Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-18T04:23:29.072Z Has data issue: false hasContentIssue false
  • English
  • Français

FtsZ1/FtsZ2 Turnover in Chloroplasts and the Role of ARC3

Published online by Cambridge University Press:  03 March 2015

Carol B. Johnson ,
Rahamthulla Shaik ,
Rehab Abdallah ,
Stanislav Vitha  and
Andreas Holzenburg
Carol B. Johnson
Affiliation:
Microscopy & Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA
Rahamthulla Shaik
Affiliation:
Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA
Rehab Abdallah
Affiliation:
Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA
Stanislav Vitha
Affiliation:
Microscopy & Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA
Andreas Holzenburg*
Affiliation:
Microscopy & Imaging Center, Texas A&M University, College Station, TX 77843-2257, USA Department of Biology, Texas A&M University, College Station, TX 77843-3258, USA Department of Biochemistry and Biophysics, Texas A&M University, College Station, TX 77843-2128, USA
*
*Corresponding author. holzen@tamu.edu
Get access

Abstract

Chloroplast division requires filamentation temperature-sensitive Z (FtsZ), a tubulin-like GTPase of cyanobacterial endosymbiotic origin. Plants and algae possess two distinct FtsZ protein families, FtsZ1 and FtsZ2 that co-assemble into a ring (Z-ring) at the division site. Z-ring assembly and disassembly and division site positioning is controlled by both positive and negative factors via their specific interactions with FtsZ1 and FtsZ2. Here we present the in planta analysis of Arabidopsis FtsZ1 and FtsZ2 turnover in the context of a native chloroplast division machinery. Fluorescence recovery after photobleaching analysis was conducted using fluorescently tagged FtsZ at wild-type (WT)-like levels. Rapid photobleaching, low signal-to-noise ratio, and phototropic movements of chloroplasts were overcome by (i) using progressive intervals in time-lapse imaging, (ii) analyzing epidermal rather than stromal chloroplasts, and (iii) employing image stack alignment during postprocessing. In plants of WT background, fluorescence recovery half-times averaged 117 and 325 s for FtsZ1 and FtsZ2, respectively. In plants lacking ARC3, the key negative regulator of FtsZ assembly, the turnover was threefold slower. The findings are discussed in the context of previous results conducted in a heterologous system.

Keywords

plastid divisionFtsZ assemblyARC3FRAP analysisArabidopsis
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 21 , Issue 2 , April 2015 , pp. 313 - 323
Copyright
© Microscopy Society of America 2015 

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

†

Current address: Department of Biology, Lone Star College–North Harris, 2700 W.W. Thorne Drive, Houston, TX 77073-3499, USA.

‡

Current address: Department of Biology, The American University in Cairo, P.O. Box 74, New Cairo 11835, Cairo, Egypt.

