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Plant Molecular Biology

, Volume 82, Issue 6, pp 505–517 | Cite as

Update on the biochemistry of chlorophyll breakdown

  • Stefan HörtensteinerEmail author
Article

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.

Keywords

Chlorophyll catabolites Chlorophyll breakdown Detoxification Fruit ripening Leaf senescence 

Notes

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.

References

  1. 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 120:645–651CrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  3. Arkus KAJ, Cahoon EB, Jez JM (2005) Mechanistic analysis of wheat chlorophyllase. Arch Biochem Biophys 438:146–155PubMedCrossRefGoogle Scholar
  4. 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 67:243–256PubMedCrossRefGoogle Scholar
  5. 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 148:108–118PubMedCrossRefGoogle Scholar
  6. 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 126:593–600CrossRefGoogle Scholar
  7. Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol 10(Suppl. 1):63–75PubMedCrossRefGoogle Scholar
  8. 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 49:5174–5177CrossRefGoogle Scholar
  9. 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 74:109–119PubMedCrossRefGoogle Scholar
  10. Berghold J, Eichmüller C, Hörtensteiner S, Kräutler B (2004) Chlorophyll breakdown in tobacco: on the structure of two nonfluorescent chlorophyll catabolites. Chem Biodivers 1:657–668PubMedCrossRefGoogle Scholar
  11. 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 137:751–763CrossRefGoogle Scholar
  12. 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 23:873–894PubMedCrossRefGoogle Scholar
  13. Bréhélin C, Kessler F, van Wijk KJ (2007) Plastoglobules: versatile lipoprotein particles in plastids. Trends Plant Sci 12:260–266PubMedCrossRefGoogle Scholar
  14. Brown SB, Houghton JD, Hendry GAF (1991) Chlorophyll breakdown. In: Scheer H (ed) Chlorophylls. CRC Press, Boca Raton, pp 465–489Google Scholar
  15. 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 42:567–585PubMedCrossRefGoogle Scholar
  16. Büchert AM, Civello PM, Martínez GA (2011) Chlorophyllase versus pheophytinase as candidates for chlorophyll dephytilation during senescence of broccoli. J Plant Physiol 168:337–343PubMedCrossRefGoogle Scholar
  17. 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 174:25–31CrossRefGoogle Scholar
  18. 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 158:628–641PubMedCrossRefGoogle Scholar
  19. Curty C, Engel N (1996) Detection, isolation and structure elucidation of a chlorophyll a catabolite from autumnal senescent leaves of Cercidiphyllum japonicum. Phytochemistry 42:1531–1536CrossRefGoogle Scholar
  20. 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 13:965–978PubMedGoogle Scholar
  21. 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 49:557–569PubMedCrossRefGoogle Scholar
  22. Ginsburg S, Matile P (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol 102:521–527PubMedGoogle Scholar
  23. Ginsburg S, Schellenberg M, Matile P (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol 105:545–554PubMedGoogle Scholar
  24. 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 89:25–31PubMedCrossRefGoogle Scholar
  25. 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 130:1894–1907PubMedCrossRefGoogle Scholar
  26. 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 54:39–54PubMedCrossRefGoogle Scholar
  27. Greenberg JT, Ausubel FM (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4:327–341PubMedCrossRefGoogle Scholar
  28. 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 77:551–563PubMedCrossRefGoogle Scholar
  29. 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 96:227–231PubMedCrossRefGoogle Scholar
  30. Guo YF, Gan SS (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612PubMedCrossRefGoogle Scholar
  31. 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 19:1007–1022PubMedCrossRefGoogle Scholar
  32. Hendry GAF, Houghton JD, Brown SB (1987) The degradation of chlorophyll: a biological enigma. New Phytol 107:255–302CrossRefGoogle Scholar
  33. 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 271:27233–27236PubMedCrossRefGoogle Scholar
  34. Hirashima M, Tanaka R, Tanaka A (2009) Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol 50:719–729PubMedCrossRefGoogle Scholar
  35. 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 284:17449–17456PubMedCrossRefGoogle Scholar
  36. Hörtensteiner S (1998) NCC malonyltransferase catalyses the final step of chlorophyll breakdown in rape (Brassica napus). Phytochemistry 49:953–956PubMedCrossRefGoogle Scholar
  37. Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77PubMedCrossRefGoogle Scholar
  38. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162PubMedCrossRefGoogle Scholar
  39. Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochem Biophys Acta 1807:977–988PubMedCrossRefGoogle Scholar
  40. 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 129:237–246CrossRefGoogle Scholar
