Abstract
Steady-state levels of chloroplast proteins rely on the balance between synthesis and degradationrates. Thus, the importance of protein-degradation processes in shaping the chloroplast proteome,and hence proper organellar functioning, cannot be overestimated. Chloroplast proteases and peptidasesparticipate in chloroplast biogenesis through maturation or activation of pre-proteins, adaptationto changing environmental conditions through degradation of certain proteins, and maintenance of proteinquality through degradation of unassembled or damaged proteins. These activities are mediated byATP-dependent and -independent proteases, many of which are encoded by multigene families. Newlyimported proteins are processed by stroma- and thylakoid-localized peptidases that remove signal sequences,which are then further degraded. The multisubunit ATP-dependent Clp and FtsH complexes degrade housekeepingand oxidatively damaged proteins in the stroma and thylakoid membranes, respectively. A numberof other chloroplast proteases have been identified, but their function and substrates are still unknown,as are the nature of degradation signals and determinants of protein instability. Future researchis expected to focus on these questions.
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell A, Vallon O, Rodermel SR, Shinozaki K, Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol 125:1912–1918
Adam Z, Zaltsman A, Sinvany-Villalobo G, Sakamoto W (2005) FtsH proteases in chloroplasts and cyanobacteria. Physiol Plant 123:386–390
Adam Z, Rudella A, van Wijk KJ (2006) Recent advances in the study of Clp, FtsH, and other proteases located in chloroplasts. Curr Opin Plant Biol 9:234–240
Adamska I, Kloppstech K, Ohad I (1993) Early light-inducible protein in pea is stable during light stress but is degraded during recovery at low light intensity. J Biol Chem 268:5438–5444
Adamska I, Lindahl M, Roobol-Boza M, Andersson B (1996) Degradation of the light-stress protein is mediated by an ATP-independent, serine-type protease under low-light conditions. Eur J Biochem 236:591–599
Andersson B, Aro E-M (2001) Photodamage and D1 protein turnover in photosystem II. In: Andersson B, Aro E-M (eds) Regulation of photosynthesis. Dordrecht/Boston/London, Kluwer Academic Publishers, pp 377–393
Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277:2006–2011
Barakat S, Pearce DA, Sherman F, Rapp WD (1998) Maize contains a Lon protease gene that can partially complement a yeast pim1-deletion mutant. Plant Mol Biol 37:141–154
Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66
Barrett AJ, Rawlings ND, Woessner JF (2004) Handbook of proteolytic enzymes, 2nd edn. Amsterdam, Elsevier Ltd
Baumeister W, Walz J, Zuhl F, Seemuller E (1998) The proteasome: paradigm of a self-compartmentalizing protease. Cell 92:367–380
Bhushan S, Lefebvre B, Stahl A, Wright SJ, Bruce BD, Boutry M, Glaser E (2003) Dual targeting and function of a protease in mitochondria and chloroplasts. EMBO Rep 4:1073–1078
Bieniossek C, Schalch T, Bumann M, Meister M, Meier R, Baumann U (2006) The molecular architecture of the metalloprotease FtsH. Proc Natl Acad Sci USA 103:3066–3071
Bolter B, Nada A, Fulgosi H, Soll J (2006) A chloroplastic inner envelope membrane protease is essential for plant development. FEBS Lett 580:789–794
Botos I, Melnikov EE, Cherry S, Khalatova AG, Rasulova FS, Tropea JE, Maurizi MR, Rotanova TV, Gustchina A, Wlodawer A (2004) Crystal structure of the AAA+ alpha domain of E. coli Lon protease at 1.9A resolution. J Struct Biol 146:113–122
Chaal BK, Mould RM, Barbrook AC, Gray JC, Howe CJ (1998) Characterization of a cDNA encoding the thylakoidal processing peptidase from Arabidopsis thaliana. Implications for the origin and catalytic mechanism of the enzyme. J Biol Chem 273:689–692
Chassin Y, Kapri-Pardes E, Sinvany G, Arad T, Adam Z (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis thaliana. Plant Physiol 130:857–864
Chen G, Bi YR, Li N (2005) EGY1 encodes a membrane-associated and ATP-independent metalloprotease that is required for chloroplast development. Plant J 41:364–375
Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84
Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22:303–313
Clarke AK, MacDonald TM, Sjogren LLE (2005) The ATP-dependent Clp protease in chloroplasts of higher plants. Physiol Plant 123:406–412
Clausen T, Southan C, Ehrmann M (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10:443–455
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
