A dynamin-like protein in Arabidopsis thaliana is involved in biogenesis of thylakoid membranes (original) (raw)
Abstract
Dynamin, a GTP-binding protein found in rat brain, plays a role in endocytosis. Suborganellar fractionation studies of Arabidopsis leaf tissue revealed that a dynamin-like protein, ADL1, is localized in the thylakoid membranes of chloroplasts. This notion was supported further by in vivo targeting experiments using an ADL1-green fluorescent fusion protein and immunogold labeling with the anti-ADL1 antibody. Transgenic plants harboring various deletion mutant genes of ADL1 had a yellow leaf phenotype where the cells had very few chloroplasts. In addition, the remaining chloroplasts appeared morphologically not fully developed. The detailed structure of the chloroplasts revealed by electron microscopy showed a greatly reduced amount of thylakoid membranes. Also, the level of thylakoid membrane proteins such as the light-harvesting complex II and CP29 was greatly reduced in these transgenic plants. When we examined the expression of the ADL1 deletion mutant genes, these genes were highly expressed at the transcriptional level. However, the mutant ADL1s were not detectable at the protein level by Western blot analysis. Moreover, the endogenous ADL1 protein level was greatly reduced in these transgenic plants, probably due to a post-transcriptional silencing effect of the transgenes. We propose, therefore, that ADLl is involved in the biogenesis of thylakoid membranes.
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- Aebi M., Fäh J., Hurt N., Samuel C. E., Thomis D., Bazzigher L., Pavlovic J., Haller O., Staeheli P. cDNA structures and regulation of two interferon-induced human Mx proteins. Mol Cell Biol. 1989 Nov;9(11):5062–5072. doi: 10.1128/mcb.9.11.5062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Apel K., Gollmer I., Batschauer A. The light-dependent control of chloroplast development in barley (Hordeum vulgare L). J Cell Biochem. 1983;23(1-4):181–189. doi: 10.1002/jcb.240230115. [DOI] [PubMed] [Google Scholar]
- Bergantino E., Dainese P., Cerovic Z., Sechi S., Bassi R. A post-translational modification of the photosystem II subunit CP29 protects maize from cold stress. J Biol Chem. 1995 Apr 14;270(15):8474–8481. doi: 10.1074/jbc.270.15.8474. [DOI] [PubMed] [Google Scholar]
- Chen M. S., Obar R. A., Schroeder C. C., Austin T. W., Poodry C. A., Wadsworth S. C., Vallee R. B. Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature. 1991 Jun 13;351(6327):583–586. doi: 10.1038/351583a0. [DOI] [PubMed] [Google Scholar]
- Cline K., Werner-Washburne M., Lubben T. H., Keegstra K. Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. J Biol Chem. 1985 Mar 25;260(6):3691–3696. [PubMed] [Google Scholar]
- Cook T. A., Urrutia R., McNiven M. A. Identification of dynamin 2, an isoform ubiquitously expressed in rat tissues. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):644–648. doi: 10.1073/pnas.91.2.644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Damke H., Baba T., Warnock D. E., Schmid S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol. 1994 Nov;127(4):915–934. doi: 10.1083/jcb.127.4.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dombrowski J. E., Raikhel N. V. Isolation of a cDNA encoding a novel GTP-binding protein of Arabidopsis thaliana. Plant Mol Biol. 1995 Sep;28(6):1121–1126. doi: 10.1007/BF00032672. [DOI] [PubMed] [Google Scholar]
- Gammie A. E., Kurihara L. J., Vallee R. B., Rose M. D. DNM1, a dynamin-related gene, participates in endosomal trafficking in yeast. J Cell Biol. 1995 Aug;130(3):553–566. doi: 10.1083/jcb.130.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gout I., Dhand R., Hiles I. D., Fry M. J., Panayotou G., Das P., Truong O., Totty N. F., Hsuan J., Booker G. W. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell. 1993 Oct 8;75(1):25–36. [PubMed] [Google Scholar]
