REDUCED CHLOROPLAST COVERAGE genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment

Larkin, Robert M.; Stefano, Giovanni; Ruckle, Michael E.; Stavoe, Andrea K.; Sinkler, Christopher A.; Brandizzi, Federica; Malmstrom, Carolyn M.; Osteryoung, Katherine W.

doi:10.1073/pnas.1515741113

Title: REDUCED CHLOROPLAST COVERAGE genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment

Journal Article · Tue Feb 09 00:00:00 EST 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1515741113· OSTI ID:1237516

Larkin, Robert M. ^[1]; Stefano, Giovanni ^[2]; Ruckle, Michael E. ^[3]; Stavoe, Andrea K. ^[2]; Sinkler, Christopher A. ^[2]; Brandizzi, Federica ^[4]; Malmstrom, Carolyn M. ^[5]; Osteryoung, Katherine W. ^[5]

Department of Plant Biology, Michigan State University, East Lansing, MI 48824,, Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824
Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824
Department of Plant Biology, Michigan State University, East Lansing, MI 48824,, Michigan State University-Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
Department of Plant Biology, Michigan State University, East Lansing, MI 48824,

Eukaryotic cells require mechanisms to establish the proportion of cellular volume devoted to particular organelles. These mechanisms are poorly understood. From a screen for plastid-to-nucleus signaling mutants in Arabidopsis thaliana, we cloned a mutant allele of a gene that encodes a protein of unknown function that is homologous to two other Arabidopsis genes of unknown function and Arabidopsis. In contrast to FRIENDLY, these three homologs of FRIENDLY are found only in photosynthetic organisms. Based on these data, we proposed that FRIENDLY expanded into a small gene family to help regulate the energy metabolism of cells that contain both mitochondria and chloroplasts. Indeed, we found that knocking out these genes caused a number of chloroplast phenotypes, including a reduction in the proportion of cellular volume devoted to chloroplasts to 50% of wild type. Thus, we refer to these genes as REDUCED CHLOROPLAST COVERAGE (REC). The size of the chloroplast compartment was reduced most in rec1 mutants. The REC1 protein accumulated in the cytosol and the nucleus. REC1 was excluded from the nucleus when plants were treated with amitrole, which inhibits cell expansion and chloroplast function. Finally, we conclude that REC1 is an extraplastidic protein that helps to establish the size of the chloroplast compartment, and that signals derived from cell expansion or chloroplasts may regulate REC1.

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Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-91ER20021; FG02-06ER15808; NNX12AN71G; MCB-1121943; MCB1243792; IOB 0517841; IOS 1021755

OSTI ID:: 1237516

Alternate ID(s):: OSTI ID: 1348392

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 113 Journal Issue: 8; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 28 works

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References (58)

Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signalling Vinti, Giovanna; Hills, Alison; Campbell, Shona The Plant Journal, Vol. 24, Issue 6 https://doi.org/10.1046/j.1365-313x.2000.00936.x	journal	December 2000
GUN4, a Regulator of Chlorophyll Synthesis and Intracellular Signaling Larkin, R. M. Science, Vol. 299, Issue 5608 https://doi.org/10.1126/science.1079978	journal	February 2003
A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis Terry, Matthew J.; Smith, Alison G. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00014	journal	January 2013
Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II - effects on photosynthesis, grana stacking and fitness Jenny, Andersson; Mark, Wentworth; Robin G., Walters The Plant Journal, Vol. 35, Issue 3 https://doi.org/10.1046/j.1365-313X.2003.01811.x	journal	August 2003
Oxidative Stress: Antagonistic Signaling for Acclimation or Cell Death?: Figure 1. Mullineaux, Philip M.; Baker, Neil R. Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.161406	journal	October 2010
Structural and Functional Discussion of the Tetra-Trico-Peptide Repeat, a Protein Interaction Module Zeytuni, Natalie; Zarivach, Raz Structure, Vol. 20, Issue 3 https://doi.org/10.1016/j.str.2012.01.006	journal	March 2012
SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis Peragine, A. Genes & Development, Vol. 18, Issue 19, p. 2368-2379 https://doi.org/10.1101/gad.1231804	journal	September 2004
FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis El Zawily, A. M.; Schwarzlander, M.; Finkemeier, I. PLANT PHYSIOLOGY, Vol. 166, Issue 2 https://doi.org/10.1104/pp.114.243824	journal	August 2014
Cell and plastid division are coordinated through the prereplication factor AtCDT1 Raynaud, C.; Perennes, C.; Reuzeau, C. Proceedings of the National Academy of Sciences, Vol. 102, Issue 23 https://doi.org/10.1073/pnas.0502564102	journal	May 2005
Hormonal control of cell division and elongation along differentiation trajectories in roots Takatsuka, Hirotomo; Umeda, Masaaki Journal of Experimental Botany, Vol. 65, Issue 10 https://doi.org/10.1093/jxb/ert485	journal	January 2014
A Genetic Analysis of Chloroplast Division and Expansion in Arabidopsis thaliana Pyke, K. A.; Leech, R. M. Plant Physiology, Vol. 104, Issue 1 https://doi.org/10.1104/pp.104.1.201	journal	January 1994
Sternopleural is a Regulatory Mutation of wingless With Both Dominant and Recessive Effects on Larval Development of Drosophila melanogaster Neumann, Carl J.; Cohen, Stephen M. Genetics, Vol. 142, Issue 4 https://doi.org/10.1093/genetics/142.4.1147	journal	April 1996
Rapid Image Analysis Screening Procedure for Identifying Chloroplast Number Mutants in Mesophyll Cells of Arabidopsis thaliana (L.) Heynh. Pyke, Kevin A.; Leech, Rachel M. Plant Physiology, Vol. 96, Issue 4 https://doi.org/10.1104/pp.96.4.1193	journal	August 1991
PDV1 and PDV2 Mediate Recruitment of the Dynamin-Related Protein ARC5 to the Plastid Division Site Miyagishima, Shin-ya; Froehlich, John E.; Osteryoung, Katherine W. The Plant Cell, Vol. 18, Issue 10 https://doi.org/10.1105/tpc.106.045484	journal	September 2006
Functional insights of nucleocytoplasmic transport in plants Tamura, Kentaro; Hara-Nishimura, Ikuko Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00118	journal	April 2014
Plant Cells Without Detectable Plastids are Generated in the crumpled leaf Mutant of Arabidopsis thaliana Chen, Yuling; Asano, Tomoya; Fujiwara, Makoto T. Plant and Cell Physiology, Vol. 50, Issue 5 https://doi.org/10.1093/pcp/pcp047	journal	March 2009
Recent advances in understanding the molecular mechanism of chloroplast photorelocation movement Kong, Sam-Geun; Wada, Masamitsu Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 4 https://doi.org/10.1016/j.bbabio.2013.12.004	journal	April 2014
Chloroplast Division and Expansion Is Radically Altered by Nuclear Mutations in Arabidopsis thaliana Pyke, Kevin A.; Leech, Rachel M. Plant Physiology, Vol. 99, Issue 3 https://doi.org/10.1104/pp.99.3.1005	journal	July 1992
arc6, A Fertile Arabidopsis Mutant with Only Two Mesophyll Cell Chloroplasts Pyke, K. A.; Rutherford, S. M.; Robertson, E. J. Plant Physiology, Vol. 106, Issue 3 https://doi.org/10.1104/pp.106.3.1169	journal	November 1994
Chloroplast Division in Higher Plants Requires Members of Two Functionally Divergent Gene Families with Homology to Bacterial ftsZ Osteryoung, Katherine W.; Stokes, Kevin D.; Rutherford, Stephen M. The Plant Cell, Vol. 10, Issue 12 https://doi.org/10.1105/tpc.10.12.1991	journal	December 1998
