Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-18T20:59:26.007Z Has data issue: false hasContentIssue false
  • English
  • Français

Single Particle Tracking Analysis of the Chloroplast Division Protein FtsZ Anchoring to the Inner Envelope Membrane

Published online by Cambridge University Press:  12 April 2013

Carol B. Johnson ,
Leung K. Tang ,
Aaron G. Smith ,
Akshaya Ravichandran ,
Zhiping Luo ,
Stanislav Vitha  and
Andreas Holzenburg
Carol B. Johnson
Affiliation:
Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA
Leung K. Tang
Affiliation:
Department Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA
Aaron G. Smith
Affiliation:
Department Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA Department of Structural Biology, University of Pittsburgh, Pittsburgh, PA 15260, USA
Akshaya Ravichandran
Affiliation:
Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA
Zhiping Luo
Affiliation:
Microscopy and Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA Department of Chemistry and Physics, Fayetteville State University, Fayetteville, NC 28301, USA
Stanislav Vitha
Affiliation:
Microscopy and Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA
Andreas Holzenburg*
Affiliation:
Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA Department Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA Microscopy and Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

Replication of chloroplast in plant cells is an essential process that requires co-assembly of the tubulin-like plastid division proteins FtsZ1 and FtsZ2 at mid-chloroplast to form a ring structure called the Z-ring. The Z-ring is stabilized via its interaction with the transmembrane protein ARC6 on the inner envelope membrane of chloroplasts. Plants lacking ARC6 are defective in plastid division and contain only one or two enlarged chloroplasts per cell with abnormal localization of FtsZ: instead of a single Z-ring, many short FtsZ filaments are distributed throughout the chloroplast. ARC6 is thought to be the anchoring point for FtsZ assemblies. To investigate the role of ARC6 in FtsZ anchoring, the mobility of green fluorescent protein–tagged FtsZ assemblies was assessed by single particle tracking in mutant plants lacking the ARC6 protein. Mean square displacement analysis showed that the mobility of FtsZ assemblies is to a large extent characterized by anomalous diffusion behavior (indicative of intermittent binding) and restricted diffusion suggesting that besides ARC6-mediated anchoring, an additional FtsZ-anchoring mechanism is present in chloroplasts.

Keywords

ARC6FtsZ anchoringchloroplast divisionArabidopsis thalianaparticle trackinganomalous diffusion
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 3 , June 2013 , pp. 507 - 512
Copyright
Copyright © Microscopy Society of America 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

These authors contributed equally to this work.

References

Clough, S.J. & Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana . Plant J 16, 735–743.CrossRefGoogle Scholar
Douglas, S.E. (1998). Plastid evolution: Origins, diversity, trends. Curr Opin Genet Dev 8, 655–661.CrossRefGoogle ScholarPubMed
Glynn, J.M., Froehlich, J.E. & Osteryoung, K.W. (2008). Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20, 2460–2470.CrossRefGoogle ScholarPubMed
Glynn, J.M., Yang, Y., Vitha, S., Schmitz, A.J., Hemmes, M., Miyagishima, S.Y. & Osteryoung, K.W. (2009). PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis . Plant J 59, 700–711.CrossRefGoogle ScholarPubMed
Leech, R.M., Thomson, W.W. & Platt-Aloia, K.A. (1981). Observations on the mechanism of chloroplast division in higher plants. New Phytol 87, 1–9.CrossRefGoogle Scholar
Littlejohn, G.R., Gouveia, J.D., Edner, C., Smirnoff, N. & Love, J. (2010). Perfluorodecalin enhances in vivo confocal microscopy resolution of Arabidopsis thaliana mesophyll. New Phytol 186, 1018–1025.CrossRefGoogle ScholarPubMed
Maple, J., Vojta, L., Soll, J. & Møller, S.G. (2007). ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8, 293–299.CrossRefGoogle ScholarPubMed
Martin, W. & Herrmann, R.G. (1998). Gene transfer from organelles to the nucleus: How much, what happens, and why? Plant Physiol 118, 9–17.CrossRefGoogle Scholar
McAndrew, R.S., Froehlich, J.E., Vitha, S., Stokes, K.D. & Osteryoung, K.W. (2001). Colocalization of plastid division proteins in the chloroplast stromal compartment establishes a new functional relationship between FtsZ1 and FtsZ2 in higher plants. Plant Physiol 127, 1656–1666.CrossRefGoogle ScholarPubMed
McFadden, G.I. (1999). Endosymbiosis and evolution of the plant cell. Curr Opin Plant Biol 2, 513–519.CrossRefGoogle ScholarPubMed
Menchón, S.A., Martin, M.G. & Dotti, C.G. (2012). APM_GUI: Analyzing particle movement on the cell membrane and determining confinement. BMC Biophys 5, 4.CrossRefGoogle ScholarPubMed
Miyagishima, S.Y., Nozaki, H., Nishida, K., Nishida, K., Matsuzaki, M. & Kuroiwa, T. (2004). Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: The duplication of FtsZ is implicated in endosymbiosis. J Mol Evol 58, 291–303.CrossRefGoogle ScholarPubMed
Osteryoung, K.W. (2000). Organelle division: Crossing the evolutionary divide. Plant Physiol 123, 1213–1216.CrossRefGoogle ScholarPubMed
Osteryoung, K.W. & McAndrew, R.S. (2001). The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52, 315–333.CrossRefGoogle ScholarPubMed
Osteryoung, K.W. & Nunnari, J. (2003). The division of endosymbiotic organelles. Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Science 302, 1698–1704.CrossRefGoogle Scholar
Osteryoung, K.W. & Vierling, E. (1995). Conserved cell and organelle division. Nature 376, 473–474.CrossRefGoogle ScholarPubMed
Pyke, K.A., Rutherford, S.M., Robertson, E.J. & Leech, R.M. (1994). arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106, 1169–1177.CrossRefGoogle ScholarPubMed
Ruthardt, N., Lamb, D.C. & Brauchle, C. (2011). Single-particle tracking as a quantitative microscopy-based approach to unravel cell entry mechanisms of viruses and pharmaceutical nanoparticles. Mol Ther 19, 1199–1211.CrossRefGoogle ScholarPubMed
Sage, D., Neumann, F.R., Hediger, F., Gasser, S.M. & Unser, M. (2005). Automatic tracking of individual fluorescence particles: Application to the study of chromosome dynamics. IEEE Trans Image Process 14, 1372–1383.CrossRefGoogle Scholar
Saxton, M.J. & Jacobson, K. (1997). Single-particle tracking: Applications to membrane dynamics. Annu Rev Biophys Biomol Struct 26, 373–399.CrossRefGoogle ScholarPubMed
Stokes, K.D., McAndrew, R.S., Figueroa, R., Vitha, S. & Osteryoung, K.W. (2000). Chloroplast division and morphology are differentially affected by overexpression of FtsZ1 and FtsZ2 genes in Arabidopsis . Plant Physiol 124, 1668–1677.CrossRefGoogle ScholarPubMed
TerBush, A.D. & Osteryoung, K.W. (2012). Distinct functions of chloroplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J Cell Biol 199, 623–637.CrossRefGoogle ScholarPubMed
Vitha, S., Froehlich, J.E., Koksharova, O., Pyke, K.A., van Erp, H. & Osteryoung, K.W. (2003). ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15, 1918–1933.CrossRefGoogle Scholar
Vitha, S., McAndrew, R.S. & Osteryoung, K.W. (2001). FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153, 111–119.CrossRefGoogle ScholarPubMed