A Light-Induced Protease from Barley Plastids Degrades NADPH:Protochlorophyllide Oxidoreductase Complexed with Chlorophyllide

REFERENCES

• Apel, K., and K. Kloppstech. 1980. The effect of light on the biosynthesis of the light-harvesting chlorophyll a/b protein. Evidence for the requirement of chlorophyll a for the stabilization of the apoprotein. Planta 150:426–430.
   Google Scholar
• Apel, K., H.-J. Santel, T. E. Redlinger, and H. Falk. 1980. The protochlo-rophyllide holochrome of barley (Hordeum vulgare L.). Isolation and char-acterization of the NADPH:protochlorophyllide oxidoreductase. Eur. J. Biochem. 311:251–258.
   Google Scholar
• Beale, S. I., and J. D. Weinstein. 1990. Tetrapyrrole metabolism in photo synthetic organisms, p. 287–391. In H. A. Dailey (ed.), Biosynthesis of heme and chlorophylls. McGraw-Hill Publishing Company, New York.
   Google Scholar
• Benli, M., R. Schulz, and K. Apel. 1991. Effect of light on the NADPH-protochlorophyllide oxidoreductase of Arabidopsis thaliana. Plant Mol. Biol. 16:615–625.
   PubMedGoogle Scholar
• Chiang, H.-L., and R. Schekman. 1991. Regulated import and degradation of a cytosolic protein into the yeast vacuole. Nature (London) 350:313–318.
   PubMed Web of Science ®Google Scholar
• Cohen, J. A., R. A. Osterbaan, and F. Berends. 1967. Organophosphorous compounds. Methods Enzymol. 11:686–702.
   Google Scholar
• Dehesh, K., M. Klaas, I. Häuser, and K. Apel. 1986. Light-induced changes in the distribution of the 36000-Mr polypeptide of NADPH-protochlorophyl-lide oxidoreductase within different cellular compartments of barley (Hor-deum vulgare L.). Planta 169:162–171.
   PubMedGoogle Scholar
• Dehesh, K., and M. Ryberg. 1985. The NADPH-protochlorophyllide oxi-doreductase is the major protein constituent of prolamellar bodies in wheat (Triticum aestivum L.). Planta 164:396–399.
   PubMedGoogle Scholar
• Forreiter, C., B. van Cleve, A. Schmidt, and K. Apel. 1990. Evidence for a general light-dependent negative control of NADPH-protochlorophyllide oxidoreductase in angiosperms. Planta 183:126–132.
   Google Scholar
• Gatenby, A. A., T. H. Lubben, P. Ahlquist, and K. Keegstra. 1988. Imported large subunits of ribulose bisphosphate carboxylase/oxygenase, but not imported β-ATP synthase subunits, are assembled into holoenzyme in isolated chloroplasts. EMBO J. 7:1307–1314.
   PubMedGoogle Scholar
• Gold, A. M. 1967. Sulfonylation with sulfonyl halides. Methods Enzymol. 11:706–711.
   Google Scholar
• Gomez-Silva, B., M. P. Timko, and J. A. Schiff. 1985. Chlorophyll biosyn-thesis from glutamate or 5-aminolevulinate in intact Euglena chloroplasts. Planta 165:12–22.
   PubMedGoogle Scholar
• Gottesman, S., and M. R. Maurizi. 1992. Regulation by proteolysis: energy-dependent proteases and their targets. Microbiol. Rev. 56:592–621.
   PubMedGoogle Scholar
• Griffiths, W. T. 1975. Characterization of the terminal stages of chlorophyll(ide) synthesis in etioplast membrane preparations. Biochem. J. 152:623–635.
   PubMed Web of Science ®Google Scholar
• Griffiths, W. T. 1978. Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem. J. 174:681–692.
   PubMedGoogle Scholar
• Grossman, A. R., S. G. Bartlett, G. W. Schmidt, J. E. Mullet, and N.-H. Chua. 1982. Optimal conditions for post-translational uptake of proteins by isolated chloroplasts. J. Biol. Chem. 257:1558–1563.
   PubMedGoogle Scholar
• Häuser, I., K. Dehesh, and K. Apel. 1984. The proteolytic degradation in vitro of the NADPH-protochlorophyllide oxidoreductase of barley (Hordeum vulgare L.). Arch. Biochem. Biophys. 228:577–586.
