Skip to main content

The first α-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid binding

Abstract

The vesicle-inducing protein in plastids 1 (Vipp1) is an essential component for thylakoid biogenesis in cyanobacteria and chloroplasts. Vipp1 proteins share significant structural similarity with their evolutionary ancestor PspA (bacterial phage shock protein A), namely a predominantly α-helical structure, the formation of oligomeric high molecular weight complexes (HMW-Cs) and a tight association with membranes. Here, we elucidated domains of Vipp1 from Arabidopsis thaliana involved in homo-oligomerization as well as association with chloroplast inner envelope membranes. We could show that the 21 N-terminal amino acids of Vipp1, which form the first α-helix of the protein, are essential for assembly of the 2 MDa HMW-C but are not needed for formation of smaller subcomplexes. Interestingly, removal of this domain also interferes with association of the Vipp1 protein to the inner envelope. Fourier transform infrared spectroscopy of recombinant Vipp1 further indicates that Escherichia coli lipids bind tightly enough that they can be co-purified with the protein. This feature also depends on the presence of the first helix, which strongly supports an interaction of lipids with the Vipp1 HMW-C but not with smaller subcomplexes. Therefore, Vipp1 oligomerization appears to be a prerequisite for its membrane association. Our results further highlight structural differences between Vipp1 and PspA, which might be important in regard to their different function in thylakoid biogenesis and bacterial stress response, respectively.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

ATR-FTIR:

Attenuated total reflectance Fourier transform infrared spectroscopy

EM:

Electron microscopy

HMW-C:

High molecular weight complex

PspA:

Phage shock protein A

SEC:

Size exclusion chromatography

Vipp1:

Vesicle-inducing protein in plastids 1

References

  • Adam Z, Charuvi D, Tsabari O, Knopf R, Reich Z (2011) Biogenesis of thylakoid networks in angiosperms: knowns and unknowns. Plant Mol Biol 76:221–234

    PubMed  Article  CAS  Google Scholar 

  • Adams H, Teertstra W, Demmers J, Boesten R, Tommassen J (2003) Interactions between phage-shock proteins in Escherichia coli. J Bacteriol 185:1174–1180

    PubMed  Article  CAS  Google Scholar 

  • Andersson MX, Sandelius AS (2004) A chloroplast-localized vesicular transport system: a bio-informatics approach. BMC Genomics 5:40

    PubMed  Article  Google Scholar 

  • Aseeva E, Ossenbuhl F, Eichacker LA, Wanner G, Soll J, Vothknecht UC (2004) Complex formation of Vipp 1 depends on its alpha-helical PspA-like domain. J Biol Chem 279:35535–35541

    PubMed  Article  CAS  Google Scholar 

  • Aseeva E, Ossenbuhl F, Sippel C, Cho WK, Stein B, Eichacker LA, Meurer J, Wanner G, Westhoff P, Soll J, Vothknecht UC (2007) Vipp 1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol Biochem 45:119–128

    PubMed  Article  CAS  Google Scholar 

  • Benning C (2009) Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25:71–91

    PubMed  Article  CAS  Google Scholar 

  • Bergler H, Abraham D, Aschauer H, Turnowsky F (1994) Inhibition of lipid biosynthesis induces the expression of the pspA gene. Microbiology 140:1937–1944

    PubMed  Article  CAS  Google Scholar 

  • Blume A, Hubner W, Messner G (1988) Fourier transform infrared spectroscopy of 13C = O-labeled phospholipids hydrogen bonding to carbonyl groups. Biochemistry 27:8239–8249

    Google Scholar 

  • Brissette JL, Russel M, Weiner L, Model P (1990) Phage shock protein, a stress protein of Escherichia coli. Proc Natl Acad Sci USA 87:862–866

    PubMed  Article  CAS  Google Scholar 

  • Bultema JB, Fuhrmann E, Boekema EJ, Schneider D (2010) Vipp 1 and PspA: related but not twins. Commun Integr Biol 3:162–165

    PubMed  Article  Google Scholar 

  • Cole C, Barber JD, Barton GJ (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36:W197–W201

    PubMed  Article  CAS  Google Scholar 

  • Combet C, Blanchet C, Geourjon C, Deleage G (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25:147–150

    PubMed  Article  CAS  Google Scholar 

  • DeLisa MP, Lee P, Palmer T, Georgiou G (2004) Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186:366–373

    PubMed  Article  CAS  Google Scholar 

  • Elderkin S, Bordes P, Jones S, Rappas M, Buck M (2005) Molecular determinants for PspA-mediated repression of the AAA transcriptional activator PspF. J Bacteriol 187:3238–3248

    PubMed  Article  CAS  Google Scholar 

  • Frishman D, Argos P (1996) Incorporation of non-local interactions in protein secondary structure prediction from the amino acid sequence. Protein Eng 9:133–142

    PubMed  Article  CAS  Google Scholar 

  • Fuhrmann E, Bultema JB, Kahmann U, Rupprecht E, Boekema EJ, Schneider D (2009a) The vesicle-inducing protein 1 from Synechocystis sp. PCC 6803 organizes into diverse higher-ordered ring structures. Mol Biol Cell 20:4620–4628

    PubMed  Article  CAS  Google Scholar 

  • Fuhrmann E, Gathmann S, Rupprecht E, Golecki J, Schneider D (2009b) Thylakoid membrane reduction affects the photosystem stoichiometry in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 149:735–744

