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http://dx.doi.org/10.14348/molcells.2018.0033

Evolution and Design Principles of the Diverse Chloroplast Transit Peptides  

Lee, Dong Wook (Division of Integrative Biosciences and Biotechnology, Pohang University of Science and Technology)
Hwang, Inhwan (Division of Integrative Biosciences and Biotechnology, Pohang University of Science and Technology)
Publication Information
Molecules and Cells / v.41, no.3, 2018 , pp. 161-167 More about this Journal
Abstract
Chloroplasts are present in organisms belonging to the kingdom Plantae. These organelles are thought to have originated from photosynthetic cyanobacteria through endosymbiosis. During endosymbiosis, most cyanobacterial genes were transferred to the host nucleus. Therefore, most chloroplast proteins became encoded in the nuclear genome and must return to the chloroplast after translation. The N-terminal cleavable transit peptide (TP) is necessary and sufficient for the import of nucleus-encoded interior chloroplast proteins. Over the past decade, extensive research on the TP has revealed many important characteristic features of TPs. These studies have also shed light on the question of how the many diverse TPs could have evolved to target specific proteins to the chloroplast. In this review, we summarize the characteristic features of TPs. We also highlight recent advances in our understanding of TP evolution and provide future perspectives about this important research area.
Keywords
chloroplast evolution; endosymbiosis; protein import into chloroplasts; transit peptide;
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1 Lee, S., Lee, D.W., Yoo, Y.J., Duncan, O., Oh, Y.J., Lee, Y.J., Lee, G., Whelan, J., and Hwang, I. (2012). Mitochondrial targeting of the Arabidopsis F1-ATPase gamma-subunit via multiple compensatory and synergistic presequence motifs. Plant Cell 24, 5037-5057.   DOI
2 Lee, D.W., Jung, C., and Hwang, I. (2013). Cytosolic events involved in chloroplast protein targeting. Biochim. Biophys. Acta 1833, 245-252.   DOI
3 Lee, D.W., Woo, S., Geem, K.R., and Hwang, I. (2015). Sequence motifs in transit peptides act as independent functional units and can be transferred to new sequence contexts. Plant Physiol 169, 471-484.   DOI
4 Lee, D.W., Kim, S.J., Oh, Y.J., Choi, B., Lee, J., and Hwang, I. (2016). Arabidopsis BAG1 functions as a cofactor in Hsc70-mediated proteasomal degradation of unimported plastid proteins. Mol. Plant 9, 1428-1431.   DOI
5 Lee, D.W., Lee, J., and Hwang, I. (2017). Sorting of nuclear-encoded chloroplast membrane proteins. Curr. Opin. Plant Biol. 40, 1-7.
6 Lee, D.W., Yoo, Y.J., Razzak, M.A., and Hwang, I. (2018). Prolines in transit peptides Are crucial for efficient preprotein translocation into chloroplasts. Plant Physiol. 176, 663-677.   DOI
7 Leister, D. (2003). Chloroplast research in the genomic age. Trends Genet. 19, 47-56.   DOI
8 Li, H.M., and Chiu, C.C. (2010). Protein Transport into Chloroplasts. Ann. Rev. Plant Biol. 61, 157-180.   DOI
9 Li, H.M., and Teng, Y.S. (2013). Transit peptide design and plastid import regulation. Trends Plant Sci. 18, 360-366.
10 Liu, L., McNeilage, R.T., Shi, L.X., and Theg, S.M. (2014). ATP Requirement for Chloroplast Protein Import Is Set by the K-m for ATP Hydrolysis of Stromal Hsp70 in Physcomitrella patens. Plant Cell 26, 1246-1255.   DOI
11 May, T., and Soll, J. (2000). 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12, 53-64.   DOI
12 McFadden, G.I. (2014). Origin and evolution of plastids and photosynthesis in eukaryotes. Cold Spring Harb. Perspect Biol. 6, a016105.   DOI