Dougan DA, Reid BG, Horwich AL, Bukau B (2002) ClpS, a substrate modulator of the ClpAP machine. Mol Cell 9:673–683
Erbse A, Schmidt R, Bornemann T, Schneider-Mergener J, Mogk A, Zahn R, Dougan DA, Bukau B (2006) ClpS is an essential component of the N-end rule pathway in Escherichia coli. Nature 439:753–756
Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, van Wijk KJ (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16:478–499
Fukui T, Eguchi T, Atomi H, Imanaka T (2002) A membrane-bound archaeal Lon protease displays ATP-independent proteolytic activity towards unfolded proteins and ATP-dependent activity for folded proteins. J Bacteriol 184:3689–3698
Giacomelli L, Rudella A, van Wijk KJ (2006) High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2–2. A comparative proteomics study. Plant Physiol 141:685–701
Giglione C, Meinnel T (2001) Organellar peptide deformylases: universality of the N-terminal methionine cleavage mechanism. Trends Plant Sci 6:566–572
Giglione C, Vallon O, Meinnel T (2003) Control of protein life-span by N-terminal methionine excision. EMBO J 22:13–23
Glaser E, Nilsson S, Bhushan S (2006) Two novel mitochondrial and chloroplastic targeting-peptide-degrading peptidasomes in A. thaliana, AtPreP1 and AtPreP2. Biol Chem 387:1441–1447
Gottesman S (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30:465–506
Gueneau de Novoa P, Williams KP (2004) The tmRNA website: reductive evolution of tmRNA in plastids and other endosymbionts. Nucl Acids Res 32:D104–108
Halperin T, Adam Z (1996) Degradation of mistargeted OEE33 in the chloroplast stroma. Plant Mol Biol 30:925–933
Halperin T, Ostersetzer O, Adam Z (2001a) ATP-dependent association between subunits of Clp protease in pea chloroplasts. Planta 213:614–619
Halperin T, Zheng B, Itzhaki H, Clarke AK, Adam Z (2001b) Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol Biol 45:461–468
Haussuhl K, Andersson B, Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J 20:713–722
Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J, Millar AH (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256
Heazlewood JL, Millar AH (2005) AMPDB: the Arabidopsis mitochondrial protein database. Nuc Acids Res 33:D605–610
Hortensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937
Huesgen PH, Schuhmann H, Adamska I (2005) The family of Deg proteases in cyanobacteria and chloroplasts of higher plants. Physiol Plant 123:413–420
Huesgen P, Schumann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929–6932
Inagaki N, Yamamoto Y, Mori H, Satoh K (1996) Carboxyl-terminal processing protease for the D1 precursor protein: cloning and sequencing of the spinach cDNA. Plant Mol Biol 30:39–50
Inoue K, Keegstra K (2003) A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant J 34:661–669
Inoue K, Baldwin AJ, Shipman RL, Matsui K, Theg SM, Ohme-Takagi M (2005) Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J Cell Biol 171:425–430
Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231
Itzhaki H, Naveh L, Lindahl M, Cook M, Adam Z (1998) Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. J Biol Chem 273:7094–7098
Johnson KA, Bhushan S, Stahl A, Hallberg BM, Frohn A, Glaser E, Eneqvist T (2006) The closed structure of presequence protease PreP forms a unique 10,000 Angstroms3 chamber for proteolysis. EMBO J 25:1977–1986
Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidospsis. Plant Cell 19:1039–1047
Karzai AW, Roche ED, Sauer RT (2000) The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat Struct Biol 7:449–455
Kato Y, Murakami S, Yamamoto Y, Chatani H, Kondo Y, Nakano T, Yokota A, Sato F (2004) The DNA-binding protease, CND41, and the degradation of ribulose-1,5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 220:97–104
Kato Y, Yamamoto Y, Murakami S, Sato F (2005) Post-translational regulation of CND41 protease activity in senescent tobacco leaves. Planta 222:643–651
Kim J, Klein PG, Mullet JE (1994) Vir-115 gene product is required to stabilize D1 translation intermediates in chloroplasts. Plant Mol Biol 25:459–467
Koussevitzky S, Stanne TM, Peto CA, Giap T, Sjogren LL, Zhao Y, Clarke AK, Chory J (2007) An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol Biol 63:85–96
Kovacheva S, Bedard J, Patel R, Dudley P, Twell D, Rios G, Koncz C, Jarvis P (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 41:412–428
Krojer T, Garrido-Franco M, Huber R, Ehrmann M, Clausen T (2002) Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416:455–459
