Skip to main content

The Pathway of Chlorophyll Degradation: Catabolites, Enzymes and Pathway Regulation

  • 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 senescence and fruit ripening, chlorophyll is broken down to colorless linear tetrapyrroles, which are stored in the vacuoles of degreened cells. The pathway of chlorophyll degradation that is active in these developmental processes is fairly well known regarding its biochemistry and cell biology. It comprises at least six enzymatic and one non-enzymatic reaction and the chemical structures of several intermediary and final chlorophyll catabolites have been elucidated. In the last few years, genes coding for a number of chlorophyll catabolic enzymes have been characterized and mutants in these genes have been analyzed. This includes pheophorbide a oxygenase (PAO), the key enzyme of the pathway, which is responsible for opening of the chlorine macrocycle present in chlorophyll, thereby providing the characteristic structural basis of all further downstream breakdown products. The pathway is therefore nowadays termed the ‘PAO pathway’. This review summarizes information on the structures of chlorophyll breakdown products and the reactions involved in their formation. In addition cell biological and regulatory aspects of the PAO pathway are discussed.

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

ABC:

ATP binding cassette;

ACD:

Accelerated cell death;

Chl:

Chlorophyll;

Chlide:

Chlorophyllide;

CLH:

Chlorophyllase;

Fd:

Ferre­doxin;

hFCC –:

Hypermodified fluorescent Chl catabo­lite;

HMR:

Hydroxymethyl Chl reductase;

LHC:

Light harvesting complex;

MCS:

Metal chelating substance;

mFCC –:

Modified fluorescent Chl catabolite;

NCC:

Nonfluorescent Chl catabolite;

NOL:

NYC1-like;

NYC:

Non yellow coloring;

NYE:

Non yellowing;

PAO:

Pheophorbide a oxygenase;

pFCC:

Primary fluorescent Chl catabolite;

Pheide:

Pheophorbide;

Phein:

Pheophytin;

PPH:

Pheophytinase;

PS:

Photosystem;

RCC:

Red chl catabolite;

RCCR:

Red Chl catabolite reductase;

ROS:

Reactive oxygen species

References

  • 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  PubMed  CAS  Google Scholar 

  • Aiamla-or S, Kaewsuksaeng S, Shigyo M, Yamauchi N (2010) Impact of UV-B irradiation on chlorophyll degradation and chlorophyll-degrading enzyme activities in stored broccoli (Brassica oleracea L. Italica Group) florets. Food Chem 120:645–651

    Article  CAS  Google Scholar 

  • Amir-Shapira D, Goldschmidt EE, Altman A (1987) Chlorophyll catabolism in senescing plant tissues: in vivo breakdown intermediates suggest different degradative pathways for Citrus fruit and parsley leaves. Proc Natl Acad Sci USA 84:1901–1905

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Arkus KAJ, Cahoon EB, Jez JM (2005) Mechanistic analysis of wheat chlorophyllase. Arch Biochem Biophys 438:146–155

    Article  PubMed  CAS  Google Scholar 

  • Armstead I, Donnison I, Aubry S, Harper J, Hörtensteiner S, James C, Mani J, Moffet M, Ougham H, Roberts L, Thomas A, Weeden N, Thomas H, King I (2006) From crop to model to crop: identifying the genetic basis of the staygreen mutation in the Lolium/Festuca forage and amenity grasses. New Phytol 172:592–597

    Article  PubMed  Google Scholar 

  • Armstead I, Donnison I, Aubry S, Harper J, Hörtensteiner S, James C, Mani J, Moffet M, Ougham H, Roberts L, Thomas A, Weeden N, Thomas H, King I (2007) Cross-species identification of Mendel’s I locus. Science 315:73

    Article  PubMed  CAS  Google Scholar 

  • Aubry S, Mani J, Hörtensteiner S (2008) Stay-green protein, defective in Mendel’s green cotyledon mutant, acts independent and upstream of pheophorbide a oxygenase in the chlorophyll catabolic pathway. Plant Mol Biol 67:243–256

    Article  PubMed  CAS  Google Scholar 

  • Azoulay Shemer T, Harpaz-Saad S, Belausov E, Lovat N, Krokhin O, Spicer V, Standing KG, Goldschmidt EE, Eyal Y (2008) Citrus chlorophyllase dynamics at ethylene-induced fruit color-break; a study of chlorophyllase expression, post-translational processing kinetics and in-situ intracellular localization. Plant Physiol 148:108–118

    Article  PubMed  CAS  Google Scholar 

  • Bachmann A, Fernández-López J, Ginsburg S, Thomas H, Bouwcamp JC, Solomos T, Matile P (1994) Stay-green genotypes of Phaseolus vulgaris L.: chloroplast proteins and chlorophyll catabolites during foliar senescence. New Phytol 126:593–600

    Article  CAS  Google Scholar 

  • Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol 10(suppl 1):63–75

    Article  PubMed  CAS  Google Scholar 

  • Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958

    Article  PubMed  CAS  Google Scholar 

  • Banala S, Moser S, Müller T, Kreutz CR, Holzinger A, Lütz C, Kräutler B (2010) Hypermodified fluorescent chlorophyll catabolites: source of blue luminescence in senescent leaves. Angew Chem Int Ed 49:5174–5177

    Article  CAS  Google Scholar 

  • Barry CS, McQuinn RP, Chung MY, Besuden A, Giovannoni JJ (2008) Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol 147:179–187

