The plastid outer envelope protein OEP16 affects metabolic fluxes during ABA-controlled seed development and germination

Journal of Experimental Botany

Volumn 63, Issue 5, 2012, Pages 1919-1936

  Pudelski, Birgit ^a   Schock, Annette ^a   Hoth, Stefan ^b,c   Radchuk, Ruslana ^d   Weber, Hans ^d   Hofmann, Jörg ^b   Sonnewald, Uwe ^b   Soll, Jürgen ^a   Philippar, Katrin ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

^d LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Abscisic acid; amino acid transport; Arabidopsis; outer envelope protein; pea; plastid; seed development; seed metabolite content

Indexed keywords

ABSCISIC ACID; CHLOROPLAST PROTEIN; ISOPROTEIN; PHYTOHORMONE;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PEA; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; PLANT SEED; PLASTID; TRANSPORT AT THE CELLULAR LEVEL;

ABSCISIC ACID; ARABIDOPSIS; BIOLOGICAL TRANSPORT; CHLOROPLAST PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; GERMINATION; MUTATION; PEAS; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT LEAVES; PLASTIDS; PROTEIN ISOFORMS; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; PISUM SATIVUM;

EID: 84858025406     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err375     Document Type: Article

References (72)

1. Angelovici R, Fait A, Fernie AR, Galili G. 2011. A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytologist 189, 148-159.
2. Angelovici R, Fait A, Zhu X, Szymanski J, Feldmesser E, Fernie AR, Galili G. 2009. Deciphering transcriptional and metabolic networks associated with lysine metabolism during Arabidopsis seed development. Plant Physiology 151, 2058-2072.
3. Angelovici R, Galili G, Fernie AR, Fait A. 2010. Seed desiccation: a bridge between maturation and germination. Trends in Plant Science 15, 211-218.
4. Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, Bonner AJ, Holdsworth MJ, Provart NJ. 2011. Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proceedings of the National Academy of Sciences, USA 108, 9709-9714.
5. Bonneville JM, Tichtinsky G. 2010. Correction for 'A plant porphyria related to defects in plastid import of protochlorophyllide oxidoreductase'. Proceedings of the National Academy of Sciences, USA 107, 5693.
6. Bräutigam A, Hofmann-Benning S, Weber APM. 2008a. Comparative proteomics of chloroplast envelopes from C-3 and C-4 plants reveals specific adaptations of the plastid envelope to C-4 photosynthesis and candidate proteins required for maintaining C-4 metabolite fluxes. Plant Physiology 148, 568-579. (Pubitemid 352847591)
7. Bräutigam A, Shrestha RP, Whitten D, Wilkerson CG, Carr KM, Froehlich JE, Weber APM. 2008b. Low-coverage massively parallel pyrosequencing of cDNAs enables proteomics in non-model species: comparison of a species-specific database generated by pyrosequencing with databases from related species for proteome analysis of pea chloroplast envelopes. Journal of Biotechnology 136, 44-53.
8. Bräutigam A, Weber APM. 2009. Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Molecular Plant 6, 1247-1261.
9. Bryant N, Lloyd J, Sweeney C, Myouga F, Meinke D. 2011. Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis. Plant Physiology 155, 1678-1689.
10. Cadman CS, Toorop PE, Hilhorst HW, Finch-Savage WE. 2006. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. The Plant Journal 46, 805-822; (Pubitemid 43780627)
11. Erratum in: Plant Journal 47, 164.
12. Carrera E, Holman T, Medhurst A, Dietrich D, Footitt S, Theodoulou FL, Holdsworth MJ. 2008. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. The Plant Journal 53, 214-224.
13. Carrera E, Holman T, Medhurst A, Peer W, Schmuths H, Footitt S, Theodoulou FL, Holdsworth MJ. 2007. Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination. Plant Physiology 143, 1669-1679. (Pubitemid 46849477)
14. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J. 2004. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131, 5263-5276. (Pubitemid 39562172)
15. Clausen C, Ilkavets I, Thomson R, Philippar K, Vojta A, Möhlmann T, Neuhaus E, Fulgosi H, Soll J. 2004. Intracellular localization of VDAC proteins in plants. Planta 220, 30-37. (Pubitemid 40032996)
16. Drea SC, Lao NT, Wolfe KH, Kavanagh TA. 2006. Gene duplication, exon gain and neofunctionalization of OEP16-related genes in land plants. The Plant Journal 46, 723-735. (Pubitemid 43780620)
17. Drechsel G, Raab S, Hoth S. 2010. Arabidopsis zinc-finger protein 2 is a negative regulator of ABA signaling during seed germination. Plant Physiology 167, 1418-1421.
18. Duy D, Soll J, Philippar K. 2007. Solute channels of the outer membrane: from bacteria to chloroplasts. Biological Chemistry 388, 879-889. (Pubitemid 47258542)
19. Ferro M, Salvi D, Brugiè re S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N. 2003. Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Molecular and Cellular Proteomics 2, 325-345.
20. Finch-Savage WE, Cadman CS, Toorop PE, Lynn JR, Hilhorst HW. 2007. Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. The Plant Journal 51, 60-78. (Pubitemid 46985549)
21. Footitt S, Slocombe SP, Larner V, Kurup S, Wu Y, Larson T, Graham I, Baker A, Holdsworth M. 2002. Control of germination and lipid mobilization by COMATOSE, the Arabidopsis homologue of human ALDP. EMBO Journal 21, 2912-2922. (Pubitemid 34670376)
22. Finkelstein R, Gampala SSL, Rock CD. 2002. Abscisic acid signaling in seeds and seedlings. The Plant Cell 14, 15-45.
23. Finkelstein R, Reeves W, Ariizumi T, Steber C. 2008. Molecular aspects of seed dormancy. Annual Reviews in Plant Biology 59, 387-415. (Pubitemid 351813036)
24. Froehlich JE, Wilkerson CG, Ray WK, McAndrew RS, Osteryoung KW, Gage DA, Phinney BS. 2003. Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilizing alternatives to traditional two-dimensional electrophoresis. Journal of Proteome Research 2, 413-425. (Pubitemid 36988420)
25. Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D. 2002. Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiologia Plantarum 116, 238-247.
26. Galili G. 2011. The aspartate-family pathway of plants: linking production of essential amino acids with energy and stress regulation. Plant Signaling Behaviour 6, 192-195.
27. Goetze TA, Philippar K, Ilkavets I, Soll J, Wagner R. 2006. OEP37 is a new member of the chloroplast outer membrane ion channels. Journal of Biological Chemistry 281, 17989-17998. (Pubitemid 44035598)
28. Gonzali S, Loreti E, Solfanelli C, Novi G, Alpi A, Perata P. 2006. Identification of sugar-modulated genes and evidence for in vivo sugar sensing in Arabidopsis. Journal of Plant Research 119, 115-123.
29. Gould SB, Waller RF, McFadden GI. 2008. Plastid evolution. Annual Review of Plant Biology 59, 491-517. (Pubitemid 351813040)
30. Holdsworth M, Bentsink L, Soppe WJJ. 2008a. Molecular networks regulating Arabidopsis seed maturation, after ripening, dormancy and germination. New Phytologist 179, 33-54. (Pubitemid 351783168)
31. Holdsworth MJ, Finch-Savage WE, Grappin P, Job D. 2008b. Post-genomics dissection of seed dormancy and germination. Trends in Plant Science 13, 7-13.
32. Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S. 2005. Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5, 4864-1884.
33. Honys D, Twell D. 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiology 132, 640-652. (Pubitemid 36715064)
34. Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T. 2005. Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant and Cell Physiology 46, 300-311. (Pubitemid 40413233)
