First published online February 3, 2006; 10.1104/pp.105.076083
Plant Physiology 140:984-997 (2006)
© 2006 American Society of Plant Biologists
GENETICS, GENOMICS, AND MOLECULAR EVOLUTION
Protein Profiling of Plastoglobules in Chloroplasts and Chromoplasts. A Surprising Site for Differential Accumulation of Metabolic Enzymes1,[W]
A. Jimmy Ytterberg,
Jean-Benoit Peltier2 and
Klaas J. van Wijk*
Department of Plant Biology, Cornell University, Ithaca, New York 14853
Plastoglobules (PGs) are oval or tubular lipid-rich structures present in all plastid types, but their specific functions are unclear. PGs contain quinones, -tocopherol, and lipids and, in chromoplasts, carotenoids as well. It is not known whether PGs contain any enzymes or regulatory proteins. Here, we determined the proteome of PGs from chloroplasts of stressed and unstressed leaves of Arabidopsis (Arabidopsis thaliana) as well as from pepper (Capsicum annuum) fruit chromoplasts using mass spectrometry. Together, this showed that the proteome of chloroplast PGs consists of seven fibrillins, providing a protein coat and preventing coalescence of the PGs, and an additional 25 proteins likely involved in metabolism of isoprenoid-derived molecules (quinines and tocochromanols), lipids, and carotenoid cleavage. Four unknown ABC1 kinases were identified, possibly involved in regulation of quinone monooxygenases. Most proteins have not been observed earlier but have predicted N-terminal chloroplast transit peptides and lack transmembrane domains, consistent with localization in the PG lipid monolayer particles. Quantitative differences in PG composition in response to high light stress and degreening were determined by differential stable-isotope labeling using formaldehyde. More than 20 proteins were identified in the PG proteome of pepper chromoplasts, including four enzymes of carotenoid biosynthesis and several homologs of proteins observed in the chloroplast PGs. Our data strongly suggest that PGs in chloroplasts form a functional metabolic link between the inner envelope and thylakoid membranes and play a role in breakdown of carotenoids and oxidative stress defense, whereas PGs in chromoplasts are also an active site for carotenoid conversions.
1 This work was supported by grants from the U.S. Department of Agriculture (USDA-Biochemistry; grant no. 20033510013579) and New York Science and Technology and Research to K.J.v.W.
2 Present address: Laboratoire de Protéomique 2, Place Viala 34060, Montpellier cedex 1, France.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Klaas J. van Wijk (kv35{at}cornell.edu).
[W] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.076083.
* Corresponding author; e-mail kv35{at}cornell.edu; fax 6072555407.
Received December 22, 2005;
returned for revision January 19, 2006;
accepted January 19, 2006.
Related articles in Plant Physiol.:
- On the Inside
- Peter V. Minorsky
Plant Physiol. 2006 140: 791-792.
[Full Text]
This article has been cited by other articles:

|
 |

|
 |
 
F.-C. Huang, P. Molnar, and W. Schwab
Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes
J. Exp. Bot.,
May 12, 2009;
(2009)
erp137v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Schelbert, S. Aubry, B. Burla, B. Agne, F. Kessler, K. Krupinska, and S. Hortensteiner
Pheophytin Pheophorbide Hydrolase (Pheophytinase) Is Involved in Chlorophyll Breakdown during Leaf Senescence in Arabidopsis
PLANT CELL,
March 1, 2009;
21(3):
767 - 785.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Desplats, F. Mus, S. Cuine, E. Billon, L. Cournac, and G. Peltier
Characterization of Nda2, a Plastoquinone-reducing Type II NAD(P)H Dehydrogenase in Chlamydomonas Chloroplasts
J. Biol. Chem.,
February 13, 2009;
284(7):
4148 - 4157.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. S. Kudryashov, Z. A. O. Durer, A. J. Ytterberg, M. R. Sawaya, I. Pashkov, K. Prochazkova, T. O. Yeates, R. R. O. Loo, J. A. Loo, K. J. F. Satchell, et al.
Connecting actin monomers by iso-peptide bond is a toxicity mechanism of the Vibrio cholerae MARTX toxin
PNAS,
November 25, 2008;
105(47):
18537 - 18542.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. S. Floss, W. Schliemann, J. Schmidt, D. Strack, and M. H. Walter
RNA Interference-Mediated Repression of MtCCD1 in Mycorrhizal Roots of Medicago truncatula Causes Accumulation of C27 Apocarotenoids, Shedding Light on the Functional Role of CCD1
Plant Physiology,
November 1, 2008;
148(3):
1267 - 1282.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Rubio, J. L. Rambla, M. Santaella, M. D. Gomez, D. Orzaez, A. Granell, and L. Gomez-Gomez
Cytosolic and Plastoglobule-targeted Carotenoid Dioxygenases from Crocus sativus Are Both Involved in {beta}-Ionone Release
J. Biol. Chem.,
September 5, 2008;
283(36):
24816 - 24825.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Majeran, B. Zybailov, A. J. Ytterberg, J. Dunsmore, Q. Sun, and K. J. van Wijk
Consequences of C4 Differentiation for Chloroplast Membrane Proteomes in Maize Mesophyll and Bundle Sheath Cells
Mol. Cell. Proteomics,
September 1, 2008;
7(9):
1609 - 1638.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Rutschow, A. J. Ytterberg, G. Friso, R. Nilsson, and K. J. van Wijk
Quantitative Proteomics of a Chloroplast SRP54 Sorting Mutant and Its Genetic Interactions with CLPC1 in Arabidopsis
Plant Physiology,
September 1, 2008;
148(1):
156 - 175.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Grennan
Plastoglobule Proteome
Plant Physiology,
June 1, 2008;
147(2):
443 - 445.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Jasinski, D. Sudre, G. Schansker, M. Schellenberg, S. Constant, E. Martinoia, and L. Bovet
AtOSA1, a Member of the Abc1-Like Family, as a New Factor in Cadmium and Oxidative Stress Response
Plant Physiology,
June 1, 2008;
147(2):
719 - 731.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. S. Merchant, S. E. Prochnik, O. Vallon, E. H. Harris, S. J. Karpowicz, G. B. Witman, A. Terry, A. Salamov, L. K. Fritz-Laylin, L. Marechal-Drouard, et al.
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions
Science,
October 12, 2007;
318(5848):
245 - 250.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Kleine, P. Kindgren, C. Benedict, L. Hendrickson, and A. Strand
Genome-Wide Gene Expression Analysis Reveals a Critical Role for CRYPTOCHROME1 in the Response of Arabidopsis to High Irradiance
Plant Physiology,
July 1, 2007;
144(3):
1391 - 1406.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Padham, M. T. Hopkins, T.-W. Wang, L. M. McNamara, M. Lo, L. G.L. Richardson, M. D. Smith, C. A. Taylor, and J. E. Thompson
Characterization of a Plastid Triacylglycerol Lipase from Arabidopsis
Plant Physiology,
March 1, 2007;
143(3):
1372 - 1384.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Leitner-Dagan, M. Ovadis, E. Shklarman, Y. Elad, D. Rav David, and A. Vainstein
Expression and Functional Analyses of the Plastid Lipid-Associated Protein CHRC Suggest Its Role in Chromoplastogenesis and Stress
Plant Physiology,
September 1, 2006;
142(1):
233 - 244.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Austin II, E. Frost, P.-A. Vidi, F. Kessler, and L. A. Staehelin
Plastoglobules Are Lipoprotein Subcompartments of the Chloroplast That Are Permanently Coupled to Thylakoid Membranes and Contain Biosynthetic Enzymes
PLANT CELL,
July 1, 2006;
18(7):
1693 - 1703.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Rudella, G. Friso, J. M. Alonso, J. R. Ecker, and K. J. van Wijk
Downregulation of ClpR2 Leads to Reduced Accumulation of the ClpPRS Protease Complex and Defects in Chloroplast Biogenesis in Arabidopsis
PLANT CELL,
July 1, 2006;
18(7):
1704 - 1721.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Giacomelli, A. Rudella, and K. J. van Wijk
High Light Response of the Thylakoid Proteome in Arabidopsis Wild Type and the Ascorbate-Deficient Mutant vtc2-2. A Comparative Proteomics Study
Plant Physiology,
June 1, 2006;
141(2):
685 - 701.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E Olmos, G Kiddle, T. Pellny, S Kumar, and C. Foyer
Modulation of plant morphology, root architecture, and cell structure by low vitamin C in Arabidopsis thaliana
J. Exp. Bot.,
May 1, 2006;
57(8):
1645 - 1655.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|