References

Anderson, D.E., Guerios-Filho, F.J. & Erickson, H.P. (2004). Assembly dynamics of ftsz rings in Bacillus subtilis and Escherichia coli and effects of ftsz-regulating proteins. J Bacteriol 186, 5775–5781.CrossRefGoogle ScholarPubMed
Blasios, V., Bisson-Filho, A.W., Castellen, P., Nogueira, M.L., Bettini, J., Portugal, R.V., Zeri, A.C. & Gueiros-Filho, F.J. (2013). Genetic and biochemical characterization of the MinC-FtsZ interaction in Bacillus subtilis . PLoS One 8, e60690.CrossRefGoogle ScholarPubMed
Chen, Y., Anderson, D.E., Rajagopalan, M. & Erickson, H.P. (2007). Assembly dynamics of Mycobacterium tuberculosis FtsZ. J Biol Chem 282, 27736–27743.CrossRefGoogle ScholarPubMed
Chen, Y.D. & Erickson, H.P. (2005). Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J Biol Chem 280, 22549–22554.CrossRefGoogle ScholarPubMed
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
Dajkovic, A., Lan, G., Sun, S.X., Wirtz, D. & Lutkenhaus, J. (2008). MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18, 235–244.CrossRefGoogle ScholarPubMed
Davis, S.J. & Vierstra, R.D. (1996). Soluble derivatives of green fluorescent protein (GFP) for use in Arabidopsis thaliana . Weeds World 3, 43–48.Google Scholar
de Boer, P.A. (2010). Advances in understanding E. coli cell fission. Curr Opin Microbiol 13, 730–737.CrossRefGoogle ScholarPubMed
de Boer, P.A.J., Crossley, R.E. & Rothfield, L.I. (1992). Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli . J Bacteriol 174, 63–70.CrossRefGoogle ScholarPubMed
de Oliveira, I.F.F., de Sousa Borges, A., Kooij, V., Bartosiak-Jentys, J., Luirink, J. & Scheffers, D.-J. (2010). Characterization of ftsZ mutations that render Bacillus subtilis resistant to MinC. PLoS One 5, e12048.CrossRefGoogle ScholarPubMed
Ferris, A.M., Giberson, R.T., Sanders, M.A. & Day, J.R. (2009). Advanced laboratory techniques for sample processing and immunolabeling using microwave radiation. J Neurosci Meth 182, 157–164.CrossRefGoogle ScholarPubMed
Fujiwara, M.T., Hashimoto, H., Kazama, Y., Abe, T., Yoshida, S., Sato, N. & Itoh, R.D. (2008). The assembly of the FtsZ ring at the mid-chloroplast division site depends on a balance between the activities of AtMinE1 and ARC11/AtMinD1. Plant Cell Physiol 49, 345–361.CrossRefGoogle ScholarPubMed
Gao, H., Sage, T.L. & Osteryoung, K.W. (2006). FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc Natl Acad Sci USA 103, 6759–6764.CrossRefGoogle ScholarPubMed
Geissler, B., Elraheb, D. & Margolin, W. (2003). A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli . Proc Natl Acad Sci USA 100, 4197–4202.CrossRefGoogle ScholarPubMed
Geissler, B., Shiomi, D. & Margolin, W. (2007). The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153, 814–825.CrossRefGoogle ScholarPubMed
Gleave, P. (1992). A versatile binary vector system with T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20, 1203–1207.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., Miyagishima, S., Yoder, D.W., Osteryoung, K.W. & Vitha, S. (2007). Chloroplast division. Traffic 8, 451–461.CrossRefGoogle ScholarPubMed
Gray, M.W. (1989). The evolutionary origins of organelles. Trends Genet 5, 294–299.CrossRefGoogle ScholarPubMed
Hirota, Y., Ryter, A. & Jacob, F. (1968). Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb Symp Quant Biol 33, 677–693.CrossRefGoogle ScholarPubMed
Hu, Z. & Lutkenhaus, J. (2003). A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 47, 345–355.CrossRefGoogle Scholar
Hu, Z., Mukherjee, A., Pichoff, S. & Lutkenhaus, J. (1999). The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci USA 96, 14819–14824.CrossRefGoogle ScholarPubMed
Hu, Z., Saez, C. & Lutkenhaus, J. (2003). Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: Role of MinD and MinE. J Bacteriol 185, 196–203.CrossRefGoogle Scholar
Johnson, C.B., Tang, L.K., Smith, A.G., Ravichandran, A., Luo, Z., Vitha, S. & Holzenburg, A. (2013). Single particle tracking analysis of the chloroplast division protein FtsZ anchoring to the inner envelope membrane. Microsc Microanal 19, 507–512.CrossRefGoogle Scholar
Kiessling, J., Kruse, S., Rensing, S.A., Harter, K., Decker, E.L. & Reski, R. (2000). Visualization of a cytoskeleton-like FtsZ network in chloroplasts. J Cell Biol 151, 945–950.CrossRefGoogle ScholarPubMed
Lutkenhaus, J., Pichoff, S. & Du, S. (2012). Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton 69, 778–790.CrossRefGoogle ScholarPubMed
Lutkenhaus, J., Wolf-Watz, H. & Donachie, W.D. (1980). Organization of genes in the ftsZ-envA region of the Escherichia coli genes map and identification of a new fts locus (ftsZ) . J Bacteriol 142, 615–620.CrossRefGoogle ScholarPubMed
Maple, J., Aldridge, C. & Møller, S.G. (2005). Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43, 811–823.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
