Biogenesis of photosynthetic complexes in the chloroplast of Chlamydomonas reinhardtii requires ARSA1, a homolog of prokaryotic arsenite transporter and eukaryotic TRC40 for guided entry of tail-anchored proteins

Plant Journal

Volumn 73, Issue 5, 2013, Pages 850-861

  Formighieri, Cinzia ^a   Cazzaniga, Stefano ^a   Kuras, Richard ^b   Bassi, Roberto ^a,c  

^a UNIVERSITY OF VERONA   (Italy)

^b CNRS   (France)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

ARSA; Chlamydomonas; chloroplast; protein targeting; tail anchored proteins; TOC34

Indexed keywords

ARSA; CHLAMYDOMONAS; CHLOROPLAST; PROTEIN TARGETING; TAIL-ANCHORED PROTEINS; TOC34;

BIOSYNTHESIS; GENES; PROTEINS;

CHLOROPHYLL;

ALGAL PROTEIN; ARSENIC TRIOXIDE; ARSENOUS ACID DERIVATIVE; CHLOROPHYLL; MEMBRANE PROTEIN; RECOMBINANT PROTEIN; THYLAKOID POLYPEPTIDES; TOC34 PROTEIN, PLANT; VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CHROMOSOME MAP; CYTOSOL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHOTOSYNTHESIS; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALGAL PROTEINS; ARSENITES; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; CHLOROPLASTS; CHROMOSOME MAPPING; CYTOSOL; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS, INSERTIONAL; MUTATION; PHOTOSYNTHESIS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; EUKARYOTA; MAMMALIA; PROKARYOTA;

EID: 84874451112     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12077     Document Type: Article

References (55)

