Skip to main content

Plastid Protein Degradation During Leaf Development and Senescence: Role of Proteases and Chaperones

  • Chapter
  • First Online:
Plastid Development in Leaves during Growth and Senescence

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 36))

Summary

During leaf development, plastids undergo dynamic changes in morphology. Chloroplasts develop from proplastids during leaf growth: this process includes synthesis, import, and maturation of numerous chloroplast proteins. During leaf senescence, chloroplasts change gradually into a senescing form termed gerontoplast, with the breakdown of thylakoid membranes and the degradation of photosynthetic proteins. In these developmental processes, it is apparent that the proteolytic activity within chloroplasts is a key to control such remarkable morphological/functional changes. Processing and maturation of chloroplast proteins are very important since chloroplast development requires numerous proteins that are imported from the cytosol. Various efforts to elucidate the functions of chloroplast proteases have revealed the existence of signal peptidases (SPP, PreP, TPP, and PlsP1) that are involved in the processing and the maturation steps. In addition, the quality control of proteins is ­necessary for proper chloroplast development. Recent studies using Arabidopsis mutants have identified several important chloroplastic proteases (Clp, FtsH, Deg, and some intramembrane-proteases), which originated from bacterial homologs, in the quality control of proteins during chloroplast development. In contrast, studies on the degradation of chloroplast proteins during senescence implied that multiple pathways, not limited to chloroplast proteases, control protein degradation in this process. In addition to protein degradation inside the chloroplasts, degradation of engulfed whole-chloroplasts within the vacuole, and small spherical bodies like senescence-associated vacuoles (SAV), and Rubisco-containing bodies (RCB) that include chloroplast stromal proteins are known to occur during leaf senescence. The latter implicates that autophagy plays an important role in delivering chloroplast proteins into the vacuole. This chapter provides an integrated summary on the roles of chloroplast proteases during chloroplast development, and the current view of the chloroplast protein degradation during senescence.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AAA:

ATPases associated with diverse cellular activities;

ATG:

Autophagy-related gene;

Cpn60:

Chaperonin 60;

cpSec:

Chloroplast secretory pathway;

cpSRP:

Chloroplast signal recognition particle;

cpTat:

Chloroplast twin-argnine translocation;

GroEL:

Hsp60 class oligomeric molecular chaperone;

Hsc:

Heat shock cognate protein;

Hsp:

Heat shock protein;

LHC:

Light-harvesting complex;

MEP:

Methylerythritol phosphate;

OEC:

Oxygen-evolving complex of photosystem II;

PAO:

Pheophorbide a oxygenase;

Plsp:

Plastidic type I signal peptidase;

PPH:

Pheophytin pheophorbide hydrolase;

PreP:

Presequence protease;

PSII:

Photosystem II;

RCB:

Rubisco-containing body;

Rubisco:

Ribulose 1,5-bisphosphate carboxylase-oxygenase;

SAG:

Senescence-associated gene;

SAV:

Senescence-associated vacuoles;

SPaseI:

Type I signal peptidase;

SPP:

Stromal processing peptidase;

SREBP:

Sterol-regulatory element binding protein;

TIC:

Translocon at the inner envelope membrane of chloroplasts;

TOC:

Translocon at the outer envelope membrane of chloroplasts;

TPP:

Thylakoidal processing peptidase

References

  • Adam Z (2000) Chloroplast proteases: possible regulators of gene expression? Biochimie 82:647–654

    Article  CAS  PubMed  Google Scholar 

  • Adam Z, Clarke AK (2002) Cutting edge of chloroplast proteolysis. Trends Plant Sci 7:451–456

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Akita M, Nielsen E, Keegstra K (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136:983–994

    Article  CAS  PubMed  Google Scholar 

  • Andersson FI, Tryggvesson A, Sharon M, Diemand AV, Classen M, Best C, Schmidt R, Schelin J, Stanne TM, Bukau B, Robinson CV, Witt S, Mogk A, Clarke AK (2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284:13519–13532

    Article  CAS  PubMed  Google Scholar 

  • Andres C, Agne B, Kessler F (2010) The TOC complex: preprotein gateway to the chloroplast. Biochim Biophys Acta 1803:715–723