   PubMedGoogle Scholar
• Honda, T., A. Tanaka, and H. Tsuji. 1994. Proteolytic activity in intact barley etioplasts: endoproteolysis of NADPH-protochlorophyllide oxidoreductase protein. Plant Sci. (Limerick) 97:129–135.
   Google Scholar
• Hoober, K. J., and M. Hughes. 1992. Purification and characterization of a membrane-bound protease from Chlamydomonas reinhardtii. Plant Physiol. (Bethesda) 99:932–937.
   PubMed Web of Science ®Google Scholar
• Kay, S. A., and W. T. Griffiths. 1983. Light-induced breakdown of NADPH: protochlorophyllide oxidoreductase in vitro. Plant Physiol. (Bethesda) 72: 229–236.
   PubMedGoogle Scholar
• Klein, R. R., and J. E. Mullet. 1986. Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast bio-genesis. J. Biol. Chem. 261:11138–11145.
   PubMed Web of Science ®Google Scholar
• Klein, R. R., and J. E. Mullet. 1987. Control of gene expression during higher plant chloroplast biogenesis. Protein synthesis and transcript levels of psbA, psaA-psaB, and rbcL in dark-grown and illuminated seedlings. J. Biol. Chem. 262:4341–4348.
   Google Scholar
• Krauspe, R., and A. Scheer. 1986. Proteolysis in Euglena gracilis. III. Cysteine, but not serine proteinases are involved in chloroplast formation in resting cells. J. Plant Physiol. 123:441–454.
   Google Scholar
• Krauspe, R., A. Scheer, S. Schaper, and P. Bohley. 1986. Proteolysis in Euglena gracilis. II. Soluble and particle-bound proteinase activities of the cysteine and aspartic acid types during growth and chloroplast development. Planta 167:482–490.
   PubMedGoogle Scholar
• Krieg, P. A., and D. A. Melton. 1984. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 12:7057–7070.
   PubMed Web of Science ®Google Scholar
• Kyle, D. J., I. Ohad, and C. J. Arntzen. 1984. Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl. Acad. Sci. USA 81:4070–4074.
   PubMed Web of Science ®Google Scholar
• Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680–685.
   PubMed Web of Science ®Google Scholar
• Langner, J., A. Wakil, M. Zimmermann, S. Ansorge, P. Bohley, H. Kirschke, and B. Wiederanders. 1973. Aktivitätsbestimmung proteolytischer Enzyme mit Azokasein als Substrat. Acta Med. Biol. Germ. 31:1–18.
   PubMedGoogle Scholar
• Liu, X.-Q., and A. T. Jagendorf. 1986. A variety of chloroplast-located pro-teases, p. 597–606. In G. Akoyunoglou, and H. Senger (ed.), Regulation of chloroplast differentiation. Alan R. Liss, New York.
   Google Scholar
• Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265–275.
   PubMed Web of Science ®Google Scholar
• Matile, P. 1982. Protein degradation, p. 169–188. In D. Boulter, and B. Parthier (ed.), Encyclopedia of plant physiology, new series, vol. 14A. Nucleic acids and proteins in plants. Springer, Berlin.
   Google Scholar
• Mattoo, A. K., E. Hoffmann-Falk, J. B. Marder, and M. Edelman. 1984. Regulation of protein metabolism: coupling of photosynthetic electron transport to in vitro degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc. Natl. Acad. Sci. USA 81:1380–1384.
   PubMed Web of Science ®Google Scholar
• Maurizi, M. R., W. P. Clark, S.-H. Kim, and S. Gottesman. 1990. ClpP represents a unique family of serine proteases. J. Biol. Chem. 265:12546–12552.
   PubMed Web of Science ®Google Scholar
• McIlvaine, T. C. 1921. A buffer solution for colorimetric comparison. J. Biol. Chem. 49:183–186.
   Google Scholar
• Meigs, T. E., and R. D. Simoni. 1992. Regulated degradation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase in permeabilized cells. J. Biol. Chem. 267:13547–13552.
   PubMedGoogle Scholar
• Mullet, J. E. 1988. Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39:475–502.
   Web of Science ®Google Scholar
• Nicholson, D. W., and W. Neupert. 1989. Import of cytochrome c into mitochondria: reduction of heme, mediated by NADH and flavin nucleotides, is obligatory for its covalent linkage to apocytochrome c. Proc. Natl. Acad. Sci. USA 86:4340–4344.
   PubMedGoogle Scholar
• Nover, L., K.-D. Scharf, and D. Neumann. 1989. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs. Mol. Cell. Biol. 9:1298–1308.
