Arabidopsis J-Protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control

Plant Cell

Volumn 25, Issue 10, 2013, Pages 4183-4194

  Pulido, Pablo ^a   Toledo Ortiz, Gabriela ^a,c   Phillips, Michael A ^a   Wright, Louwrance P ^b   Rodríguez Concepción, Manuel ^a  

^a CSIC   (Spain)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

ARABIDOPSIS PROTEIN; DEOXYXYLULOSE-5-PHOSPHATE SYNTHASE; HEAT SHOCK PROTEIN 70; TERPENE; TRANSFERASE;

ARABIDOPSIS; CHLOROPLAST; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN ANALYSIS; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; HSP70 HEAT-SHOCK PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PLANTS, GENETICALLY MODIFIED; PROTEIN INTERACTION MAPPING; TERPENES; TRANSFERASES;

EID: 84888422431     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.113001     Document Type: Article

References (75)

1. Al-Babili, S., von Lintig, J., Haubruck, H., and Beyer, P. (1996). A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J. 9: 601-612.
2. Araki, N., Kusumi, K., Masamoto, K., Niwa, Y., and Iba, K. (2000). Temperature-sensitive Arabidopsis mutant defective in 1-deoxy-Dxylulose 5-phosphate synthase within the plastid non-mevalonate pathway of isoprenoid biosynthesis. Physiol. Plant. 108: 19-24.
3. Bonk, M., Tadros, M., Vandekerckhove, J., Al-Babili, S., and Beyer, P. (1996). Purification and characterization of chaperonin 60 and heat-shock protein 70 from chromoplasts of Narcissus pseudonarcissus. Plant Physiol. 111: 931-939.
4. Boston, R.S., Viitanen, P.V., and Vierling, E. (1996). Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32: 191-222.
5. Botella-Pavía, P., and Rodríguez-Concepción, M. (2006). Carotenoid biotechnology in plants for nutritionally improved foods. Physiol. Plant. 126: 369-381.
6. Carretero-Paulet, L., Ahumada, I., Cunillera, N., Rodríguez-Concepción, M., Ferrer, A., Boronat, A., and Campos, N. (2002). Expression and molecular analysis of the Arabidopsis DXR gene encoding 1-deoxy-D-xylulose 5-phosphate reductoisomerase, the first committed enzyme of the 2-C-methyl-D-erythritol 4-phosphate pathway. Plant Physiol. 129: 1581-1591.
7. Carretero-Paulet, L., Cairó, A., Botella-Pavía, P., Besumbes, O., Campos, N., Boronat, A., and Rodríguez-Concepción, M. (2006). Enhanced flux through the methylerythritol 4-phosphate pathway in Arabidopsis plants overexpressing deoxyxylulose 5-phosphate reductoisomerase. Plant Mol. Biol. 62: 683-695.
8. Chen, K.M., Holmström, M., Raksajit, W., Suorsa, M., Piippo, M., and Aro, E.M. (2010). Small chloroplast-targeted DnaJ proteins are involved in optimization of photosynthetic reactions in Arabidopsis thaliana. BMC Plant Biol. 10: 43.
9. Cordoba, E., Salmi, M., and León, P. (2009). Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J. Exp. Bot. 60: 2933-2943.
10. Craig, E.A., Huang, P., Aron, R., and Andrew, A. (2006). The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol. 156: 1-21.
11. DellaPenna, D., and Pogson, B.J. (2006). Vitamin synthesis in plants: Tocopherols and carotenoids. Annu. Rev. Plant Biol. 57: 711-738.
12. Enfissi, E.M.A., Fraser, P.D., Lois, L.M., Boronat, A., Schuch, W., and Bramley, P.M. (2005). Metabolic engineering of the mevalonate and nonmevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol. J. 3: 17-27.
13. Estévez, J.M., Cantero, A., Reindl, A., Reichler, S., and León, P. (2001). 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem. 276: 22901-22909.
14. Estévez, J.M., Cantero, A., Romero, C., Kawaide, H., Jiménez, L.F., Kuzuyama, T., Seto, H., Kamiya, Y., and León, P. (2000). Analysis of the expression of CLA1, a gene that encodes the 1-deoxyxylulose 5-phosphate synthase of the 2-C-methyl-D-erythritol-4-phosphate pathway in Arabidopsis. Plant Physiol. 124: 95-104.
