RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana
Abstract
Summary Ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBis CO ) catalyzes the reaction between gaseous carbon dioxide ( CO 2 ) and ribulose‐1,5‐bisphosphate. Although it is one of the most studied enzymes, the assembly mechanisms of the large hexadecameric RuBis CO is still emerging. In bacteria and in the C4 plant Zea mays , a protein with distant homology to p terin‐4α‐ c arbinolamine d ehydratase ( PCD ) has recently been shown to be involved in RuBis CO assembly. However, studies of the homologous PCD ‐like protein ( RAF 2, RuBis CO assembly factor 2) in the C3 plant Arabidopsis thaliana ( A . thaliana ) have so far focused on its role in hormone and stress signaling. We investigated whether A . thaliana RAF 2 is also involved in RuBis CO assembly. We localized RAF 2 to the soluble chloroplast stroma and demonstrated that raf2 A . thaliana mutant plants display a severe pale green phenotype with reduced levels of stromal RuBis CO . We concluded that the RAF 2 protein is probably involved in RuBis CO assembly in the C3 plant A . thaliana .
- Authors:
-
- Biophysics of Photosynthesis VU University Amsterdam Amsterdam The Netherlands, Department of Chemistry and Biochemistry and Institute for Genomics and Proteomics UCLA Los Angeles CA USA
- Biophysics of Photosynthesis VU University Amsterdam Amsterdam The Netherlands
- Department of Chemistry and Biochemistry and Institute for Genomics and Proteomics UCLA Los Angeles CA USA
- School of Molecular Sciences and Center for Bioenergy and Photosynthesis Arizona State University Tempe AZ USA
- Department of Energy Plant Research Laboratory Department of Biochemistry and Molecular Biology Michigan State University East Lansing USA
- Horticulture and Product Physiology Group Wageningen University Wageningen The Netherlands
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1432069
- Grant/Contract Number:
- DE‐FG02‐09‐ER16123
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- The Plant Journal
- Additional Journal Information:
- Journal Name: The Plant Journal Journal Volume: 94 Journal Issue: 1; Journal ID: ISSN 0960-7412
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Fristedt, Rikard, Hu, Chen, Wheatley, Nicole, Roy, Laura M., Wachter, Rebekka M., Savage, Linda, Harbinson, Jeremy, Kramer, David M., Merchant, Sabeeha S., Yeates, Todd, and Croce, Roberta. RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana. United Kingdom: N. p., 2018.
Web. doi:10.1111/tpj.13849.
Fristedt, Rikard, Hu, Chen, Wheatley, Nicole, Roy, Laura M., Wachter, Rebekka M., Savage, Linda, Harbinson, Jeremy, Kramer, David M., Merchant, Sabeeha S., Yeates, Todd, & Croce, Roberta. RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana. United Kingdom. https://doi.org/10.1111/tpj.13849
Fristedt, Rikard, Hu, Chen, Wheatley, Nicole, Roy, Laura M., Wachter, Rebekka M., Savage, Linda, Harbinson, Jeremy, Kramer, David M., Merchant, Sabeeha S., Yeates, Todd, and Croce, Roberta. Mon .
"RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana". United Kingdom. https://doi.org/10.1111/tpj.13849.
