Document Detail

Possible function of VIPP1 in thylakoids: Protection but not formation?
Jump to Full Text
MedLine Citation:
PMID:  23154508     Owner:  NLM     Status:  Publisher    
Abstract/OtherAbstract:
VIPP1 protein in photosynthetic organisms is homologous to bacterial PspA, which protects plasma membrane integrity upon stresses. Despite the proposed role of VIPP1 in thylakoid biogenesis, its precise function remains unclear. Recently, our in-depth analysis of Arabidopsis vipp1 mutants revealed VIPP1's involvement in the maintenance of chloroplast envelopes. Chloroplasts in intact vipp1 leaves exhibited spherical balloon-like morphology, which resulted from osmotic stress across envelopes. In fact, observation of VIPP1 fused to green fluorescence protein in vivo revealed that most VIPP1 is localized as a lattice-like macro complex attached along with the envelope. Because of the proposed function in thylakoids, we examined whether vipp1 also exhibited altered morphologies in thylakoids. Results show that thylakoid morphologies were detected irregularly, but vipp1 chloroplasts retained normal-appearing grana stacks. We infer that VIPP1 might influence thylakoids as well as envelopes, but that it is not involved directly in thylakoid membrane formation.
Authors:
Lingang Zhang; Wataru Sakamoto
Related Documents :
24171768 - Nad+-dependent enzymes at the endoplasmic reticulum.
16374718 - Intercellular trafficking of the major tegument protein vp22 of bovine herpesvirus-1 an...
25136968 - Characterizing of functional human coding rna editing from evolutionary, structural and...
3584058 - Molecular characterization of the virc genes of the ti plasmid.
6340738 - Photochemical cross-linking of translation initiation factor 3 to escherichia coli 50s ...
2982148 - Identification of new gene products coded from x regions of human t-cell leukemia viruses.
Publication Detail:
Type:  JOURNAL ARTICLE     Date:  2012-11-15
Journal Detail:
Title:  Plant signaling & behavior     Volume:  8     ISSN:  1559-2324     ISO Abbreviation:  Plant Signal Behav     Publication Date:  2012 Nov 
Date Detail:
Created Date:  2012-11-16     Completed Date:  -     Revised Date:  -    
Medline Journal Info:
Nlm Unique ID:  101291431     Medline TA:  Plant Signal Behav     Country:  -    
Other Details:
Languages:  ENG     Pagination:  -     Citation Subset:  -    
Affiliation:
Institute of Plant Science and Resources; Okayama University; Kurashiki, Okayama, Japan.
Export Citation:
APA/MLA Format     Download EndNote     Download BibTex
MeSH Terms
Descriptor/Qualifier:

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

Full Text
Journal Information
Journal ID (nlm-ta): Plant Signal Behav
Journal ID (iso-abbrev): Plant Signal Behav
Journal ID (publisher-id): PSB
ISSN: 1559-2316
ISSN: 1559-2324
Publisher: Landes Bioscience
Article Information
Download PDF
Copyright © 2013 Landes Bioscience
open-access:
Received Day: 08 Month: 11 Year: 2012
Accepted Day: 12 Month: 11 Year: 2012
Print publication date: Day: 01 Month: 2 Year: 2013
Electronic publication date: Day: 15 Month: 11 Year: 2012
pmc-release publication date: Day: 15 Month: 11 Year: 2012
Volume: 8 Issue: 2
E-location ID: e22860
PubMed Id: 23154508
ID: 3656985
Publisher Id: 2012PSB0402
DOI: 10.4161/psb.22860
Publisher Item Identifier: 22860

Possible function of VIPP1 in thylakoids : Protection but not formation?
Lingang Zhang
Wataru Sakamoto*
Institute of Plant Science and Resources; Okayama University; Kurashiki, Okayama, Japan
*Correspondence to: Wataru Sakamoto, Email: saka@rib.okayama-u.ac.jp

Text

Biomembranes of chloroplasts have been proposed as a prime site of vulnerability to heat and cold stresses in plants.1,2 In general, such abiotic stresses induce damage in any biomembrane and ultimately engender disturbance in the membrane potential.3,4 Because of the presence of multiple membrane systems (outer and inner envelopes and thylakoid membrane), maintenance of membrane integrity within chloroplasts is critically important for plant growth.5,6 However, little has been documented about the mechanism(s) controlling plastid membrane integrity. Chloroplastic biomembranes, when ruptured, are presumably resealed spontaneously. Membrane maintenance has therefore been regarded as a physical process rather than a biochemical reaction. Nevertheless, accumulated evidence in various organisms implies that resealing of the plasma membrane is conducted via a dynamic and complex mechanism that requires novel cytoplasmic factors.7-9 It is reasonable to assume that organelles have similar mechanisms to protect biomembranes from damage.

