Mechanism and Significance of Chlorophyll Breakdown

Journal of Plant Growth Regulation

Volumn 33, Issue 1, 2014, Pages 4-20

  Christ, Bastien ^a   Hörtensteiner, Stefan ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Chlorophyll breakdown; Chlorophyll catabolites; Detoxification; Nutrient remobilization; Senescence

Indexed keywords

EMBRYOPHYTA; TRACHEOPHYTA;

EID: 84897572075     PISSN: 07217595     EISSN: 14358107     Source Type: Journal    
DOI: 10.1007/s00344-013-9392-y     Document Type: Review

References (139)

1. Armstead I, Donnison I, Aubry S et al (2007) Cross-species identification of Mendel's I locus. Science 315: 73.
2. 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.
3. Azoulay-Shemer T, Harpaz-Saad S, Cohen-Peer R et al (2011) Dual N- and C-terminal processing of citrus chlorophyllase precursor within the plastid membranes leads to the mature enzyme. Plant Cell Physiol 52: 70-83.
4. Bak S, Beisson F, Bishop G et al (2011) Cytochromes P450. Arabidopsis Book 9: e0144.
5. Banala S, Moser S, Müller T et al (2010) Hypermodified fluorescent chlorophyll catabolites: source of blue luminescence in senescent leaves. Angew Chem Int Ed 49: 5174-5177.
6. Barrett J, Jeffrey SW (1964) Chlorophyllase and formation of an atypical chlorophyllide in marine algae. Plant Physiol 39: 44-47.
7. Barry CS, McQuinn RP, Chung MY (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 Biochem 147: 179-187.
8. Benedetti CE, Arruda P (2002) Altering the expression of the chlorophyllase gene ATHCOR1 in transgenic Arabidopsis caused changes in the chlorophyll-to-chlorophyllide ratio. Plant Physiol 128: 1255-1263.
9. Berghold J, Breuker K, Oberhuber M et al (2002) Chlorophyll breakdown in spinach: on the structure of five nonfluorescent chlorophyll catabolites. Photosynth Res 74: 109-119.
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: 657-668.
11. Berghold J, Müller T, Ulrich M (2006) Chlorophyll breakdown in maize: on the structure of two nonfluorescent chlorophyll catabolites. Monatsh Chem 137: 751-763.
12. Brandis A, Vainstein A, Goldschmidt EE (1996) Distribution of chlorophyllase among components of chloroplast membranes in Citrus sinensis organs. Plant Physiol Biochem 34: 49-54.
13. Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46: 471-510.
14. Büchert AM, Civello PM, Martínez GA (2011) Characterization of Mg-dechelating substance in senescent and pre-senescent Arabidopsisthaliana leaves. Biol Plant 55: 75-82.
15. Christ B, Schelbert S, Aubry S et al (2012) MES16, a member of the methylesterase protein family, specifically demethylates fluorescent chlorophyll catabolites during chlorophyll breakdown in Arabidopsis. Plant Physiol 158: 628-641.
16. Christ B, Süssenbacher I, Moser S et al (2013) Cytochrome P450 CYP89A9 is involved in the formation of major chlorophyll catabolites during leaf senescence in Arabidopsis. Plant Cell 25: 1868-1880.
17. 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.
18. Dosnon-Olette R, Schröder P, Bartha B et al (2011) Enzymatic basis for fungicide removal by Elodea canadensis. Environ Sci Pollut Res 18: 1015-1021.
19. Downie A, Miyazaki S, Bohnert H et al (2004) Expression profiling of the response of Arabidopsisthaliana to methanol stimulation. Phytochemistry 65: 2305-2316.
20. Fall R, Benson AA (1996) Leaf methanol-the simplest natural product from plants. Trends Plant Sci 1: 296-301.
21. Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of Rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59: 1615-1624.