@article{osti_1432069,
title = {RAF 2 is a RuBis CO assembly factor in Arabidopsis thaliana},
author = {Fristedt, Rikard and Hu, Chen and Wheatley, Nicole and Roy, Laura M. and Wachter, Rebekka M. and Savage, Linda and Harbinson, Jeremy and Kramer, David M. and Merchant, Sabeeha S. and Yeates, Todd and Croce, Roberta},
abstractNote = {Summary Ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBis CO ) catalyzes the reaction between gaseous carbon dioxide ( CO 2 ) and ribulose‐1,5‐bisphosphate. Although it is one of the most studied enzymes, the assembly mechanisms of the large hexadecameric RuBis CO is still emerging. In bacteria and in the C4 plant Zea mays , a protein with distant homology to p terin‐4α‐ c arbinolamine d ehydratase ( PCD ) has recently been shown to be involved in RuBis CO assembly. However, studies of the homologous PCD ‐like protein ( RAF 2, RuBis CO assembly factor 2) in the C3 plant Arabidopsis thaliana ( A . thaliana ) have so far focused on its role in hormone and stress signaling. We investigated whether A . thaliana RAF 2 is also involved in RuBis CO assembly. We localized RAF 2 to the soluble chloroplast stroma and demonstrated that raf2 A . thaliana mutant plants display a severe pale green phenotype with reduced levels of stromal RuBis CO . We concluded that the RAF 2 protein is probably involved in RuBis CO assembly in the C3 plant A . thaliana .},
doi = {10.1111/tpj.13849},
journal = {The Plant Journal},
number = 1,
volume = 94,
place = {United Kingdom},
year = {Mon Mar 12 00:00:00 EDT 2018},
month = {Mon Mar 12 00:00:00 EDT 2018}
}
https://doi.org/10.1111/tpj.13849
Web of Science
Works referenced in this record:
RBF1, a Plant Homolog of the Bacterial Ribosome-Binding Factor RbfA, Acts in Processing of the Chloroplast 16S Ribosomal RNA
journal, November 2013
- Fristedt, R.; Scharff, L. B.; Clarke, C. A.
- PLANT PHYSIOLOGY, Vol. 164, Issue 1
RBCS1A and RBCS3B, two major members within the Arabidopsis RBCS multigene family, function to yield sufficient Rubisco content for leaf photosynthetic capacity
journal, January 2012
- Izumi, Masanori; Tsunoda, Honami; Suzuki, Yuji
- Journal of Experimental Botany, Vol. 63, Issue 5
Rubisco, Rubisco activase, and global climate change
journal, April 2008
- Sage, Rowan F.; Way, Danielle A.; Kubien, David S.
- Journal of Experimental Botany, Vol. 59, Issue 7
Role of auxiliary proteins in Rubisco biogenesis and function
journal, June 2015
- Hauser, Thomas; Popilka, Leonhard; Hartl, F. Ulrich
- Nature Plants, Vol. 1, Issue 6
Structure and Identification of a Pterin Dehydratase-like Protein as a Ribulose-bisphosphate Carboxylase/Oxygenase (RuBisCO) Assembly Factor in the α-Carboxysome
journal, January 2014
- Wheatley, Nicole M.; Sundberg, Christopher D.; Gidaniyan, Soheil D.
- Journal of Biological Chemistry, Vol. 289, Issue 11
Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase
journal, April 1979
- Farquhar, Graham D.
- Archives of Biochemistry and Biophysics, Vol. 193, Issue 2
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
The role of transitory starch in C3, CAM, and C4 metabolism and opportunities for engineering leaf starch accumulation
journal, March 2011
- Weise, Sean E.; van Wijk, Klaas J.; Sharkey, Thomas D.
- Journal of Experimental Botany, Vol. 62, Issue 9
2-Cysteine Peroxiredoxins and Thylakoid Ascorbate Peroxidase Create a Water-Water Cycle That Is Essential to Protect the Photosynthetic Apparatus under High Light Stress Conditions
journal, February 2015
- Awad, Jasmin; Stotz, Henrik U.; Fekete, Agnes
- Plant Physiology, Vol. 167, Issue 4
The chloroplast protein CPSAR1, dually localized in the stroma and the inner envelope membrane, is involved in thylakoid biogenesis: CPSAR1 is involved in thylakoid biogenesis
journal, April 2010
- Garcia, Christel; Khan, Nadir Z.; Nannmark, Ulf
- The Plant Journal
Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes
journal, September 2011
- Järvi, Sari; Suorsa, Marjaana; Paakkarinen, Virpi
- Biochemical Journal, Vol. 439, Issue 2
Dynamic Environmental Photosynthetic Imaging Reveals Emergent Phenotypes
journal, June 2016
- Cruz, Jeffrey A.; Savage, Linda J.; Zegarac, Robert
- Cell Systems, Vol. 2, Issue 6
Redox regulation of the Calvin–Benson cycle: something old, something new
journal, January 2013
- Michelet, Laure; Zaffagnini, Mirko; Morisse, Samuel
- Frontiers in Plant Science, Vol. 4
Molecular Chaperone Functions in Protein Folding and Proteostasis
journal, June 2013
- Kim, Yujin E.; Hipp, Mark S.; Bracher, Andreas
- Annual Review of Biochemistry, Vol. 82, Issue 1
The GreenCut2 Resource, a Phylogenomically Derived Inventory of Proteins Specific to the Plant Lineage
journal, April 2011
- Karpowicz, Steven J.; Prochnik, Simon E.; Grossman, Arthur R.