    Article  PubMed  CAS  Google Scholar 

  • Bartsch S, Monnet J, Selbach K, Quigley F, Gray J, von Wettstein D, Reinbothe S, Reinbothe C (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc Natl Acad Sci USA 105:4933–4938

    Article  PubMed  CAS  Google Scholar 

  • Beisel KG, Jahnke S, Hofmann D, Köppchen S, Schurr U, Matsubara S (2010) Continuous turnover of carotenes and chlorophyll a in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling. Plant Physiol 152:2188–2199

    Article  PubMed  CAS  Google Scholar 

  • Berghold J, Breuker K, Oberhuber M, Hörtensteiner S, Kräutler B (2002) Chlorophyll breakdown in spinach: on the structure of five nonfluorescent chlorophyll catabolites. Photosynth Res 74:109–119

    Article  PubMed  CAS  Google Scholar 

  • Berghold J, Eichmüller C, Hörtensteiner S, Kräutler B (2004) Chlorophyll breakdown in tobacco: on the structure of two nonfluorescent chlorophyll catabolites. Chem Biodivers 1:657–668

    Article  PubMed  CAS  Google Scholar 

  • Berghold J, Müller T, Ulrich M, Hörtensteiner S, Kräutler B (2006) Chlorophyll breakdown in maize: on the structure of two nonfluorescent chlorophyll catabolites. Monatsh Chem 137:751–763

    Article  CAS  Google Scholar 

  • Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266

    Article  PubMed  CAS  Google Scholar 

  • Brown SB, Houghton JD, Hendry GAF (1991) Chlorophyll breakdown. In: Scheer H (ed) Chlorophylls. CRC Press, Boca Raton, pp 465–489

    Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  PubMed  CAS  Google Scholar 

  • Büchert AM, Civello PM, Martínez GA (2011) Chlorophyllase versus pheophytinase as candidates for chlorophyll dephytilation during senescence of broccoli. J Plant Physiol 168:337–343

    Article  PubMed  CAS  Google Scholar 

  • Chen LFO, Lin CH, Kelkar SM, Chang YM, Shaw JF (2008) Transgenic broccoli (Brassica oleracea var. italicia) with antisense chlorophyllase (BoCLH1) delays postharvest yellowing. Plant Sci 174:25–31

    Article  CAS  Google Scholar 

  • Cornah JE, Terry MJ, Smith AG (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8:224–230

    Article  PubMed  CAS  Google Scholar 

  • Costa ML, Civello PM, Chaves AR, Martinez GA (2002) Characterization of Mg-dechelatase activity obtained from Fragaria x ananassa fruit. Plant Physiol Biochem 40:111–118

    Article  CAS  Google Scholar 

  • Curty C, Engel N (1996) Detection, isolation and structure elucidation of a chlorophyll a catabolite from autumnal senescent leaves of Cercidiphyllum japonicum. Phytochemistry 42:1531–1536

    Article  CAS  Google Scholar 

  • Dammeyer T, Hofmann E, Frankenberg-Dinkel N (2008) Phycoerythrobilin synthase (PebS) of a marine virus – crystal structures of the biliverdin complex and the substrate-free form. J Biol Chem 283:27547–27554

    Article  PubMed  CAS  Google Scholar 

  • Efrati A, Eyal Y, Paran I (2005) Molecular mapping of the chlorophyll retainer (cl) mutation in pepper (Capsicum spp.) and screening for candidate genes using tomato ESTs homologous to structural genes of the chlorophyll catabolism pathway. Genome 48:347–351

    Article  PubMed  CAS  Google Scholar 

  • Engel N, Curty C, Gossauer A (1996) Chlorophyll catabolism in Chlorella protothecoides. 8. Facts and artefacts. Plant Physiol Biochem 34:77–83

    CAS  Google Scholar 

  • Feierabend J, Dehne S (1996) Fate of the porphyrin cofactors during the light-dependent turnover of catalase and of the photosystem II reaction-center protein D1 in mature rye leaves. Planta 198:413–422

    Article  CAS  Google Scholar 

  • Fiedor L, Rosenbach-Belkin V, Scherz A (1992) The stereospecific interaction between chlorophylls and chlorophyllase – possible implication for chlorophyll biosynthesis and degradation. J Biol Chem 267:22043–22047

    PubMed  CAS  Google Scholar 

  • Folley P, Engel N (1999) Chlorophyll b to chlorophyll a conversion precedes chlorophyll degradation in Hordeum vulgare L. J Biol Chem 274:21811–21816

    Article  Google Scholar 

  • Frankenberg N, Mukougawa K, Kohchi T, Lagarias JC (2001) Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13:965–978

    PubMed  CAS  Google Scholar 

  • Frelet-Barrand A, Kolukisaoglu HU, Plaza S, Rüffer M, Azevedo L, Hörtensteiner S, Marinova K, Weder B, Schulz B, Klein M (2008) Comparative mutant analysis of Arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxification, vacuolar organic anion transport and chlorophyll degradation. Plant Cell Physiol 49:557–569

    Article  PubMed  CAS  Google Scholar 

  • Gaude N, Brehelin C, Tischendorf G, Kessler F, Dörmann P (2007) Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. Plant J 49:729–739

    Article  PubMed  CAS  Google Scholar 

  • Ginsburg S, Matile P (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol 102:521–527