Our recent work provided insight into a mechanism of plastid envelope maintenance in which Vesicle-Inducing Protein in Plastids1 (VIPP1) plays a pivotal role.10 Although VIPP1 has been originally identified as a factor involved in thylakoid biogenesis, its precise role remains unclear.11,12 VIPP1 is homologous to Phage-shock Protein A (PspA) in Escherichia coli, which is involved in plasma membrane integrity,11-14 and which was shown to recover the defective proton leakage when expressed in E. coli pspA mutant.10 Results showed that the Arabidopsis vipp1 mutants have globular, swollen, balloon-like chloroplasts representing increased osmotic stress of plastid envelope. A series of experiments, including the expression of VIPP1 fused to green fluorescent protein (VIPP1-GFP) in vipp1 mutants, demonstrated that the lattice-like macro complex of VIPP1 acts as scaffold to facilitate the resealing of osmotically damaged chloroplast envelope.10 It is particularly interesting that the dynamic movement of VIPP1-GFP along with envelopes was detectable, which was correlated with osmotic stress (presented as Supplemental Movies). Based on these observations, we concluded that VIPP1 is necessary for plastid envelope maintenance. The question remains as to whether VIPP1 is also involved in thylakoid membrane as originally proposed. Here, we characterize the morphological alteration of thylakoids in vipp1 knock-down mutants (vipp1-kd).

First, the thylakoid ultrastructure in fixed leaf tissues from wild-type Columbia (Col) and vipp1-kd was examined using electron microscopy (Fig. 1). In addition to the balloon-like structure, vipp1-kd chloroplasts exhibited irregular distorted thylakoids. Although thylakoids in Col were abundant in granal stacks that developed uniformly within the chloroplast (Fig. 1A), vipp1-kd showed distorted thylakoids that appeared to segregate into either well-stacked grana or single-membrane regions such as stroma thylakoid (Fig. 1B). In an extreme case, some vipp1-kd chloroplasts contained only several stacks that were tightly clustered (Fig. 1C). It is noteworthy that the clustered granal stacks frequently contained a large lumenal area (Fig. 1B, indicated by an arrow) that was similar to swollen stroma in the balloon-like chloroplasts and which might represent osmotic stress of thylakoid membranes. A similar fluffy structure of thylakoids has also been observed in chloroplasts suffered from water-osmotic stress or high/low temperature,3,15,16 implying that VIPP1 is involved in the maintenance of thylakoid membranes as well as of envelopes.

In addition to these data obtained from electron microscopy, observation of chlorophyll fluorescence with fresh tissue supported the existence of altered grana-like structures (Fig. 2A). Protoplasts prepared from vipp1-kd contained balloon-like chloroplasts in which chlorophyll fluorescence signals tended to form a larger cluster. To test whether the grana stacks observed in vipp1-kd indeed retained functional thylakoid membranes, we attempted to detect light-harvesting complexes of PSII (LHCII). Blue-native gel electrophoresis of solubilized thylakoid membranes indicated that LHCII trimer had accumulated significantly in both Col and vipp1-kd mutant (Fig. 2B). Accumulation of LHCII was confirmed further by SDS-PAGE and subsequent western blot analysis (Fig. 2C). We concluded that the reduction of VIPP1 engenders altered thylakoid morphology, raising the possibility that VIPP1 is a multifunctional protein that affects both envelope and thylakoid membranes. However, the morphological alteration in thylakoids was not a simple reduction but rather a reorganization of the functional thylakoid membranes. Although further analysis is needed, experimental data obtained from our laboratory do not support the model that VIPP1 is involved in the direct formation of thylakoid membranes. Consistent with this inference, recent observations from other laboratories suggest that VIPP1 affects thylakoid formation indirectly through protein complex formation and maintenance, or through protein import across thylakoid membranes.17,18 These data are favorable to a scenario in which VIPP1 acts to protect membranes.


Notes

Previously published online: www.landesbioscience.com/journals/psb/article/22860

Acknowledgments

This work was supported by the Japan Science and Technology Agency (Core Research for Evolutional Science and Technology, to W.S.) and by Oohara Foundation (to W.S.).


Notes


Glossary
Abbreviation:
Col wild-type Columbia
DGDG digalactosyldiacylglycerol
GFP Green Fluorescent Protein
LHCII Light Harvesting Complexes of PSII
MGDG monogalactosyldiacylglycerol
PspA Phage-shock Protein A
VIPP1 Vesicle-Inducing Protein in Plastids1
vipp1-kd vipp1 knock down mutant