    Article  CAS  PubMed  Google Scholar 

  • Apuya NR, Yadegari R, Fischer RL, Harada JJ, Zimmerman JL, Goldberg RB (2001) The Arabidopsis embryo mutant schlepperless has a defect in the chaperonin-60alpha gene. Plant Physiol 126:717–730

    Article  CAS  PubMed  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:81–88

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bhushan S, Lefebvre B, Ståhl 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

    Article  CAS  PubMed  Google Scholar 

  • Bhushan S, Ståhl A, Nilsson S, Lefebvre B, Seki M, Roth C, McWilliam D, Wright SJ, Liberles DA, Shinozaki K, Bruce BD, Boutry M, Glaser E (2005) Catalysis, subcellular localization, expression and evolution of the targeting peptides degrading protease, AtPreP2. Plant Cell Physiol 46:985–996

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bölter B, Nada A, Fulgosi H, Soll J (2006) A chloroplastic inner envelope membrane protease is essential for plant development. FEBS Lett 580:789–794

    Article  PubMed  CAS  Google Scholar 

  • Bushnell TP, Bushnell D, Jagendorf AT (1993) A purified zinc protease of pea chloroplasts, EP1, degrades the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 103:585–591

    CAS  PubMed  Google Scholar 

  • Cao D, Froehlich JE, Zhang H, Cheng CL (2003) The chlorate-resistant and photomorphogenesis-defective mutant cr88 encodes a chloroplast-targeted HSP90. Plant J 33:107–118

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chassin Y, Kapri-Pardes E, Sinvany G, Arad T, Adam Z (2002) Expression and characterization of the thylakoid lumen protease DegP1 from Arabidopsis. Plant Physiol 130:857–864

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84

    Article  CAS  PubMed  Google Scholar 

  • Chi W, Sun X, Zhang L (2011) The roles of chloroplast proteases in the biogenesis and maintenance of photosystem II. Biochim Biophys Acta 1817:239–246

    PubMed  Google Scholar 

  • Chiba A, Ishida H, Nishizawa NK, Makino A, Mae T (2003) Exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts by specific bodies in naturally senescing leaves of wheat. Plant Cell Physiol 44:914–921

    Article  CAS  PubMed  Google Scholar 

  • Clarke AK, MacDonald MT, Sjögren LLE (2005) The ATP-dependent Clp protease in chloroplasts of higher plants. Physiol Plant 123:406–412

    Article  CAS  Google Scholar 

  • Clausen T, Southan C, Ehrmann M (2002) The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell 10:443–455

    Article  CAS  PubMed  Google Scholar 

  • Cline K, Dabney-Smith C (2008) Plastid protein import and sorting: different paths to the same compartments. Curr Opin Plant Biol 11:585–592

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Diaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry JF, Le Dily F, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147:1437–1449

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624

    Article  CAS  PubMed  Google Scholar 

  • Friedrich JW, Huffaker RC (1980) Photosynthesis, leaf resistances, and ribulose-1,5-bisphosphate carboxylase degradation in senescing barley leaves. Plant Physiol 65:1103–1107

    Article  CAS  PubMed  Google Scholar 

  • Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, Sun Q, 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

    Article  CAS  PubMed  Google Scholar 

  • Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol (Stuttg) 10(Suppl 1):37–49

    Article  CAS  Google Scholar 

  • Grimaud R, Kessel M, Beuron F, Steven AC, Maurizi MR (1998) Enzymatic and structural similarities between the Escherichia coli ATP-dependent proteases, ClpXP and ClpAP. J Biol Chem 273:12476–12481

    Article  CAS  PubMed  Google Scholar 

  • Gunning B (2005) Plastid stromules: video microscopy of their outgrowth, retraction, tensioning, anchoring, branching, bridging, and tip-shedding. Protoplasma 225:33–42

    Article  PubMed  Google Scholar 

  • Haussühl 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

    Article  PubMed  Google Scholar 

  • Hortensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53:927–937

    Article  CAS  PubMed  Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2005) The family of Deg proteases in cyanobacteria and chloroplasts of higher plants. Physiol Plant 123:413–420

    Article  CAS  Google Scholar 

  • Huesgen PF, Schuhmann H, Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580:6929–6932

    Article  CAS  PubMed  Google Scholar 

  • Inada N, Sakai A, Kuroiwa H, Kuroiwa T (1998) Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles. Investigations of tissues and cells by fluorescence microscopy. Planta 205:153–164