- Gu X., Verma D. P. Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division. Plant Cell. 1997 Feb;9(2):157–169. doi: 10.1105/tpc.9.2.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gu X., Verma D. P. Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants. EMBO J. 1996 Feb 15;15(4):695–704. [PMC free article] [PubMed] [Google Scholar]
- Hall A., Brown R. Human N-ras: cDNA cloning and gene structure. Nucleic Acids Res. 1985 Jul 25;13(14):5255–5268. doi: 10.1093/nar/13.14.5255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herskovits J. S., Burgess C. C., Obar R. A., Vallee R. B. Effects of mutant rat dynamin on endocytosis. J Cell Biol. 1993 Aug;122(3):565–578. doi: 10.1083/jcb.122.3.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herskovits J. S., Shpetner H. S., Burgess C. C., Vallee R. B. Microtubules and Src homology 3 domains stimulate the dynamin GTPase via its C-terminal domain. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11468–11472. doi: 10.1073/pnas.90.24.11468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horisberger M. A., McMaster G. K., Zeller H., Wathelet M. G., Dellis J., Content J. Cloning and sequence analyses of cDNAs for interferon- and virus-induced human Mx proteins reveal that they contain putative guanine nucleotide-binding sites: functional study of the corresponding gene promoter. J Virol. 1990 Mar;64(3):1171–1181. doi: 10.1128/jvi.64.3.1171-1181.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hugueney P., Bouvier F., Badillo A., d'Harlingue A., Kuntz M., Camara B. Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5630–5634. doi: 10.1073/pnas.92.12.5630. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones B. A., Fangman W. L. Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 1992 Mar;6(3):380–389. doi: 10.1101/gad.6.3.380. [DOI] [PubMed] [Google Scholar]
- Karlin-Neumann G. A., Tobin E. M. Transit peptides of nuclear-encoded chloroplast proteins share a common amino acid framework. EMBO J. 1986 Jan;5(1):9–13. doi: 10.1002/j.1460-2075.1986.tb04170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li H. M., Moore T., Keegstra K. Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell. 1991 Jul;3(7):709–717. doi: 10.1105/tpc.3.7.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma H., Yanofsky M. F., Meyerowitz E. M. Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1990 May;87(10):3821–3825. doi: 10.1073/pnas.87.10.3821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Melis A. Light regulation of photosynthetic membrane structure, organization, and function. J Cell Biochem. 1984;24(3):271–285. doi: 10.1002/jcb.240240308. [DOI] [PubMed] [Google Scholar]
- Miki H., Miura K., Matuoka K., Nakata T., Hirokawa N., Orita S., Kaibuchi K., Takai Y., Takenawa T. Association of Ash/Grb-2 with dynamin through the Src homology 3 domain. J Biol Chem. 1994 Feb 25;269(8):5489–5492. [PubMed] [Google Scholar]
- Morré D. J., Selldén G., Sundqvist C., Sandelius A. S. Stromal low temperature compartment derived from the inner membrane of the chloroplast envelope. Plant Physiol. 1991 Dec;97(4):1558–1564. doi: 10.1104/pp.97.4.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakata T., Takemura R., Hirokawa N. A novel member of the dynamin family of GTP-binding proteins is expressed specifically in the testis. J Cell Sci. 1993 May;105(Pt 1):1–5. doi: 10.1242/jcs.105.1.1. [DOI] [PubMed] [Google Scholar]
- Obar R. A., Collins C. A., Hammarback J. A., Shpetner H. S., Vallee R. B. Molecular cloning of the microtubule-associated mechanochemical enzyme dynamin reveals homology with a new family of GTP-binding proteins. Nature. 1990 Sep 20;347(6290):256–261. doi: 10.1038/347256a0. [DOI] [PubMed] [Google Scholar]