1. Albus, C.A., Ruf, S., Schottler, M.A., Lein, W., Kehr, J., and, Bock, R., (2010) Y3IP1, a nucleus-encoded thylakoid protein, cooperates with the plastid-encoded Ycf3 protein in photosystem I assembly of tobacco and Arabidopsis. Plant Cell 22, 2838-2855.
2. Asakura, Y., Hirohashi, T., Kikuchi, S., Belcher, S., Osborne, E., Yano, S., Terashima, I., Barkan, A., and, Nakai, M., (2004) Maize mutants lacking chloroplast FtsY exhibit pleiotropic defects in the biogenesis of thylakoid membranes. Plant Cell 16 (1), 201-214. (Pubitemid 38162363)
3. Asamizu, E., Nakamura, Y., Miura, K., et al. (2004) Establishment of publicly available cDNA material and information resource of Chlamydomonas reinhardtii (Chlorophyta) to facilitate gene function analysis. Phycologia 43, 722-726. (Pubitemid 40084811)
4. Bassi, R., and, Wollman, F.A., (1991) The Chlorophyll-a/b proteins of photosystem-II in Chlamydomonas-reinhardtii-isolation, characterization and immunological cross-reactivity to higher-plant polypeptides. Planta 183, 423-433.
5. Bauer, J., Chen, K.H., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D., and, Kessler, F., (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403, 203-207. (Pubitemid 30050964)
6. Beilharz, T., Egan, B., Silver, P.A., Hofmann, K., and, Lithgow, T., (2003) Bipartite signals mediate subcellular targeting of tail-anchored membrane proteins in Saccharomyces cerevisiae. J. Biol. Chem. 278, 8219-8223. (Pubitemid 36800565)
7. Bonente, G., Formighieri, C., Mantelli, M., Catalanotti, C., Giuliano, G., Morosinotto, T., and, Bassi, R., (2011) Mutagenesis and phenotypic selection as a strategy toward domestication of Chlamydomonas reinhardtii strains for improved performance in photobioreactors. Photosynth. Res. 108, 107-120.
8. Borgese, N., and, Fasana, E., (2011) Targeting pathways of C-tail-anchored proteins. Biochim. Biophys. Acta. 1808, 937-946.
9. Borgese, N., and, Righi, M., (2010) Remote origin of tail anchored proteins. Traffic 11, 877-885.
10. Borgese, N., Brambillasca, S., and, Colombo, S., (2007) How tails guide tail-anchored proteins to their destinations. Curr. Opin. Cell Biol. 19, 368-375. (Pubitemid 47268760)
11. Chen, M.H., Huang, L.F., Li, H.M., Chen, Y.R., and, Yu, S.M., (2004) Signal peptide-dependent targeting of a rice a-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol. 135, 1367-1377.
12. Constan, D., Patel, R., Keegstra, K., and, Jarvis, P., (2004) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J. 38, 93-106. (Pubitemid 38448447)
13. Croce, R., Canino, G., Ros, F., and, Bassi, R., (2002) Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41, 7334-7343. (Pubitemid 34602450)
14. Dhanoa, P.K., Richardson, L.G.L., Smith, M.D., Gidda, S.K., Henderson, M.P.A., Andrews, D.W., and, Mullen, R.T., (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS ONE 5 (4), e10098.
15. Falkowski, P.G., and, Raven, J.A., (1997) Aquatic photosynthesis. Malden, Mass: Blackwell Science.
16. Ferro, M., Salvi, D., Riviere-Rolland, H., Vermat, T., Seigneurin-Berny, D., Grunwald, D., Garin, J., Joyard, J. and Rolland, N., (2002) Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc. Natl Acad. Sci. USA, 99, 11487-11492. (Pubitemid 34924952)
17. Gutensohn, M., Pahnke, S., Kolukisaoglu, U., et al. (2004) Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts. Mol. Genet. Gen. 272, 379-396. (Pubitemid 40064522)
18. Harris, E.H., (1989) The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. San Diego: Academic Press.
19. Hu, J.B., Li, J.Z., Qian, X.G., Denic, V., and, Sha, B.D., (2009) The crystal structures of yeast Get3 suggest a mechanism for tail-anchored protein membrane insertion. PLoS ONE. 4, e8061.
20. Huesemann, M.H., Hausmann, T.S., Bartha, R., Aksoy, M., Weissman, J.C., and, Benemann, J.R., (2008) Biomass productivities in wild type and pigment mutant of Cyclotella sp (Diatom). Appl. Biochem. Biotechnol. 157, 507-526.
21. Jans, F., Mignolet, E., Houyoux, P.A., Cardol, P., Ghysels, B., Cuine, S., Cournac, L., Peltier, G., Remacle, C., and, Franck, F., (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. PNAS 105, 20246-20551.
22. Jarvis, P., Chen, L.J., Li, H.M., Pete, C.A., Fankhauser, C., and, Chory, J., (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282, 100-103. (Pubitemid 28471137)
23. Jonikas, M.C., Collins, S.R., Denic, V., et al. (2009) Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323, 1693-1697.
24. Kalanon, M., and, McFadden, G.I., (2008) The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: a bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 179, 95-112.
25. Kalbfleisch, T., Cambon, A., and, Wattenberg, B.W., (2007) A bioinformatics approach to identifying tail-anchored proteins in the human genome. Traffic 8, 1687-1694. (Pubitemid 350066681)
26. Kriechbaumer, V., Shaw, R., Mukherjee, J., Bowsher, C.G., Harrison, A.M., and, Abell, B.M., (2009) Subcellular distribution of tail-anchored proteins in Arabidopsis. Traffic 10, 1753-1764.