35. Karimi M, De Meyer B, Hilson P. 2005. Modular cloning in plant cells. Trends in Plant Science 10, 103-105. (Pubitemid 40323292)
36. Keegstra K, Youssif AE. 1986. Isolation and characterization of chloroplast envelope membranes. Methods in Enzymology 118, 316-325.
37. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 14, 354-362. (Pubitemid 38431168)
38. Kogel KH, Voll LM, Schäfer P, et al. 2010. Transcriptome and metabolome profiling of field-grown transgenic barley lack induced differences but show cultivar-specific differences. Proceedings of the National Academy of Sciences, USA 107, 6198-6203.
39. Linka N, Weber APM. 2010. Intracellular metabolite transporters in plants. Molecular Plant 3, 21-53.
40. Linke D, Frank J, Pope MS, Soll J, Ilkavets I, Fromme P, Burstein EA, Reshetnyak YK, Emelyanenko VI. 2004. Folding kinetics and structure of OEP16. Biophysical Journal 86, 1479-1487. (Pubitemid 38295583)
41. Lopez-Juez E, Pyke KA. 2005. Plastids unleashed: their development and their integration in plant development. International Journal of Developmental Biology 49, 557-577. (Pubitemid 41615610)
42. Makarevich G, Leroy O, Akinci U, Schubert D, Clarenz O, Goodrich J, Grossniklaus U, Köhler C. 2006. Different polycomb group complexes regulate common target genes in Arabidopsis. EMBO Reports 7, 947-952. (Pubitemid 44523976)
43. Miranda M, Borisjuk L, Tewes A, Heim U, Sauer N, Wobus U, Weber H. 2001. Amino acid permeases in developing seeds of Vicia faba L: expression precedes storage protein synthesis and is regulated by amino acid supply. The Plant Journal 28, 61-71. (Pubitemid 33011509)
44. Murcha MW, Elhafez D, Lister R, Tonti-Filippini J, Baumgartner M, Philippar K, Carrie C, Mokranjac D, Soll J, Whelan J. 2007. Characterisation of the preprotein and amino acids transporter gene family in Arabidopsis. Plant Physiology 134, 199-212. (Pubitemid 46133629)
45. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E. 2005. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. The Plant Journal 41, 697-709. (Pubitemid 40336001)
46. Penfield S, Rylott EL, Gilday AD, Graham S, Larson TR, Graham IA. 2004. Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. The Plant Cell 16, 2705-2718. (Pubitemid 41071357)
47. Philippar K, Geis T, Ilkavets I, Oster U, Schwenkert S, Meurer J, Soll J. 2007. Chloroplast biogenesis: the use of mutants to study the etioplast-chloroplast transition. Proceedings of the National Academy of Sciences, USA 104, 678-683. (Pubitemid 46123084)
48. Philippar K, Soll J. 2007. Intracellular transport: solute transport in chloroplasts, mitochondria, peroxisomes and vacuoles, and between organelles. In: Yeo AR, Flowers TJ, eds. Plant solute transport. Oxford: Blackwell Publishing Ltd, 133-192.
49. Pohlmeyer K, Soll J, Steinkamp T, Hinnah S, Wagner R. 1997. Isolation and characterization of an amino acid-selective channel protein present in the chloroplastic outer envelope membrane. Proceedings of the National Academy of Sciences, USA 94, 9504-9509. (Pubitemid 27357859)
50. Pollmann S, Springer A, Buhr F, Lahroussi A, Samol I, Bonneville JM, Tichtinsky G, von Wettstein D, Reinbothe C, Reinbothe S. 2007. A plant porphyria related to defects in plastid import of protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 104, 2019-2023. (Pubitemid 46239896)
51. Pudelski B, Kraus S, Soll J, Philippar K. 2010. The plant PRAT proteins-preprotein and amino acid transport in mitochandria and chloroplasts. Plant Biology (Stuttgart) 12(Suppl 1), 42-55.
52. Pudelski B, Soll J, Philippar K. 2009. A search for factors influencing etioplast-chloroplast transition. Proceedings of the National Academy of Sciences, USA 106, 12201-12206.