Stromules: Recent Insights into a Long Neglected Feature of Plastid Morphology and Function Hanson, Maureen R.; Sattarzadeh, Amirali Plant Physiology, Vol. 155, Issue 4 https://doi.org/10.1104/pp.110.170852	journal	February 2011
Clueless regulates aPKC activity and promotes self-renewal cell fate in Drosophila lgl mutant larval brains Goh, Li Hui; Zhou, Xiu; Lee, Mei Chin Developmental Biology, Vol. 381, Issue 2 https://doi.org/10.1016/j.ydbio.2013.06.031	journal	September 2013
Quantitating the subtleties of microglial morphology with fractal analysis Karperien, Audrey; Ahammer, Helmut; Jelinek, Herbert F. Frontiers in Cellular Neuroscience, Vol. 7 https://doi.org/10.3389/fncel.2013.00003	journal	January 2013
Arabidopsis FtsZ2-1 and FtsZ2-2 Are Functionally Redundant, But FtsZ-Based Plastid Division Is Not Essential for Chloroplast Partitioning or Plant Growth and Development Schmitz, Aaron J.; Glynn, Jonathan M.; Olson, Bradley J. S. C. Molecular Plant, Vol. 2, Issue 6 https://doi.org/10.1093/mp/ssp077	journal	November 2009
From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis Sage, Rowan F.; Khoshravesh, Roxana; Sage, Tammy L. Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru180	journal	May 2014
Insights into chloroplast biogenesis and development Pogson, Barry J.; Ganguly, Diep; Albrecht-Borth, Verónica Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9 https://doi.org/10.1016/j.bbabio.2015.02.003	journal	September 2015
arc6, an extreme chloroplast division mutant of Arabidopsis also alters proplastid proliferation and morphology in shoot and root apices Robertson, E. J.; Pyke, K. A.; Leech, R. M. Journal of Cell Science, Vol. 108, Issue 9 https://doi.org/10.1242/jcs.108.9.2937	journal	September 1995
CLUH regulates mitochondrial biogenesis by binding mRNAs of nuclear-encoded mitochondrial proteins Gao, Jie; Schatton, Désirée; Martinelli, Paola The Journal of Cell Biology, Vol. 207, Issue 2 https://doi.org/10.1083/jcb.201403129	journal	October 2014
Photosynthesis in Arabidopsis thaliana Mutants with Reduced Chloroplast Number Ii, Jotham Austin; Webber, Andrew N. Photosynthesis Research, Vol. 85, Issue 3 https://doi.org/10.1007/s11120-005-7708-x	journal	September 2005
Promotion of chloroplast proliferation upon enhanced post-mitotic cell expansion in leaves Kawade, Kensuke; Horiguchi, Gorou; Ishikawa, Naoko BMC Plant Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2229-13-143	journal	January 2013
Production and Scavenging of Reactive Oxygen Species in Chloroplasts and Their Functions: Figure 1. Asada, Kozi Plant Physiology, Vol. 141, Issue 2 https://doi.org/10.1104/pp.106.082040	journal	June 2006
Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato Cookson, P. J.; Kiano, J. W.; Shipton, C. A. Planta, Vol. 217, Issue 6 https://doi.org/10.1007/s00425-003-1065-9	journal	October 2003
CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis Yang, Y.; Sage, T. L.; Liu, Y. Proceedings of the National Academy of Sciences, Vol. 108, Issue 45 https://doi.org/10.1073/pnas.1106706108	journal	October 2011
Monitoring and screening plant populations with combined thermal and chlorophyll fluorescence imaging Chaerle, Laury; Leinonen, Ilkka; Jones, Hamlyn G. Journal of Experimental Botany, Vol. 58, Issue 4 https://doi.org/10.1093/jxb/erl257	journal	December 2006
GUN4-Porphyrin Complexes Bind the ChlH/GUN5 Subunit of Mg-Chelatase and Promote Chlorophyll Biosynthesis in Arabidopsis Adhikari, Neil D.; Froehlich, John E.; Strand, Deserah D. The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.110.082503	journal	April 2011
Mitochondrial fusion, division and positioning in plants Logan, David C. Biochemical Society Transactions, Vol. 38, Issue 3 https://doi.org/10.1042/BST0380789	journal	May 2010
The genetic control of plant mitochondrial morphology and dynamics Logan, David C.; Scott, Iain; Tobin, Alyson K. The Plant Journal, Vol. 36, Issue 4 https://doi.org/10.1046/j.1365-313X.2003.01894.x	journal	November 2003
The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Wang, H.; Lockwood, S. K.; Hoeltzel, M. F. Genes & Development, Vol. 11, Issue 6 https://doi.org/10.1101/gad.11.6.799	journal	March 1997
Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction Mochizuki, N.; Brusslan, J. A.; Larkin, R. Proceedings of the National Academy of Sciences, Vol. 98, Issue 4 https://doi.org/10.1073/pnas.98.4.2053	journal	February 2001