Mateos-Gil, P., Paez, A., Horger, I., Rivas, G., Vicente, M., Tarazona, P. & Velez, M. (2012). Depolymerization dynamics of individual filaments of bacterial cytoskeletal protein FtsZ. Proc Natl Acad Sci USA 109, 8133–8138.CrossRefGoogle ScholarPubMed
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
Mereschkowsky, C. (1905). Über natur un ursprung der chromatophoren im pflanzenreiche. Biol Centralbl 25, 593–604. (English translation in Martin, W. & Kowallik, K.V. (1999). Annotated English translation of Mereschkowsky’s 1905 paper “Über Natur und Ursprung der Chromatophoren im Pflanzenreiche”. Eur J Phycol 24, 287–296.Google Scholar
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
Morisaki, T. & McNally, J.G. (2014). Photoswitching-free FRAP analysis with a genetically encoded fluorescent tag. PLoS One 9, e107730.CrossRefGoogle ScholarPubMed
Olson, B.J., Wang, Q. & Osteryoung, K.W. (2010). GTP-dependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J Biol Chem 285, 20634–20643.CrossRefGoogle ScholarPubMed
Osawa, M. & Erickson, H.P. (2005). Probing the domain structure of FtsZ by random truncation and insertion of GFP. Microbiology 151, 4033–4043.CrossRefGoogle ScholarPubMed
Osteryoung, K.W. (2001). Organelle fission in eukaryotes. Curr Opin Microbiol 4, 639–646.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. & Pyke, K.A. (1998). Plastid division: Evidence for a prokaryotically derived mechanism. Curr Opin Plant Biol 1, 475–479.CrossRefGoogle ScholarPubMed
Osteryoung, K.W., Stokes, K.D., Rutherford, S.M., Percival, A.L. & Lee, W.Y. (1998). Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ . Plant Cell 10, 1991–2004.CrossRefGoogle ScholarPubMed
Pyke, K.A. & Leech, R.M. (1991). Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol 96, 1193–1195.CrossRefGoogle ScholarPubMed
Rajagopalan, M., Atkinson, M.A.L., Lofton, H., Chauhan, A. & Madiraju, M.V. (2005). Mutations in the GTP-binding and synergy loop domains of Mycobacterium tuberculosis ftsZ compromise its function in vitro and in vivo. Biochem Biophys Res Commun 331, 1171–1177.CrossRefGoogle ScholarPubMed
Raskin, D.M. & de Boer, P.A.J. (1999). MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli . J Bacteriol 181, 6419–6424.CrossRefGoogle ScholarPubMed
Redick, S.D., Stricker, J., Briscoe, G. & Erickson, H.P. (2005). Mutants of FtsZ targeting the protofilament interface: Effects on cell division and GTPase activity. J Bacteriol 187, 2727–2736.CrossRefGoogle ScholarPubMed
Scheffers, D.J. (2008). The effect of MinC on FtsZ polymerization is pH dependent and can be counteracted by ZapA. FEBS Lett 582, 2601–2608.CrossRefGoogle ScholarPubMed
Schmitz, A.J., Glynn, J.M., Olson, B.J.S.C., Stokes, K.D. & Osteryoung, K.W. (2009). 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. Mol Plant 2, 1211–1222.CrossRefGoogle ScholarPubMed
Shaner, N.C., Lin, M.Z., McKeown, M.R., Steinbach, P.A., Hazelwood, K.L., Davidson, M.W. & Tsien, R.Y. (2008). Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5, 545–551.CrossRefGoogle ScholarPubMed
Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T. & Takamiya, K.-I. (2004). ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45, 960–967.CrossRefGoogle ScholarPubMed
Sinnecker, D., Voigt, P., Hellwig, N. & Schaefer, M. (2005). Reversible photobleaching of enhanced green fluorescent proteins. Biochemistry 44, 7085–7094.CrossRefGoogle ScholarPubMed
Smith, A.G., Johnson, C.B., Ellis, A.E., Vitha, S. & Holzenburg, A. (2008). Protein screening using cold microwave technology. Anal Biochem 375, 313–317.CrossRefGoogle ScholarPubMed
Smith, A.G., Johnson, C.B., Vitha, S. & Holzenburg, A. (2010). Plant FtsZ1 and FtsZ2 expressed in a eukaryotic host: GTPase activity and self-assembly. FEBS Lett 584, 166–172.CrossRefGoogle Scholar
Srinivasan, R., Mishra, M., Wu, L., Yin, Z. & Balasubramanian, M.K. (2008). The bacterial cell division protein FtsZ assembles into cytoplasmic rings in fission yeast. Genes Dev 22, 1741–1746.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
Stokes, K.D. & Osteryoung, K.W. (2003). Early divergence of the FtsZ1 and FtsZ2 plastid division gene families in photosynthetic eukaryotes. Gene 320, 97–108.CrossRefGoogle ScholarPubMed
Stricker, J., Maddox, P., Salmon, E.D. & Erickson, H.P. (2002). Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA 99, 3171–3175.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
Thévenaz, P., Ruttimann, U.E. & Unser, M. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7, 27–41.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
Zacharias, D.A., Violin, J.D., Newton, A.C. & Tsien, R.Y. (2002). Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296, 913–916.CrossRefGoogle ScholarPubMed
Zhang, M., Schmitz, A.J., Kadirjan-Kalbach, D.K., Terbush, A.D. & Osteryoung, K.W. (2013). Chloroplast division protein ARC3 regulates chloroplast FtsZ-ring assembly and positioning in Arabidopsis through interaction with FtsZ2. Plant Cell 25, 1787–1802.CrossRefGoogle ScholarPubMed