Opposing effects of folding and assembly chaperones on evolvability of Rubisco

Nature Chemical Biology

Volumn 11, Issue 2, 2015, Pages 148-155

  Duraõ, Paulo ^a   Aigner, Harald ^a   Nagy, Péter ^a   Mueller Cajar, Oliver ^a,b   Hartl, F Ulrich ^a   Hayer Hartl, Manajit ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; ESCHERICHIA COLI PROTEIN; GROE PROTEIN, E COLI; HEAT SHOCK PROTEIN; RBCX PROTEIN, CYANOBACTERIA; RIBULOSEBISPHOSPHATE CARBOXYLASE;

CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; MUTATION; PHOTOSYNTHESIS; PROCEDURES; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SYNECHOCOCCUS; SYNECHOCYSTIS;

BACTERIAL PROTEINS; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; MOLECULAR CHAPERONES; MUTATION; PHOTOSYNTHESIS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SYNECHOCOCCUS; SYNECHOCYSTIS;

EID: 84928069254     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1715     Document Type: Article

References (48)

1. Whitney, S. M., Houtz, R. L., Alonso, H. Advancing our understanding and capacity to engineer nature's CO2-sequestering enzyme, Rubisco. Plant Physiol. 155, 27-35 (2011).
2. Hohmann-Marriott, M. F., Blankenship, R. E. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62, 515-548 (2011).
3. Andersson, I., Taylor, T. C. Structural framework for catalysis and regulation in ribulose-1, 5-bisphosphate carboxylase/oxygenase. Arch. Biochem. Biophys. 414, 130-140 (2003).
4. John Andrews, T., Whitney, S. M. Manipulating ribulose bisphosphate carboxylase/oxygenase in the chloroplasts of higher plants. Arch. Biochem. Biophys. 414, 159-169 (2003).
5. Barraclough, R., Ellis, R. J. Protein synthesis in chloroplasts. IX. Assembly of newly-synthesized large subunits into ribulose bisphosphate carboxylase in isolated intact pea chloroplasts. Biochim. Biophys. Acta 608, 19-31 (1980).
6. Goloubinoff, P., Christeller, J. T., Gatenby, A. A., Lorimer, G. H. Reconstitution of active dimeric ribulose bisphosphate carboxylase from an unfolded state depends on 2 chaperonin proteins and Mg-ATP. Nature 342, 884-889 (1989).
7. Goloubinoff, P., Gatenby, A. A., Lorimer, G. H. GroE heat-shock proteins promote assembly of foreign prokaryotic ribulose bisphosphate carboxylase oligomers in Escherichia coli. Nature 337, 44-47 (1989).
8. Brinker, A. et al. Dual function of protein confinement in chaperonin-assisted protein folding. Cell 107, 223-233 (2001).
9. Saschenbrecker, S. et al. Structure and function of RbcX, an assembly chaperone for hexadecameric Rubisco. Cell 129, 1189-1200 (2007).
10. Liu, C. et al. Coupled chaperone action in folding and assembly of hexadecameric Rubisco. Nature 463, 197-202 (2010).
11. Kerner, M. J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
12. Tsai, Y.-C. C., Mueller-Cajar, O., Saschenbrecker, S., Hartl, F. U., Hayer-Hartl, M. Chaperonin cofactors, Cpn10 and Cpn20, of green algae and plants function as hetero-oligomeric ring complexes. J. Biol. Chem. 287, 20471-20481 (2012).
13. Onizuka, T. et al. The rbcX gene product promotes the production and assembly of ribulose-1, 5-bisphosphate carboxylase/oxygenase of Synechococcus sp PCC7002 in Escherichia coli. Plant Cell Physiol. 45, 1390-1395 (2004).
14. Emlyn-Jones, D., Woodger, F. J., Price, G. D., Whitney, S. M. RbcX can function as a Rubisco chaperonin, but is non-essential in Synechococcus PCC7942. Plant Cell Physiol. 47, 1630-1640 (2006).
15. Bracher, A., Starling-Windhof, A., Hartl, F. U., Hayer-Hartl, M. Crystal structure of a chaperone-bound assembly intermediate of form I Rubisco. Nat. Struct. Mol. Biol. 18, 875-880 (2011).
16. Tabita, F. R. Rubisco: the enzyme that keeps on giving. Cell 129, 1039-1040 (2007).
17. Feiz, L. et al. Ribulose-1, 5-bis-phosphate carboxylase/oxygenase accumulation factor 1 is required for holoenzyme assembly in maize. Plant Cell 24, 3435-3446 (2012).
18. Wheatley, N. M., Sundberg, C. D., Gidaniyan, S. D., Cascio, D., Yeates, T. O. Structure and identification of a pterin dehydratase-like protein as a RuBisCO assembly factor in the ?-carboxysome. J. Biol. Chem. 289, 7973-7981 (2014).
19. Tcherkez, G., Farquhar, G. D. Carbon isotope effect predictions for enzymes involved in the primary carbon metabolism of plant leaves. Funct. Plant Biol. 32, 277-291 (2005).
20. Parry, M. A. J. et al. Rubisco activity and regulation as targets for crop improvement. J. Exp. Bot. 64, 717-730 (2013).
21. Zeldovich, K. B., Chen, P. Q., Shakhnovich, E. I. Protein stability imposes limits on organism complexity and speed of molecular evolution. Proc. Natl. Acad. Sci. USA 104, 16152-16157 (2007).