    PubMed  CAS  Google Scholar 

  • Ginsburg S, Schellenberg M, Matile P (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol 105:545–554

    PubMed  CAS  Google Scholar 

  • Gray J, Close PS, Briggs SP, Johal GS (1997) A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89:25–31

    Article  PubMed  CAS  Google Scholar 

  • Gray J, Janick-Bruckner D, Bruckner B, Close PS, Johal GS (2002) Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol 130:1894–1907

    Article  PubMed  CAS  Google Scholar 

  • Gray J, Wardzala E, Yang M, Reinbothe S, Haller S, Pauli F (2004) A small family of LLS1–related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers. Plant Mol Biol 54:39–54

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JT, Ausubel FM (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4:327–341

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JT, Guo A, Klessig DF, Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77:551–563

    Article  PubMed  CAS  Google Scholar 

  • Griebel T, Zeier J (2008) Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol 147:790–801

    Article  PubMed  CAS  Google Scholar 

  • Guiamét JJ, Schwartz E, Pichersky E, Noodén LD (1991) Characterization of cytoplasmic and nuclear mutations affecting chlorophyll and chlorophyll-binding proteins during senescence in soybean. Plant Physiol 96:227–231

    Article  PubMed  Google Scholar 

  • Guiamét JJ, Pichersky E, Noodén LD (1999) Mass exodus from senescing soybean chloroplasts. Plant Cell Physiol 40:986–992

    Article  Google Scholar 

  • Hagiwara Y, Sugishima M, Takahashi Y, Fukuyama K (2006) Crystal structure of phycocyanobilin: ferredoxin oxidoreductase in complex with biliverdin IXα, a key enzyme in the biosynthesis of phycocyanobilin. Proc Natl Acad Sci USA 103:27–32

    Article  PubMed  CAS  Google Scholar 

  • Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A, Shiboleth YM, Hörtensteiner S, Gidoni D, Gal-On A, Goldschmidt EE, Eyal Y (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19:1007–1022

    Article  PubMed  CAS  Google Scholar 

  • Harrison MA, Nemson JA, Melis A (1993) Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynth Res 38:141–151

    Article  CAS  Google Scholar 

  • Heaton JW, Marangoni AG (1996) Chlorophyll degradation in processed foods and senescent plant tissues. Trends Food Sci Technol 7:8–15

    Article  CAS  Google Scholar 

  • Hendry GAF, Stobart AK (1986) Chlorophyll turnover in greening barley. Phytochemistry 25:2735–2737

    CAS  Google Scholar 

  • Hendry GAF, Houghton JD, Brown SB (1987) The degradation of chlorophyll – a biological enigma. New Phytol 107:255–302

    Article  CAS  Google Scholar 

  • Hilditch P, Thomas H, Rogers LJ (1986) Two processes for the breakdown of the QB protein of chloroplasts. FEBS Lett 208:313–316

    Article  CAS  Google Scholar 

  • Hinder B, Schellenberg M, Rodoni S, Ginsburg S, Vogt E, Martinoia E, Matile P, Hörtensteiner S (1996) How plants dispose of chlorophyll catabolites. Directly energized uptake of tetrapyrrolic breakdown products into isolated vacuoles. J Biol Chem 271:27233–27236

    Article  PubMed  CAS  Google Scholar 

  • Hirashima M, Tanaka R, Tanaka A (2009) Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol 50:719–729

    Article  PubMed  CAS  Google Scholar 

  • Horie Y, Ito H, Kusaba M, Tanaka R, Tanaka A (2009) Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J Biol Chem 284:17449–17456

    Article  PubMed  CAS  Google Scholar 

  • Horn R, Paulsen H (2004) Early steps in the assembly of light-harvesting chlorophyll a/b complex – time-resolved fluorescence measurements. J Biol Chem 279:44400–44406

    Article  PubMed  CAS  Google Scholar 

  • Hörtensteiner S (1998) NCC malonyltransferase catalyses the final step of chlorophyll breakdown in rape (Brassica napus). Phytochemistry 49:953–956

    Article  PubMed  Google Scholar 

  • Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77

    Article  PubMed  CAS  Google Scholar 

  • Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162

    Article  PubMed  CAS  Google Scholar 

  • Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochem Biophys Acta 1807:977–988

    Article  PubMed  CAS  Google Scholar 

  • Hörtensteiner S, Vicentini F, Matile P (1995) Chlorophyll breakdown in senescent cotyledons of rape, Brassica napus L.: enzymatic cleavage of phaeophorbide a in vitro. New Phytol 129:237–246

    Article  Google Scholar 

  • Hörtensteiner S, Wüthrich KL, Matile P, Ongania K-H, Kräutler B (1998) The key step in chlorophyll breakdown in higher plants. Cleavage of pheophorbide a macrocycle by a monooxygenase. J Biol Chem 273:15335–15339

    Article  PubMed  Google Scholar 

  • Hörtensteiner S, Rodoni S, Schellenberg M, Vicentini F, Nandi OI, Qiu Y-L, Matile P (2000) Evolution of chlorophyll degradation: the significance of RCC reductase. Plant Biol 2:63–67

    Article  Google Scholar 

  • Hu G, Yalpani N, Briggs SP, Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10:1095–1105