Kuras R, Wollman FA (1994) The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. EMBO J 13:1019–1027
Kuroda H, Maliga P (2003) The plastid clpP1 protease gene is essential for plant development. Nature 425:86–89
Lensch M, Herrmann RG, Sokolenko A (2001) Identification and characterization of SppA, a novel light-inducible chloroplast protease complex associated with thylakoid membranes. J Biol Chem 276:33645–33651
Li HH, Merchant S (1995) Degradation of plastocyanin in copper-deficient C. reinhardtii— evidence for a protease-susceptible conformation of the apoprotein and regulated proteolysis. J Biol Chem 270:23504–23510
Lindahl M, Yang DH, Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light-induced membrane-associated enzymic system. Eur J Biochem 231:503–509
Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B, Adam Z (1996) Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J Biol Chem 271:29329–29334
Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12:419–431
Majeran W, Wollman F-A, Vallon O (2000) Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b6f complex. Plant Cell 12:137–149
Majeran W, Olive J, Drapier D, Vallon O, Wollman FA (2001) The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol 126:421–433
Minai L, Wostrikoff K, Wollman FA, Choquet Y (2006) Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18:159–175
Murakami S, Kondo Y, Nakano T, Sato F (2000) Protease activity of CND41, a chloroplast nucleoid DNA-binding protein, isolated from cultured tobacco cells. FEBS Lett 468:15–18
Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43
Ostersetzer O, Adam Z (1997) Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell 9:957–965
Ostersetzer O, Kato Y, Adam Z, Sakamoto W (2007) Multiple intracellular locations of Lon protease in Arabidopsis: Evidence for the localization of AtLon4 to chloroplasts. Plant Cell Physiol (in press)
Paetzel M, Karla A, Strynadka NC, Dalbey RE (2002) Signal peptidases. Chem Rev 102:4549–4580
Park S, Rodermel SR (2004) Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis. Proc Natl Acad Sci USA 101:12765–12770
Peltier J-B, Ytterberg J, Liberles DA, Roepstorff P, van Wijk KJ (2001) Identification of a 350 kDa ClpP protease complex with 10 different Clp isoforms in chloroplasts of Arabidopsis thaliana. J Biol Chem 276:16318–16327
Peltier J-B, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Soderberg L, Roepstorff P, von Heijne G, van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14:211–236
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 3-D structures and functional implications. J Biol Chem 279:4768–4781
Rawlings ND, Morton FR, Barrett AJ (2006) MEROPS: the peptidase database. Nucl Acids Res 34:D270–D272
Richter S, Lamppa GK (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci USA 95:7463–7468
Richter S, Lamppa GK (1999) Stromal processing peptidase binds transit peptides and initiates their ATP-dependent turnover in chloroplasts. J Cell Biol 147:33–43
Richter S, Lamppa GK (2005) Function of the stromal processing peptidase in the chloroplast import pathway. Physiol Plant 123:362–368
Rudella A, Friso G, Alonso JM, Ecker JR, van Wijk KJ (2006) Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis. Plant Cell 18:1704–1721
Sakamoto W (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57:599–621
Sakamoto W, Tamura T, Hanba-Tomita Y, Sodmergen, Murata M (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7:769–780
Sakamoto W, Zaltsman A, Adam Z, Takahashi Y (2003) Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15:2843–2855
Sarria R, Lyznik A, Vallejos CE, Mackenzie SA (1998) A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell 10:1217–1228
Sauer RT, Bolon DN, Burton BM, Burton RE, Flynn JM, Grant RA, Hersch GL, Joshi SA, Kenniston JA, Levchenko I, Neher SB, Oakes ES, Siddiqui SM, Wah DA, Baker TA (2004) Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119:9–18
Schmidt GW, Mishkind ML (1983) Rapid degradation of unassembled ribulose 1,5-biphosphate carboxylase small subunit in chloroplasts. Proc Natl Acad Sci USA 80:2632–2636
Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365
Shikanai T, Shimizu K, Ueda K, Nishimura Y, Kuroiwa T, Hashimoto T (2001) The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco. Plant Cell Physiol 42:264–273
Sinvany-Villalobo G, Davydov O, Ben-Ari G, Zaltsman A, Raskind A, Adam Z (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol 135:1336–1345
Sjogren LL, MacDonald TM, Sutinen S, Clarke AK (2004) Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol 136:4114–4126