22. Povolotskaya, I. S., Kondrashov, F. A. Sequence space and the ongoing expansion of the protein universe. Nature 465, 922-926 (2010).
23. Rutherford, S. L., Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336-342 (1998).
24. DePristo, M. A., Weinreich, D. M., Hartl, D. L. Missense meanderings in sequence space: a biophysical view of protein evolution. Nat. Rev. Genet. 6, 678-687 (2005).
25. Tokuriki, N., Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668-673 (2009).
26. Bogumil, D., Dagan, T. Chaperonin-dependent accelerated substitution rates in prokaryotes. Genome Biol. Evol. 2, 602-608 (2010).
27. Bogumil, D., Landan, G., Ilhan, J., Dagan, T. Chaperones divide yeast proteins into classes of expression level and evolutionary rate. Genome Biol. Evol. 4, 618-625 (2012).
28. Bershtein, S., Mu, W., Serohijos, A. W. R., Zhou, J., Shakhnovich, E. I. Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol. Cell 49, 133-144 (2013).
29. Mueller-Cajar, O., Whitney, S. M. Evolving improved Synechococcus Rubisco functional expression in Escherichia coli. Biochem. J. 414, 205-214 (2008).
30. Cai, Z., Liu, G., Zhang, J., Li, Y. Development of an activity-directed selection system enabled significant improvement of the carboxylation efficiency of Rubisco. Protein Cell 5, 552-562 (2014).
31. Parikh, M. R., Greene, D. N., Woods, K. K., Matsumura, I. Directed evolution of Rubisco hypermorphs through genetic selection in engineered E. coli. Protein Eng. Des. Sel. 19, 113-119 (2006).
32. Mueller-Cajar, O., Morell, M., Whitney, S. M. Directed evolution of Rubisco in Escherichia coli reveals a specificity-determining hydrogen bond in the form II enzyme. Biochemistry 46, 14067-14074 (2007).
33. Hudson, G. S., Morell, M. K., Arvidsson, Y. B. C., Andrews, T. J. Synthesis of spinach phosphoribulokinase and ribulose 1, 5-bisphosphate in Escherichia coli. Aust. J. Plant Physiol. 19, 213-221 (1992).
34. Newman, J., Branden, C. I., Jones, T. A. Structure determination and refinement of ribulose 1, 5-bisphosphate carboxylase/oxygenase from Synechococcus PCC6301. Acta Crystallogr. D Biol. Crystallogr. 49, 548-560 (1993).
35. Chen, Z., Hong, S., Spreitzer, R. J. Thermal-instability of ribulose-1, 5-bisphosphate carboxylase oxygenase from a temperature-conditional chloroplast mutant of Chlamydomonas reinhardtii. Plant Physiol. 101, 1189-1194 (1993).
36. Smith, S. A., Tabita, F. R. Positive and negative selection of mutant forms of prokaryotic (cyanobacterial) ribulose-1, 5-bisphosphate carboxylase/oxygenase. J. Mol. Biol. 331, 557-569 (2003).
37. Yeates, T. O., Kerfeld, C. A., Heinhorst, S., Cannon, G. C., Shively, J. M. Protein-based organelles in bacteria: carboxysomes and related microcompartments. Nat. Rev. Microbiol. 6, 681-691 (2008).
38. Yeates, T. O., Thompson, M. C., Bobik, T. A. The protein shells of bacterial microcompartment organelles. Curr. Opin. Struct. Biol. 21, 223-231 (2011).
39. Espie, G. S., Kimber, M. S. Carboxysomes: cyanobacterial Rubisco comes in small packages. Photosynth. Res. 109, 7-20 (2011).
40. Amichay, D., Levitz, R., Gurevitz, M. Construction of a Synechocystis PCC6803 mutant suitable for the study of variant hexadecameric ribulose-bisphosphate carboxylase oxygenase enzymes. Plant Mol. Biol. 23, 465-476 (1993).
41. Marcus, Y., Altman-Gueta, H., Finkler, A., Gurevitz, M. Mutagenesis at two distinct phosphate-binding sites unravels their differential roles in regulation of Rubisco activation and catalysis. J. Bacteriol. 187, 4222-4228 (2005).
42. Tokuriki, N., Tawfik, D. S. Stability effects of mutations and protein evolvability. Curr. Opin. Struct. Biol. 19, 596-604 (2009).
43. Tang, Y. C. et al. Structural features of the GroEL-GroES nano-cage required for rapid folding of encapsulated protein. Cell 125, 903-914 (2006).
44. Wyganowski, K. T., Kaltenbach, M., Tokuriki, N. GroEL/ES buffering and compensatory mutations promote protein evolution by stabilizing folding intermediates. J. Mol. Biol. 425, 3403-3414 (2013).
45. Chakraborty, K. et al. Chaperonin-catalyzed rescue of kinetically trapped states in protein folding. Cell 142, 112-122 (2010).
46. Georgescauld, F. et al. GroEL/ES chaperonin modulates the mechanism and accelerates the rate of TIM-barrel domain folding. Cell 157, 922-934 (2014).
47. Tóth-Petróczy, A., Tawfik, D. S. Slow protein evolutionary rates are dictated by surface-core association. Proc. Natl. Acad. Sci. USA 108, 11151-11156 (2011).
48. Machado, I. M., Atsumi, S. Cyanobacterial biofuel production. J. Biotechnol. 162, 50-56 (2012).