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008) Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–155

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jackson-Constan D, Akita M, Keegstra K (2001) Molecular chaperones involved in chloroplast protein import. Biochim Biophys Acta 1541:102–113

    Article  CAS  PubMed  Google Scholar 

  • Johnson KA, Bhushan S, Ståhl A, Hallberg BM, Frohn A, Glaser E, Eneqvist T (2006) The closed structure of presequence protease PreP forms a unique 10,000 Å3 chamber for proteolysis. EMBO J 25:1977–1986

    Article  CAS  PubMed  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Sakamoto W (2009) Protein quality control in chloroplasts: a current model of D1 protein ­degradation in the photosystem II repair cycle. J Biochem 146:463–469

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Sakamoto W (2010) New insight into the type and function of proteases in plastids. In: Jeon KW (ed) International review of cell and molecular biology, vol 161. Burlington Academic Press, Burlington, pp 185–218

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Yamamoto Y, Murakami S, Sato F (2005) Post-translational regulation of CND41 protease activity in senescent tobacco leaves. Planta 222:643–651

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol 144:952–960

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol 151:1790–1801

    Article  CAS  PubMed  Google Scholar 

  • Kessel M, Maurizi MR, Kim B, Kocsis E, Trus BL, Singh SK, Steven AC (1995) Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26S proteasome. J Mol Biol 250:587–594

    Article  CAS  PubMed  Google Scholar 

  • Kessler F, Blobel G (1996) Interaction of the protein import and folding machineries of the chloroplast. Proc Natl Acad Sci USA 93:7684–7689

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Rudella A, Ramirez Rodriguez V, Zybailov B, Olinares PD, van Wijk KJ (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

    Article  CAS  PubMed  Google Scholar 

  • Kimec-Wisniewska B, Krumpe K, Urantowka A, Sakamoto W, Pratje E, Janska H (2008) Plant mitochondrial rhomboid, AtRBL12, has different substrate specificity from its yeast counterpart. Plant Mol Biol 68:159–171

    Article  CAS  Google Scholar 

  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of cDNA for a dehydration-inducible gene that encodes a CLP A, B-like protein in Arabidopsis thaliana L. Biochem Biophys Res Commun 196:1214–1220

    Article  CAS  PubMed  Google Scholar 

  • Kourtz L, Ko K (1997) The early stage of chloroplast protein import involves Com70. J Biol Chem 272:2808–2813

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kovacheva S, Bedard J, Wardle A, Patel R, Jarvis P (2007) Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 50:364–379

    Article  CAS  PubMed  Google Scholar 

  • Kovacs-Bogdan E, Soll J, Bolter B (2010) Protein import into chloroplasts: the Tic complex and its regulation. Biochim Biophys Acta 1803:740–747

    Article  CAS  PubMed  Google Scholar 

  • Krupinska K (2007) Fate and activity of plastids during leaf senescence. In: Wise RR, Hoober J (eds) The structure and function of plastids, advances in photosynthesis and respiration, vol 23, Series Ed., Govindjee. Springer, Dordrecht, pp 433–449

    Chapter  Google Scholar 

  • Krzywda S, Brzozowski AM, Verma C, Karata K, Ogura T, Wilkinson AJ (2002) The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 Å resolution. Structure 10:1073–1083

    Article  CAS  PubMed  Google Scholar 

  • Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M, Tanaka A (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19:1362–1375

    Article  CAS  PubMed  Google Scholar 

  • Latijnhouwers M, Xu XM, Moller SG (2010) Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232:567–578

    Article  CAS  PubMed  Google Scholar 

  • Lee U, Rioflorido I, Hong SW, Larkindale J, Waters ER, Vierling E (2007) The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49:115–127

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Levy-Rimler G, Bell RE, Ben-Tal N, Azem A (2002) Type I chaperonins: not all are created equal. FEBS Lett 529:1–5

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Liu X, Yu F, Rodermel S (2010) An Arabidopsis pentatricopeptide repeat protein, SVR7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol 154:1588–1601

    Article  CAS  PubMed  Google Scholar 

  • Mae T (2004) Leaf senescence and nitrogen metabolism. In: Nooden L (ed) Plant cell death processes. Elsevier Academic Press, San Diego, pp 157–168