    PubMed  Article  CAS  Google Scholar 

  • Gao H, Xu X (2009) Depletion of Vipp 1 in Synechocystis sp. PCC 6803 affects photosynthetic activity before the loss of thylakoid membranes. FEMS Microbiol Lett 292:63–70

    PubMed  Article  CAS  Google Scholar 

  • Garnier J, Gibrat JF, Robson B (1996) GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol 266:540–553

    PubMed  Article  CAS  Google Scholar 

  • Hankamer BD, Elderkin SL, Buck M, Nield J (2004) Organization of the AAA(+) adaptor protein PspA is an oligomeric ring. J Biol Chem 279:8862–8866

    PubMed  Article  CAS  Google Scholar 

  • Jakob-Grun S, Radek J, Braun P (2012) Ca2+-binding reduces conformational flexibility of RC–LH1 core complex from thermophile Thermochromatium tepidum. Photosynth Res 111:139–147

    PubMed  Article  CAS  Google Scholar 

  • Joly N, Burrows PC, Engl C, Jovanovic G, Buck M (2009) A lower-order oligomer form of phage shock protein A (PspA) stably associates with the hexameric AAA(+) transcription activator protein PspF for negative regulation. J Mol Biol 394:764–775

    PubMed  Article  CAS  Google Scholar 

  • Joly N, Engl C, Jovanovic G, Huvet M, Toni T, Sheng X, Stumpf MPH, Buck M (2010) Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol Rev 34:797–827

    PubMed  CAS  Google Scholar 

  • Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292:195–202

    PubMed  Article  CAS  Google Scholar 

  • Kader JC (1996) Lipid-transfer proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 47:627–654

    PubMed  Article  CAS  Google Scholar 

  • Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371

    PubMed  Article  CAS  Google Scholar 

  • Kleerebezem M, Tommassen J (1993) Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol Microbiol 7:947–956

    PubMed  Article  CAS  Google Scholar 

  • Kleerebezem M, Crielaard W, Tommassen J (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the proton motive force under stress conditions. EMBO J 15:162–171

    PubMed  CAS  Google Scholar 

  • Kobayashi R, Suzuki T, Yoshida M (2007) Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol Microbiol 66:100–109

    PubMed  Article  CAS  Google Scholar 

  • Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98:4238–4242

    PubMed  Article  CAS  Google Scholar 

  • Lewis RN, McElhaney RN, Pohle W, Mantsch HH (1994) Components of the carbonyl stretching band in the infrared spectra of hydrated 1,2-diacylglycerolipid bilayers: a reevaluation. Biophys J 67:2367–2375

    Google Scholar 

  • Li HM, Kaneko Y, Keegstra K (1994) Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes. Plant Mol Biol 25:619–632

    PubMed  Article  CAS  Google Scholar 

  • Liu C, Willmund F, Whitelegge JP, Hawat S, Knapp B, Lodha M, Schroda M (2005) J-domain protein CDJ2 and HSP70B are a plastidic chaperone pair that interacts with vesicle-inducing protein in plastids 1. Mol Biol Cell 16:1165–1177

    PubMed  Article  CAS  Google Scholar 

  • Liu CM, Willmund F, Golecki JR, Cacace S, Hess B, Markert C, Schroda M (2007) The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J 50:265–277

    PubMed  Article  CAS  Google Scholar 

  • Nordhues A, Schottler MA, Unger AK, Geimer S, Schonfelder S, Schmollinger S, Rutgers M, Finazzi G, Soppa B, Sommer F, Muhlhaus T, Roach T, Krieger-Liszkay A, Lokstein H, Crespo JL, Schroda M (2012) Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24:637–659

    PubMed  Article  CAS  Google Scholar 

  • Sakamoto W, Miyagishima SY, Jarvis P (2008) Chloroplast biogenesis: control of plastid development, protein import, division and inheritance. Arabidopsis Book 6:e0110

    PubMed  Google Scholar 

  • Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101

    PubMed  Article  CAS  Google Scholar 

  • Vothknecht UC, Otters S, Hennig R, Schneider D (2011) Vipp 1: a very important protein in plastids?! J Exp Bot 63:1699–1712

    PubMed  Article  Google Scholar 

  • Waegemann K, Soll J (1991) Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J 1:149–158

    Article  Google Scholar 

  • Wessel D, Flugge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141–143

    PubMed  Article  CAS  Google Scholar 

  • Westphal S, Heins L, Soll J, Vothknecht UC (2001a) Vipp 1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc Natl Acad Sci USA 98:4243–4248

    PubMed  Article  CAS  Google Scholar 

  • Westphal S, Soll J, Vothknecht UC (2001b) A vesicle transport system inside chloroplasts. FEBS Lett 506:257–261

    PubMed  Article  CAS  Google Scholar 

  • Zhang L, Kato Y, Otters S, Vothknecht UC, Sakamoto W (2012) Essential Role of VIPP1 in Chloroplast Envelope Maintenance in Arabidopsis. Plant Cell. http://dx.doi.org/10.1105/tpc.112.103606

Download references

Acknowledgments

This work was supported by grants from the Deutsche Forschungsgemeinschaft to UCV (SFB-TR1, project A6) and PB (BR-1991/2-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ute C. Vothknecht.

Additional information

A contribution to the Special Issue on Evolution and Biogenesis of Chloroplasts and Mitochondria.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 12893 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Otters, S., Braun, P., Hubner, J. et al. The first α-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid binding. Planta 237, 529–540 (2013). https://doi.org/10.1007/s00425-012-1772-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1772-1

Keywords

  • Lipid binding
  • Protein complex formation
  • PspA
  • Thylakoid biogenesis
  • Vipp1