Cain, Peter, Holdermann, Iris, Sinning, Irmgard, Johnson, Arthur E. (Arthur Edward), 1942- and Robinson, Colin. (2011) Binding of chloroplast signal recognition particle to a thylakoid membrane protein substrate in aqueous solution and delineation of the cpSRP43–substrate interaction domain. Biochemical Journal, Vol.437 (No.1). pp. 149-155. ISSN 0264-6021

Preview

PDF WRAP_cain_0380313-lf-101111-cain_et_al.pdf - Accepted Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (3278Kb)

Abstract

A cpSRP [chloroplast SRP (signal recognition particle)] comprising cpSRP54 and cpSRP43 subunits mediates the insertion of light-harvesting proteins into the thylakoid membrane. We dissected its interaction with a full-length membrane protein substrate in aqueous solution by insertion of site-specific photoactivatable cross-linkers into in vitro-synthesized Lhcb1 (major light-harvesting chlorophyll-binding protein of photosystem II). We show that Lhcb1 residues 166-176 cross-link specifically to the cpSRP43 subunit. Some cross-link positions within Lhcb1 are in the 'L18' peptide required for targeting of cpSRP substrates, whereas other cross-linking positions define a new targeting signal in the third transmembrane span. Lhcb1 was not found to cross-link to cpSRP54 at any position, and cross-linking to cpSRP43 is unaffected by the absence of cpSRP54. cpSRP43 thus effectively binds substrates autonomously, and its ability to independently bind an extended 20+-residue substrate region highlights a major difference with other SRP types where the SRP54 subunit binds to hydrophobic target sequences. The results also show that cpSRP43 can bind to a hydrophobic, three-membrane span, substrate in aqueous solution, presumably reflecting a role for cpSRP in the chloroplast stroma. This mode of action, and the specificity of the cpSRP43 substrate interaction, may be associated with cpSRP's unique post-translational mode of action.

[error in script] [error in script]