22. Ginsburg S, Matile P (1993) Identification of catabolites of chlorophyll porphyrin in senescent rape cotyledons. Plant Physiol 102: 521-527.
23. Ginsburg S, Schellenberg M, Matile P (1994) Cleavage of chlorophyll-porphyrin. Requirement for reduced ferredoxin and oxygen. Plant Physiol 105: 545-554.
24. Gout E, Aubert S, Bligny R et al (2000) Metabolism of methanol in plant cells. Carbon-13 nuclear magnetic resonance studies. Plant Physiol 123: 287-296.
25. Gray J, Janick-Bruckner D, Bruckner B et al (2002) Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol 130: 1894-1907.
26. Greenberg JT, Ausubel FM (1993) Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J 4: 327-341.
27. Harpaz-Saad S, Azoulay T, Arazi T et al (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19: 1007-1022.
28. Hirashima M, Satoh S, Tanaka R, Tanaka A (2006) Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J Biol Chem 281: 15385-15393.
29. Hirashima M, Tanaka R, Tanaka A (2009) Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsisthaliana. Plant Cell Physiol 50: 719-729.
30. Holden M (1961) The breakdown of chlorophyll by chlorophyllase. Biochem J 78: 359-364.
31. Horie Y, Ito H, Kusaba M et al (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.
32. Hörtensteiner S (1998) NCC malonyltransferase catalyses the final step of chlorophyll breakdown in rape (Brassica napus). Phytochemistry 49: 953-956.
33. Hörtensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57: 55-77.
34. Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14: 155-162.
35. Hörtensteiner S (2013) Update on the biochemistry of chlorophyll breakdown. Plant Mol Biol 82(6): 505-517.
36. Hörtensteiner S, Feller U (2002) Nitrogen metabolism and remobilization during senescence. J Exp Bot 53: 927-937.
37. Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807: 977-988.
38. 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.
39. Hörtensteiner S, Wüthrich KL, Matile P et al (1998) The key step in chlorophyll breakdown in higher plants. Cleavage of pheophorbide a macrocycle by a monooxygenase. J Biol Chem 273: 15335-15339.
40. Hörtensteiner S, Rodoni S, Schellenberg M et al (2000) Evolution of chlorophyll degradation: the significance of RCC reductase. Plant Biol 2: 63-67.
41. Igamberdiev AU, Bykova NV, Kleczkowski LA (1999) Origins and metabolism of formate in higher plants. Plant Physiol Biochem 37: 503-513.
42. Ischebeck T, Zbierzak AM, Kanwischer M, Dörmann P (2006) A salvage pathway for phytol metabolism in Arabidopsis. J Biol Chem 281: 2470-2477.
43. 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.
44. Jakob-Wilk D, Holland D, Goldschmidt EE et al (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.
45. Jiang H, Li M, Liang N et al (2007) Molecular cloning and function analysis of the stay green gene in rice. Plant J 52: 197-209.
46. Jonker JW, Buitelaar M, Wagenaar E et al (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA 99: 15649-15654.
47. Kang K, Kim Y-S, Park S, Back K (2009) Senescence-induced serotonin biosynthesis and its role in delaying senescence in rice leaves. Plant Physiol 150: 1380-1393.
48. Kang J, Park J, Choi H et al (2011a) Plant ABC transporters. Arabidopsis Book 9: e0153.
49. Kang K, Park S, Natsagdorj U et al (2011b) Methanol is an endogenous elicitor molecule for the synthesis of tryptophan and tryptophan-derived secondary metabolites upon senescence of detached rice leaves. Plant J 66: 247-257.
50. 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.
51. Kleffmann T, Russenberger D, von Zychlinski A et al (2004) The Arabidopsisthaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14: 354-362.
52. Kräutler B, Jaun B, Bortlik K-H et al (1991) On the enigma of chlorophyll degradation: the constitution of a secoporphinoid catabolite. Angew Chem Int Ed 30: 1315-1318.