    PubMed  CAS  Google Scholar 

  • Ischebeck T, Zbierzak AM, Kanwischer M, Dörmann P (2006) A salvage pathway for phytol metabolism in Arabidopsis. J Biol Chem 281:2470–2477

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Ishikawa A, Okamoto H, Iwasaki Y, Asahi T (2001) A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J 27:89–99

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Ohysuka T, Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271:1475–1479

    Article  PubMed  CAS  Google Scholar 

  • Iturraspe J, Engel N, Gossauer A (1994) Chlorophyll catabolism. Isolation and structure elucidation of chlorophyll b catabolites in Chlorella protothecoides. Phytochemistry 35:1387–1390

    Article  CAS  Google Scholar 

  • Iturraspe J, Moyano N, Frydman B (1995) A new 5-formylbilinone as the major chlorophyll a catabolite in tree senescent leaves. J Org Chem 60:6664–6665

    Article  CAS  Google Scholar 

  • Jakob-Wilk D, Holland D, Goldschmidt EE, Riov J, Eyal Y (1999) Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the Chlase1 gene from ethylene-treated Citrus fruit and its regulation during development. Plant J 20:653–661

    Article  Google Scholar 

  • Jiang H, Li M, Liang N, Yan H, Wei Y, Xu X, Liu J, Xu Z, Chen F, Wu G (2007) Molecular cloning and function analysis of the stay green gene in rice. Plant J 52:197–209

    Article  PubMed  CAS  Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2:1154–1180

    Article  PubMed  CAS  Google Scholar 

  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282–294

    Article  PubMed  CAS  Google Scholar 

  • Kohchi T, Mukougawa K, Frankenberg N, Masuda M, Yokota A, Lagarias JC (2001) The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 13:425–436

    PubMed  CAS  Google Scholar 

  • Kräutler B (2003) Chlorophyll breakdown and chlorophyll catabolites. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook. Elsevier Science, Amsterdam, pp 183–209

    Chapter  Google Scholar 

  • Kräutler B (2008) Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit. Photochem Photobiol Sci 7:1114–1120

    Article  PubMed  CAS  Google Scholar 

  • Kräutler B, Hörtensteiner S (2006) Chlorophyll catabolites and the biochemistry of chlorophyll breakdown. In: Grimm B, Porra R, Rüdiger W, Scheer H (eds) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. Springer, Dordrecht, pp 237–260

    Chapter  Google Scholar 

  • Kräutler B, Jaun B, Bortlik K-H, Schellenberg M, Matile P (1991) On the enigma of chlorophyll degradation: the constitution of a secoporphinoid catabolite. Angew Chem Int Ed Engl 30:1315–1318

    Article  Google Scholar 

  • Kräutler B, Mühlecker W, Anderl M, Gerlach B (1997) Breakdown of chlorophyll: partial synthesis of a putative intermediary catabolite. Helv Chim Acta 80:1355–1362

    Article  Google Scholar 

  • Kräutler B, Banala S, Moser S, Vergeiner C, Müller T, Lütz C, Holzinger A (2010) A novel blue fluorescent chlorophyll catabolite accumulates in senescent leaves of the peace lily (Spathiphyllum wallisii) and indicates a divergent path of chlorophyll breakdown. FEBS Lett 584:4215–4221

    Article  PubMed  CAS  Google Scholar 

  • Kruse E, Mock HP, Grimm B (1995) Reduction of coproporphyrinogen oxidase level by antisense RNA synthesis leads to deregulated gene expression of plastid proteins and affects the oxidative defense system. EMBO J 14:3712–3720

    PubMed  CAS  Google Scholar 

  • Kunieda T, Amano T, Shioi Y (2005) Search for chlorophyll degradation enzyme, Mg-dechelatase, from extracts of Chenopodium album with native and artificial substrates. Plant Sci 169:177–183

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Langmeier M, Ginsburg S, Matile P (1993) Chlorophyll breakdown in senescent leaves: demonstration of Mg-dechelatase activity. Physiol Plant 89:347–353

    Article  CAS  Google Scholar 

  • Lee KP, Kim C, Landgraf F, Apel K (2007) EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:10270–10275

    Article  PubMed  CAS  Google Scholar 

  • Liao Y, An K, Zhou X, Chen W-J, Kuai B-K (2007) AtCLH2, a typical but possibly distinctive chlorophyllase gene in Arabidopsis. J Integr Plant Biol 49:531–539

    Article  CAS  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2006) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  Google Scholar 

  • Liu J, Wu YH, Yan JJ, Liu YD, Shen FF (2008) Protein degradation and nitrogen remobilization during leaf senescence. J Plant Biol 51:11–19

    Article  CAS  Google Scholar 

  • Losey FG, Engel N (2001) Isolation and characterization of a urobilinogenoidic chlorophyll catabolite from Hordeum vulgare L. J Biol Chem 276:27233–27236

    Article  Google Scholar 

  • Lu Y-P, Li Z-S, Drozdowicz Y-M, Hörtensteiner S, Martinoia E, Rea PA (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell 10:267–282

    PubMed  CAS  Google Scholar 

  • Mach JM, Castillo AR, Hoogstraten R, Greenberg JT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci USA 98:771–776

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Matile P, Schellenberg M (1996) The cleavage of pheophorbide a is located in the envelope of barley gerontoplasts. Plant Physiol Biochem 34:55–59