15. Flores-Pérez, U., and Jarvis, P. (2013). Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta 1833: 332-340.
16. Flores-Pérez, U., Pérez-Gil, J., Closa, M., Wright, L.P., Botella-Pavía, P., Phillips, M.A., Ferrer, A., Gershenzon, J., and Rodríguez-Concepción, M. (2010). Pleiotropic regulatory locus 1 (PRL1) integrates the regulation of sugar responses with isoprenoidmetabolism in Arabidopsis. Mol. Plant 3: 101-112.
17. Flores-Pérez, U., Sauret-Güeto, S., Gas, E., Jarvis, P., and Rodríguez-Concepción, M. (2008). A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20: 1303-1315.
18. Guevara-García, A., San Román, C., Arroyo, A., Cortés, M.E., de la Luz Gutiérrez-Nava, M., and León, P. (2005). Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-D-erythritol 4-phosphate pathway. Plant Cell 17: 628-643.
19. Hafrén, A., Hofius, D., Rönnholm, G., Sonnewald, U., and Mäkinen, K. (2010). HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell 22: 523-535.
20. Hans, J., Hause, B., Strack, D., and Walter, M.H. (2004). Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbusculecontaining cells of maize. Plant Physiol. 134: 614-624.
21. Hayes, S.A., and Dice, J.F. (1996). Roles of molecular chaperones in protein degradation. J. Cell Biol. 132: 255-258.
22. Hemmerlin, A. (2013). Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis. Plant Sci. 203-204: 41-54.
23. Huang, H.C., Sherman, M.Y., Kandror, O., and Goldberg, A.L. (2001). The molecular chaperone DnaJ is required for the degradation of a soluble abnormal protein in Escherichia coli. J. Biol. Chem. 276: 3920-3928.
24. Kampinga, H.H., and Craig, E.A. (2010). The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11: 579-592.
25. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
26. Kato, Y., and Sakamoto, W. (2010). New insights into the types and function of proteases in plastids. Int. Rev. Cell Mol. Biol. 280: 185-218.
27. Kato, Y., Sun, X., Zhang, L., and Sakamoto, W. (2012). Cooperative D1 degradation in the photosystem II repair mediated by chloroplastic proteases in Arabidopsis. Plant Physiol. 159: 1428-1439.
28. Kim, J., Rudella, A., Ramirez Rodriguez, V., Zybailov, B., Olinares, P.D., and van Wijk, K.J. (2009). Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21: 1669-1692.
29. Kuzuyama, T., Takahashi, S., Watanabe, H., and Seto, H. (1998). Direct formation of 2-C-methyl-D-erythritol 4-phosphate from 1-Deoxy-D-xylulose 5-phosphate by 1-Deoxy-D-xylulose 5-phosphate reductoisomerase, a new enzyme in the non-mevalonate pathway to isopentenyl diphosphate. Tetrahedron Lett. 39: 4509-4512.
30. Lange, B.M., Wildung, M.R., McCaskill, D., and Croteau, R. (1998). A family of transketolases that directs isoprenoid biosynthesis via a mevalonateindependent pathway. Proc. Natl. Acad. Sci. USA 95: 2100-2104.
31. Laule, O., Fürholz, A., Chang, H.S., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., and Lange, M. (2003). Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100: 6866-6871.
32. Lee, S., Lee, D.W., Lee, Y., Mayer, U., Stierhof, Y.D., Lee, S., Jürgens, G., and Hwang, I. (2009). 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. PlantCell 21: 3984-4001.
33. Lichtenthaler, H.K., and Wellburn, A.R. (1983). Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 603: 591-592.
34. Lin, B.L., Wang, J.S., Liu, H.C., Chen, R.W., Meyer, Y., Barakat, A., and Delseny, M. (2001). Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress Chaperones 6: 201-208.
35. Liu, C., Willmund, F., Golecki, J.R., Cacace, S., Hess, B., Markert, C., and Schroda, M. (2007). The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J. 50: 265-277.
36. Lois, L.M., Campos, N., Putra, S.R., Danielsen, K., Rohmer, M., and Boronat, A. (1998). Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA 95: 2105-2110.