53. Kräutler B, Banala S, Moser S et al (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.
54. Kusaba M, Ito H, Morita R et al (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19: 1362-1375.
55. Li R, Ziola B, King J (2000) Purification and characterization of formate dehydrogenase from Arabidopsisthaliana. J Plant Physiol 157: 161-167.
56. Li R, Moore M, Bonham-Smith PC, King J (2002) Overexpression of formate dehydrogenase in Arabidopsisthaliana resulted in plants tolerant to high concentrations of formate. J Plant Physiol 159: 1069-1076.
57. Lippold F, Dorp K, vom Abraham M et al (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24: 2001-2014.
58. Losey FG, Engel N (2001) Isolation and characterization of a urobilinogenoidic chlorophyll catabolite from Hordeum vulgare L. J Biol Chem 276: 27233-27236.
59. Lu YP, Li ZS, Drozdowicz YM et al (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.
60. Lundquist PK, Poliakov A, Bhuiyan NH et al (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genome-wide coexpression analysis. Plant Physiol 158: 1172-1192.
61. Luo Z, Zhang J, Li J et al (2013) A STAY-GREEN protein SlSGR1 regulates lycopene and β-carotene accumulation by interacting directly with SlPSY1 during ripening processes in tomato. New Phytol 198(2): 442-452.
62. 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.
63. Makino A, Osmond B (1991) Effect of nitrogen nutrition on nitrogen partitioning between chloroplasts and mitochondria in pea and wheat. Plant Physiol 96: 355-362.
64. Matile P, Schellenberg M, Peisker C (1992) Production and release of a chlorophyll catabolite in isolated senescent chloroplasts. Planta 187: 230-235.
65. Matile P, Hörtensteiner S, Thomas H, Kräutler B (1996) Chlorophyll breakdown in senescent leaves. Plant Physiol 112: 1403-1409.
66. Matile P, Schellenberg M, Vicentini F (1997) Localization of chlorophyllase in the chloroplast envelope. Planta 201: 96-99.
67. Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50: 67-95.
68. Mayer H (1930) Untersuchungen über die Chlorophyllase. Planta 11: 294-330.
69. Mecey C, Hauck P, Trapp M et al (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.
70. Meguro M, Ito H, Takabayashi A et al (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23: 3442-3453.
71. Mendel G (1866) Versuche über Pflanzenhybriden. Verh Naturforsch Ver Brünn 4: 3-47.
72. Mochizuki N, Brusslan JA, Larkin R et al (2001) Arabidopsisgenomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053-2058.
73. Morita R, Sato Y, Masuda Y et al (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.
74. Moser S, Aarts M, Müller T, Kräutler B (2008a) A yellow chlorophyll catabolite is a pigment of the fall colours. Photochem Photobiol Sci 7: 1577-1581.
75. Moser S, Müller T, Ebert MO et al (2008b) Blue luminescence of ripening bananas. Angew Chem Int Ed 47: 8954-8957.
76. Moser S, Müller T, Holzinger A et al (2009) Fluorescent chlorophyll catabolites in bananas light up blue halos of cell death. Proc Natl Acad Sci USA 106: 15538-15543.
77. 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.
78. Mühlecker W, Ongania KH, Kräutler B et al (1997) Tracking down chlorophyll breakdown in plants: elucidation of the constitution of a "fluorescent" chlorophyll catabolite. Angew Chem Int Ed 36: 401-404.
79. Mühlecker W, Kräutler B, Moser D et al (2000) Breakdown of chlorophyll: a fluorescent chlorophyll catabolite from sweet pepper (Capsicum annuum). Helv Chim Acta 83: 278-286.
80. Müller T, Moser S, Ongania KH et al (2006) A divergent path of chlorophyll breakdown in the model plant Arabidopsisthaliana. ChemBioChem 7: 40-42.
81. 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.
82. 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.