- Park J. M., Kang S. G., Pih K. T., Jang H. J., Piao H. L., Yoon H. W., Cho M. J., Hwang I. A dynamin-like protein, ADL1, is present in membranes as a high-molecular-mass complex in Arabidopsis thaliana. Plant Physiol. 1997 Oct;115(2):763–771. doi: 10.1104/pp.115.2.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robinson P. J., Sontag J. M., Liu J. P., Fykse E. M., Slaughter C., McMahon H., Südhof T. C. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature. 1993 Sep 9;365(6442):163–166. doi: 10.1038/365163a0. [DOI] [PubMed] [Google Scholar]
- Roth J., Bendayan M., Carlemalm E., Villiger W., Garavito M. Enhancement of structural preservation and immunocytochemical staining in low temperature embedded pancreatic tissue. J Histochem Cytochem. 1981 May;29(5):663–671. doi: 10.1177/29.5.6166664. [DOI] [PubMed] [Google Scholar]
- Rothman J. H., Raymond C. K., Gilbert T., O'Hara P. J., Stevens T. H. A putative GTP binding protein homologous to interferon-inducible Mx proteins performs an essential function in yeast protein sorting. Cell. 1990 Jun 15;61(6):1063–1074. doi: 10.1016/0092-8674(90)90070-u. [DOI] [PubMed] [Google Scholar]
- Seedorf K., Kostka G., Lammers R., Bashkin P., Daly R., Burgess W. H., van der Bliek A. M., Schlessinger J., Ullrich A. Dynamin binds to SH3 domains of phospholipase C gamma and GRB-2. J Biol Chem. 1994 Jun 10;269(23):16009–16014. [PubMed] [Google Scholar]
- Seedorf M., Waegemann K., Soll J. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 1995 Mar;7(3):401–411. doi: 10.1046/j.1365-313x.1995.7030401.x. [DOI] [PubMed] [Google Scholar]
- Seo S., Okamoto M., Seto H., Ishizuka K., Sano H., Ohashi Y. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science. 1995 Dec 22;270(5244):1988–1992. doi: 10.1126/science.270.5244.1988. [DOI] [PubMed] [Google Scholar]
- Sheen J., Hwang S., Niwa Y., Kobayashi H., Galbraith D. W. Green-fluorescent protein as a new vital marker in plant cells. Plant J. 1995 Nov;8(5):777–784. doi: 10.1046/j.1365-313x.1995.08050777.x. [DOI] [PubMed] [Google Scholar]
- Shpetner H. S., Vallee R. B. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell. 1989 Nov 3;59(3):421–432. doi: 10.1016/0092-8674(89)90027-5. [DOI] [PubMed] [Google Scholar]
- Smeekens S., Bauerle C., Hageman J., Keegstra K., Weisbeek P. The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell. 1986 Aug 1;46(3):365–375. doi: 10.1016/0092-8674(86)90657-4. [DOI] [PubMed] [Google Scholar]
- Sundqvist C., Björn L. O., Virgin H. I. Factors in chloroplast differentiation. Results Probl Cell Differ. 1980;10:201–224. doi: 10.1007/978-3-540-38255-3_7. [DOI] [PubMed] [Google Scholar]
- Takeuchi Y., Dotson M., Keen N. T. Plant transformation: a simple particle bombardment device based on flowing helium. Plant Mol Biol. 1992 Feb;18(4):835–839. doi: 10.1007/BF00020031. [DOI] [PubMed] [Google Scholar]
- Vallee R. B., Okamoto P. M. The regulation of endocytosis: identifying dynamin's binding partners. Trends Cell Biol. 1995 Feb;5(2):43–47. doi: 10.1016/s0962-8924(00)88937-0. [DOI] [PubMed] [Google Scholar]
- Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vater C. A., Raymond C. K., Ekena K., Howald-Stevenson I., Stevens T. H. The VPS1 protein, a homolog of dynamin required for vacuolar protein sorting in Saccharomyces cerevisiae, is a GTPase with two functionally separable domains. J Cell Biol. 1992 Nov;119(4):773–786. doi: 10.1083/jcb.119.4.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilsbach K., Payne G. S. Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. EMBO J. 1993 Aug;12(8):3049–3059. doi: 10.1002/j.1460-2075.1993.tb05974.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Carvalho F., Gheysen G., Kushnir S., Van Montagu M., Inzé D., Castresana C. Suppression of beta-1,3-glucanase transgene expression in homozygous plants. EMBO J. 1992 Jul;11(7):2595–2602. doi: 10.1002/j.1460-2075.1992.tb05324.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van der Bliek A. M., Meyerowitz E. M. Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature. 1991 May 30;351(6325):411–414. doi: 10.1038/351411a0. [DOI] [PubMed] [Google Scholar]