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. 1999 Jan;11(1):87–99. doi: 10.1105/tpc.11.1.87

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.

V I Klimyuk 1, F Persello-Cartieaux 1, M Havaux 1, P Contard-David 1, D Schuenemann 1, K Meiherhoff 1, P Gouet 1, J D Jones 1, N E Hoffman 1, L Nussaume 1
PMCID: PMC144089  PMID: 9878634

Abstract

A recessive mutation in Arabidopsis, named chaos (for chlorophyll a/b binding protein harvesting-organelle specific; designated gene symbol CAO), was isolated by using transposon tagging. Characterization of the phenotype of the chaos mutant revealed a specific reduction of pigment binding antenna proteins in the thylakoid membrane. These nuclear-encoded proteins utilize a chloroplast signal recognition particle (cpSRP) system to reach the thylakoid membrane. Both prokaryotes and eukaryotes possess a cytoplasmic SRP containing a 54-kD protein (SRP54) and an RNA. In chloroplasts, the homolog of SRP54 was found to bind a 43-kD protein (cpSRP43) rather than to an RNA. We cloned the CAO gene, which encodes a protein identified as Arabidopsis cpSRP43. The product of the CAO gene does not resemble any protein in the databases, although it contains motifs that are known to mediate protein-protein interactions. These motifs include ankyrin repeats and chromodomains. Therefore, CAO encodes an SRP component that is unique to plants. Surprisingly, the phenotype of the cpSRP43 mutant (i.e., chaos) differs from that of the Arabidopsis cpSRP54 mutant, suggesting that the functions of the two proteins do not strictly overlap. This difference also suggests that the function of cpSRP43 is most likely restricted to protein targeting into the thylakoid membrane, whereas cpSRP54 may be involved in an additional process(es), such as chloroplast biogenesis, perhaps through chloroplast-ribosomal association with chloroplast ribosomes.