    Chapter  Google Scholar 

  • Mae T, Kai N, Makino A, Ohira S (1984) Relation between riblose bisphosphate carboxylase content and chloroplast number in naturally senescing primary leaves of wheat. Plant Cell Physiol 25:333–336

    CAS  Google Scholar 

  • Majeran W, Wollman FA, Vallon O (2000) Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b6f complex. Plant Cell 12:137–150

    CAS  PubMed  Google Scholar 

  • Martinez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ (2008a) ‘Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves. Plant J 56:196–206

    Article  CAS  PubMed  Google Scholar 

  • Martinez DE, Costa ML, Guiamet JJ (2008b) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10:15–22

    Article  CAS  Google Scholar 

  • Minamikawa T, Toyooka K, Okamoto T, Hara-Nishimura I, Nishimura M (2001) Degradation of ribulose-bisphosphate carboxylase by vacuolar enzymes of senescing French bean leaves: immunocytochemical and ultrastructural observations. Protoplasma 218:144–153

    Article  CAS  PubMed  Google Scholar 

  • Mitsuhashi W, Feller U (1992) Effects of light and external solutes on the catabolism of nuclear-encoded stromal proteins in intact chloroplasts isolated from pea leaves. Plant Physiol 100:2100–2105

    Article  CAS  PubMed  Google Scholar 

  • Miura E, Kato Y, Matsushima R, Albrecht V, Laalami S, Sakamoto W (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell 19:1313–1328

    Article  CAS  PubMed  Google Scholar 

  • Moberg P, Stahl A, Bhushan S, Wright SJ, Eriksson A, Bruce BD, Glaser E (2003) Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant J 36:616–628

    Article  CAS  PubMed  Google Scholar 

  • Moore T, Keegstra K (1993) Characterization of a cDNA clone encoding a chloroplast-targeted Clp homologue. Plant Mol Biol 21:525–537

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Myouga F, Motohashi R, Kuromori T, Nagata N, Shinozaki K (2006) An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloroplast development as well as heat-stress response. Plant J 48:249–260

    Article  CAS  PubMed  Google Scholar 

  • Nakabayashi K, Ito M, Kiyosue T, Shinozaki K, Watanabe A (1999) Identification of clp genes expressed in senescing Arabidopsis leaves. Plant Cell Physiol 40:504–514

    Article  CAS  PubMed  Google Scholar 

  • Nakano T, Murakami S, Shoji T, Yoshida S, Yamada Y, Sato F (1997) A novel protein with DNA binding activity from tobacco chloroplast nucleoids. Plant Cell 9:1673–1682

    CAS  PubMed  Google Scholar 

  • Nakashima K, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1997) A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant J 12:851–861

    Article  CAS  PubMed  Google Scholar 

  • Nielsen E, Akita M, Davila-Aponte J, 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

    Article  CAS  PubMed  Google Scholar 

  • Nilsson CS, Backman HG, Pesaresi P, Leister D, Glaser E (2009) Deletion of an organellar peptidasome PreP affects early development in Arabidopsis thaliana. Plant Mol Biol 71:497–508

    Article  CAS  Google Scholar 

  • Niwa H, Tsuchiya D, Makyio H, Yoshida M, Morikawa K (2002) Hexameric ring structure of the ATPase domain of the membrane-integrated metalloprotease FtsH from Thermus thermophilus HB8. Structure 10:1415–1423

    Article  CAS  PubMed  Google Scholar 

  • Olinares PD, Kim J, van Wijk KJ (2011) The Clp protease system; a central component of the chloroplast protease network. Biochim Biophys Acta 1807:999–1011

    Article  CAS  PubMed  Google Scholar 

  • Ono K, Hashimoto H, Katoh S (1995) Changes in the number and size of chloroplasts during senescence of primary leaves of wheat grown under different conditions. Plant Cell Physiol 36:9–17

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 48:881–885

    Article  CAS  PubMed  Google Scholar 

  • Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Parrott DL, McInnerney K, Feller U, Fischer AM (2007) Steam-girdling of barley (Hordeum ­vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. New Phytol 176:56–69

    Article  CAS  PubMed  Google Scholar 

  • Peltier JB, 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

    Article  CAS  PubMed  Google Scholar 

  • Peltier JB, 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

    Article  CAS  PubMed  Google Scholar 

  • 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 three-dimensional structures, and functional implications. J Biol Chem 279:4768–4781