83. Mur LAJ, Aubry S, Mondhe M et al (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol 188: 161-174.
84. Nakajima S, Ito H, Tanaka R, Tanaka A (2012) Chlorophyll b reductase plays an essential role in maturation and storability of Arabidopsis seeds. Plant Physiol 160: 261-273.
85. Obayashi T, Hayashi S, Saeki M et al (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res 37: D987-D991.
86. Oberhuber M, Berghold J, Mühlecker W et al (2001) Chlorophyll breakdown-on a nonfluorescent chlorophyll catabolite from spinach. Helv Chim Acta 84: 2615-2627.
87. Oberhuber M, Berghold J, Breuker K et al (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.
88. Olson BJ, Skavdahl M, Ramberg H, Osterman JC, Markwell J (2000) Formate dehydrogenase in Arabidopsisthaliana: characterization and possible targeting to the chloroplast. Plant Sci 159: 205-212.
89. Osmani SA, Bak S, Møller BL (2009) Substrate specificity of plant UDP-dependent glycosyltransferases predicted from crystal structures and homology modeling. Phytochemistry 70: 325-347.
90. Paquette S, Møller BL, Bak S (2003) On the origin of family 1 plant glycosyltransferases. Phytochemistry 62: 399-413.
91. Park SY, Yu JW, Park JS et al (2007) The senescence-induced STAYGREEN protein regulates chlorophyll degradation. Plant Cell 19: 1649-1664.
92. Pattanayak GK, Venkataramani S, Hortensteiner S et al (2012) ACCELERATED CELL DEATH 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis. Plant J 69: 589-600.
93. Pedras MSC, Zaharia IL, Gai Y et al (2001) In planta sequential hydroxylation and glycosylation of a fungal phytotoxin: avoiding cell death and overcoming the fungal invader. Proc Natl Acad Sci USA 98: 747-752.
94. 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 Aging Plants. Academic Press, San Diego, pp 181-217.
95. Pružinská A, Anders I, Tanner G et al (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.
96. Pružinská A, Tanner G, Aubry S et al (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.
97. Pružinská A, Anders I, Aubry S et al (2007) In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. Plant Cell 19: 369-387.
98. Ren G, An K, Liao Y et al (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol 144: 1429-1441.
99. Ren GD, Zhou Q, Wu SX et al (2010) Reverse genetic identification of CRN1 and its distinctive role in chlorophyll degradation in Arabidopsis. J Integr Plant Biol 52: 496-504.
100. Rodoni S, Mühlecker W, Anderl M et al (1997) Chlorophyll breakdown in senescent chloroplasts. Cleavage of pheophorbide a in two enzymic steps. Plant Physiol 115: 669-676.
101. Saga Y, Tamiaki H (2012) Demetalation of chlorophyll pigments. Chem Biodivers 9: 1659-1683.
102. Sakuraba Y, Yokono M, Akimoto S et al (2010) Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in Arabidopsisthaliana. Plant Cell Physiol 51: 1055-1065.
103. Sakuraba Y, Balazadeh S, Tanaka R et al (2012a) Overproduction of Chl b retards senescence through transcriptional reprogramming in Arabidopsis. Plant Cell Physiol 53: 505-517.
104. Sakuraba Y, Schelbert S, Park SY et al (2012b) 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.
105. Sakuraba Y, Kim YS, Yoo SC et al (2013) 7-Hydroxymethyl chlorophyll a reductase functions in metabolic channeling of chlorophyll breakdown intermediates during leaf senescence. Biochem Biophys Res Commun 430: 32-37.
106. Sato Y, Moria R, Katsuma S (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.
107. Scheer H (2006) An overview of chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. In: Grimm B, Porra R, Rüdiger W, Scheer H (eds) Chlorophylls bacteriochlorophylls biochemistry biophysics functions and applications. Springer, Dordrecht, pp 1-26.
108. Schelbert S, Aubry S, Burla B et al (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21: 767-785.
109. 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.
