Translocons on the inner and outer envelopes of chloroplasts share similar evolutionary origin in Arabidopsis thaliana

Journal of Evolutionary Biology

Volumn 22, Issue 7, 2009, Pages 1418-1428

  Lv, H X ^a   Guo, G Q ^a   Yang, Z N ^a,b  

^a LANZHOU UNIVERSITY   (China)

^b SHANGHAI NORMAL UNIVERSITY   (China)

Author keywords

Arabidopsis; AtTic21; Channel protein; Chloroplasts; Cia5; Evolution; Synechocystis; SynTic21; TIC complex; TOC complex

Indexed keywords

ARABIDOPSIS PROTEIN; CATION TRANSPORT PROTEIN; TIC21 PROTEIN, ARABIDOPSIS;

CHLOROPLAST; CYANOBACTERIUM; DICOTYLEDON; EVOLUTIONARY BIOLOGY; MUTATION; PEPTIDE; PHOTOSYNTHESIS; PHYLOGENETICS; PROTEIN;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; CYTOLOGY; EVOLUTION; GENE INACTIVATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PHYLOGENY; SYNECHOCYSTIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATION TRANSPORT PROTEINS; CHLOROPLASTS; EVOLUTION; GENE KNOCKOUT TECHNIQUES; PHOTOSYNTHESIS; PHYLOGENY; SYNECHOCYSTIS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CYANOBACTERIA; SYNECHOCYSTIS;

EID: 67649198684     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2009.01755.x     Document Type: Article

References (43)