    CAS  Google Scholar 

  • Matile P, Ginsburg S, Schellenberg M, Thomas H (1988) Catabolites of chlorophyll in senescing barley leaves are localized in the vacuoles of mesophyll cells. Proc Natl Acad Sci USA 85:9529–9532

    Article  PubMed  CAS  Google Scholar 

  • Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235

    Article  CAS  Google Scholar 

  • Matile P, Hörtensteiner S, Thomas H, Kräutler B (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol 112:1403–1409

    PubMed  CAS  Google Scholar 

  • Matile P, Schellenberg M, Vicentini F (1997) Localization of chlorophyllase in the chloroplast envelope. Planta 201:96–99

    Article  CAS  Google Scholar 

  • Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95

    Article  PubMed  CAS  Google Scholar 

  • Maunders MJ, Brown SB, Woolhouse HW (1983) The appearance of chlorophyll derivatives in senescing tissue. Phytochemistry 22:2443–2446

    Article  CAS  Google Scholar 

  • McFeeters RF (1975) Substrate specificity of chlorophyllase. Plant Physiol 55:377–381

    Article  PubMed  CAS  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:12826–12831

    Article  PubMed  CAS  Google Scholar 

  • Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15:488–498

    Article  PubMed  CAS  Google Scholar 

  • Morita R, Sato Y, Masuda Y, Nishimura M, Kusaba M (2009) Defect in non-yellow coloring 3, an α/β hydrolase-fold family protein, causes a stay-green phenotype during leaf senescence in rice. Plant J 59:940–952

    Article  PubMed  CAS  Google Scholar 

  • Moser D, Matile P (1997) Chlorophyll breakdown in ripening fruits of Capsicum annuum. J Plant Physiol 150:759–761

    Article  CAS  Google Scholar 

  • Moser S, Müller T, Ebert MO, Jockusch S, Turro NJ, Kräutler B (2008a) Blue luminescence of ripening bananas. Angew Chem Int Ed 47:8954–8957

    Article  CAS  Google Scholar 

  • Moser S, Ulrich M, Müller T, Kräutler B (2008b) A yellow chlorophyll catabolite is a pigment of the fall colours. Photochem Photobiol Sci 7:1577–1581

    Article  PubMed  CAS  Google Scholar 

  • Moser S, Müller T, Holzinger A, Lutz C, Jockusch S, Turro NJ, Kräutler B (2009) Fluorescent chlorophyll catabolites in bananas light up blue halos of cell death. Proc Natl Acad Sci USA 106:15538–15543

    Article  PubMed  CAS  Google Scholar 

  • Mühlecker W, Kräutler B (1996) Breakdown of chlorophyll: constitution of nonfluorescing chlorophyll-catabolites from senescent cotyledons of the dicot rape. Plant Physiol Biochem 34:61–75

    Google Scholar 

  • Mühlecker W, Kräutler B, Ginsburg S, Matile P (1993) Breakdown of chlorophyll: a tetrapyrrolic chlorophyll catabolite from senescent rape leaves. Helv Chim Acta 76:2976–2980

    Article  Google Scholar 

  • Mühlecker W, Ongania K-H, Kräutler B, Matile P, Hörtensteiner S (1997) Tracking down chlorophyll breakdown in plants: elucidation of the constitution of a ‘fluorescent’ chlorophyll catabolite. Angew Chem Int Ed Engl 36:401–404

    Article  Google Scholar 

  • Mühlecker W, Kräutler B, Moser D, Matile P, Hörtensteiner S (2000) Breakdown of chlorophyll: a fluorescent chlorophyll catabolite from sweet pepper (Capsicum annuum). Helv Chim Acta 83:278–286

    Article  Google Scholar 

  • Müller T, Moser S, Ongania K-H, Pružinská A, Hörtensteiner S, Kräutler B (2006) A divergent path of chlorophyll breakdown in the model plant Arabidopsis thaliana. Chembiochem 7:40–42

    Article  PubMed  CAS  Google Scholar 

  • Müller T, Ulrich M, Ongania KH, Kräutler B (2007) Colorless tetrapyrrolic chlorophyll catabolites found in ripening fruit are effective antioxidants. Angew Chem Int Ed 46:8699–8702

    Article  CAS  Google Scholar 

  • Mur LAJ, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hörtensteiner S, Thomas H, Ougham H (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188:161–174

    Article  PubMed  CAS  Google Scholar 

  • Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res 37:D987–D991

    Article  PubMed  CAS  Google Scholar 

  • Oberhuber M, Berghold J, Mühlecker W, Hörtensteiner S, Kräutler B (2001) Chlorophyll breakdown – on a nonfluorescent chlorophyll catabolite from spinach. Helv Chim Acta 84:2615–2627

    Article  CAS  Google Scholar 

  • Oberhuber M, Berghold J, Breuker K, Hörtensteiner S, Kräutler B (2003) Breakdown of chlorophyll: a nonenzymatic reaction accounts for the formation of the colorless “nonfluorescent” chlorophyll catabolites. Proc Natl Acad Sci USA 100:6910–6915

    Article  PubMed  CAS  Google Scholar 

  • Oberhuber M, Berghold J, Kräutler B (2008) Chlorophyll breakdown by a biomimetic route. Angew Chem Int Ed 47:3057–3061

    Article  CAS  Google Scholar 

  • Oh MH, Moon YH, Lee CH (2003) Increased stability of LHCII by aggregate formation during dark-induced leaf senescence in the Arabidopsis mutant, ore10. Plant Cell Physiol 44:1368–1377