Phytochrome signaling mechanisms and the control of plant development Chen, Meng; Chory, Joanne Trends in Cell Biology, Vol. 21, Issue 11 https://doi.org/10.1016/j.tcb.2011.07.002	journal	November 2011
Architectural switches in plant thylakoid membranes Kirchhoff, Helmut Photosynthesis Research, Vol. 116, Issue 2-3 https://doi.org/10.1007/s11120-013-9843-0	journal	May 2013
The mutants of Arabidopsis Estelle, M. A.; Somerville, C. R. Trends in Genetics, Vol. 2 https://doi.org/10.1016/0168-9525(86)90190-3	journal	January 1986
ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants Brandizzi, Federica; Hanton, Sally; daSilva, Luis L. Pinto The Plant Journal, Vol. 34, Issue 3 https://doi.org/10.1046/j.1365-313X.2003.01728.x	journal	May 2003
Biogenesis and homeostasis of chloroplasts and other plastids Jarvis, Paul; López-Juez, Enrique Nature Reviews Molecular Cell Biology, Vol. 14, Issue 12 https://doi.org/10.1038/nrm3702	journal	November 2013
In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase: RHD3 involvement in Golgi movement and ER architecture Stefano, Giovanni; Renna, Luciana; Moss, Tyler The Plant Journal, Vol. 69, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04846.x	journal	December 2011
A greener world: The revolution in plant bioimaging Brandizzi, Federica; Fricker, Mark; Hawes, Chris Nature Reviews Molecular Cell Biology, Vol. 3, Issue 7 https://doi.org/10.1038/nrm861	journal	July 2002
clueless, a conserved Drosophila gene required for mitochondrial subcellular localization, interacts genetically with parkin Cox, R. T.; Spradling, A. C. Disease Models & Mechanisms, Vol. 2, Issue 9-10 https://doi.org/10.1242/dmm.002378	journal	July 2009
Plastid Division and Development Pyke, Kevin A. The Plant Cell, Vol. 11, Issue 4 https://doi.org/10.1105/tpc.11.4.549	journal	April 1999
Division and Dynamic Morphology of Plastids Osteryoung, Katherine W.; Pyke, Kevin A. Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-035748	journal	April 2014
Mesophyll cells of C ₄ plants have fewer chloroplasts than those of closely related C ₃ plants : C Stata, Matt; Sage, Tammy L.; Rennie, Troy D. Plant, Cell & Environment, Vol. 37, Issue 11 https://doi.org/10.1111/pce.12331	journal	May 2014
Plastid Signals Remodel Light Signaling Networks and Are Essential for Efficient Chloroplast Biogenesis in Arabidopsis Ruckle, Michael E.; DeMarco, Stephanie M.; Larkin, Robert M. The Plant Cell, Vol. 19, Issue 12 https://doi.org/10.1105/tpc.107.054312	journal	December 2007
Primary Site of Action of Amitrole in Arabidopsis thaliana Involves Inhibition of Root Elongation but Not of Histidine or Pigment Biosynthesis Heim, Dale R.; Larrinua, Ignacio M. Plant Physiology, Vol. 91, Issue 3 https://doi.org/10.1104/pp.91.3.1226	journal	November 1989
Rapid GDP release from Gsα in patients with gain and loss of endocrine function Iiri, Taroh; Herzmark, Paul; Nakamoto, Jon M. Nature, Vol. 371, Issue 6493 https://doi.org/10.1038/371164a0	journal	September 1994
Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato Liu, Y.; Roof, S.; Ye, Z. Proceedings of the National Academy of Sciences, Vol. 101, Issue 26 https://doi.org/10.1073/pnas.0400935101	journal	June 2004
Influence of plastids on light signalling and development Larkin, Robert M. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1640 https://doi.org/10.1098/rstb.2013.0232	journal	April 2014
The Development of C ₄ Rice: Current Progress and Future Challenges von Caemmerer, Susanne; Quick, W. Paul; Furbank, Robert T. Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1220177	journal	June 2012
Ethylmethanesulfonate Saturation Mutagenesis in Arabidopsis to Determine Frequency of Herbicide Resistance Jander, Georg; Baerson, Scott R.; Hudak, Jebecka A. Plant Physiology, Vol. 131, Issue 1 https://doi.org/10.1104/pp.102.010397	journal	January 2003
Chloroplasts of Arabidopsis thaliana homozygous for the ch-1 locus lack chlorophyll b, lack stable LHCPII and have stacked thylakoids Murray, David L.; Kohorn, Bruce D. Plant Molecular Biology, Vol. 16, Issue 1 https://doi.org/10.1007/BF00017918	journal	January 1991

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59 BASIC BIOLOGICAL SCIENCES
Arabidopsis
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chloroplast
chloroplast coverage
plastid signaling

Title: REDUCED CHLOROPLAST COVERAGE genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment

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