  41. 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 273:15335–15339PubMedCrossRefGoogle Scholar
  42. 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 2:63–67CrossRefGoogle Scholar
  43. Ito H, Ohysuka T, Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271:1475–1479PubMedCrossRefGoogle Scholar
  44. Iturraspe J, Moyano N, Frydman B (1995) A new 5-formylbilinone as the major chlorophyll a catabolite in tree senescent leaves. J Org Chem 60:6664–6665CrossRefGoogle Scholar
  45. 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 20:653–661CrossRefGoogle Scholar
  46. 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 52:197–209PubMedCrossRefGoogle Scholar
  47. 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 17:282–294PubMedCrossRefGoogle Scholar
  48. 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 183–209CrossRefGoogle Scholar
  49. Kräutler B (2008) Chlorophyll breakdown and chlorophyll catabolites in leaves and fruit. Photochem Photobiol Sci 7:1114–1120PubMedCrossRefGoogle Scholar
  50. 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 237–260CrossRefGoogle Scholar
  51. 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 30:1315–1318CrossRefGoogle Scholar
  52. 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 584:4215–4221PubMedCrossRefGoogle Scholar
  53. 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 169:177–183CrossRefGoogle Scholar
  54. 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 19:1362–1375PubMedCrossRefGoogle Scholar
  55. Langmeier M, Ginsburg S, Matile P (1993) Chlorophyll breakdown in senescent leaves: demonstration of Mg-dechelatase activity. Physiol Plant 89:347–353CrossRefGoogle Scholar
  56. 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 49:531–539CrossRefGoogle Scholar
  57. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  58. Losey FG, Engel N (2001) Isolation and characterization of a urobilinogenoidic chlorophyll catabolite from Hordeum vulgare L. J Biol Chem 276:27233–27236CrossRefGoogle Scholar
  59. 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 10:267–282PubMedGoogle Scholar
  60. 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 158:1172–1192PubMedCrossRefGoogle Scholar
  61. 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 98:771–776PubMedCrossRefGoogle Scholar
  62. Matile P, Schellenberg M (1996) The cleavage of pheophorbide a is located in the envelope of barley gerontoplasts. Plant Physiol Biochem 34:55–59Google Scholar
  63. 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 85:9529–9532PubMedCrossRefGoogle Scholar
  64. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187:230–235CrossRefGoogle Scholar
  65. Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95PubMedCrossRefGoogle Scholar
  66. 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 157:1965–1974PubMedCrossRefGoogle Scholar
  67. 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 23:3442–3453PubMedCrossRefGoogle Scholar
  68. 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 15:488–498PubMedCrossRefGoogle Scholar
  69. 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 59:940–952PubMedCrossRefGoogle Scholar
  70. Moser S, Müller T, Ebert MO, Jockusch S, Turro NJ, Kräutler B (2008a) Blue luminescence of ripening bananas. Angew Chem Int Ed 47:8954–8957CrossRefGoogle Scholar
  71. Moser S, Ulrich M, Müller T, Kräutler B (2008b) A yellow chlorophyll catabolite is a pigment of the fall colours. Photochem Photobiol Sci 7:1577–1581PubMedCrossRefGoogle Scholar
  72. 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 106:15538–15543PubMedCrossRefGoogle Scholar
  73. Mühlecker W, Kräutler B (1996) Breakdown of chlorophyll: constitution of nonfluorescing chlorophyll-catabolites from senescent cotyledons of the dicot rape. Plant Physiol Biochem 34:61–75Google Scholar
  74. 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 36:401–404CrossRefGoogle Scholar
  75. 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 83:278–286CrossRefGoogle Scholar
  76. 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 7:40–42PubMedCrossRefGoogle Scholar
  77. Müller T, Ulrich M, Ongania KH, Kräutler B (2007) Colorless tetrapyrrolic chlorophyll catabolites found in ripening fruit are effective antioxidants. Angew Chem Int Ed 46:8699–8702CrossRefGoogle Scholar
  78. 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 50:10724–10727CrossRefGoogle Scholar
  79. 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 188:161–174PubMedCrossRefGoogle Scholar
  80. Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucl Acids Res 37:D987–D991PubMedCrossRefGoogle Scholar
  81. Oberhuber M, Berghold J, Mühlecker W, Hörtensteiner S, Kräutler B (2001) Chlorophyll breakdown—on a nonfluorescent chlorophyll catabolite from spinach. Helv Chim Acta 84:2615–2627CrossRefGoogle Scholar
  82. 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 100:6910–6915PubMedCrossRefGoogle Scholar
  83. 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 44:1368–1377PubMedCrossRefGoogle Scholar
  84. 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 19:1649–1664PubMedCrossRefGoogle Scholar