    Article  PubMed  CAS  Google Scholar 

  • Okazawa A, Tang L, Itoh Y, Fukusaki E, Kobayashi A (2006) Characterization and subcellular localization of chlorophyllase from Ginkgo biloba. Z Naturforsch C 61:111–117

    PubMed  CAS  Google Scholar 

  • op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332

    Article  PubMed  CAS  Google Scholar 

  • Oster U, Tanaka R, Tanaka A, Rüdiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21:305–310

    Article  PubMed  CAS  Google Scholar 

  • Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Andrew Staehelin L, 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  PubMed  CAS  Google Scholar 

  • Ougham H, Hörtensteiner S, Armstead I, Donnison I, King I, Thomas H, Mur L (2008) The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. Plant Biol 10(suppl 1):4–14

    Article  PubMed  CAS  Google Scholar 

  • Park S-Y, Yu J-W, Park J-S, Li J, Yoo S-C, Lee N-Y, Lee S-K, Jeong S-W, Seo HS, Koh H-J, Jeon J-S, Park Y-I, Paek N-C (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19:1649–1664

    Article  PubMed  CAS  Google Scholar 

  • Peisker C, Düggelin T, Rentsch D, Matile P (1989) Phytol and the breakdown of chlorophyll in senescent leaves. J Plant Physiol 135:428–432

    Article  CAS  Google Scholar 

  • Peoples MB, Dalling MJ (1988) The interplay between proteolysis and amino acid metabolism during senescence and nitrogen allocation. In: Noodén LD, Leopold AC (eds) Senescence and aging in plants. Academic, San Diego, pp 181–217

    Google Scholar 

  • Pretty J, Peakock J, Hine R, Sellens M, South N, Griffin M (2007) Green exercise in the UK countryside: effects on health and physiological well-being, and implications for policy and planning. J Environ Plan Manag 50:211–231

    Article  Google Scholar 

  • Pružinská A, Anders I, Tanner G, Roca M, Hörtensteiner 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  PubMed  CAS  Google Scholar 

  • Pružinská A, Tanner G, Aubry S, Anders I, Moser S, Müller T, Ongania K-H, Kräutler B, Youn J-Y, Liljegren SJ, Hörtensteiner S (2005) Chlorophyll breakdown in senescent Arabidopsis leaves: characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139:52–63

    Article  PubMed  CAS  Google Scholar 

  • Pružinská A, Anders I, Aubry S, Schenk N, Tapernoux-Lüthi E, Müller T, Kräutler B, Hörtensteiner S (2007) In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19:369–387

    Article  PubMed  CAS  Google Scholar 

  • Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H, Ge X, Kuai B (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol 144:1429–1441

    Article  PubMed  CAS  Google Scholar 

  • Ren GD, Zhou Q, Wu SX, Zhang YF, Zhang LG, Huang JR, Sun ZF, Kuai BK (2010) Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J Integr Plant Biol 52:496–504

    PubMed  CAS  Google Scholar 

  • Rise M, Cojocaru M, Gottlieb HE, Goldschmidt EE (1989) Accumulation of α-tocopherol in senescing organs as related to chlorophyll degradation. Plant Physiol 89:1028–1030

    Article  PubMed  CAS  Google Scholar 

  • Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170:677–699

    Article  PubMed  CAS  Google Scholar 

  • Rodoni S, Mühlecker W, Anderl M, Kräutler B, Moser D, Thomas H, Matile P, Hörtensteiner S (1997a) Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps. Plant Physiol 115:669–676

    Article  PubMed  CAS  Google Scholar 

  • Rodoni S, Vicentini F, Schellenberg M, Matile P, Hörtensteiner S (1997b) Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chlorophyll breakdown. Plant Physiol 115:677–682

    Article  PubMed  CAS  Google Scholar 

  • Rüdiger W (2002) Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth Res 74:187–193

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sakuraba Y, Yamasato A, Tanaka R, Tanaka A (2007) Functional analysis of N-terminal domains of Arabidopsis chlorophyllide a oxygenase. Plant Physiol Biochem 45:740–749

    Article  PubMed  CAS  Google Scholar 

  • Sakuraba Y, Tanaka R, Yamasato A, Tanaka A (2009) Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J Biol Chem 284:36689–36699

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Morita R, Nishimura M, Yamaguchi H, Kusaba M (2007) Mendel’s green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc Natl Acad Sci USA 104:14169–14174

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Moria 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schellenberg M, Matile P, Thomas H (1990) Breakdown of chlorophyll in chloroplasts of senescent barley leaves depends on ATP. J Plant Physiol 136:564–568

    Article  CAS  Google Scholar 

  • Schenk N, Schelbert S, Kanwischer M, Goldschmidt EE, Dörmann P, Hörtensteiner S (2007) The chlorophyllases AtCLH1 and AtCLH2 are not essential for senescence-related chlorophyll breakdown in Arabidopsis thaliana. FEBS Lett 581:5517–5525

    Article  PubMed  CAS  Google Scholar 

  • Scheumann V, Schoch S, Rüdiger W (1998) Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273:35102–35108

    Article  PubMed  CAS  Google Scholar 

  • Scheumann V, Schoch S, Rüdiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209:364–370