    Article  CAS  PubMed  Google Scholar 

  • Peoples MB, Beilharz VC, Waters SP, Simpson RJ, Dalling MJ (1980) Nitrogen redistribution during grain growth in wheat (Triticum aestivum L.). Planta 149:241–251

    Article  CAS  Google Scholar 

  • Porankiewicz J, Wang J, Clarke AK (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32:449–458

    Article  CAS  PubMed  Google Scholar 

  • Prins A, van Heerden PD, Olmos E, Kunert KJ, Foyer CH (2008) Cysteine proteinases regulate chloroplast protein content and composition in tobacco leaves: a model for dynamic interactions with ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) vesicular bodies. J Exp Bot 59:1935–1950

    Article  CAS  PubMed  Google Scholar 

  • Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S (2003) Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci USA 100:15259–15264

    Article  CAS  PubMed  Google Scholar 

  • Ragster LE, Chrispeels MJ (1981) Autodigestion in crude extracts of soybean leaves and isolated chloroplasts as a measure of proteolytic activity. Plant Physiol 67:104–109

    Article  CAS  PubMed  Google Scholar 

  • Richter S, Zhang R, Lamppa GK (2005) Function of the stromal processing peptidase in the chloroplast import pathway. Physiol Plant 123:362–368

    Article  CAS  Google Scholar 

  • Roulin S, Feller U (1998) Light-independent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: requirement for divalent cations. Planta 205:297–304

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57:599–621

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W, Tamura T, Hanba-Tomita Y, 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W, Uno Y, Zhang Q, Miura E, Kato Y, Sodmergen (2009) Arrested differentiation of proplastids into chloroplasts in variegated leaves characterized by plastid ultrastructure and nucleoid morphology. Plant Cell Physiol 50:2069–2083

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J 57:120–131

    Article  CAS  PubMed  Google Scholar 

  • Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hortensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21:767–785

    Article  CAS  PubMed  Google Scholar 

  • Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266:1007–1012

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Seo S, Okamoto M, Iwai T, Iwano M, Fukui K, Isogai A, Nakajima N, Ohashi Y (2000) Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 12:917–932

    CAS  PubMed  Google Scholar 

  • Shanklin J, DeWitt ND, Flanagan JM (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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shipman RL, Inoue K (2009) Suborganellar localization of plastidic type I signal peptidase 1 depends on chloroplast development. FEBS Lett 583:938–942

    Article  CAS  PubMed  Google Scholar 

  • Shipman-Roston RL, Ruppel NJ, Damoc C, Phinney BS, Inoue K (2010) The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts. Plant Physiol 152:1297–1308

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sjögren LL, Clarke AK (2011) Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins. Plant Cell 23:322–332

    Article  PubMed  CAS  Google Scholar 

  • Sjögren 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

    Article  PubMed  CAS  Google Scholar 

  • Sjögren 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

    Article  PubMed  CAS  Google Scholar 

  • Skorko-Glonek J, Wawrzynow A, Krzewski K, Kurpierz K, Lipinska B (1995) Site-directed mutagenesis of the HtrA (DegP) serine protease, whose proteolytic activity is indispensable for Escherichia coli survival at elevated temperatures. Gene 163:47–52

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ståhl 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

    Article  PubMed  CAS  Google Scholar 

  • Ståhl 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

    Article  PubMed  CAS  Google Scholar 

  • Stanne TM, Sjogren LL, Koussevitzky S, Clarke AK (2009) Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem J 417:257–268

    Article  CAS  PubMed  Google Scholar 

  • Su PH, Li HM (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

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Peng L, Guo J, Chi W, Ma J, Lu C, Zhang L (2007) Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell 19:1347–1361

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Fu T, Chen N, Guo J, Ma J, Zou M, Lu C, Zhang L (2010a) The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol 152:1263–1273

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Ouyang M, Guo J, Ma J, Lu C, Adam Z, Zhang L (2010b) The thylakoid protease Deg1 is involved in photosystem-II assembly in Arabidopsis thaliana. Plant J 62:240–249

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Takechi K, Sodmergen, 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

    Article  CAS  PubMed  Google Scholar 

  • Tomoyasu T, Yuki T, Morimura S, Mori H, Yamanaka K, Niki H, Hiraga S, Ogura T (1993) The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol 175:1344–1351