13 Nakai, M. (2015). YCF1: A green TIC: response to the de Vries et al. Commentary. Plant Cell 27, 1834-1838.
14 Nouet, C., Motte, P., and Hanikenne, M. (2011). Chloroplastic and mitochondrial metal homeostasis. Trends Plant Sci. 16, 395-404.   DOI
15 Okawa, K., Inoue, H., Adachi, F., Nakayama, K., Ito-Inaba, Y., Schnell, D.J., Uehara, S., and Inaba, T. (2014). Targeting of a polytopic membrane protein to the inner envelope membrane of chloroplasts in vivo involves multiple transmembrane segments. J. Exp. Bot. 65, 5257-5265.   DOI
16 Paila, Y.D., Richardson, L.G.L., and Schnell, D.J. (2015). New insights into the mechanism of chloroplast protein import and its integration with protein quality control, organelle biogenesis and development. J. Mol. Biol. 427, 1038-1060.   DOI
17 Paila, Y.D., Richardson, L.G., Inoue, H., Parks, E.S., McMahon, J., Inoue, K., and Schnell, D.J. (2016). Multi-functional roles for the polypeptide transport associated domains of Toc75 in chloroplast protein import. Elife 5, pii: e12631.
18 Qbadou, S., Becker, T., Mirus, O., Tews, I., Soll, J., and Schleiff, E. (2006). The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J. 25, 1836-1847.   DOI
19 Bhushan, S., Kuhn, C., Berglund, A.K., Roth, C., and Glaser, E. (2006). The role of the N-terminal domain of chloroplast targeting peptides in organellar protein import and miss-sorting. FEBS Lett. 580, 3966-3972.   DOI
20 Abe, Y., Shodai, T., Muto, T., Mihara, K., Torii, H., Nishikawa, S., Endo, T., and Kohda, D. (2000). Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100, 551-560.   DOI
21 Bruce, B.D. (2000). Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol. 10, 440-447.   DOI
22 Chotewutmontri, P., and Bruce, B.D. (2015). Non-native, N-terminal Hsp70 molecular motor recognition elements in transit peptides support plastid protein translocation. J. Biol. Chem. 290, 7602-7621.   DOI
23 Chotewutmontri, P., Reddick, L.E., McWilliams, D.R., Campbell, I.M., and Bruce, B.D. (2012). Differential transit peptide recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 24, 3040-3059.   DOI
24 Chotewutmontri, P., Holbrook, K., and Bruce, B.D. (2017). Plastid Protein Targeting: Preprotein Recognition and Translocation. Int. Rev. Cell Mol. Biol. 330, 227-294.
25 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.   DOI
26 de Vries, J., Sousa, F.L., Bolter, B., Soll, J., and Gould, S.B. (2015). YCF1: A Green TIC? Plant Cell 27, 1827-1833.   DOI
27 Garg, S.G., and Gould, S.B. (2016). The role of charge in protein targeting evolution. Trends Cell Biol. 26, 894-905.   DOI
28 Razzak, M.A., Lee, D.W., Yoo, Y.J., and Hwang, I. (2017). Evolution of rubisco complex small subunit transit peptides from algae to plants. Sci. Rep. 7.
29 Dempsey, D.A., Vlot, A.C., Wildermuth, M.C., and Klessig, D.F. (2011). Salicylic Acid biosynthesis and metabolism. Arabidopsis Book 9, e0156.   DOI
30 Facchinelli, F., and Weber, A.P. (2011). The metabolite transporters of the plastid envelope: an update. Front. Plant Sci. 2, 50.
