ATP requirement for chloroplast protein import is set by the Km for ATP hydrolysis of stromal Hsp70 in Physcomitrella patens

Plant Cell

Volumn 26, Issue 3, 2014, Pages 1246-1255

  Liu, Li ^a   McNeilage, Robert T ^a   Shi, Lan Xin ^a   Theg, Steven M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CHLOROPLAST PROTEIN; COMPLEMENTARY DNA; HEAT SHOCK PROTEIN 70;

AMINO ACID SEQUENCE; BRYOPSIDA; CHEMISTRY; GENETICS; HYDROLYSIS; METABOLISM; MOLECULAR GENETICS; MUTATION; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BRYOPSIDA; CHLOROPLAST PROTEINS; DNA, COMPLEMENTARY; HSP70 HEAT-SHOCK PROTEINS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MUTATION; PLANTS, GENETICALLY MODIFIED; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84899144012     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.121822     Document Type: Article

References (45)

1. Akita, M., Nielsen, E., and Keegstra, K. (1997). Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J. Cell Biol. 136: 983-994.
2. Alder, N.N., and Theg, S.M. (2003). Protein transport via the cpTat pathway displays cooperativity and is stimulated by transportincompetent substrate. FEBS Lett. 540: 96-100.
3. Aronsson, H., and Jarvis, P. (2002). A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett. 529: 215-220.
4. Bagola, K., Mehnert, M., Jarosch, E., and Sommer, T. (2011). Protein dislocation from the ER. Biochim. Biophys. Acta 1808: 925-936.
5. Becker, T., Böttinger, L., and Pfanner, N. (2012). Mitochondrial protein import: From transport pathways to an integrated network. Trends Biochem. Sci. 37: 85-91.
6. Benfey, P.N., and Chua, N.H. (1990). The cauliflower mosaic virus 35S promoter: Combinatorial regulation of transcription in plants. Science 250: 959-966.
7. Berthold, J., Bauer, M.F., Schneider, H.C., Klaus, C., Dietmeier, K., Neupert, W., and Brunner, M. (1995). The MIM complex mediates preprotein translocation across the mitochondrial inner membrane and couples it to the mt-Hsp70/ATP driving system. Cell 81: 1085-1093.
8. Chang, L., Bertelsen, E.B., Wisén, S., Larsen, E.M., Zuiderweg, E.R., and Gestwicki, J.E. (2008). High-throughput screen for small molecules that modulate the ATPase activity of the molecular chaperone DnaK. Anal. Biochem. 372: 167-176.
9. Flores-Pérez, Ú., and Jarvis, P. (2013). Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta 1833: 332-340.
10. Flügge, U.I., and Hinz, G. (1986). Energy dependence of protein translocation into chloroplasts. Eur. J. Biochem. 160: 563-570.
11. Gragerov, A., Zeng, L., Zhao, X., Burkholder, W., and Gottesman, M.E. (1994). Specificity of DnaK-peptide binding. J. Mol. Biol. 235: 848-854.
12. Hofmann, N.R., and Theg, S.M. (2003). Physcomitrella patens as a model for the study of chloroplast protein transport: Conserved machineries between vascular and non-vascular plants. Plant Mol. Biol. 53: 621-632.
13. Horstmann, V., Huether, C.M., Jost, W., Reski, R., and Decker, E.L. (2004). Quantitative promoter analysis in Physcomitrella patens: A set of plant vectors activating gene expression within three orders of magnitude. BMC Biotechnol. 4: 13.
14. Jarvis, P. (2008). Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 179: 257-285.
15. Kang, P.J., Ostermann, J., Shilling, J., Neupert, W., Craig, E.A., and Pfanner, N. (1990). Requirement for hsp70 in the mitochondrial matrix for translocation and folding of precursor proteins. Nature 348: 137-143.
16. Krzewska, J., Langer, T., and Liberek, K. (2001). Mitochondrial Hsp78, a member of the Clp/Hsp100 family in Saccharomyces cerevisiae, cooperates with Hsp70 in protein refolding. FEBS Lett. 489: 92-96.
17. 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.
18. Kubis, S., Patel, R., Combe, J., Bédard, J., Kovacheva, S., Lilley, K., Biehl, A., Leister, D., Ríos, G., Koncz, C., and Jarvis, P. (2004). Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16: 2059-2077.
19. Leheny, E.A., and Theg, S.M. (1994). Apparent inhibition of chloroplast protein import by cold temperatures is due to energetic considerations, not by membrane fluidity. Plant Cell 6: 427-437.