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Selected References

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  1. Aasland R., Stewart A. F. The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucleic Acids Res. 1995 Aug 25;23(16):3168–3173. doi: 10.1093/nar/23.16.3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Auchincloss A. H., Alexander A., Kohorn B. D. Requirement for three membrane-spanning alpha-helices in the post-translational insertion of a thylakoid membrane protein. J Biol Chem. 1992 May 25;267(15):10439–10446. [PubMed] [Google Scholar]
  4. Ball L. J., Murzina N. V., Broadhurst R. W., Raine A. R., Archer S. J., Stott F. J., Murzin A. G., Singh P. B., Domaille P. J., Laue E. D. Structure of the chromatin binding (chromo) domain from mouse modifier protein 1. EMBO J. 1997 May 1;16(9):2473–2481. doi: 10.1093/emboj/16.9.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bassi R., Pineau B., Dainese P., Marquardt J. Carotenoid-binding proteins of photosystem II. Eur J Biochem. 1993 Mar 1;212(2):297–303. doi: 10.1111/j.1432-1033.1993.tb17662.x. [DOI] [PubMed] [Google Scholar]
  6. Bork P. Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins. 1993 Dec;17(4):363–374. doi: 10.1002/prot.340170405. [DOI] [PubMed] [Google Scholar]
  7. Boutry M., Chua N. H. A nuclear gene encoding the beta subunit of the mitochondrial ATP synthase in Nicotiana plumbaginifolia. EMBO J. 1985 Sep;4(9):2159–2165. doi: 10.1002/j.1460-2075.1985.tb03910.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cline K., Henry R. Import and routing of nucleus-encoded chloroplast proteins. Annu Rev Cell Dev Biol. 1996;12:1–26. doi: 10.1146/annurev.cellbio.12.1.1. [DOI] [PubMed] [Google Scholar]
  9. Cline K. Import of proteins into chloroplasts. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J Biol Chem. 1986 Nov 5;261(31):14804–14810. [PubMed] [Google Scholar]
  10. Cowell I. G., Austin C. A. Self-association of chromo domain peptides. Biochim Biophys Acta. 1997 Feb 8;1337(2):198–206. doi: 10.1016/s0167-4838(96)00165-3. [DOI] [PubMed] [Google Scholar]
  11. Dörmann P., Hoffmann-Benning S., Balbo I., Benning C. Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell. 1995 Nov;7(11):1801–1810. doi: 10.1105/tpc.7.11.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fedoroff N. V. About maize transposable elements and development. Cell. 1989 Jan 27;56(2):181–191. doi: 10.1016/0092-8674(89)90891-x. [DOI] [PubMed] [Google Scholar]
  13. Franklin A. E., Hoffman N. E. Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J Biol Chem. 1993 Oct 15;268(29):22175–22180. [PubMed] [Google Scholar]
  14. Gavel Y., von Heijne G. A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 1990 Feb 26;261(2):455–458. doi: 10.1016/0014-5793(90)80614-o. [DOI] [PubMed] [Google Scholar]
  15. Hand J. M., Szabo L. J., Vasconcelos A. C., Cashmore A. R. The transit peptide of a chloroplast thylakoid membrane protein is functionally equivalent to a stromal-targeting sequence. EMBO J. 1989 Nov;8(11):3195–3206. doi: 10.1002/j.1460-2075.1989.tb08478.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Henikoff S., Comai L. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics. 1998 May;149(1):307–318. doi: 10.1093/genetics/149.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hoffman N. E., Franklin A. E. Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b-binding polypeptide into thylakoid membranes. Plant Physiol. 1994 May;105(1):295–304. doi: 10.1104/pp.105.1.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Huang L., Adam Z., Hoffman N. E. Deletion Mutants of Chlorophyll a/b Binding Proteins Are Efficiently Imported into Chloroplasts but Do Not Integrate into Thylakoid Membranes. Plant Physiol. 1992 May;99(1):247–255. doi: 10.1104/pp.99.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hwang B. J., Smith A. J., Chu G. Internal sequence analysis of proteins eluted from polyacrylamide gels. J Chromatogr B Biomed Appl. 1996 Nov 15;686(2):165–175. doi: 10.1016/s0378-4347(96)00230-7. [DOI] [PubMed] [Google Scholar]
  20. Klimyuk V. I., Nussaume L., Harrison K., Jones J. D. Novel GUS expression patterns following transposition of an enhancer trap Ds element in Arabidopsis. Mol Gen Genet. 1995 Dec 10;249(4):357–365. doi: 10.1007/BF00287097. [DOI] [PubMed] [Google Scholar]
  21. Lamppa G. K. The chlorophyll a/b-binding protein inserts into the thylakoids independent of its cognate transit peptide. J Biol Chem. 1988 Oct 15;263(29):14996–14999. [PubMed] [Google Scholar]
  22. Lemesle-Varloot L., Henrissat B., Gaboriaud C., Bissery V., Morgat A., Mornon J. P. Hydrophobic cluster analysis: procedures to derive structural and functional information from 2-D-representation of protein sequences. Biochimie. 1990 Aug;72(8):555–574. doi: 10.1016/0300-9084(90)90120-6. [DOI] [PubMed] [Google Scholar]
  23. Li Q., Hunt A. G. A near-upstream element in a plant polyadenylation signal consists of more than six nucleotides. Plant Mol Biol. 1995 Aug;28(5):927–934. doi: 10.1007/BF00042076. [DOI] [PubMed] [Google Scholar]
  24. Li X., Henry R., Yuan J., Cline K., Hoffman N. E. 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 U S A. 1995 Apr 25;92(9):3789–3793. doi: 10.1073/pnas.92.9.3789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lütcke H. Signal recognition particle (SRP), a ubiquitous initiator of protein translocation. Eur J Biochem. 1995 Mar 15;228(3):531–550. doi: 10.1111/j.1432-1033.1995.tb20293.x. [DOI] [PubMed] [Google Scholar]
  26. Meurer J., Berger A., Westhoff P. A nuclear mutant of Arabidopsis with impaired stability on distinct transcripts of the plastid psbB, psbD/C, ndhH, and ndhC operons. Plant Cell. 1996 Jul;8(7):1193–1207. doi: 10.1105/tpc.8.7.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Packer J. C., Howe C. J. Algal plastid genomes encode homologues of the SRP-associated RNA. Mol Microbiol. 1998 Jan;27(2):508–510. doi: 10.1046/j.1365-2958.1998.00709.x. [DOI] [PubMed] [Google Scholar]
  28. Parker J. E., Coleman M. J., Szabò V., Frost L. N., Schmidt R., van der Biezen E. A., Moores T., Dean C., Daniels M. J., Jones J. D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell. 1997 Jun;9(6):879–894. doi: 10.1105/tpc.9.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Payan L. A., Cline K. A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J Cell Biol. 1991 Feb;112(4):603–613. doi: 10.1083/jcb.112.4.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pilgrim M. L., van Wijk K. J., Parry D. H., Sy D. A., Hoffman N. E. Expression of a dominant negative form of cpSRP54 inhibits chloroplast biogenesis in Arabidopsis. Plant J. 1998 Jan;13(2):177–186. doi: 10.1046/j.1365-313x.1998.00021.x. [DOI] [PubMed] [Google Scholar]
  32. Platero J. S., Hartnett T., Eissenberg J. C. Functional analysis of the chromo domain of HP1. EMBO J. 1995 Aug 15;14(16):3977–3986. doi: 10.1002/j.1460-2075.1995.tb00069.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rapoport T. A. Transport of proteins across the endoplasmic reticulum membrane. Science. 1992 Nov 6;258(5084):931–936. doi: 10.1126/science.1332192. [DOI] [PubMed] [Google Scholar]
  34. Rost B., Sander C. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins. 1994 May;19(1):55–72. doi: 10.1002/prot.340190108. [DOI] [PubMed] [Google Scholar]
  35. Schuenemann D., Gupta S., Persello-Cartieaux F., Klimyuk V. I., Jones J. D., Nussaume L., Hoffman N. E. A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10312–10316. doi: 10.1073/pnas.95.17.10312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Singh P. B., Miller J. R., Pearce J., Kothary R., Burton R. D., Paro R., James T. C., Gaunt S. J. A sequence motif found in a Drosophila heterochromatin protein is conserved in animals and plants. Nucleic Acids Res. 1991 Feb 25;19(4):789–794. doi: 10.1093/nar/19.4.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  38. Thompson C. C., Brown T. A., McKnight S. L. Convergence of Ets- and notch-related structural motifs in a heteromeric DNA binding complex. Science. 1991 Aug 16;253(5021):762–768. doi: 10.1126/science.1876833. [DOI] [PubMed] [Google Scholar]
  39. Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wu L., Ueda T., Messing J. Sequence and spatial requirements for the tissue- and species-independent 3'-end processing mechanism of plant mRNA. Mol Cell Biol. 1994 Oct;14(10):6829–6838. doi: 10.1128/mcb.14.10.6829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yuan J., Henry R., Cline K. Stromal factor plays an essential role in protein integration into thylakoids that cannot be replaced by unfolding or by heat shock protein Hsp70. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8552–8556. doi: 10.1073/pnas.90.18.8552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zhang H., Scheirer D. C., Fowle W. H., Goodman H. M. Expression of antisense or sense RNA of an ankyrin repeat-containing gene blocks chloroplast differentiation in arabidopsis. Plant Cell. 1992 Dec;4(12):1575–1588. doi: 10.1105/tpc.4.12.1575. [DOI] [PMC free article] [PubMed] [Google Scholar]

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