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Plant Molecular Biology

, Volume 81, Issue 3, pp 235–244 | Cite as

Analysis of the chloroplast proteome in arc mutants and identification of novel protein components associated with FtsZ2

  • Daniela Gargano
  • Jodi Maple-Grødem
  • Veronika Reisinger
  • Lutz Andreas Eichacker
  • Simon Geir Møller
Article

Abstract

Chloroplasts are descendants of cyanobacteria and divide by binary fission. The number of chloroplasts is regulated in a cell type-specific manner to ensure that specialized cell types can perform their functions optimally. Several protein components of the chloroplast division apparatus have been identified in the past several years, but how this process is regulated in response to developmental status, environmental signals and stress is still unknown. To begin to address this we undertook a proteomic analysis of three accumulation and replication of chloroplasts mutants that show a spectrum of plastid division perturbations. We show that defects in the chloroplast division process results in changes in the abundance of proteins when compared to wild type, but that the profile of the native stromal and membrane complexes remains unchanged. Furthermore, by combining BN-PAGE with protein interaction assays we show that AtFtsZ2-1 and AtFtsZ2-2 assemble together with rpl12A and EF-Tu into a novel chloroplast membrane complex.

Keywords

2D-DIGE BN-PAGE FtsZ Chloroplast division LC–MS/MS 

Notes

Acknowledgments

We thank Astrid Elisabeth Tveitaskog for assistance with 2D-PAGE and chloroplast isolation. This work was supported by a FUGE Norwegian Research Council grant to SGM.

Supplementary material

11103_2012_9994_MOESM1_ESM.tif (3.8 mb)
Supplementary Fig. 1. Detection of phosphoproteins by Pro-Q Diamond from wild type and arc mutants chloroplast proteins separated by 2-D gel (TIFF 3916 kb)
11103_2012_9994_MOESM2_ESM.tif (9.7 mb)
Supplementary Fig. 2. 2D-native/SDS-PAGE gels of chloroplast membrane (A) and stromal (B) complexes (TIFF 9905 kb)