    Article  PubMed  CAS  Google Scholar 

  • Schmidt CL, Shaw L (2001) A comprehensive phylogenetic analysis of Rieske and Rieske-type iron-sulfur proteins. J Bioenerg Biomembr 33:9–26

    Article  PubMed  CAS  Google Scholar 

  • Schoch S, Scheer H, Schiff JA, Rüdiger W, Siegelman HW (1981) Pyropheophytin a accompanies pheophytin a in darkened light grown cells of Euglena. Z Naturforsch C 36:827–833

    Google Scholar 

  • Schoch S, Rüdiger W, Lüthy B, Matile P (1984) 132_hydroxychlorophyll a, the first product of the reaction of chlorophyll-oxidase. J Plant Physiol 115:85–89

    Article  PubMed  CAS  Google Scholar 

  • Shimokawa K, Hashizume A, Shioi Y (1990) Pyropheophorbide a, a catabolite of ethylene-induced chlorophyll a degradation. Phytochemistry 29:2105–2106

    Article  CAS  Google Scholar 

  • Shioi Y, Tatsumi Y, Shimokawa K (1991) Enzymatic degradation of chlorophyll in Chenopodium album. Plant Cell Physiol 32:87–93

    CAS  Google Scholar 

  • Shioi Y, Tomita N, Tsuchiya T, Takamiya K (1996a) Conversion of chlorophyllide to pheophorbide by Mg-dechelating substance in extracts of Chenopodium album. Plant Physiol Biochem 34:41–47

    CAS  Google Scholar 

  • Shioi Y, Watanabe K, Takamiya K (1996b) Enzymatic conversion of pheophorbide a to a precursor of pyropheophorbide a in leaves of Chenopodium album. Plant Cell Physiol 37:1143–1149

    Article  CAS  Google Scholar 

  • Smart CM (1994) Gene expression during leaf senescence. New Phytol 126:419–448

    Article  CAS  Google Scholar 

  • Soll J, Kemmerling M, Schultz G (1980) Tocopherol and plastoquinone synthesis in spinach chloroplast subfractions. Arch Biochem Biophys 204:544–550

    Article  PubMed  CAS  Google Scholar 

  • Spassieva S, Hille J (2002) A lesion mimic phenotype in tomato obtained by isolating and silencing an Lls1 homologue. Plant Sci 162:543–549

    Article  CAS  Google Scholar 

  • Stobart AK, Hendry GAF (1984) The turnover of chlorophyll in greening wheat leaves. Phytochemistry 23:27–30

    Article  CAS  Google Scholar 

  • Sugishima M, Kitamori Y, Noguchi M, Kohchi T, Fukuyama K (2009) Crystal structure of red chlorophyll catabolite reductase: enlargement of the ferredoxin-dependent bilin reductase family. J Mol Biol 389:376–387

    Article  PubMed  CAS  Google Scholar 

  • Sugishima M, Okamoto Y, Noguchi M, Kohchi T, Tamiaki H, Fukuyama K (2010) Crystal structures of the substrate-bound forms of red chlorophyll catabolite reductase: implications for site-specific and stereospecific reaction. J Mol Biol 402:879–891

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Shioi Y (1999) Detection of chlorophyll breakdown products in the senescent leaves of higher plants. Plant Cell Physiol 40:909–915

    Article  CAS  Google Scholar 

  • Suzuki T, Shioi Y (2002) Re-examination of Mg-dechelation reaction in the degradation of chlorophylls using chlorophyllin a as substrate. Photosynth Res 74:217–223

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Doi M, Shioi Y (2002) Two enzymatic reaction pathways in the formation of pyropheophorbide a. Photosynth Res 74:225–233

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Kunieda T, Murai F, Morioka S, Shioi Y (2005) Mg-dechelation activity in radish cotyledons with artificial and native substrates, Mg-chlorophyllin a and chlorophyllide a. Plant Physiol Biochem 43:459–464

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Amano T, Shioi Y (2006) Characterization and cloning of the chlorophyll-degrading enzyme pheophorbidase from cotyledons of radish. Plant Physiol 140:716–725

    Article  PubMed  CAS  Google Scholar 

  • Takamiya K, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5:426–431

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255

    Article  PubMed  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  PubMed  CAS  Google Scholar 

  • Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K, Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95:12719–12723

    Article  PubMed  CAS  Google Scholar 

  • Tanaka R, Hirashima M, Satoh S, Tanaka A (2003) The Arabidopsis-accelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of pheophorbide a oxygenase activity does not lead to the “stay-green” phenotype in Arabidopsis. Plant Cell Physiol 44:1266–1274

    Article  PubMed  CAS  Google Scholar 

  • Tang L, Okazawa A, Itoh Y, Fukusaki E, Kobayashi A (2004) Expression of chlorophyllase is not induced during autumnal yellowing in Ginkgo biloba. Z Naturforsch C 59:415–420

    PubMed  CAS  Google Scholar 

  • Thomas H, Howarth CJ (2000) Five ways to stay green. J Exp Bot 51:329–337

    Article  PubMed  CAS  Google Scholar 

  • Thomas H, Schellenberg M, Vicentini F, Matile P (1996) Gregor Mendel’s green and yellow pea seeds. Bot Acta 109:3–4

    Google Scholar 

  • Thomas H, Huang L, Young M, Ougham H (2009) Evolution of plant senescence. BMC Evol Biol 9:163