Sjogren LL, Stanne TM, Zheng B, Sutinen S, Clarke AK (2006) Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis. Plant Cell 18:2635–2649
Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann RG, Shestakov SV (2002) The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Curr Genet 41:291–310
Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347
Stahl A, Moberg P, Ytterberg J, Panfilov O, Brockenhuus Von Lowenhielm H, Nilsson F, Glaser E (2002) Isolation and identification of a novel mitochondrial metalloprotease (PreP) that degrades targeting presequences in plants. J Biol Chem 277:41931–41939
Stahl A, Nilsson S, Lundberg P, Bhushan S, Biverstahl H, Moberg P, Morisset M, Vener A, Maler L, Langel U, Glaser E (2005) Two novel targeting peptide degrading proteases, PrePs, in mitochondria and chloroplasts, so similar and still different. J Mol Biol 349:847–860
Suno R, Niwa H, Tsuchiya D, Zhang X, Yoshida M, Morikawa K (2006) Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol Cell 22:575–585
Taguchi F, Yamamoto Y, Satoh K (1995) Recognition of the structure around the site of cleavage by the carboxyl-terminal processing protease for D1 precursor protein of the photosystem II reaction center. J Biol Chem 270:10711–10716
Takechi K, Sodmergen, Murata M, Motoyoshi F, Sakamoto W (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP- dependent protease in Arabidopsis. Plant Cell Physiol 41:1334–1346
Tobias JW, Shrader TE, Rocap G, Varshavsky A (1991) The N-end rule in bacteria. Science 254:1374–1377
Tranel PJ, Keegstra K (1996) A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8:2093–2104
Tsugane K, Maekawa M, Takagi K, Takahara H, Qian Q, Eun CH, Iida S (2006) An active DNA transposon nDart causing leaf variegation and mutable dwarfism and its related elements in rice. Plant J 45:46–57
Urantowka A, Knorpp C, Olczak T, Kolodziejczak M, Janska H (2005) Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol Biol 59:239–252
Varshavsky A (1992) The N-end rule. Cell 69:725–735
Weihofen A, Martoglio B (2003) Intramembrane-cleaving proteases: controlled liberation of proteins and bioactive peptides. Trends Cell Biol 13:71–78
Wolfe MS, Kopan R (2004) Intramembrane proteolysis: theme and variations. Science 305:1119–1123
Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42:121–128
Yamamoto Y, Inagaki N, Satoh K (2001) Overexpression and characterization of carboxyl-terminal processing protease for precursor D1 protein: regulation of enzyme-substrate interaction by molecular environments. J Biol Chem 276:7518–7525
Yang DH, Webster J, Adam Z, Lindahl M, Andersson B (1998) Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiol 118:827–834
Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J 37:864–876
Yu F, Park S, Rodermel SR (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol 138:1957–1966
Zaltsman A, Feder A, Adam Z (2005a) Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts—implications for thylakoid formation and photosystem II maintenance. Plant J 42:609–617
Zaltsman A, Ori N, Adam Z (2005b) Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis. Plant Cell 17:2782–2790
Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S, Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102:13699–13704
Zheng B, Halperin T, Hruskova-Heidingsfeldova O, Adam Z, Clarke AK (2002) Characterization of chloroplast Clp proteins in Arabidopsis: localization, tissue specificity and stress responses. Physiol Plant 114:92–101
Zheng B, Macdonald TM, Sutinen S, Hurry V, Clarke AK (2006) A nuclear-encoded ClpP subunit of the chloroplast ATP-dependent Clp protease is essential for early development in Arabidopsis thaliana. Planta 224:1103–1115
Zhong R, Wan J, Jin R, Lamppa G (2003) A pea antisense gene for the chloroplast stromal processing peptidase yields seedling lethals in Arabidopsis: survivors show defective GFP import in vivo. Plant J 34:802–812
Author information
Authors and Affiliations
Corresponding author
Editor information
Rights and permissions
Copyright information
© 2007 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Adam, Z. (2007). Protein stability and degradation in plastids. In: Bock, R. (eds) Cell and Molecular Biology of Plastids. Topics in Current Genetics, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/4735_2007_0227
Download citation
DOI: https://doi.org/10.1007/4735_2007_0227
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-75375-9
Online ISBN: 978-3-540-75376-6
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)