References

  1. Aronsson H, Jarvis P (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett 529:215–220PubMedCrossRefGoogle Scholar
  2. Austin JA, Webber AN (2005) Photosynthesis in Arabidopsis thaliana mutants with reduced chloroplast number. Photosynth Res 85:373–384CrossRefGoogle Scholar
  3. Baginsky S, Hennig L, Zimmermann P, Gruissem W (2010) Gene expression analysis, proteomics, and network discovery. Plant Physiol 152:402–410PubMedCrossRefGoogle Scholar
  4. Cerny M, Dycka F, Bobal’ova J, Brzobohaty B (2011) Early cytokinin response proteins and phosphoproteins of Arabidopsis thaliana identified by proteome and phosphoproteome profiling. J Exp Bot 62:921–937PubMedCrossRefGoogle Scholar
  5. Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516PubMedCrossRefGoogle Scholar
  6. Defeu Soufo HJ, Reimold C, Linne U, Knust T, Gescher J, Graumann PL (2010) Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc Natl Acad Sci USA 107:3163–3168PubMedCrossRefGoogle Scholar
  7. Dickson R, Weiss C, Howard RJ, Alldrick SP, Ellis RJ, Lorimer G, Azem A, Viitanen PV (2000) Reconstitution of higher plant chloroplast chaperonin 60 tetradecamers active in protein folding. J Biol Chem 275:11829–11835PubMedCrossRefGoogle Scholar
  8. Douglas SE (1998) Plastid evolution: origins, diversity, trends. Curr Opin Genet Dev 8:655–661PubMedCrossRefGoogle Scholar
  9. Eubel H, Braun HP, Millar AH (2005) Blue-native PAGE in plants: a tool in analysis of protein-protein interactions. Plant Methods 1:11PubMedCrossRefGoogle Scholar
  10. Friedman DB, Lilley KS (2008) Optimizing the difference gel electrophoresis (DIGE) technology. Methods Mol Biol 428:93–124PubMedCrossRefGoogle Scholar
  11. Fujiwara MT, Nakamura A, Itoh R, Shimada Y, Yoshida S, Moller SG (2004) Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J Cell Sci 117:2399–2410PubMedCrossRefGoogle Scholar
  12. Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100:4328–4333PubMedCrossRefGoogle Scholar
  13. Gargano D, Maple-Grødem J, Møller SG (2012) In vivo phosphorylation of Ftsz2 in Arabidopsis thaliana. Biochem J 446:517–521 Google Scholar
  14. Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470PubMedCrossRefGoogle Scholar
  15. Granvogl B, Reisinger V, Eichacker LA (2006) Mapping the proteome of thylakoid membranes by de novo sequencing of intermembrane peptide domains. Proteomics 6:3681–3695PubMedCrossRefGoogle Scholar
  16. Hutchison CE, Kieber JJ (2002) Cytokinin signaling in Arabidopsis. Plant Cell 14(Suppl):S47–S59PubMedGoogle Scholar
  17. Karamoko M, El-Kafafi ES, Mandaron P, Lerbs-Mache S, Falconet D (2011) Multiple FtsZ2 isoforms involved in chloroplast division and biogenesis are developmentally associated with thylakoid membranes in Arabidopsis. FEBS Lett 585:1203–1208PubMedCrossRefGoogle Scholar
  18. Lilley KS (2003) Protein profiling using two-dimensional difference gel electrophoresis (2-D DIGE). Curr Protoc Protein Sci Chapter 22: Unit 22.2Google Scholar
  19. Lowe J, Amos LA (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203–206PubMedCrossRefGoogle Scholar
  20. Maple J, Moller SG (2010) The complexity and evolution of the plastid-division machinery. Biochem Soc Trans 38:783–788PubMedCrossRefGoogle Scholar
  21. Maple J, Chua NH, Moller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31:269–277PubMedCrossRefGoogle Scholar
  22. Maple J, Aldridge C, Moller SG (2005) Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J 43:811–823PubMedCrossRefGoogle Scholar
  23. Maple J, Vojta L, Soll J, Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8:293–299PubMedCrossRefGoogle Scholar
  24. Maple J, Winge P, Tveitaskog AE, Gargano D, Bones AM, Moller SG (2011) Genome-wide gene expression profiles in response to plastid division perturbations. Planta 234:1055–1063PubMedCrossRefGoogle Scholar
  25. Martin A, Lang D, Hanke ST, Mueller SJ, Sarnighausen E, Vervliet-Scheebaum M, Reski R (2009) Targeted gene knockouts reveal overlapping functions of the five Physcomitrella patens FtsZ isoforms in chloroplast division, chloroplast shaping, cell patterning, plant development, and gravity sensing. Mol Plant 2:1359–1372PubMedCrossRefGoogle Scholar
  26. McAndrew RS, Olson BJ, Kadirjan-Kalbach DK, Chi-Ham CL, Vitha S, Froehlich JE, Osteryoung KW (2008) In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem J 412:367–378PubMedCrossRefGoogle Scholar
  27. Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517–2530PubMedCrossRefGoogle Scholar
  28. Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, Miyagishima SY (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21:1769–1780PubMedCrossRefGoogle Scholar
  29. Olinares PD, Ponnala L, van Wijk KJ (2010) Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Mol Cell Proteomics 9:1594–1615PubMedCrossRefGoogle Scholar
  30. Olson BJ, Wang Q, Osteryoung KW (2010) GTP-dependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J Biol Chem 285:20634–20643PubMedCrossRefGoogle Scholar
  31. Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197PubMedCrossRefGoogle Scholar
  32. Pyke KA, Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99:1005–1008PubMedCrossRefGoogle Scholar
  33. Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207PubMedGoogle Scholar
  34. Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T, Takamiya K (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45:960–967PubMedCrossRefGoogle Scholar
  35. Suzuki K, Nakanishi H, Bower J, Yoder DW, Osteryoung KW, Miyagishima SY (2009) Plastid chaperonin proteins Cpn60 alpha and Cpn60 beta are required for plastid division in Arabidopsis thaliana. BMC Plant Biol 9:38PubMedCrossRefGoogle Scholar
  36. Weglohner W, Subramanian AR (1994) Multicopy GTPase center protein L12 of Arabidopsis chloroplast ribosome is encoded by a clustered nuclear gene family with the expressed members closely linked to tRNA(Pro) genes. J Biol Chem 269:7330–7336PubMedGoogle Scholar
  37. Yamaguchi K, von Knoblauch K, Subramanian AR (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275:28455–28465PubMedCrossRefGoogle Scholar
  38. Yang Y, Glynn JM, Olson BJ, Schmitz AJ, Osteryoung KW (2008) Plastid division: across time and space. Curr Opin Plant Biol 11:577–584PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Daniela Gargano
    • 1
  • Jodi Maple-Grødem
    • 1
    • 2
  • Veronika Reisinger
    • 1
  • Lutz Andreas Eichacker
    • 1
  • Simon Geir Møller
    • 1
    • 2
    • 3
  1. 1.Faculty of Science and Technology, Centre for Organelle ResearchUniversity of StavangerStavangerNorway
  2. 2.The Norwegian Centre for Movement DisordersStavanger University HospitalStavangerNorway
  3. 3.Department of Biological SciencesSt John’s UniversityNew YorkUSA

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