    Article  PubMed  CAS  Google Scholar 

  • Tommasini R, Vogt E, Fromenteau M, Hörtensteiner S, Matile P, Amrhein N, Martinoia E (1998) An ABC transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773–780

    Article  PubMed  CAS  Google Scholar 

  • Trebitsh T, Goldschmidt EE, Riov J (1993) Ethylene induces de novo synthesis of chlorophyllase, a chlorophyll degrading enzyme, in Citrus fruit peel. Proc Natl Acad Sci USA 90:9441–9445

    Article  PubMed  CAS  Google Scholar 

  • Tsuchiya T, Ohta H, Masuda T, Mikami B, Kita N, Shioi Y, Takamiya K (1997) Purification and characterization of two isozymes of chlorophyllase from mature leaves of Chenopodium album. Plant Cell Physiol 38:1026–1031

    Article  CAS  Google Scholar 

  • Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362–15367

    Article  PubMed  CAS  Google Scholar 

  • Tu SL, Gunn A, Toney MD, Britt RD, Lagarias JC (2004) Biliverdin reduction by cyanobacterial phycocyanobilin: ferredoxin oxidoreductase (PcyA) proceeds via linear tetrapyrrole radical intermediates. J Am Chem Soc 126:8682–8693

    Article  PubMed  CAS  Google Scholar 

  • Tu SL, Chen HC, Ku LW (2008) Mechanistic studies of the phytochromobilin synthase HY2 from Arabidopsis. J Biol Chem 283:27555–27564

    Article  PubMed  CAS  Google Scholar 

  • Tzoulas K, Korpela K, Venn S, Yli-Pelkonen V, Kazmierczak A, Niemela J, James P (2007) Promoting ecosystem and human health in urban areas using Green Infrastructure: a literature review. Landsc Urban Plan 81:167–178

    Article  Google Scholar 

  • Valentin HE, Lincoln K, Moshiri F, Jensen PK, Qi Q, Venkatesh TV, Karunanandaa B, Baszis SR, Norris SR, Savidge B, Gruys KJ, Last RL (2006) The arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18:212–224

    Article  PubMed  CAS  Google Scholar 

  • Van der Graaff E, Schwacke R, Schneider A, Desimone M, Flugge UI, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141:776–792

    Article  PubMed  CAS  Google Scholar 

  • Vavilin D, Vermaas W (2007) Continuous chlorophyll degradation accompanied by chlorophyllide and phytol reutilization for chlorophyll synthesis in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:920–929

    Article  PubMed  CAS  Google Scholar 

  • Vicentini F, Hörtensteiner S, Schellenberg M, Thomas H, Matile P (1995a) Chlorophyll breakdown in senescent leaves: identification of the biochemical lesion in a stay-green genotype of Festuca pratensis Huds. New Phytol 129:247–252

    Article  CAS  Google Scholar 

  • Vicentini F, Iten F, Matile P (1995b) Development of an assay for Mg-dechelatase of oilseed rape cotyledons, using chlorophyllin as the substrate. Physiol Plant 94:57–63

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP, Würsch M, Laloi C, Nater M, Hideg E, Apel K (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306:1183–1185

    Article  PubMed  CAS  Google Scholar 

  • Willstätter R, Stoll A (1913) Die Wirkungen der Chlorophyllase. In: Willstätter R, Stoll A (eds) Untersuchungen über Chlorophyll. Verlag Julius Springer, Berlin, pp 172–187

    Google Scholar 

  • Wüthrich KL, Bovet L, Hunziker PE, Donnison IS, Hörtensteiner S (2000) Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. Plant J 21:189–198

    Article  PubMed  Google Scholar 

  • Xiong J, Bauer CE (2002) Complex evolution of photosynthesis. Annu Rev Plant Biol 53:503–521

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Wardzala E, Johal GS, Gray J (2004) The wound-inducible Lls1 gene from maize is an orthologue of the Arabidopsis Acd1 gene, and the LLS1 protein is present in non-photosynthetic tissues. Plant Mol Biol 54:175–191

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Xu R, Ma CJ, Vlot AC, Klessig DF, Pichersky E (2008) Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol 147:1034–1045

    Article  PubMed  CAS  Google Scholar 

  • Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397–411

    Article  PubMed  CAS  Google Scholar 

  • Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion – an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40:596–610

    Article  PubMed  CAS  Google Scholar 

  • Zeier J, Pink B, Mueller MJ, Berger S (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219:673–683

    Article  PubMed  CAS  Google Scholar 

  • Ziegler R, Blaheta A, Guha N, Schönegge B (1988) Enzymatic formation of pheophorbide and pyropheophorbide during chlorophyll degradation in a mutant of Chlorella fusca SHIRIA et KRAUS. J Plant Physiol 132:327–332

    Article  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I would like to thank Bernhard Kräutler for many stimulating discussions and fruitful long-term collaboration. Many thanks also to my present and former group members for their important contributions in the area of chlorophyll breakdown. I thank Helen Ougham for critical reading and language editing of the manuscript. My work is financially supported by grants from the Swiss National Science Foundation and by the National Center of Competence in Research Plant Survival, a research program of the Swiss National Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefan Hörtensteiner .

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

Hörtensteiner, S. (2013). The Pathway of Chlorophyll Degradation: Catabolites, Enzymes and Pathway Regulation. 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_16

Download citation

Publish with us

Policies and ethics