27. Kubis, S., Baldwin, A., Patel, R., Razzaq, A., Dupree, P., Lilley, K., Kurth, J., Leister, D., and, Jarvis, P., (2003) The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 15, 1859-1871. (Pubitemid 37078340)
28. Kuroda, M., Dey, S., Sanders, O.I., and, Rosen, B.P., (1997) Alternate energy coupling of ArsB, the membrane subunit of the Ars anion-translocating ATPase. J. Biol. Chem. 272, 326-331. (Pubitemid 27021162)
29. Kutay, U., Hartmann, E., and, Rapoport, T.A., (1993) A class of membrane proteins with a C-terminal anchor. Trends Cell Biol. 3, 72-75. (Pubitemid 23072280)
30. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 15 (5259), 680-685.
31. Li, H.M., and, Chiu, C.C., (2010) Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61 (61), 157-180.
32. Li, R.Q., Yu, C., Li, Y.R., Lam, T.W., Yiu, S.M., Kristiansen, K., and, Wang, J., (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966-1967.
33. Maggio, C., Barbante, A., Ferro, F., Frigerio, L., and, Pedrazzini, E., (2007) Intracellular sorting of the tail-anchored protein cytochrome b5 in plants: a comparative study using different isoforms from rabbit and Arabidopsis. J. Exp. Bot. 58, 1365-1379. (Pubitemid 47355638)
34. Martin, W., and, Herrmann, R.G., (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118, 9-17. (Pubitemid 128652964)
35. Mason, C.B., Bricker, T.M., and, Moroney, J.V., (2006) A rapid method for chloroplast isolation from the green alga Chlamydomonas reinhardtii. Nat. Protoc. 1 (5), 2227-2230.
36. May, T., and, Soll, J., (1998) Positive charges determine the topology and functionality of the transmembrane domain in the chloroplastic outer envelope protein Toc34. J. Cell Biol. 141, 895-904. (Pubitemid 28243958)
37. Merchant, S.S., Prochnik, S.E., Vallon, O., et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-251. (Pubitemid 47574847)
38. Mukhopadhyay, R., Ho, Y.S., Swiatek, P.J., Rosen, B.P., and, Bhattacharjee, H., (2006) Targeted disruption of the mouse Asna1 gene results in embryonic lethality. FEBS Lett. 580, 3889-3894. (Pubitemid 43946879)
39. Nanjo, Y., Oka, H., Ikarashi, N., Kaneko, K., Kitajima, A., Mitsui, T., Munoz, F.J., Rodriguez-Lopez, M., Baroja-Fernandez, E., and, Pozueta-Romero, J., (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/ phosphodiesterase is transported from the ER-Golgi to the chloroplast through the secretory pathway. Plant Cell 18, 2582-2592. (Pubitemid 44749891)
40. Pogson, B.J., Woo, N.S., Forster, B., and, Small, I.D., (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci. 13, 602-609.
41. Qbadou, S., Tien, R., Soll, J., and, Schleiff, E., (2003) Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J. Cell Sci. 116, 837-846. (Pubitemid 36367633)
42. Rabu, C., Schmid, V., Schwappach, B., and, High, S., (2009) Biogenesis of tail-anchored proteins: the beginning for the end? J. Cell Sci. 122, 3605-3612.
43. Rahire, M., Laroche, F., Cerutti, L., and, Rochaix, J.D., (2012) Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I. Plant J. 72, 652-661.
44. Raven, J.A., and, Allen, J.F., (2003) Genomics and chloroplast evolution: what did cyanobacteria do for plants? Genome Biol. 4, 209.
45. Reinbothe, S., Pollmann, S., Springer, A., James, R.J., Tichtinsky, G., and, Reinbothe, C., (2005) A role of Toc33 in the protochlorophyllide-dependent plastid import pathway of NADPH: protochlorophyllide oxidoreductase (POR) A. Plant J. 42, 1-12.
46. Reyes-Prieto, A., Weber, A.P.M., and, Bhattacharya, D., (2007) The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41, 147-168.
47. Rochaix, J.D., (2011) Assembly of the Photosynthetic Apparatus. Plant Physiol. 155, 1493-1500.
48. Schuldiner, M., Metz, J., Schmid, V., Denic, V., Rakwalska, M., Schmitt, H.D., Schwappach, B., and, Weissman, J.S., (2008) The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134, 634-645.
49. Schunemann, D., (2004) Structure and function of the chloroplast signal recognition particle. Curr. Genet. 44, 295-304. (Pubitemid 38111493)
50. Shimogawara, K., Fujiwara, S., Grossman, A., and, Usuda, H., (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148, 1821-1828. (Pubitemid 28180707)
51. Stefanovic, S., and, Hegde, R.S., (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128, 1147-1159. (Pubitemid 46427870)
52. Villarejo, A., Buren, S., Larsson, S., et al. (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 7, 1224-1231.
53. Waegemann, K., and, Soll, J., (1991) Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J. 1, 149-158. (Pubitemid 121001056)
54. Zhang, H.B., Zhao, X., Ding, X., Paterson, A.H., and, Wing., R.A., (1995) Preparation of megabase-size DNA from plant nuclei. Plant J. 7, 175-184.
55. Zhou, T.Q., Radaev, S., Rosen, B.P., and, Gatti, D.L., (2000) Structure of the ArsA ATPase: the catalytic subunit of a heavy metal resistance pump. EMBO J. 19, 4838-4845.