Chloroplast Hsp93 directly binds to transit peptides at an early stage of the preprotein import process

Plant Physiology

Volumn 170, Issue 2, 2016, Pages 857-866

  Huang, Po Kai ^a   Chan, Po Ting ^a,b   Su, Pai Hsiang ^a,c   Chen, Lih Jen ^a   Li, Hsou Min ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b ABBVIE INC   (United States)

^c ACADEMIA SINICA   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CHAPERONE; CHLOROPLAST 93-KD HEAT SHOCK PROTEIN, ARABIDOPSIS; CHLOROPLAST PROTEIN; HEAT SHOCK PROTEIN; PEPTIDE;

ARABIDOPSIS; CHLOROPLAST; ENZYMOLOGY; GENETICS; METABOLISM; PEA; PROTEIN TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLAST PROTEINS; CHLOROPLASTS; HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; PEAS; PEPTIDES; PROTEIN TRANSPORT;

EID: 84956798761     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01830     Document Type: Article

References (41)

1. Akita M, Inoue H (2009) Evaluating the energy-dependent "binding" in the early stage of protein import into chloroplasts. Methods Enzymol 466: 43-64
2. Akita M, Nielsen E, Keegstra K (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical crosslinking. J Cell Biol 136: 983-994
3. Baker TA, Sauer RT (2006) ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem Sci 31: 647-653
4. Bölter B,May T, Soll J (1998) A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett 441: 59-62
5. Chotewutmontri P, Bruce BD (2015) Non-native, N-terminal Hsp70 molecular motor recognition elements in transit peptides support plastid protein translocation. J Biol Chem 290: 7602-7621
6. Chotewutmontri P, Reddick LE, McWilliams DR, Campbell IM, Bruce BD (2012) Differential transit peptide recognition during preprotein binding and translocation into flowering plant plastids. Plant Cell 24: 3040-3059
7. Chou ML, Chu CC, Chen LJ, Akita M, Li HM (2006) Stimulation of transitpeptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J Cell Biol 175: 893-900
8. Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, LiHM(2003) Tic40, amembrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J 22: 2970-2980
9. Chu C-C, Li HM (2012) The amino-terminal domain of chloroplast Hsp93 is important for its membrane association and functions in vivo. Plant Physiol 158: 1656-1665
10. Clark SA, Theg SM (1997) A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Mol Biol Cell 8: 923- 934
11. Constan D, Froehlich JE, Rangarajan S, Keegstra K (2004) A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 136: 3605-3615
12. Fitzpatrick LM, Keegstra K (2001) A method for isolating a high yield of Arabidopsis chloroplasts capable of efficient import of precursor proteins. Plant J 27: 59-65
13. Flores-Perez U, Bedard J, Tanabe N, Lymperopoulos P, Clarke AK, Jarvis P (2015) Functional analysis of the Hsp93/ClpC chaperone at the chloroplast envelope. Plant Physiol http://dx.doi.org/pp.15.01538
14. Guéra A, America T, van Waas M, Weisbeek PJ (1993) A strong protein unfolding activity is associated with the binding of precursor chloroplast proteins to chloroplast envelopes. Plant Mol Biol 23: 309-324
15. Inoue H, Li M, Schnell DJ (2013) An essential role for chloroplast heat shock protein 90 (Hsp90C) in protein import into chloroplasts. Proc Natl Acad Sci USA 110: 3173-3178
16. Inoue H, Rounds C, Schnell DJ (2010) The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 22: 1947-1960
17. Ivey RA III, Subramanian C, Bruce BD (2000) Identification of a Hsp70 recognition domain within the rubisco small subunit transit peptide. Plant Physiol 122: 1289-1299
18. Kovacheva S, Bédard J, Wardle A, Patel R, Jarvis P (2007) Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 50: 364-379
19. Kress W, Maglica Z, Weber-Ban E (2009) Clp chaperone-proteases: structure and function. Res Microbiol 160: 618-628
20. Lee DW, Woo S, Geem KR, 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
21. Li HM, Chiu CC (2010) Protein transport into chloroplasts. Annu Rev Plant Biol 61: 157-180
22. Li M, Schnell DJ (2006) Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J Cell Biol 175: 249-259
23. Liu L, McNeilage RT, Shi LX, Theg SM (2014) ATP requirement for chloroplast protein import is set by the Km for ATP hydrolysis of stromal Hsp70 in Physcomitrella patens. Plant Cell 26: 1246-1255
24. Lubben TH, Keegstra K (1986) Efficient in vitro import of a cytosolic heat shock protein into pea chloroplasts. Proc Natl Acad Sci USA 83: 5502-5506
25. Moore T, Keegstra K (1993) Characterization of a cDNA clone encoding a chloroplast-targeted Clp homologue. Plant Mol Biol 21: 525-537
26. Nielsen E, Akita M, Davila-Aponte J, Keegstra K (1997) Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 16: 935-946
27. Nishimura K, van Wijk KJ (2015) Organization, function and substrates of the essential Clp protease system in plastids. Biochim Biophys Acta 1847: 915-930
28. Paila YD, Richardson LG, Schnell DJ (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
29. Pain D, Blobel G (1987) Protein import into chloroplasts requires a chloroplast ATPase. Proc Natl Acad Sci USA 84: 3288-3292
30. Peltier JB, Ripoll DR, Friso G, Rudella A, Cai Y, Ytterberg J, Giacomelli L, Pillardy J, van Wijk KJ (2004) Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications. J Biol Chem 279: 4768-4781
31. Perry SE, Li HM, Keegstra K (1991) In vitro reconstitution of protein transport into chloroplasts. Methods Cell Biol 34: 327-344
32. Robinson C, Thompson SJ, Woolhead C (2001) Multiple pathways used for the targeting of thylakoid proteins in chloroplasts. Traffic 2: 245-251
33. Rosano GL, Bruch EM, Ceccarelli EA (2011) Insights into the Clp/HSP100 chaperone system from chloroplasts of Arabidopsis thaliana. J Biol Chem 286: 29671-29680
34. Ruprecht M, Bionda T, Sato T, Sommer MS, Endo T, Schleiff E (2010) On the impact of precursor unfolding during protein import into chloroplasts. Mol Plant 3: 499-508
35. Shi LX, Theg SM (2010) A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 22: 205-220
36. Shi LX, Theg SM (2013) The chloroplast protein import system: from algae to trees. Biochim Biophys Acta 1833: 314-331
37. Sjögren LL, Tanabe N, Lymperopoulos P, Khan NZ, Rodermel SR, Aronsson H, Clarke AK (2014) Quantitative analysis of the chloroplast molecular chaperone ClpC/Hsp93 in Arabidopsis reveals new insights into its localization, interaction with the Clp proteolytic core, and functional importance. J Biol Chem 289: 11318-11330
38. Su PH, Li HM (2010) Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 22: 1516-1531
39. Theg SM, Bauerle C, Olsen LJ, Selman BR, Keegstra K (1989) Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J Biol Chem 264: 6730-6736
40. Tu SL, Chen LJ, Smith MD, Su YS, Schnell DJ, Li HM (2004) Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 16: 2078-2088
41. White SR, Lauring B (2007) AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8: 1657-1667