Abstract
In land plants, chlorophyll is broken down to colorless linear tetrapyrroles in a highly conserved multi-step pathway. The pathway is termed the ‘PAO pathway’, because the opening of the chlorine macrocycle present in chlorophyll catalyzed by pheophorbide a oxygenase (PAO), the key enzyme of the pathway, provides the characteristic structural basis found in all further downstream chlorophyll breakdown products. To date, most of the biochemical steps of the PAO pathway have been elucidated and genes encoding many of the chlorophyll catabolic enzymes been identified. This review summarizes the current knowledge on the biochemistry of the PAO pathway and provides insight into recent progress made in the field that indicates that the pathway is more complex than thought in the past.
Similar content being viewed by others
References
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
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Arkus KAJ, Cahoon EB, Jez JM (2005) Mechanistic analysis of wheat chlorophyllase. Arch Biochem Biophys 438:146–155
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
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
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
Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol 10(Suppl. 1):63–75
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
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
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
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
Breeze E, Harrison E, McHattie S, Hughes L, Hickman R, Hill C, Kiddle S, Kim YS, Penfold CA, Jenkins D, Zhang C, Morris K, Jenner C, Jackson S, Thomas B, Tabrett A, Legaie R, Moore JD, Wild DL, Ott S, Rand D, Beynon J, Denby K, Mead A, Buchanan-Wollaston V (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894
Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266
Brown SB, Houghton JD, Hendry GAF (1991) Chlorophyll breakdown. In: Scheer H (ed) Chlorophylls. CRC Press, Boca Raton, pp 465–489
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
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
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
Christ B, Schelbert S, Aubry S, Süssenbacher I, Müller T, Kräutler B, Hörtensteiner S (2012) MES16, a member of the methylesterase protein family, specifically demethylates fluorescent chlorophyll catabolites during chlorophyll breakdown in Arabidopsis. Plant Physiol 158:628–641
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
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
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
Ginsburg S, Matile P (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol 102:521–527
Ginsburg S, Schellenberg M, Matile P (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol 105:545–554
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
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
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
Greenberg JT, Ausubel FM (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4:327–341
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
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
Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612
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
Hendry GAF, Houghton JD, Brown SB (1987) The degradation of chlorophyll: a biological enigma. New Phytol 107:255–302
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
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
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
Hörtensteiner S (1998) NCC malonyltransferase catalyses the final step of chlorophyll breakdown in rape (Brassica napus). Phytochemistry 49:953–956
Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77
Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162
Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochem Biophys Acta 1807:977–988
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
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
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
Ito H, Ohysuka T, Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271:1475–1479
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
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
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
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
Kräutler B (2003) Chlorophyll breakdown and chlorophyll catabolites. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook, vol 13. Elsevier Science, Amsterdam, pp 183–209
Kräutler B (2008) Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit. Photochem Photobiol Sci 7:1114–1120
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, vol 25., Advances in photosynthesis and respirationSpringer, Dordrecht, pp 237–260
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
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 and indicates a divergent path of chlorophyll breakdown. FEBS Lett 584:4215–4221
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
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
Langmeier M, Ginsburg S, Matile P (1993) Chlorophyll breakdown in senescent leaves: demonstration of Mg-dechelatase activity. Physiol Plant 89:347–353
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
Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136
Losey FG, Engel N (2001) Isolation and characterization of a urobilinogenoidic chlorophyll catabolite from Hordeum vulgare L. J Biol Chem 276:27233–27236
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
Lundquist PK, Poliakov A, Bhuiyan NH, Zybailov B, Sun Q, van Wijk KJ (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158:1172–1192
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
Matile P, Schellenberg M (1996) The cleavage of pheophorbide a is located in the envelope of barley gerontoplasts. Plant Physiol Biochem 34:55–59
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
Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235
Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95
Mecey C, Hauck P, Trapp M, Pumplin N, Plovanich A, Yao J, He SY (2011) A critical role of STAYGREEN/Mendel’s I locus in controlling disease symptom development during Pseudomonas syringae pv tomato infection of Arabidopsis. Plant Physiol 157:1965–1974
Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23:3442–3453
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
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
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
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
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
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
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
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
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
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
Müller T, Rafelsberger M, Vergeiner C, Kräutler B (2011) A dioxobilane as product of a divergent path of chlorophyll breakdown in Norway maple. Angew Chem Int Ed 50:10724–10727
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
Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucl Acids Res 37:D987–D991
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
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
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
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
Pattanayak GK, Venkataramani S, Hörtensteiner S, Kunz L, Christ B, Moulin M, Smith AG, Okamoto Y, Tamiaki H, Sugishima M, Greenberg JT (2012) ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis. Plant J 69:589–600
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
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
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
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
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
Rodoni S, Vicentini F, Schellenberg M, Matile P, Hörtensteiner S (1997) Partial purification and characterization of red chlorophyll catabolite reductase, a stroma protein involved in chlorophyll breakdown. Plant Physiol 115:677–682
Sakuraba Y, Schelbert S, Park S-Y, Han S-H, Lee B-D, Besagni Andrès C, Kessler F, Hörtensteiner S, Paek N-C (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24:507–518
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
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
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
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
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
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
Scheumann V, Schoch S, Rüdiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209:364–370
Schmidt CL, Shaw L (2001) A comprehensive phylogenetic analysis of Rieske and Rieske-type iron-sulfur proteins. J Bioenerg Biomembr 33:9–26
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
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
Spassieva S, Hille J (2002) A lesion mimic phenotype in tomato obtained by isolating and silencing an Lls1 homologue. Plant Sci 162:543–549
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
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
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
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
Takamiya K, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5:426–431
Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255
Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346
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
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
Thomas H, Huang L, Young M, Ougham H (2009) Evolution of plant senescence. BMC Evol Biol 9:163
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
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
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
Tu SL, Chen HC, Ku LW (2008) Mechanistic studies of the phytochromobilin synthase HY2 from Arabidopsis. J Biol Chem 283:27555–27564
Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301
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
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
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
Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T, Fernie AR, Kaufmann K, Xue GP, Mueller-Roeber B, Balazadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24:482–506
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
Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397–411
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
Zhang X, Zhang Z, Li J, Wu L, Guo J, Ouyang L, Xia Y, Huang X, Pang X (2011) Correlation of leaf senescence and gene expression/activities of chlorophyll degradation enzymes in harvested Chinese flowering cabbage (Brassica rapa var. parachinensis). J Plant Physiol 168:2081–2087
Zhou C, Han L, Pislariu C, Nakashima J, Fu C, Jiang Q, Quan L, Blancaflor EB, Tang Y, Bouton JH, Udvardi M, Xia G, Wang ZY (2011) From model to crop: functional analysis of a STAY-GREEN gene in the model legume Medicago truncatula and effective use of the gene for alfalfa improvement. Plant Physiol 157:1483–1496
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
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632
Acknowledgments
I would like to thank Bernhard Kräutler from the University of Innsbruck, Austria for many stimulating discussions and the long-term and extremely fruitful collaboration between his and my own group. My work on chlorophyll breakdown is financially supported by grants from the Swiss National Science Foundation, the National Center of Competence in Research Plant Survival, a research program of the Swiss National Science Foundation, and CropLife, an European FP7 Marie-Curie Initial Training Network project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hörtensteiner, S. Update on the biochemistry of chlorophyll breakdown. Plant Mol Biol 82, 505–517 (2013). https://doi.org/10.1007/s11103-012-9940-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-012-9940-z