- Journal of Biological Chemistry, Vol. 286, Issue 24
Biogenesis and Metabolic Maintenance of Rubisco
journal, April 2017
- Bracher, Andreas; Whitney, Spencer M.; Hartl, F. Ulrich
- Annual Review of Plant Biology, Vol. 68, Issue 1
Chloroplast function revealed through analysis of GreenCut2 genes
journal, March 2017
- Fristedt, Rikard
- Journal of Experimental Botany, Vol. 68, Issue 9
Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase from Thermophilic Red Algae with a Strong Specificity for CO2Fixation
journal, April 1997
- Uemura, K.; Miyachi, S.
- Biochemical and Biophysical Research Communications, Vol. 233, Issue 2
Subunit Interface Dynamics in Hexadecameric Rubisco
journal, September 2011
- van Lun, Michiel; van der Spoel, David; Andersson, Inger
- Journal of Molecular Biology, Vol. 411, Issue 5
Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2
journal, December 2017
- Aigner, H.; Wilson, R. H.; Bracher, A.
- Science, Vol. 358, Issue 6368
Assembly chaperones: a perspective
journal, May 2013
- Ellis, R. John
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1617
Phylogenomic analysis of the Chlamydomonas genome unmasks proteins potentially involved in photosynthetic function and regulation
journal, May 2010
- Grossman, Arthur R.; Karpowicz, Steven J.; Heinnickel, Mark
- Photosynthesis Research, Vol. 106, Issue 1-2
Structure and mechanism of the Rubisco-assembly chaperone Raf1
journal, August 2015
- Hauser, Thomas; Bhat, Javaid Y.; Miličić, Goran
- Nature Structural & Molecular Biology, Vol. 22, Issue 9
Ribulose-1,5-Bis-Phosphate Carboxylase/Oxygenase Accumulation Factor1 Is Required for Holoenzyme Assembly in Maize
journal, August 2012
- Feiz, Leila; Williams-Carrier, Rosalind; Wostrikoff, Katia
- The Plant Cell, Vol. 24, Issue 8
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
The GroEL–GroES Chaperonin Machine: A Nano-Cage for Protein Folding
journal, January 2016
- Hayer-Hartl, Manajit; Bracher, Andreas; Hartl, F. Ulrich
- Trends in Biochemical Sciences, Vol. 41, Issue 1
Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response
journal, May 2004
- Wang, Wangxia; Vinocur, Basia; Shoseyov, Oded
- Trends in Plant Science, Vol. 9, Issue 5
The GreenCut: re-evaluation of physiological role of previously studied proteins and potential novel protein functions
journal, July 2013
- Heinnickel, Mark L.; Grossman, Arthur R.
- Photosynthesis Research, Vol. 116, Issue 2-3
Models of Photosynthesis
journal, January 2001
- Farquhar, Graham D.; von Caemmerer, Susanne; Berry, Joseph A.