   PubMed Web of Science ®Google Scholar
• Oblong, J. E., and G. Lamppa. 1992. Identification of two structurally related proteins involved in proteolytic processing of precursors targeted to the chloroplast. EMBO J. 11:4401–4409.
   PubMedGoogle Scholar
• Parthier, B. 1973. Cytoplasmic site of synthesis of chloroplast aminoacyl-tRNA synthetases in Euglena gracilis. FEBS Lett. 38:70–74.
   PubMedGoogle Scholar
• Reinbothe, C. Unpublished results.
   Google Scholar
• Reinbothe, S., R. Krauspe, and B. Parthier. 1990. In-vitro transport of chloroplast proteins in a homologous Euglena system with particular reference to plastid leucyl-tRNA synthetase. Planta 181:176–183.
   PubMedGoogle Scholar
• Reinbothe, S., C. Reinbothe, C. Heintzen, C. Seidenbecher, and B. Parthier. 1993. A methyl jasmonate-induced shift in the length of the 59 untranslated region impairs translation of the plastid rbcL transcript in barley. EMBO J. 12:1505–1512.
   PubMed Web of Science ®Google Scholar
• Reinbothe, S., C. Reinbothe, and B. Parthier. 1993. Methyl jasmonate-regulated translation of nuclear-encoded chloroplast proteins in barley. J. Biol. Chem. 268:10606–10611.
   PubMed Web of Science ®Google Scholar
• Reinbothe, S., C. Reinbothe, S. Runge, and K. Apel. 1995. Enzymatic product formation impairs both the chloroplast receptor binding function as well as translocation competence of the NADPH:protochlorophyllide oxidoreduc-tase, a nuclear-encoded plastid precursor protein. J. Cell Biol. 129:299–308.
   PubMedGoogle Scholar
• Reinbothe, S., S. Runge, C. Reinbothe, B. van Cleve, and K. Apel. 1995. Substrate-dependent transport of the NADPH:protochlorophyllide oxi-doreductase into isolated plastids. Plant Cell 7:161–172.
   PubMedGoogle Scholar
• Rich, D. R., M. S. Bernatowicz, N. S. Agarwal, M. Kawai, and F. G. Salituro. 1985. Inhibition of aspartic proteases by pepstatin and 3-methylstatin derivatives of pepstatin. Evidence for collected-substrate enzyme inhibition. Biochemistry 24:3165–3173.
   Google Scholar
• Rivett, A. J. 1986. Regulation of intracellular protein turnover: covalent modifications as a mechanism of marking proteins for degradation. Curr. Top. Cell. Regul. 28:291–337.
   PubMedGoogle Scholar
• Robinson, C., and R. Ellis. 1984. Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of imported precursor polypeptides. Eur. J. Biochem. 142:337–342.
   Google Scholar
• Santel, H.-J., and K. Apel. 1981. The protochlorophyllide holochrome of barley (Hordeum vulgare L.). The effect of light on the NADPH-protochlo-rophyllide oxidoreductase. Eur. J. Biochem. 120:95–103.
   Google Scholar
• Schulz, R., K. Steinmüller, M. Klaas, C. Forreiter, S. Rasmussen, C. Hiller, and K. Apel. 1989. Nucleotide sequence of a cDNA coding for the NADPH-protochlorophyllide oxidoreductase (PCR) of barley (Hordeum vulgare L.) and its expression in Escherichia coli. Mol. Gen. Genet. 217:355–361.
   PubMedGoogle Scholar
• Shipton, C. A., and J. Barber. 1991. Photoinduced degradation of the D1 polypeptide in isolated reaction centers of photosystem II: evidence for an autoproteolytic process triggered by the oxidizing side of the photosystem. Proc. Natl. Acad. Sci. USA 88:6691–6695.
   PubMed Web of Science ®Google Scholar
• Sugiura, M. 1992. The chloroplast genome. Plant Mol. Biol. 19:149–168.
   PubMed Web of Science ®Google Scholar
• Thompson, W. F., and M. J. White. 1991. Chloroplast development and gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:423–466.
   Google Scholar
• Towbin, M., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets; procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350–4354.
   PubMed Web of Science ®Google Scholar
• Vierstra, R. D. 1989. Protein degradation, p. 521–536. In P. K. Stumpf, and E. E. Conn (ed.), Biochemistry of plants. A comprehensive treatise, vol. 15. Academic Press, New York.
   Google Scholar