110. Schellenberg M, Matile P, Thomas H (1993) Production of a presumptive chlorophyll catabolite in vitro: requirement for reduced ferredoxin. Planta 191: 417-420.
111. Schenk N, Schelbert S, Kanwischer M et al (2007) The chlorophyllases AtCLH1 and AtCLH2 are not essential for senescence-related chlorophyll breakdown in Arabidopsisthaliana. FEBS Lett 581: 5517-5525.
112. Scherl M, Müller T, Kräutler B (2012) Chlorophyll catabolites in senescent leaves of the lime tree (Tilia cordata). Chem Biodivers 9: 2605-2617.
113. Schuler MA, Duan H, Bilgin M, Ali S (2006) Arabidopsis cytochrome P450s through the looking glass: a window on plant biochemistry. Phytochem Rev 5: 205-237.
114. Shimoda Y, Ito H, Tanaka A (2012) Conversion of chlorophyll b to chlorophyll a precedes magnesium dechelation for protection against necrosis in Arabidopsis. Plant J 72: 501-511.
115. 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.
116. 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.
117. Spassieva S, Hille J (2002) A lesion mimic phenotype in tomato obtained by isolating and silencing an Lls1 homologue. Plant Sci 162: 543-549.
118. Sugishima M, Kitamori Y, Noguchi M et al (2009) Crystal structure of red chlorophyll catabolite reductase: enlargement of the ferredoxin-dependent bilin reductase family. J Mol Biol 389: 376-387.
119. Sugishima M, Okamoto Y, Noguchi M et al (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.
120. Suzuki Y, Shioi Y (1999) Detection of chlorophyll breakdown products in the senescent leaves of higher plants. Plant Cell Physiol 40: 909-915.
121. 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.
122. Suzuki Y, Tanabe K, Shioi Y (1999) Determination of chemical oxidation products of chlorophyll and porphyrin by high-performance liquid chromatography. J Chromatogr A 839: 85-91.
123. Suzuki Y, Doi M, Shioi Y (2002) Two enzymatic reaction pathways in the formation of pyropheophorbide a. Photosynth Res 74: 225-233.
124. 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.
125. Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807: 968-976.
126. 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.
127. Tang Y, Li M, Chen Y et al (2011) Knockdown of OsPAO and OsRCCR1 causes different plant death phenotypes in rice. J Plant Physiol 168: 1952-1959.
128. Thomas H, Howarth CJ (2000) Five ways to stay green. J Exp Bot 51: 329-337.
129. Tommasini R, Vogt E, Fromenteau M et al (1998) An ABC transporter of Arabidopsisthaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13: 773-780.
130. Tsuchiya T, Ohta H, Okawa K et al (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.
131. Valentin HE, Lincoln K, Moshiri F et al (2006) The Arabidopsisvitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis. Plant Cell 18: 212-224.
132. Vergeiner C, Banala S, Kräutler B (2013) Chlorophyll breakdown in senescent banana leaves: catabolism reprogrammed for biosynthesis of persistent blue fluorescent tetrapyrroles. Chem Eur J 19(37): 12294-12305.
133. Vicentini F, Iten F, Matile P (1995) Development of an assay for Mg-dechelatase of oilseed rape cotyledons, using chlorophyllin as the substrate. Physiol Plant 94: 57-63.
134. Wagner D, Przybyla D, op den Camp R et al (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsisthaliana. Science 306: 1183-1185.
135. Willstätter R, Stoll A (1911) Examinations on chlorophyll, XI chlorophyllase. Justus Liebigs Ann Chem 378: 18-72.
136. Wüthrich KL, Bovet L, Hunziker PE et al (2000) Molecular cloning, functional expression and characterisation of RCC reductase involved in chlorophyll catabolism. Plant J 21: 189-198.
137. Yao N, Greenberg JT (2006) Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell 18: 397-411.
138. Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158: 961-969.
139. Zhou C, Han L, Pislariu C et al (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.