- Plant Physiology, Vol. 125, Issue 1
AtAIRP2 E3 Ligase Affects ABA and High-Salinity Responses by Stimulating Its ATP1/SDIRIP1 Substrate Turnover
journal, June 2017
- Oh, Tae Rin; Kim, Jong Hum; Cho, Seok Keun
- Plant Physiology, Vol. 174, Issue 4
A faster Rubisco with potential to increase photosynthesis in crops
journal, September 2014
- Lin, Myat T.; Occhialini, Alessandro; Andralojc, P. John
- Nature, Vol. 513, Issue 7519
A Chloroplast-Targeted Heat Shock Protein 70 (HSP70) Contributes to the Photoprotection and Repair of Photosystem II during and after Photoinhibition
journal, June 1999
- Schroda, Michael; Vallon, Olivier; Wollman, Francis-André
- The Plant Cell, Vol. 11, Issue 6
MET1 Is a Thylakoid-Associated TPR Protein Involved in Photosystem II Supercomplex Formation and Repair in Arabidopsis
journal, January 2015
- Bhuiyan, Nazmul H.; Friso, Giulia; Poliakov, Anton
- The Plant Cell, Vol. 27, Issue 1
Chromophore Organization in the Higher-Plant Photosystem II Antenna Protein CP26
journal, June 2002
- Croce, Roberta; Canino, Giusy; Ros, Francesca
- Biochemistry, Vol. 41, Issue 23
Structural Analysis of the Rubisco-Assembly Chaperone RbcX-II from Chlamydomonas reinhardtii
journal, August 2015
- Bracher, Andreas; Hauser, Thomas; Liu, Cuimin
- PLOS ONE, Vol. 10, Issue 8
High Light Induced Disassembly of Photosystem II Supercomplexes in Arabidopsis Requires STN7-Dependent Phosphorylation of CP29
journal, September 2011
- Fristedt, Rikard; Vener, Alexander V.
- PLoS ONE, Vol. 6, Issue 9
Structure and function of Rubisco
journal, March 2008
- Andersson, Inger; Backlund, Anders
- Plant Physiology and Biochemistry, Vol. 46, Issue 3
Effect of Light Acclimation on the Organization of Photosystem II Super- and Sub-Complexes in Arabidopsis thaliana
journal, February 2016
- Bielczynski, Ludwik W.; Schansker, Gert; Croce, Roberta
- Frontiers in Plant Science, Vol. 7
Characterization of the Arabidopsis thaliana 2-Cys peroxiredoxin interactome
journal, November 2016
- Cerveau, Delphine; Kraut, Alexandra; Stotz, Henrik U.
- Plant Science, Vol. 252
A protein with an inactive pterin-4a-carbinolamine dehydratase domain is required for Rubisco biogenesis in plants
journal, November 2014
- Feiz, Leila; Williams-Carrier, Rosalind; Belcher, Susan
- The Plant Journal, Vol. 80, Issue 5
From chaperonins to Rubisco assembly and metabolic repair: Role of Chaperones in Rubisco Biogenesis
journal, October 2017
- Hayer-Hartl, Manajit
- Protein Science, Vol. 26, Issue 12
Phylogenomic and Functional Analysis of Pterin-4a-Carbinolamine Dehydratase Family (COG2154) Proteins in Plants and Microorganisms
journal, February 2008
- Naponelli, Valeria; Noiriel, Alexandre; Ziemak, Michael J.
- Plant Physiology, Vol. 146, Issue 4
Steady-state room temperature fluorescence and CO2 assimilation rates in intact leaves
journal, January 1985
- Sharkey, Thomas D.
- Photosynthesis Research, Vol. 7, Issue 2
Cyanobacterial CO2-concentrating mechanism components: function and prospects for plant metabolic engineering
journal, June 2016
- Long, Benedict M.; Rae, Benjamin D.; Rolland, Vivien
- Current Opinion in Plant Biology, Vol. 31
The RING Finger Ubiquitin E3 Ligase SDIR1 Targets SDIR1-INTERACTING PROTEIN1 for Degradation to Modulate the Salt Stress Response and ABA Signaling in Arabidopsis
journal, January 2015
- Zhang, Huawei; Cui, Feng; Wu, Yaorong
- The Plant Cell, Vol. 27, Issue 1
Functional architecture of higher plant photosystem II supercomplexes
journal, August 2009
- Caffarri, Stefano; Kouřil, Roman; Kereïche, Sami
- The EMBO Journal, Vol. 28, Issue 19
Catalysis and regulation in Rubisco
journal, June 2007
- Andersson, I.
- Journal of Experimental Botany, Vol. 59, Issue 7