    CAS  PubMed  Google Scholar 

  • VanderVere PS, Bennett TM, Oblong JE, Lamppa GK (1995) A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc Natl Acad Sci USA 92:7177–7181

    Article  CAS  PubMed  Google Scholar 

  • Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149:885–893

    Article  CAS  PubMed  Google Scholar 

  • Wan J, Bringloe D, lamppa GK (1998) Disruption of chloroplast biogenesis and plant development upon down-regulation of a chloroplast processing enzyme involved in the import pathway. Plant J 15:459–468

    Article  CAS  Google Scholar 

  • Wang J, Hartling JA, Flanagan JM (1997) The structure of ClpP at 2.3 A resolution suggests a model for ATP-dependent proteolysis. Cell 91:447–456

    Article  CAS  PubMed  Google Scholar 

  • Wang KH, Oakes ES, Sauer RT, Baker TA (2008) Tuning the strength of a bacterial N-end rule degradation signal. J Biol Chem 283:24600–24607

    Article  CAS  PubMed  Google Scholar 

  • Weaver LM, Froehlich JE, Amasino RM (1999) Chloroplast-targeted ERD1 protein declines but its mRNA increases during senescence in Arabidopsis. Plant Physiol 119:1209–1216

    Article  CAS  PubMed  Google Scholar 

  • Weiss C, Bonshtien A, Farchi-Pisanty O, Vitlin A, Azem A (2009) Cpn20: siamese twins of the chaperonin world. Plant Mol Biol 69:227–238

    Article  CAS  PubMed  Google Scholar 

  • Wetzel CM, Harmacek LD, Yuan LH, Woperieis JL, Chubb R, Turini P (2009) Loss of chloroplast protease SPPA function alters high light acclimation processes in Arabidopsis thaliana L (Heynh.). J Exp Bot 60:1715–1727

    Article  CAS  PubMed  Google Scholar 

  • Wise RR (2007) The Structure and Function of Plastids. In: Wise RR, Hoober JK (eds) Advances in photosynthesis and respiration (Series Ed, Govindjee), vol 23. Springer, Dordrecht, pp 3–26

    Google Scholar 

  • Wittenbach VA, Lin W, Hebert RR (1982) Vacuolar localization of proteases and degradation of chloroplasts in mesophyll protoplasts from senescing primary wheat leaves. Plant Physiol 69:98–102

    Article  CAS  PubMed  Google Scholar 

  • Yin S, Sun X, Zhang L (2008) An Arabidopsis ctpA homologue is involved in the repair of photosystem II under high light. Chin Sci Bull 53:1021–1026

    Article  CAS  Google Scholar 

  • Yu AY, Houry WA (2007) ClpP: a distinctive family of cylindrical energy-dependent serine proteases. FEBS Lett 581:3749–3757

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yu F, Park S, Rodermel SR (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol 138:1957–1966

    Article  CAS  PubMed  Google Scholar 

  • Yu F, Liu X, Alsheikh M, Park S, Rodermel S (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20:1786–1804

    Article  CAS  PubMed  Google Scholar 

  • Yue G, Hu X, He Y, Yang A, Zhang J (2010) Identification and characterization of two members of the FtsH gene family in maize (Zea mays L.). Mol Biol Rep 37:855–863

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Kato Y, Zhang L, Fujimoto M, Tsutsumi N, Sodmergen, Sakamoto W (2010) The FtsH protease heterocomplex in Arabidopsis: dispensability of type-B protease activity for proper chloroplast development. Plant Cell 22:3710–3725

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zybailov B, Friso G, Kim J, Rudella A, Rodriguez VR, Asakura Y, Sun Q, van Wijk KJ (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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Drs. Lixin Zhang and Xuwu Sun for sharing unpublished data on the deg mutants. The work from our group is supported by a Grant-in-Aid for Scientific Research from MEXT (No. 22380007 to W. S and No. 22770042 to Y.K.) and by the Oohara Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wataru Sakamoto .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Kato, Y., Sakamoto, W. (2013). Plastid Protein Degradation During Leaf Development and Senescence: Role of Proteases and Chaperones. In: Biswal, B., Krupinska, K., Biswal, U. (eds) Plastid Development in Leaves during Growth and Senescence. Advances in Photosynthesis and Respiration, vol 36. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5724-0_20

Download citation

Publish with us

Policies and ethics