53. Radchuk R, Conrad U, Saalbach I, Giersberg M, Emery RJ, Küster H, Nunes-Nesi A, Fernie AR, Weschke W, Weber H. 2010a. Abscisic acid deficiency of developing pea embryos achieved by immunomodulation attenuates developmental phase transition and storage metabolism. The Plant Journal 64, 715-730.
54. Radchuk R, Emery RJ, Weier D, Vigeolas H, Geigenberger P, Lunn JE, Feil R, Weschke W, Weber H. 2010b. Sucrose nonfermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. The Plant Journal 61, 324-338.
55. Radchuk R, Radchuk V, Weschke W, Borisjuk L, Weber H. 2006. Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiology 140, 263-278. (Pubitemid 43956320)
56. Reinbothe S, Pollmann S, Springer A, James RJ, Tichtinsky G, Reinbothe C. 2005. A role of Toc33 in the protochlorophyllidedependent plastid import pathway of NADPH:protochlorophyllide oxidoreductase (POR) A. The Plant Journal 42, 1-12.
57. Reinbothe S, Quigley F, Springer A, Schemenewitz A, Reinbothe C. 2004. The outer plastid envelope protein Oep16: role as precursor translocase in import of protochlorophyllide oxidoreductase A. Proceedings of the National Academy of Sciences, USA 101, 2203-2208. (Pubitemid 38229039)
58. Riebeseel E, Häusler RE, Radchuk R, et al. 2010. The 2-oxoglutarate/malate translocator mediates amino acid and storage protein biosynthesis in pea embryos. The Plant Journal 61, 350-363.
59. Samol I, Buhr F, Springer A, Pollmann S, Lahroussi A, Rossig C, von Wettstein D, Reinbothe C, Reinbothe S. 2011a. Implication of the oep16-1 mutation in a flu-independent, singlet oxygen-regulated cell death pathway in Arabidopsis thaliana. Plant and Cell Physiology 52, 84-95.
60. Samol I, Rossig C, Buhr F, Springer A, Pollmann S, Lahroussi A, von Wettstein D, Reinbothe C, Reinbothe S. 2011b. The outer chloroplast envelope protein OEP16-1 for plastid import of NADPH:protochlorophyllide oxidoreductase A in Arabidopsis thaliana. Plant and Cell Physiology 52, 96-111.
61. Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J. 2003. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Science 12, 748-759. (Pubitemid 36348462)
62. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU. 2005. A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501-506. (Pubitemid 40617278)
63. Suzuki M, McCarty DR. 2008. Functional symmetry of the B3 network controlling seed development. Current Opinion in Plant Biology 11, 548-553.
64. Steinkamp T, Hill K, Hinnah SC, Wagner R, Rohl T, Pohlmeyer K, Soll J. 2000. Identification of the pore-forming region of the outer chloroplast envelope protein OEP16. Journal of Biological Chemistry 275, 11758-11764. (Pubitemid 30237740)
65. Tegeder M, Offler CE, Frommer WB, Patrick JW. 2000. Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiology 122, 319-326.
66. Tetlow IJ, Rawsthorne S, Raines C, Emes MJ. 2005. Plastid metabolic pathways. In: Möller SG, ed. Plastids. Oxford: Blackwell Publishing Ltd, 60-125.
67. Waegemann K, Eichacker S, Soll J. 1992. Outer envelope membranes from chloroplasts are isolated as right-side-out vesicles. Planta 187, 89-94.
68. Weber H, Borisjuk L, Wobus U. 2005. Molecular physiology of legume seed development. Annual Review of Plant Biology 56, 253-279. (Pubitemid 40802410)
69. Weigelt K, Küster H, Radchuk R, Müller M, Weichert H, Fait A, Fernie AR, Saalbach I, Weber H. 2008. Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. The Plant Journal 55, 909-926.
70. Wirtz M, Droux M. 2005. Synthesis of the sulfur amino acids: cysteine and methionine. Photosynthesis Research 86, 345-362. (Pubitemid 43042760)
71. Yamagishi K, Tatematsu K, Yano R, Preston J, Kitamura S, Takahashi H, McCourt P, Kamiya Y, Nambara E. 2009. CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant and Cell Physiology 50, 330-340.
72. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ. 2008. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994.