37. Lois, L.M., Rodríguez-Concepción, M., Gallego, F., Campos, N., and Boronat, A. (2000). Carotenoid biosynthesis during tomato fruit development: Regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J. 22: 503-513.
38. Lu, S., et al. (2006). The cauliflower Or gene encodes a DnaJ cysteinerich domain-containing protein that mediates high levels of betacarotene accumulation. Plant Cell 18: 3594-3605.
39. Madueño, F., Napier, J.A., and Gray, J.C. (1993). Newly imported Rieske iron-sulfur protein associates with both Cpn60 and Hsp70 in the chloroplast stroma. Plant Cell 5: 1865-1876.
40. Mahmoud, S.S., and Croteau, R.B. (2001). Metabolic engineering of essential oil yield and composition in mint by altering expression of deoxyxylulose phosphate reductoisomerase and menthofuran synthase. Proc. Natl. Acad. Sci. USA 98: 8915-8920.
41. Mandel, M.A., Feldmann, K.A., Herrera-Estrella, L., Rocha-Sosa, M., and León, P. (1996). CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J. 9: 649-658.
42. Matsue, Y., Mizuno, H., Tomita, T., Asami, T., Nishiyama, M., and Kuzuyama, T. (2010). The herbicide ketoclomazone inhibits 1-deoxy-Dxylulose 5-phosphate synthase in the 2-C-methyl-D-erythritol 4-phosphate pathway and shows antibacterial activity against Haemophilus influenzae. J. Antibiot. 63: 583-588.
43. Miernyk, J.A. (2001). The J-domain proteins of Arabidopsis thaliana: An unexpectedly large and diverse family of chaperones. Cell Stress Chaperones 6: 209-218.
44. Muñoz-Bertomeu, J., Arrillaga, I., Ros, R., and Segura, J. (2006). Up-regulation of 1-deoxy-D-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol. 142: 890-900.
45. Ni, M., Tepperman, J.M., and Quail, P.H. (1999). Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400: 781-784.
46. Nordhues, A., Miller, S.M., Mühlhaus, T., and Schroda, M. (2010). New insights into the roles of molecular chaperones in Chlamydomonas and Volvox. Int. Rev. Cell Mol. Biol. 285: 75-113.
47. Ohad, N., Shichrur, K., and Yalovsky, S. (2007). The analysis of protein-protein interactions in plants by bimolecular fluorescence complementation. Plant Physiol. 145: 1090-1099.
48. Phillips, M.A., León, P., Boronat, A., and Rodríguez-Concepción, M. (2008). The plastidial MEP pathway: Unified nomenclature and resources. Trends Plant Sci. 13: 619-623.
49. Pulido, P., Perello, C., and Rodriguez-Concepcion, M. (2012). New insights into plant isoprenoid metabolism. Mol. Plant 5: 964-967.
50. Rajan, V.B., and D'Silva, P. (2009). Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct. Integr. Genomics 9: 433-446.
51. Ratnayake, R.M., Inoue, H., Nonami, H., and Akita, M. (2008). Alternative processing of Arabidopsis Hsp70 precursors during protein import into chloroplasts. Biosci. Biotechnol. Biochem. 72: 2926-2935.
52. Rodriguez, F., Arsène-Ploetze, F., Rist, W., Rüdiger, S., Schneider-Mergener, J., Mayer, M.P., and Bukau, B. (2008). Molecular basis for regulation of the heat shock transcription factor sigma32 by the DnaK and DnaJ chaperones. Mol. Cell 32: 347-358.
53. Rodríguez-Concepción, M. (2006). Early steps in isoprenoid biosynthesis: Multilevel regulation of the supply of common precursors in plant cells. Phytochem. Rev. 5: 1-15.
54. Rodríguez-Concepción, M., Ahumada, I., Diez-Juez, E., Sauret-Güeto, S., Lois, L.M., Gallego, F., Carretero-Paulet, L., Campos, N., and Boronat, A. (2001). 1-Deoxy-D-xylulose 5-phosphate reductoisomerase and plastid isoprenoid biosynthesis during tomato fruit ripening. Plant J. 27: 213-222.
55. Rodríguez-Concepción, M., and Boronat, A. (2002). Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130: 1079-1089.
56. Rodríguez-Villalón, A., Gas, E., and Rodríguez-Concepción, M. (2009). Phytoene synthase activity controls the biosynthesis of carotenoids and the supply of their metabolic precursors in darkgrown Arabidopsis seedlings. Plant J. 60: 424-435.