31 Gould, S.B., Waller, R.F., and McFadden, G.I. (2008). Plastid evolution. Annu. Rev. Plant Biol. 59, 491-517.   DOI
32 Holbrook, K., Subramanian, C., Chotewutmontri, P., Reddick, L.E., Wright, S., Zhang, H., Moncrief, L., and Bruce, B.D. (2016). Functional analysis of semi-conserved transit peptide motifs and mechanistic implications in precursor targeting and recognition. Mol. Plant 9, 1286-1301.   DOI
33 Inoue, H., Li, M., and Schnell, D.J. (2013). An essential role for chloroplast heat shock protein 90 (Hsp90C) in protein import into chloroplasts. Pro. Natl. Acad. Sci. USA 110, 3173-3178.   DOI
34 Ivanova, Y., Smith, M.D., Chen, K., and Schnell, D.J. (2004). Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 15, 3379- 3392.   DOI
35 Jarvis, P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179, 257-285.   DOI
36 Kikuchi, S., Oishi, M., Hirabayashi, Y., Lee, D.W., Hwang, I., and Nakai, M. (2009). A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 21, 1781-1797.   DOI
37 Kubis, S., Patel, R., Combe, J., Bedard, J., Kovacheva, S., Lilley, K., Biehl, A., Leister, D., Rios, G., Koncz, C., et al. (2004). Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16, 2059-2077.   DOI
38 Kikuchi, S., Bedard, J., Hirano, M., Hirabayashi, Y., Oishi, M., Imai, M., Takase, M., Ide, T., and Nakai, M. (2013). Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339, 571-574.   DOI
39 Kim, C., Lee, K.P., Baruah, A., Nater, M., Gobel, C., Feussner, I., and Apel, K. (2009). (1)O2-mediated retrograde signaling during late embryogenesis predetermines plastid differentiation in seedlings by recruiting abscisic acid. Proc. Natl. Acad. Sci. USA 106, 9920-9924.   DOI
40 Kobayashi, K., and Wada, H. (2016). Role of lipids in chloroplast biogenesis. Subcell Biochem. 86, 103-125.
41 Lee, D.W., Lee, S., Lee, G.J., Lee, K.H., Kim, S., Cheong, G.W., and Hwang, I. (2006). Functional characterization of sequence motifs in the transit peptide of Arabidopsis small subunit of rubisco. Plant Physiol. 140, 466-483.   DOI
42 Lee, D.W., Kim, J.K., Lee, S., Choi, S., Kim, S., and Hwang, I. (2008). Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20, 1603-1622.   DOI
43 Lee, D.W., Lee, S., Oh, Y.J., and Hwang, I. (2009a). Multiple sequence motifs in the Rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts. Plant Physiol. 151, 129-141.   DOI
44 Shapiguzov, A., Vainonen, J.P., Wrzaczek, M., and Kangasjarvi, J. (2012). ROS-talk - how the apoplast, the chloroplast, and the nucleus get the message through. Front Plant Sci. 3.
45 Lee, S., Lee, D.W., Lee, Y., Mayer, U., Stierhof, Y.D., Lee, S., Jurgens, G., and Hwang, I. (2009b). Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 21, 3984-4001.   DOI
46 Rensink, W.A., Schnell, D.J., and Weisbeek, P.J. (2000). The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope. J. Biol. Chem. 275, 10265-10271.   DOI
47 Richter, S., and Lamppa, G.K. (1999). Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. J. Cell Biol. 147, 33-43.   DOI
48 Schaller, A., and Stintzi, A. (2009). Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochem 70, 1532-1538.   DOI
49 Schleiff, E., and Becker, T. (2011). Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 12, 48-59.   DOI
50 Shi, L.X., and Theg, S.M. (2013). The chloroplast protein import system: from algae to trees. Biochim. Biophys. Acta 1833, 314-331.   DOI
51 Su, P.H., and Li, H.M. (2010). Stromal Hsp70 Is Important for Protein Translocation into Pea and Arabidopsis Chloroplasts. Plant Cell 22, 1516-1531.   DOI
52 Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994.   DOI
53 Teng, Y.S., Chan, P.T., and Li, H.M. (2012) D.ifferential age-dependent import regulation by signal peptides. Plos Biol. 10. e1001416.   DOI
54 Trosch, R., and Jarvis, P. (2011). The stromal processing peptidase of chloroplasts is essential in Arabidopsis, with knockout mutations causing embryo arrest after the 16-cell stage. PLoS One 6, e23039.   DOI
55 Viana, A.A., Li, M., and Schnell, D.J. (2010). Determinants for stoptransfer and post-import pathways for protein targeting to the chloroplast inner envelope membrane. J. Biol. Chem. 285, 12948-12960.   DOI
56 Yagi, Y., and Shiina, T. (2014). Recent advances in the study of chloroplast gene expression and its evolution. Front Plant Sci. 5, 61.
57 Zimorski, V., Ku, C., Martin, W.F., and Gould, S.B. (2014). Endosymbiotic theory for organelle origins. Curr. Opin. Microbiol. 22, 38-48.   DOI