References
1. Quinn PJ. Regulation of membrane fluidity in plants. In: Aloia RC, Curtain CC, Gordon LM, ed. Advances in Membrane Fluidity, Physiological Regulation of Membrane Fluidity. Alan R. Liss, Inc., New York. 1988: pp 293-321.
2. Vigh L,Los DA,Horváth I,Murata N. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803.Proc Natl Acad Sci U S AYear: 1993909090410.1073/pnas.90.19.90908415659
3. Heber U. Freezing injury and uncoupling of phosphorylation from electron transport in chloroplastsPlant PhysiolYear: 19674213435010.1104/pp.42.10.134316656661
4. Hincha DK,Oliver AE,Crowe JH. The effects of chloroplast lipids on the stability of liposomes during freezing and dryingBiochim Biophys ActaYear: 199813681506010.1016/S0005-2736(97)00204-69459593
5. Uemura M,Joseph RA,Steponkus PL. Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions)Plant PhysiolYear: 1995109153012228580
6. Thomashow MF. Plant cold acclimation: Freezing tolerance genes and regulatory mechanismsAnnu Rev Plant Physiol Plant Mol BiolYear: 1999505719910.1146/annurev.arplant.50.1.57115012220
7. McNeil PL,Kirchhausen T. An emergency response team for membrane repairNat Rev Mol Cell BiolYear: 2005649950510.1038/nrm166515928713
8. Schapire AL,Voigt B,Jasik J,Rosado A,Lopez-Cobollo R,Menzel D,et al. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viabilityPlant CellYear: 20082033748810.1105/tpc.108.06385919088329
9. Yamazaki T,Kawamura Y,Minami A,Uemura M. Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1Plant CellYear: 200820338940410.1105/tpc.108.06267919088330
10. Zhang L,Kato Y,Otters S,Vothknecht UC,Sakamoto W. Essential role of VIPP1 in chloroplast envelope maintenance in ArabidopsisPlant CellYear: 201224369570710.1105/tpc.112.10360623001039
11. Kroll D,Meierhoff K,Bechtold N,Kinoshita M,Westphal S,Vothknecht UC,et al. VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formationProc Natl Acad Sci U S AYear: 20019842384210.1073/pnas.06150099811274447
12. Westphal S,Heins L,Soll J,Vothknecht UC. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis?Proc Natl Acad Sci U S AYear: 2001984243810.1073/pnas.06150119811274448
13. Brissette JL,Russel M,Weiner L,Model P. Phage shock protein, a stress protein of Escherichia coli.Proc Natl Acad Sci U S AYear: 199087862610.1073/pnas.87.3.8622105503
14. Otters S,Braun P,Hubner J,Wanner G,Vothknecht UC,Chigri F. The first α-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid bindingPlantaYear: 2012 In Press. 10.1007/s00425-012-1772-123053543
15. Ma SF,Lin CY,Chen YM. Comparative studies of chilling stress on alternations of chloroplast ultrastructure and protein synthesis in the leaves of chilling-sensitive (mungbean) and -insensitive (pea) seedlingsBot Bull Acad Sinica (Taiwan)Year: 19903126372
16. Ristic Z,Cass DD. Chloroplast structure after water and high-temperature stress in two lines of maize that differ in endogenous levels of abscisic acidInt J Plant SciYear: 19921531869610.1086/297021
17. Nordhues A,Schöttler MA,Unger AK,Geimer S,Schönfelder S,Schmollinger S,et al. Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas.Plant CellYear: 2012246375910.1105/tpc.111.09269222307852
18. Lo SM,Theg SM. Role of vesicle-inducing protein in plastids 1 in cpTat transport at the thylakoidPlant JYear: 2012716566810.1111/j.1365-313X.2012.05020.x22487220

Figures

[Figure ID: F1]

Figure 1. Chloroplasts in wild-type and vipp1-kd mutant examined using transmission electron microscopy. Chloroplast ultrastructures of Col (A) and vipp1-kd (B and C) mutants were observed using transmission electron microscopy. Extra lumen space (B, red arrow) was detected using electron micrography in vipp1-kd mutants. Furthermore, some larger blocks of mutlilayer membrane structures were found in vipp1-kd chloroplast (C). Bars show 1.0 µm.



[Figure ID: F2]

Figure 2. Accumulation of LHCII in vipp-kd mutant. (A) Chloroplast images of Col and vipp-kd protoplast photographed using fluorescence microscopy. White arrows indicate grana thylakoids. Bars show 10 µm. (B) Photosynthetic supercomplexes located on thylakoid membrane were analyzed using blue native gel. The thylakoid was extracted from the leaves of Col and vipp-kd mutant and incubated with 1% n-dodecyl-β-maltoside (DM) for 1.0 h on ice. Samples were normalized by chlorophyll content and were loaded to 0.75-mm-thick 5–13.5% acrylamide gradient gels. The black arrow indicates the LHCII trimer location. (C) The level of Lhcb1 protein in Col and vipp-kd. Upper panel, western blot probed with the antibody against Lhcb1. Lower panel, a Coomassie-stained gel image is shown as loading control. The red arrow indicates the Lhcb1 position in SDS PAGE.



Article Categories:
  • Addendum

Keywords: Keywords: Arabidopsis, PspA, chloroplast, envelope membrane, grana, osmotic stress, thylakoid biogenesis.

Previous Document:  Sequence diversity and conservation in factors influencing succinate dehydrogenase flavinylation.
Next Document:  Circadian clock and PIF4-mediated external coincidence mechanism coordinately integrates both of the...