1. Arimura, S., Takusagawa, S., Hatano, S., Nakazono, M., Hirai, A. Tsutsumi, N. 1999. A novel plant nuclear gene encoding chloroplast ribosomal protein S9 has a transit peptide related to that of rice chloroplast ribosomal protein L12. FEBS Lett. 450 : 231 234. (Pubitemid 29219520)
2. Bhattacharya, D., Yoon, H.S. Hackett, J.D. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26 : 50 60. (Pubitemid 38095348)
3. Bölter, B., Soll, J., Schulz, A., Hinnah, S. Wagner, R. 1998. Origin of a chloroplast protein importer. Proc. Natl Acad. Sci. USA 95 : 15831 15836. (Pubitemid 29018786)
4. Bruce, B.D. 2000. Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol. 10 : 440 447. (Pubitemid 30682365)
5. Cline, K., Werner-Washburne, M., Andrews, J. Keegstra, K. 1984. Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75 : 675 678.
6. Clough, S.J. Bent, A.F. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16 : 735 743.
7. Duy, D., Wanner, G., Meda, A.R., Wiren, N., Soll, J. Philippar, K. 2007. PIC1, an ancient permease in arabidopsis chloroplasts, mediates iron transport. Plant Cell. 19 : 986 1006. (Pubitemid 46953242)
8. Emanuelsson, O., Nielsen, H., Brunak, S. Heijne, G.V. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300 : 1005 1016. (Pubitemid 30708188)
9. Gray, M.W. 1992. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141 : 233 357. (Pubitemid 23072890)
10. Gross, J. Bhattacharya, D. 2009. Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci. 14 : 13 20.
11. Haughn, G.W. Somerville, C. 1986. Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol. Gen. Genet. 204 : 430 434. (Pubitemid 17200381)
12. Heins, L. Soll, J. 1998. Chloroplast biogenesis: mixing the prokaryotic and the eukaryotic? Curr. Biol. 8 : 215 217.
13. Heins, L., Mehrle, A., Hemmler, R., Wagner, R., Küchler, M., Hörmann, F., Sveshnikov, D. Soll, J. 2002. The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J. 21 : 2616 2625. (Pubitemid 34619377)
14. Hofmann, K. Stoffel, W. 1993. TMbase - a database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler 374 : 166.
15. Ishida, K. 2005. Protein targeting into plastids: a key to understanding the symbiogenetic acquisitions of plastids. J. Plant. Res. 118 : 237 245. (Pubitemid 41407026)
16. Jarvis, P. Soll, J. 2001. Toc, Tic, and chloroplast protein import. Biochim. Biophys. Acta 1541 : 64 79. (Pubitemid 34024829)
17. Joyard, J., Billecocq, A., Bartlett, S.G., Block, M.A., Chua, N.H. Douce, R. 1983. Localization of polypeptides to the cytosolic side of the outer envelope membrane of spinach chloroplasts. J. Biol. Chem. 258 : 10000 10006.
18. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M. Tabata, S. 1996. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3 : 109 136. (Pubitemid 126682789)
19. Keegstra, K. 1989. Transport and routing of proteins into chloroplasts. Cell 56 : 247 253.
20. Kouranov, A., Chen, X., Fuks, B. Schnell, D.J. 1998. Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J. Cell Biol. 143 : 991 1002. (Pubitemid 28547398)
21. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. Higgins, D.G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23 : 2947 2948. (Pubitemid 350162903)
22. Liu, Y.G., Mitsukawa, N., Oosumi, T. Whittier, R.F. 1995. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8 : 457 463.
23. Martin, W., Stoebe, B., Goremykin, V., Hansmann, S., Hasegawa, M. Kowallik, K.V. 1998. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 393 : 162 165. (Pubitemid 28242254)
24. Matsuzaki, M., Misumi, O., Shin-I, T., Maruyama, T.S., Takahara, M., Miyagishima, S.Y., Mori, T., Nishida, K., Yagisawa, F., Nishida, K., Yoshida, Y., Nishimura, Y., Nakao, S., Kobayashi, T., Momoyama, Y., Higashiyama, T., Minoda, A., Sano, M., Nomoto, H., Oishi, K., Hayashi, H., Ohta, F., Nishizaka, S., Haga, S., Miura, S., Morishita, T., Kabeya, Y., Terasawa, K., Suzuki, Y., Ishii, Y., Asakawa, S., Takano, H., Ohta, N., Kuroiwa, H., Tanaka, K., Shimizu, N., Sugano, S., Sato, N., Nozaki, H., Ogasawara, N., Kohara, Y. Kuroiwa, T. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428 : 653 657. (Pubitemid 38524807)
25. McFadden, G.I. 1999. Endosymbiosis and evolution of the plant cell. Curr. Opin. Plant Biol. 2 : 513 519.
26. McFadden, G.I. 2001. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37 : 951 959. (Pubitemid 34067654)
27. McGuffin, L.J., Bryson, K. Jones, D.T. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16 : 404 405. (Pubitemid 30417087)
28. Nishiyama, T., Fujita, T., Shin-I, T., Seki, M., Nishide, H., Uchiyama, I., Kamiya, A., Carninci, P., Hayashizaki, Y., Shinozaki, K., Kohara, Y. Hasebe, M. 2003. Comparative genomics of Physcomitrella patens gemetophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc. Natl Acad. Sci. USA 100 : 8007 8012. (Pubitemid 36760085)
29. Nozaki, H. 2005. A new scenario of plastid evolution: plastid primary endosymbiosis before the divergence of the "Plantae", emended. J. Plant. Res. 118 : 247 255. (Pubitemid 41407027)
30. Olson, J.M. 2006. Photosynthesis in the Archean era. Photosyn. Res. 88 : 109 117. (Pubitemid 43876064)
31. Osteryoung, K.W. Nunnari, J. 2003. The division of endosymbiotic organelles. Science 302 : 1698 1704. (Pubitemid 37505724)
32. Qin, G., Kang, D., Dong, Y., Shen, Y., Zhang, L., Deng, X., Zhang, Y., Li, S., Chen, N., Niu, W., Chen, C., Liu, P., Chen, H., Li, J., Ren, Y., Gu, H., Deng, X.W., Qu L.J. Chen, Z. 2003. Obtaining and analysis of flanking sequences from T-DNA transformants of Arabidopsis. Plant Science. 165 : 941 949. (Pubitemid 37231791)
33. Quigley, F., Martin, W.F. Cerff, R. 1988. Intron conservation across the prokaryote-eukaryote boundary: structure of the nuclear gene for chloroplast glyceraldehyde-3-phosphate dehydrogenase from maize. Proc. Natl Acad. Sci. USA 85 : 2672 2676.
34. Reumann, S. Keegstra, K. 1999. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 4 : 302 307. (Pubitemid 29363139)
35. Reumann, S., Davila-Aponte, J. Keegstra, K. 1999. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl Acad. Sci. USA 96 : 784 789. (Pubitemid 29061286)
36. Rippka, R., Deruelles, J., Waterbury, J., Herdman, M. Stanier, R. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111 : 1 6.
37. Saitou, N. Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 : 406 425.
38. Tamura, K., Dudley, J., Nei, M. Kumar, S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 : 1596 1599. (Pubitemid 47236692)
39. Teng, Y.S., Su, Y.S., Chen, L.J., Lee, Y.J., Hwang, I. Li, H.M. 2006. Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell. 18 : 2247 2257. (Pubitemid 44484724)
40. Thompson, J.D., Higgins, D.G. Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 : 4673 4680. (Pubitemid 24354800)
41. Timmis, J.N., Ayliffe, M.A., Huang, C.Y. Martin, W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5 : 123 135. (Pubitemid 38160279)
42. Ueda, M., Fujimoto, M., Arimura, S., Tsutsumi, N. Kadowaki, K. 2006. Evidence for transit peptide acquisition through duplication and subsequent frameshift mutation of a preexisting protein gene in rice. Mol. Biol. Evol. 23 : 2405 2412. (Pubitemid 44737134)
43. Vothknecht, U.C. Soll, J. 2005. Chloroplast membrane transport: interplay of prokaryotic and eukaryotic traits. Gene 354 : 99 109. (Pubitemid 41116688)