  85. 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 69:589–600PubMedCrossRefGoogle Scholar
  86. 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 100:15259–15264PubMedCrossRefGoogle Scholar
  87. 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 139:52–63PubMedCrossRefGoogle Scholar
  88. 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 19:369–387PubMedCrossRefGoogle Scholar
  89. 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 144:1429–1441PubMedCrossRefGoogle Scholar
  90. 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 52:496–504PubMedGoogle Scholar
  91. 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 115:677–682PubMedCrossRefGoogle Scholar
  92. 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 24:507–518PubMedCrossRefGoogle Scholar
  93. 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 104:14169–14174PubMedCrossRefGoogle Scholar
  94. 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 57:120–131PubMedCrossRefGoogle Scholar
  95. 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 21:767–785PubMedCrossRefGoogle Scholar
  96. Schellenberg M, Matile P, Thomas H (1990) Breakdown of chlorophyll in chloroplasts of senescent barley leaves depends on ATP. J Plant Physiol 136:564–568CrossRefGoogle Scholar
  97. 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 581:5517–5525PubMedCrossRefGoogle Scholar
  98. Scheumann V, Schoch S, Rüdiger W (1998) Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273:35102–35108PubMedCrossRefGoogle Scholar
  99. Scheumann V, Schoch S, Rüdiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209:364–370PubMedCrossRefGoogle Scholar
  100. Schmidt CL, Shaw L (2001) A comprehensive phylogenetic analysis of Rieske and Rieske-type iron-sulfur proteins. J Bioenerg Biomembr 33:9–26PubMedCrossRefGoogle Scholar
  101. 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 34:41–47Google Scholar
  102. 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 37:1143–1149CrossRefGoogle Scholar
  103. Spassieva S, Hille J (2002) A lesion mimic phenotype in tomato obtained by isolating and silencing an Lls1 homologue. Plant Sci 162:543–549CrossRefGoogle Scholar
  104. 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 389:376–387PubMedCrossRefGoogle Scholar
  105. 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 402:879–891PubMedCrossRefGoogle Scholar
  106. Suzuki T, Shioi Y (2002) Re-examination of Mg-dechelation reaction in the degradation of chlorophylls using chlorophyllin a as substrate. Photosynth Res 74:217–223PubMedCrossRefGoogle Scholar
  107. Suzuki Y, Amano T, Shioi Y (2006) Characterization and cloning of the chlorophyll-degrading enzyme pheophorbidase from cotyledons of radish. Plant Physiol 140:716–725PubMedCrossRefGoogle Scholar
  108. Takamiya K, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5:426–431PubMedCrossRefGoogle Scholar
  109. Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255PubMedCrossRefGoogle Scholar
  110. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346PubMedCrossRefGoogle Scholar
  111. 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 44:1266–1274PubMedCrossRefGoogle Scholar
  112. 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 59:415–420PubMedGoogle Scholar
  113. Thomas H, Huang L, Young M, Ougham H (2009) Evolution of plant senescence. BMC Evol Biol 9:163PubMedCrossRefGoogle Scholar
  114. 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 13:773–780PubMedCrossRefGoogle Scholar
  115. 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 96:15362–15367PubMedCrossRefGoogle Scholar
  116. 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 126:8682–8693PubMedCrossRefGoogle Scholar
  117. Tu SL, Chen HC, Ku LW (2008) Mechanistic studies of the phytochromobilin synthase HY2 from Arabidopsis. J Biol Chem 283:27555–27564PubMedCrossRefGoogle Scholar
  118. 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 314:1298–1301PubMedCrossRefGoogle Scholar
  119. 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 141:776–792PubMedCrossRefGoogle Scholar
  120. 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 129:247–252CrossRefGoogle Scholar
  121. 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 94:57–63CrossRefGoogle Scholar
  122. 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 24:482–506PubMedCrossRefGoogle Scholar
  123. 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 21:189–198PubMedCrossRefGoogle Scholar
  124. Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18:397–411PubMedCrossRefGoogle Scholar
  125. Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion—an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40:596–610PubMedCrossRefGoogle Scholar
  126. 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 168:2081–2087PubMedCrossRefGoogle Scholar
  127. 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 157:1483–1496PubMedCrossRefGoogle Scholar
  128. 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 132:327–332CrossRefGoogle Scholar
  129. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Institute of Plant BiologyUniversity of ZurichZurichSwitzerland

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