy
journal, July 2002
- Seyfried, M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 52, Issue 4
Role in metal homeostasis of CtpD, a Co2+ transporting P1B4-ATPase of Mycobacterium smegmatis: Mycobacteria Co2+-ATPase
journal, May 2012
- Raimunda, Daniel; Long, Jarukit E.; Sassetti, Christopher M.
- Molecular Microbiology, Vol. 84, Issue 6
A Quantitative Test for Copper Using Bicinchoninic Acid
journal, March 1995
- Brenner, A. J.; Harris, E. D.
- Analytical Biochemistry, Vol. 226, Issue 1
The Reversible Dissociation of the Alkaline Phosphatase of Escherichia coli
journal, November 1965
- Schlesinger, Milton J.; Barrett, Kathleen
- Journal of Biological Chemistry, Vol. 240, Issue 11
Confidence Limits on Phylogenies: an Approach Using the Bootstrap
journal, July 1985
- Felsenstein, Joseph
- Evolution, Vol. 39, Issue 4
Works referencing / citing this record:
Identification of Two Conserved Residues Involved in Copper Release from Chloroplast PIB-1-ATPases
journal, September 2016
- Sautron, Emeline; Giustini, Cécile; Dang, ThuyVan
- Journal of Biological Chemistry, Vol. 291, Issue 38
Specific reverse transcriptase slippage at the HIV ribosomal frameshift sequence: potential implications for modulation of GagPol synthesis
journal, August 2017
- Penno, Christophe; Kumari, Romika; Baranov, Pavel V.
- Nucleic Acids Research, Vol. 45, Issue 17
Temporal aspects of copper homeostasis and its crosstalk with hormones
journal, April 2015
- Peñarrubia, Lola; Romero, Paco; Carrió-Seguí, Angela
- Frontiers in Plant Science, Vol. 6
Copper Trafficking in Plants and Its Implication on Cell Wall Dynamics
journal, May 2016
- Printz, Bruno; Lutts, Stanley; Hausman, Jean-Francois
- Frontiers in Plant Science, Vol. 7
Regulation of Cu delivery to chloroplast proteins
journal, July 2015
- Tapken, Wiebke; Ravet, Karl; Shahbaz, Muhammad
- Plant Signaling & Behavior, Vol. 10, Issue 7
Copper Delivery to Chloroplast Proteins and its Regulation
journal, January 2016
- Aguirre, Guadalupe; Pilon, Marinus
- Frontiers in Plant Science, Vol. 6