20. Li, H.M., and Chiu, C.C. (2010). Protein transport into chloroplasts. Annu. Rev. Plant Biol. 61: 157-180.
21. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991). Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc. Natl. Acad. Sci. USA 88: 2874-2878.
22. Marshall, J.S., and Keegstra, K. (1992). Isolation and characterization of a cDNA clone encoding the major hsp70 of the pea chloroplastic stroma. Plant Physiol. 100: 1048-1054.
23. Mayer, M.P. (2010). Gymnastics of molecular chaperones. Mol. Cell 39: 321-331.
24. McCarty, J.S., and Walker, G.C. (1991). DnaK as a thermometer: Threonine-199 is site of autophosphorylation and is critical for ATPase activity. Proc. Natl. Acad. Sci. USA 88: 9513-9517.
25. Nielsen, E., Akita, M., Davila-Aponte, J., and 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.
26. O'Brien, M.C., and McKay, D.B. (1993). Threonine 204 of the chaperone protein Hsc70 influences the structure of the active site, but is not essential for ATP hydrolysis. J. Biol. Chem. 268: 24323-24329.
27. Odell, J.T., Nagy, F., and Chua, N.H. (1985). Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313: 810-812.
28. Pain, D., and Blobel, G. (1987). Protein import into chloroplasts requires a chloroplast ATPase. Proc. Natl. Acad. Sci. USA 84: 3288-3292.
29. Pesaresi, P., Varotto, C., Meurer, J., Jahns, P., Salamini, F., and Leister, D. (2001). Knock-out of the plastid ribosomal protein L11 in Arabidopsis: Effects on mRNA translation and photosynthesis. Plant J. 27: 179-189.
30. Schaefer, D., Zryd, J.-P., Knight, C.D., and Cove, D.J. (1991). Stable transformation of the moss Physcomitrella patens. Mol. Gen. Genet. 226: 418-424.
31. Schindler, C., Hracky, R., and Soll, J. (1987). Protein transport in chloroplasts: ATP is prerequisit. Z. Naturforsch. 42: 103-108.
32. Schroda, M., Vallon, O., Whitelegge, J.P., Beck, C.F., andWollman, F.A. (2001). The chloroplastic GrpE homolog of Chlamydomonas: Two isoforms generated by differential splicing. Plant Cell 13: 2823-2839.
33. Scott, S.V., and Theg, S.M. (1996). A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: Energetics and mechanistic implications. J. Cell Biol. 132: 63-75.
34. Shanklin, J., DeWitt, N.D., and Flanagan, J.M. (1995). The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: An archetypal two-component ATP-dependent protease. Plant Cell 7: 1713-1722.
35. Shi, L.X., and Theg, S.M. (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, L.X., and Theg, S.M. (2013a). The chloroplast protein import system: From algae to trees. Biochim. Biophys. Acta 1833: 314-331.
37. Shi, L.X., and Theg, S.M. (2013b). Energetic cost of protein import across the envelope membranes of chloroplasts. Proc. Natl. Acad. Sci. USA 110: 930-935.
38. Sichting, M., Mokranjac, D., Azem, A., Neupert, W., and Hell, K. (2005). Maintenance of structure and function of mitochondrial Hsp70 chaperones requires the chaperone Hep1. EMBO J. 24: 1046-1056.
39. 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.
40. Khersonsky, O., and Tawfik, D.S. (2010). Enzyme promiscuity: A mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79: 471-505.
41. Theg, S.M., Bauerle, C., Olsen, L.J., Selman, B.R., and 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.
42. Theg, S.M., Chiang, G., and Dilley, R.A. (1988). Protons in the thylakoid membrane-sequestered domains can directly pass through the coupling factor during ATP synthesis in flashing light. J. Biol. Chem. 263: 673-681.
43. Vidali, L., Augustine, R.C., Fay, S.N., Franco, P., Pattavina, K.A., and Bezanilla, M. (2009). Rapid screening for temperaturesensitive alleles in plants. Plant Physiol. 151: 506-514.
44. Voordeckers, K., Brown, C.A., Vanneste, K., van der Zande, E., Voet, A., Maere, S., and Verstrepen, K.J. (2012). Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol. 10: e1001446.
45. Willmund, F., Hinnenberger, M., Nick, S., Schulz-Raffelt, M., Mühlhaus, T., and Schroda, M. (2008). Assistance for a chaperone: Chlamydomonas HEP2 activates plastidic HSP70B for cochaperone binding. J. Biol. Chem. 283: 16363-16373.