Item Type:	Journal Article
Subjects:	Q Science > QK Botany
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Chloroplasts -- Physiology, Plant proteins
Journal or Publication Title:	Biochemical Journal
Publisher:	Portland Press
ISSN:	0264-6021
Date:	1 July 2011
Volume:	Vol.437
Number:	No.1
Page Range:	pp. 149-155
Identification Number:	10.1042/BJ20110270
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), National Institutes of Health (U.S.) (NIH), Robert A. Welch Foundation
Grant number:	GM26494 (NIH), BE-0017 (Robert A. Welch Foundation)
References:	[1]. Luirink, J. and Sinning, I. (2004). SRP-mediated protein targeting: structure and function revisited. Biochim. Biophys. Acta, 1694, 17-35. [2]. Driessen, A.J., and Nouwen, N. (2008). Protein translocation across the bacterial cytoplasmic membrane. Annu. Rev. Biochem. 77, 643-667. [3]. Eichacker, L.A. and Henry, R. (2001) Function of a chloroplast SRP in thylakoid protein export. Biochim Biophys Acta, 1541, 120-134. [4]. Kogata, N., Nishio, K., Hirohashi, T., Kikuchi, S. and Nakai, M. (1999). Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids. FEBS letts, 447, 329-333. [5]. Li, X., Henry, R., Yuan, J., Cline, K. and Hoffman, N.E. (1995). A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc. Natl. Acad. Sci. USA, 92, 3789-3793. [6]. Moore, M., Harrison, M.S., Peterson, E.C. and Henry, R. (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J. Biol. Chem. 275, 1529-1532. [7]. Schuenemann, D., Gupta, S., Persello-Cartieaux, F., Klimyuk, V.I., Jones, J.D.G., Nussaume, L. and Hoffman, N.E. (1998). A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc. Natl. Acad. Sci. USA, 95, 10312-10316. [8]. Kim, S.J., Jansson, S., Hoffman, N.E., Robinson, C. and Mant, A. (1999). Distinct "assisted" and "spontaneous" mechanisms for the insertion of polytopic chlorophyll-binding proteins into the thylakoid membrane. J. Biol. Chem. 274, 4715-4721. [9]. Robinson, C., Thompson, S.J. and Woolhead, C. (2001) Multiple pathways used for the targeting of thylakoid proteins in chloroplasts. Traffic 2, 245-251. [10]. Schleiff, E. and Klosgen, R.B. (2001) Without a little help from 'my' friends: direct insertion of proteins into chloroplast membranes? Biochim Biophys Acta, 1541, 22-33. [11]. Woolhead, C.A., Thompson, S.J., Moore, M., Tissier, C., Mant, A., Rodger, A., Henry, R. and Robinson, C. (2001) Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion. J. Biol. Chem. 276, 40841-40846. [12]. DeLille, J., Peterson, E.C., Johnson, T., Moore, M., Kight, A. and Henry, R. (2000) A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc. Natl. Acad. Sci. USA, 97, 1926-1931. [13]. Tu, C.J., Peterson, E.C., Henry, R. and Hoffman, N.E. (2000) The L18 domain of lightharvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J. Biol. Chem. 275, 13187-13190. [14]. Groves, M.R., Mant, A., Kuhn, A., Koch, J., Dubel, S., Robinson, C. and Sinning, I. (2001). Functional characterization of recombinant chloroplast signal recognition particle. J. Biol. Chem. 276, 27778-27786. [15]. Zhang, H., Wang, J. and Goodman, H.M. (1994) Expression of the Arabidopsis Gene Akr Coincides with Chloroplast Development. Plant Physiol, 106, 1261-1267. [16]. Klimyuk, V.I., Persello-Cartieaux, F., Havaux, M., Contard-David, P., Schuenemann, D., Meiherhoff, K., Gouet, P., Jones, J.D., Hoffman, N.E. and Nussaume, L. (1999) A chromodomain protein encoded by the arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11, 87-99. [17]. Sivaraja, V., Kumar, T.K., Leena, P.S., Chang, A.N., Vidya, C., Goforth, R.L., Rajalingam, D., Arvind, K., Ye, J.L., Chou, J., Henry, R. and Yu, C. (2005) Three-Dimensional Solution Structures of the Chromodomains of cpSRP43. J. Biol. Chem. 280, 41465-41471. [18]. Stengel, K.F., Holdermann, I., Cain, P., Robinson, C., Wild, K. and Sinning, I. (2008) Structural basis for specific substrate recognition by the chloroplast signal recognition rarticle protein cpSRP43. Science 321, 253-256. [19]. Wild, K., Halic, M., Sinning, I. and Beckmann, R. (2004) SRP meets the ribosome. Nat Struct Mol Biol, 11, 1049-1053. [20]. Flanagan, J.J., Chen, J.C., Miao, Y., Shao, Y., Lin, J., Bock, P.E. and Johnson, A.E. (2003). Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 278, 18628-18637. [21]. McCormick, P.J., Miao, Y., Shao, Y., Lin, J. and Johnson, A.E. (2003) Cotranslational protein integration into the ER membrane is mediated by the binding of nascent chains to translocon proteins. Molecular Cell, 12, 329-341. [22]. Crowley, K.S., Reinhart, G.D. and Johnson, A.E. (1993) The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell, 73, 1101-1115. [23]. Krieg, U.C., Walter, P. and Johnson, A.E. (1986). Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc. Natl. Acad. Sci. USA, 83, 8604-8608. [24]. Standfuss, J., Terwisscha, A.C., van Scheltinga, S., Lamborghini, M. and W Kuhlbrandt. 2005. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J. 24, 919-928. [25]. High, S., Henry, R., Mould, R.M., Valent, Q., Meacock, S., Cline, K., Gray, J.C. and Luirink, J. (1997) Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J. Biol. Chem. 272, 11622-11628. [26]. Falk S, and Sinning, I. (2010). cpSRP43 is a novel chaperone specific for light-harvesting chlorophyll a,b binding proteins. J. Biol. Chem. In press. [27]. Jaru-Ampornpan, P., Shen, K., Lam, V.Q., Ali, M., Doniach, S., Jia, T.Z. and Shan, S-O. (2010). ATP-independent reversal of a membrane protein aggregate by a chloroplast SRP subunit. Nat. Struct. Mol. Biol. 17, 696-702.
URI:	http://wrap.warwick.ac.uk/id/eprint/38677

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item