57. Sakr, S., Cirinesi, A.M., Ullers, R.S., Schwager, F., Georgopoulos, C., and Genevaux, P. (2010). Lon protease quality control of presecretory proteins in Escherichia coli and its dependence on the SecB and DnaJ (Hsp40) chaperones. J. Biol. Chem. 285: 23506-23514.
58. Sauret-Güeto, S., Botella-Pavía, P., Flores-Pérez, U., Martínez-García, J.F., San Román, C., León, P., Boronat, A., and Rodríguez-Concepción, M. (2006). Plastid cues posttranscriptionally regulate the accumulation of key enzymes of the methylerythritol phosphate pathway in Arabidopsis. Plant Physiol. 141: 75-84.
59. Schwender, J., Müller, C., Zeidler, J., and Lichtenthaler, H.K. (1999). Cloning and heterologous expression of a cDNA encoding 1-deoxy-D-xylulose-5-phosphate reductoisomerase of Arabidopsis thaliana. FEBS Lett. 455: 140-144.
60. 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.
61. Sprenger, G.A., Schörken, U., Wiegert, T., Grolle, S., deGraaf, A.A., Taylor, S.V., Begley, T.P., Bringer-Meyer, S., and Sahm, H. (1997). Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-D-xylulose 5-phosphate precursor to isoprenoids, thiamin, and pyridoxol. Proc. Natl. Acad. Sci. USA 94: 12857-12862.
62. Su, P.H., and Li, H.M. (2008). Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds. Plant Physiol. 146: 1231-1241.
63. 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.
64. Sung, D.Y., Kaplan, F., and Guy, C.L. (2001). Plant Hsp70 molecular chaperones: Protein structure, gene family, expression and function. Physiol. Plant. 113: 443-451.
65. Takahashi, S., Kuzuyama, T., Watanabe, H., and Seto, H. (1998). A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA 95: 9879-9884.
66. Tanz, S.K., Kilian, J., Johnsson, C., Apel, K., Small, I., Harter, K., Wanke, D., Pogson, B., and Albrecht, V. (2012). The SCO2 protein disulphide isomerase is required for thylakoid biogenesis and interacts with LHCB1 chlorophyll a/b binding proteins which affects chlorophyll biosynthesis in Arabidopsis seedlings. Plant J. 69: 743-754.
67. Tsai, J., and Douglas, M.G. (1996). A conserved HPD sequence of the Jdomain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J. Biol. Chem. 271: 9347-9354.
68. Tsugeki, R., and Nishimura, M. (1993). Interaction of homologues of Hsp70 and Cpn60 with ferredoxin-NADP+ reductase upon its import into chloroplasts. FEBS Lett. 320: 198-202.
69. Vitha, S., Froehlich, J.E., Koksharova, O., Pyke, K.A., van Erp, H., and Osteryoung, K.W. (2003). ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15: 1918-1933.
70. Voos, W. (2013). Chaperone-protease networks in mitochondrial protein homeostasis. Biochim. Biophys. Acta 1833: 388-399.
71. Wall, D., Zylicz, M., and Georgopoulos, C. (1994). The NH2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the ATPase activity of DnaK and are sufficient for lambda replication. J. Biol. Chem. 269: 5446-5451.
72. Wickner, S., Maurizi, M.R., and Gottesman, S. (1999). Posttranslational quality control: Folding, refolding, and degrading proteins. Science 286: 1888-1893.
73. Yalovsky, S., Paulsen, H., Michaeli, D., Chitnis, P.R., and Nechushtai, R. (1992). Involvement of a chloroplast HSP70 heat shock protein in the integration of a protein (light-harvesting complex protein precursor) into the thylakoid membrane. Proc. Natl. Acad. Sci. USA 89: 5616-5619.
74. Zeidler, J., Schwender, J., Mueller, C., and Lichtenthaler, H.K. (2000). The non-mevalonate isoprenoid biosynthesis of plants as a test system for drugs against malaria and pathogenic bacteria. Biochem. Soc. Trans. 28: 796-798.
75. Zybailov, B., Friso, G., Kim, J., Rudella, A., Rodríguez, V.R., Asakura, Y., Sun, Q., and van Wijk, K.J. (2009). Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism. Mol. Cell. Proteomics 8: 1789-1810.